Ecol Res (2011) 26: 713–723
DOI 10.1007/s11284-011-0830-7
O R I GI N A L A R T IC L E
Quansheng Ge • Junhu Dai • Jingyun Zheng
Jie Bai • Shuying Zhong • Huanjiong Wang
Wei-Chyung Wang
Advances in first bloom dates and increased occurrences of yearly
second blooms in eastern China since the 1960s: further phenological
evidence of climate warming
Received: 6 February 2010 / Accepted: 2 March 2011 / Published online: 3 May 2011
Ó The Ecological Society of Japan 2011
Abstract Confirming the results of previous regional
studies on changes in first bloom dates (FBD) in China,
this study provides evidence that complements conclusions drawn from studies of phenological changes in
other dynamic climate systems in the Northern Hemisphere. Furthermore, increased occurrences of yearly
second blooms (YSB) further reinforce results derived
from other studies indicating a recent trend of generalized climate warming across China. Additionally,
ascertaining changes in FBD and YSB against a recent
background not only provides a hitherto poorly formulated autumnal equivalent to the well-studied shifts in
FBD, but also formulates both spring and autumn
flowering changes in recent years. Data in this study are
derived from observations made from 1963 to 2006
by the Chinese Phenological Observation Network
(CPON)—a nationwide system of monitoring stations
that has made observations of over 173 species from
across China since 1963. At each site, the mean value of
each species’ annual deviation and spring mean surface
temperatures were calculated. For each species, years
and locations were also recorded for species in which
second blooms (YSB) occurred. Of the 46 FBD samples,
31 showed advances from the mean, blooming earlier
over the course of the study period. Notably, although
only 8 of the 46 FBD samples showed significance levels
Electronic supplementary material The online version of this article
(doi:10.1007/s11284-011-0830-7) contains supplementary material,
which is available to authorized users.
Q. Ge Æ J. Dai (&) Æ J. Zheng Æ J. Bai Æ S. Zhong Æ H. Wang
Institute of Geographical Sciences and Natural Resources
Research, Chinese Academy of Sciences, A 11, Datun Road,
Chaoyang District, Beijing 100101, People’s Republic of China
E-mail: [email protected]
Tel.: +86-10-64889066
Fax: +86-10-64872274
W.-C. Wang
Atmospheric Sciences Research Center,
State University of New York, Albany, NY 12203, USA
of 0.1 or better, the average FBD did advance by
5.3 days. After the 1980s, the frequency of YSB occurrence remained steady, declining a little from the peak in
the 1980s, but still exhibiting occurrences far more than
were observed earlier. The data from this study clearly
indicate that both the phenological advance of FBD in
spring and the increased occurrence of YSB are consistent with climate warming.
Keywords Phenology Æ First bloom Æ Second bloom Æ
Climate change Æ China
Introduction
Numerous studies over the past several decades have
contributed to a growing body of evidence in support of
observations that interpret phenological shifts in plants
as indicative of climate change. Although most of these
studies were conducted by researchers in Europe and
North America, including those that have greatly influenced further phenological studies (Schwartz and Reiter
2000; Schwartz et al. 2006; Menzel et al. 2006), some
studies carried out in recent years by researchers using
unique observed datasets and drawing original conclusions in Asia, including China (Schwartz and Chen 2002;
Zheng et al. 2006), Japan and South Korea (Doi and
Takahashi 2008; Doi et al. 2010; Ibáñez et al. 2010) have
complemented those original findings, not only providing empirical confirmation for observed phenological
changes in Asia but also enhancing previously acquired
data with corroborations that make studies of phenological changes truly global in scope.
Phenological studies by Chinese researchers using
remotely sensed data have since confirmed that growing
seasons are lengthening by 1.4–3.6 days per year in the
north part of eastern China, and by 1.4 days per year
across the entire eastern China on average from 1982 to
1993 (Chen et al. 2005). Observed phenological data
have proved there are different response patterns of
714
plant phenology to climate change in China (Zheng et al.
2006). Zheng et al. (2006) also reported the different
spring phenophase trends in different parts of China
from 1963 to 1996, and their study in the region north of
33°N showed that the phenophase advanced
1.1–4.3 days per decade for early spring and
1.4–5.4 days per decade for late spring, whereas in the
eastern part of the southwest China it was delayed by
2.9–6.9 days per decade in early spring and 2.4–6.2 days
per decade in late spring. Their studies showed that
spring phenology in eastern China is more sensitivity to
cooling than to warming. Zheng et al. (2002) discussed
the nonlinear response of phenophase to climate change,
and the spatial differences of phenological changes in
China. In addition, many other publications in Chinese
have revealed regional differences in phenophase changes and phenological changes for specific species
(Li et al. 2008, 2010). The only shortcoming to the sound
conclusions drawn by these and other Chinese studies,
however, is that most of them did not discuss the phenological changes on a large scale, and most have relatively shorter data series. In contrast, this study draws,
for the first time, upon comprehensive, broadly distributed data collected from the Chinese Phenological
Observation Network (CPON)—a system of 22 monitoring sites that uniformly gather periodic biological
change data from across northern and eastern China, to
confirm and extend those regional studies of first bloom
dates (FBD) (Zheng et al. 2006) and—significantly—to
report striking increases in observed yearly second
blooms (YSB) for an assortment of plants across the
area. The aim of this study, therefore, is to demonstrate
a conclusive relationship between increased surface
temperatures and the advancement of FBD, as well as to
report an increase in the exceptional phenological
occurrence of YSB over a significant land area in eastern
China.
Compared to studies on phenological change and the
response to climate change in spring and changes in
growing seasons, phenophase changes in autumn have
received less attention. However, in recent years, not
only has the delay of some phenological events in
autumn drawn many concerns (Ibáñez et al. 2010), but
also the effects of this delay on ecosystems have come
into focus (Cleland et al. 2007; Piao et al. 2008). It is well
known that flower phenology, which can be viewed as
fundamental to plant species’ reproductive ecology
(Cleland et al. 2007), responds to climate change very
sensitively (Fitter and Fitter 2002). Furthermore, the
timing of flower phonology shows complicated regional
differences, so that a discussion of the increasing
appearance of a second bloom in autumn and advances
of FBD in spring may provide some new evidence for
ecosystem responses to climate change.
Except for a couple of studies from Europe that
discuss autumnal second flowering (or spring fruiting)
phenomena (Gange et al. 2007), and for brief references
to these studies in a more generalized phenological survey (Luterbacher et al. 2007), few studies have been
conducted specifically to quantify YSB occurrences in
plants. Against this background, it is not only critically
important to study changes of second flowering, but it is
also crucial to collect national information on phenophase changes together with first bloom phenology
through such studies.
Materials and methods
Data in this study are derived from observations made
from 1963 to 2006 by the Chinese Phenological
Observation Network (CPON)—a nationwide system of
monitoring stations that has made comprehensive and
systematic phenological observations of over 173 species across China since its founding in 1963. Since that
time, CPON has been administered through the sponsorship of the Institute of Geographic Sciences and
Natural Resources Research (IGSNRR) at the Chinese
Academy of Sciences. Each station is monitored by
invested local groups, such as botanical gardens,
weather stations, research institutions, universities, and
middle schools, according to uniform observation criteria that include preparation of observational sites,
plant selection, phenophase classification, observation
times, data preparation, etc. (Wan and Liu 1979; Zhang
and Jiang 1996). The standards for data collection from
these local sites have been normalized thoroughly by
IGSNRR guidelines and continuing advice (Wan and
Liu 1979).
Since bloom phenology including FBD in spring and
YSB in late summer and autumn are the focus of this
article, it is essential to define these two phenophases.
FBD is said to have occurred if half of the observed trees
have one or a few flowers open in each tree when many
trees are observed, or if one or a few flowers are open
when just one tree is observed. For wind pollinated
plants, FBD means the date on which flowers release
pollen or when a catkin produces stamens. In contrast,
YSB is recorded when plants bloom for the second time
in summer or autumn in addition to the first bloom in
spring.
As illustrated in Fig. 1, the 22 CPON monitoring
stations are spread across eastern China from close to
23°N latitude at the southernmost station in Liuzhou to
a northern limit near 45°N latitude, close to Harbin.
Longitudinally, the easternmost station lies near 130°E
(close to the northern limit), while the westernmost is in
Chongqing, close to 106°E. Within these boundaries, the
remaining 18 sites are distributed relatively homogenously. For analytical purposes, each site has been
assigned to one of four regions—northeast China, north
and the eastern part of northwest China, southeast
China, and central southern and southwest China—based solely on geographic positioning. Although the
scope of the study is broad, most of the observation sites
are located in China’s eastern plains, so altitudinal
variations, which are relatively negligible across this area
of China, have been disregarded.
715
Fig. 1 The 22 observational sites collecting phenological data for
analysis. The shaded scale shows the trend of the 1951–1999 mean
annual surface temperature is also shown as a reference for climate
change
The mean annual surface temperature trend from
1951 to 1999 across the study region is also depicted, on
a shaded scale, in Fig. 1. Data for this trend was derived
from the Chinese Meteorological Administration. As
expected, the data shows a linear temperature increase
from south to north, which reaches a maximum increase
at the northern territorial frontier of China, the
boundary limit of the study. During this period of time,
the temperature in China increased by an average trend
of 0.22°C per decade, with a total 1.1°C increase in
temperature from 1951 to 1999. Areas south of the
Yangtze River showed little change over the study period, with some zones in the western part of the southern
region exhibiting, in essence, zero temperature change.
Northern and northeastern China, in contrast, have
undergone a notable change in mean temperature over
this nearly five-decade period, with some areas of both
northern regions exhibiting increases of up to 0.6°C per
decade (National Council on Climate Change in China
2007), which corresponds closely with the IPCC’s linear
trend analysis of global mean temperatures over the last
100 years (0.74 ± 0.18°C) (IPCC 2007).
A total of 23 species observed at one or more of the
22 CPON sites were chosen for this study. Individual
species names and site locations are presented in
Table 1. Three criteria dictated species selection: (1)
species had to be endemic to the natural ecology of their
particular sites; (2) species had to have been observed by
CPON for at least 10 years at a site (Forsythia suspensa
Vahl at the Hohhot site, observations of which began
only in 1991, is an exception); and (3) species that had
had an observed YSB at least once within the study
period (1963–2006) were automatically chosen, regardless of the other two criteria. Because the same species
were at times observed at multiple sites, a counterintuitive
Table 1 Chinese Phenological Observation Network (CPON) sites and the species (23 total) observed at each site
Site
Species
Abbreviation
Site
Species
Abbreviation
Harbin
Rhododendron dauricum L.
Prunus triloba Lindl.
Syringa oblata var. alba
Rhododendron dauricum L.
Prunus triloba var. Truncata
Syringa oblata var.alba
Syringa oblata Lindl.
Forsythia viridissima Lindl.
Syringa oblata Lindl.
Forsythia suspensa Vahl
Syringa oblata Lindl.
Malus micromalus Makino
Paulownia fortunei Hemsl.
Pyrus betulaefolia Bunge
Prunus persica Stockes.
Malus halliana Koehne
Cercis chinensis Bunge
Forsythia viridissima Lindl.
Magnolia denudata Desr.
Prunus persica Stockes.
Cercis chinensis Bunge
Michelia figo Spreng.
Liriodendron chinense Sarg.
R. D.
P. T.
S. O. V.
R. D.
P. T. V.
S. O. V.
S. O.
F. V.
S. O.
F. S.
S. O.
M. M.
P. F.
P. B.
P. P.
M. H.
C. C.
F. V.
M.D.
P. P.
C. C.
M. F.
L. C.
Ganxian
Hohhot
Prunus persica Stockes.
Forsythia suspensa Vahl
Prunus davidiana Franch.
Forsythia suspensa Vahl
Forsythia suspensa Vahl
Cerasus tomentosa Thunb.
Prunus triloba var. plena
Syringa oblata Lindl.
Magnolia denudata Desr.
Pyrus betulaefolia Bunge
Prunus salicina Lindl.
Pyrus communis L.
Magnolia denudata Desr.
Magnolia liliflora Desr.
Paulownia fortunei Hemsl.
Magnolia denudata Desr.
Prunus persica Stockes.
Forsythia viridissima Lindl.
Malus micromalus Makino
Paulownia fortunei Hemsl.
Prunus persica Stockes.
Prunus salicina Lindl.
Prunus persica Stockes.
P. P.
F. S.
P. D.
F. S.
F. S.
C. T.
P. T. V.
S. O.
M. D.
P. B.
P. S.
P. C.
M. D.
M. L.
P. F.
M. D.
P. P.
F. V.
M. M.
P. F.
P. P.
P. S.
P. P.
Mudanjiang
Changchun
Shenyang
Beijing
Liaocheng
Yancheng
Yangzhou
Shanghai
Nanchang
Luoyang
Xi’an
Wuhan
Renshou
Chongqing
Changde
Changsha
Guiyang
Guilin
Liuzhou
716
total of 46 samples for the FBD series and 36 samples
for the YSB series, all of which were broadleaved tree
species, were evaluated in the study.
At each site, the mean value of each species’ annual
deviation for FBD from 1963 to 2006 and spring
(March–April–May) mean surface temperatures were
calculated (see Fig. 2). Correlations were drawn and
significance levels were determined for FBDs and mean
annual spring temperatures. Furthermore, for each
species, years and locations were recorded for species in
which second blooms (YSB) occurred. Finally, linear
regression analyses were performed to evaluate trends
for both the advance of FBD and the frequency of YSB
occurrences within the 23 species during the four-decade
study period.
Results
Advance of first bloom dates
Of the 46 FBD samples, 31 exhibited advances from the
mean, blooming earlier over the course of the study
period. The average advancement of FBD in the study
area is 0.121 days per year during the last few decades,
which is similar to the change in spring phenophases
seen in other eastern Asian countries. For example, the
advancement for Japan is 0.168 days per year from 1953
to 2005 (Doi and Takahashi 2008), which is less than in
Europe; Menzel et al. (2006) revealed that the
advancement of spring in Europe has been 2.5 days per
decade from 1971 to 2000. As indicated in Table 2, the
magnitude of FBD trends showed a strong regional
variation (north–south). For example, in northeastern
China (Harbin, Mudanjiang, Changchun, and Shenyang), a clear trend of advance in FBD was observed. All
nine samples from this region showed a linear trend of
0.154 days/year, which implies an advance of 6.8 days
from 1963 to 2006. Among the 12 samples from northern China and the eastern part of northwestern China
(Beijing, Liaocheng, Yancheng, Hohhot, Luoyang, and
Xi’an), 11 exhibited advances in FBDs, with Liaocheng,
where observations ceased in 1994, being an exception.
The average linear trend for these 12 samples was as
high as
0.308, indicating a 13.6 day advance in
FBD—the largest change in China.
Further south, seven of the ten samples in the
southeastern region (Yangzhou, Shanghai, Nanchang,
and Ganxian) showed advances in FBD, while three
showed a delay. The average trend of these advances was
0.193 days/year, or 8.5 days over the 1963–2006 data
period. Among the three delayed samples, two were
Fig. 2 Time series of anomalous first bloom date (FBD) (bars) with years with second bloom (YSB) marked in red. The line indicates
March–April–May temperature
Rhododendron dauricum L.
Prunus triloba Lindl.
Syringa oblata var. Alba
Rhododendron dauricum L.
Prunus triloba var. truncata
Syringa oblata var.alba
Syringa oblata Lindl.
Forsythia viridissima Lindl.
Syringa oblata Lindl.
Forsythia suspensa Vahl
Syringa oblata Lindl.
Malus micromalus Makino
Paulownia fortunei Hemsl.
Pyrus betulaefolia Bunge
Prunus persica Stockes.
Malus halliana Koehne
Cercis chinensis Bunge
Forsythia viridissima Lindl.
Magnolia denudata Desr.
Prunus persica Stockes.
Cercis chinensis Bunge
Michelia figo Spreng.
Liriodendron chinense Sarg.
Harbin
1984–2006/12
1964–2006/18
1973–2006/17
1983–1996/13
1979–1996/17
1978–1996/19
1986–2006/13
1964–2005/15
1963–2006/23
1968–2006/23
1963–2006/34
1963–2006/35
1971–1994/19
1978–1996/19
1963–1996/22
1978–1995/14
1963–1996/25(26)a
1981–2006/18
1981–2006/20
1983–2006/13
1964–2006/15
1984–2006/11
1983–2006/13
Duration/sample
year
0.255
0.204
0.045
0.184
0.200
0.028
0.218
0.120
0.135
0.222
0.150
0.150
0.037
0.442
0.210
0.265
0.277
0.489
0.428
0.240
0.319
0.462
0.678
FBD trend
0.179
0.134
0.799
0.508
0.528
0.894
0.318
0.261
0.158
0.040
0.047
0.030
0.779
0.039
0.149
0.302
0.029
0.119
0.056
0.420
0.301
0.243
0.137
P
0.622
0.064
0.036
0.138
0.192
0.960
0.160
0.006
0.006
0.001
0.008
0.028
0.005
0.014
0.030
0.014
0.161
0.330
0.331
0.202
0.982
0.242
0.060
0.276
0.002
P
0.013
0.002
0.002
0.009
0.000
0.016
0.027
0.008
0.042
YSB trend
Liuzhou
Guilin
Guiyang
Changde
Changsha
Chongqing
Renshou
Wuhan
Luoyang
Xi’an
Ganxian
Hohhot
Sites
Prunus persica Stockes.
Forsythia suspensa Vahl
Prunus davidiana Franch.
Forsythia suspensa Vahl
Forsythia suspensa Vahl
Cerasus tomentosa Thunb.
Prunus triloba var. plena
Syringa oblata Lindl.
Magnolia denudata Desr.
Pyrus betulaefolia Bunge
Prunus salicina Lindl.
Pyrus communis L.
Magnolia denudata Desr.
Magnolia liliflora Desr.
Paulownia fortunei Hemsl.
Magnolia denudata Desr.
Prunus persica Stockes.
Forsythia viridissima Lindl.
Malus micromalus Makino
Paulownia fortunei Hemsl.
Prunus persica Stockes.
Prunus salicina Lindl.
Prunus persica Stockes.
Species
1978–1996/17
1979–2006/22
1991–2006/9
1966–1996/23
1979–2006/22
1979–2006/20
1964–2006/31
1963–2006/34
1963–2006/23
1982–2006/17
1973–1994/19
1973–1994/16
1963–2006/33
1980–2006/19
1973–1991/18
1965–2006/16
1963–2006/18
1979–2006/20
1986–2006/13
1980–2006/19
1964–2006/30
1964–1993/24
1964–1995/24
Duration/sample
year
FBD First bloom date, YSB Years of second bloom
p-value : a measure of the statistical significance that the regression line fits the data
a
For Cercis chinensis Bunge in Yangzhou, we have 25 years and 26 years observed phenological data for spring and autumn, respectively, from 1963 to 1996
Nanchang
Shanghai
Liaocheng
Yancheng
Yangzhou
Beijing
Changchun
Shenyang
Mudanjiang
Species
Site
0.017
1.914
0.285
0.058
0.125
0.128
0.103
0.150
0.132
0.044
0.221
0.294
0.046
0.064
0.572
0.101
0.010
0.221
0.290
0.276
0.079
0.562
0.259
FBD
trend
0.974
0.000
0.051
0.720
0.561
0.512
0.272
0.056
0.353
0.868
0.454
0.411
0.749
0.771
0.024
0.710
0.960
0.603
0.502
0.389
0.679
0.044
0.429
P
0.070
0.292
0.651
0.396
0.315
0.000
0.933
0.127
0.377
0.593
0.334
0.541
0.967
0.186
0.140
0.217
0.903
0.028
0.003
0.018
0.012
0.006
0.005
0.002
0.000
0.010
0.018
0.019
0.000
0.016
0.018
0.012
0.003
0.002
0.009
0.040
0.947
P
0.001
YSB trend
Table 2 FBD and YSB trend statistics for each species at each site, and P value (a measure of the statistical significance that the regression line fits the data) for each sample
717
718
Yangzhou saw a second occurrence (Cercis chinensis) in
the 1970s.
YSB in the 1980s
Fig. 3 Variation in average FBD trend for each region and for all
of China
observed only from 1963 to 1996, and one was observed
only from 1983 to 2006. Only 5 of the 15 samples in
South Central and Southwest China (Wuhan, Renshou,
Chongqing, Changde, Changsha, Guiyang, Guilin, and
Liuzhou) showed an advance, with a mean of
0.096 days/year or about 4.2 days from 1963 to 2006.
Among the five samples with FBD advance, four were
observed through 2006, while one was observed only
until 1995.
Notably, only 8 of the 46 FBD samples showed significance levels of 0.1 or better. Various factors, such as
the discontinuity of observations at some sites, may
account for the lack of significance, especially when
observations solidly confirm the trend of advancement.
Only three of the delayed samples were statistically significant. Average and regional FBD trends for the whole
study area can be seen in Fig. 3.
Increased occurrences of yearly second blooms
YSB in the 1960s and 1970s
In the 1960s, only three species—Magnolia denudata,
Prunus persica, and Cercis chinensis—had been observed
in second bloom and only at two sites, Yangzhou and
Chongqing (Table 3), which are in the southeast and
central southwest regions, respectively. During the
1970s, however, a total of six species at eight different
sites experienced second blooms. Two of the species
(Prunus persica and Cercis chinensis) that had been
observed in the 1960s again showed second blooms, the
former being observed at different sites (Guilin and
Liuzhou) in different years (1974 and 1977, respectively),
both of which are to the south and west of the plant’s
YSB original observation in Yangzhou. Significantly,
observed occurrences of YSB phenomena in the 1970s
expanded into both north China and the eastern part of
northwest China (Beijing, Liaocheng), as well as into
northeast China (Shenyang). Despite the increased
incidence, of the sites with YSB in the 1960s only
In the 1980s, observed occurrences of second blooms in
China rose sharply, with 15 species observed at 11 sites.
Of those sites, eight had not exhibited YSB in the previous two decades, of which one was in north China
(Xian) and one was in northeast China (Mudangjiang).
Of the 15 species demonstrating YSB in the 1980s, 8 had
not bloomed a second observable time prior to the
1980s. Interestingly, one species, Magnolia denudata,
which had a second bloom in Chongqing once in 1965,
again demonstrated YSB in the 1980s, blooming in
Wuhan in 1986. Furthermore, a second bloom of Cercis
chinensis was, in the 1980s, again observed at Yangzhou
(in two separate years, 1984 and 1989); Malus halliana,
for the first time at any site, was also observed in second
bloom at Yangzhou in both 1984 and 1986. Finally,
Prunus persica was observed for a third consecutive
decade and at three different sites, two of which, Nanchang and Ganxian (both in the southeast), had not
been observed as demonstrating occurrences of YSB
before. Markedly, Prunus persica demonstrated YSB for
a second time in Liuzhou, exhibiting YSB in a total of
8 years in the 1980s, which is the largest number of
observations of any species in one decade at any site
over the course of the study.
YSB after the 1980s
After the 1980s, the frequency of YSB occurrence, both
in terms of species and sites, remained steady, declining
a little from the peak in the 1980s, but still exhibiting
occurrences far more often than were observed in the
1960s and 1970s. In the 1990s, for example, ten species
were observed in second bloom at nine sites. Of those
sites, only one, Hohhot in the eastern part of northwest
China, had not previously presented an occurrence of
second bloom. Yangzhou, for the fourth consecutive
decade, had another occurrence of second bloom, presenting with the same species (Malus halliana) as it had
in the 1980s. Also notable was Xi’an, where four species
were observed in second bloom during the 1990s,
including the only new species, Syringa oblata, which
bloomed a second time in 1991. A noteworthy absence in
the 1990s was Cercis chinensis, which had been observed
in second bloom in each of the previous three decades.
In the twenty-first century, the same elevated trend
that marked the 1990s was maintained, with a total of 11
species at 11 sites being observed in second bloom. Three
new sites had observed occurrences of YSB in the 2000s:
Shanghai in southeast China, and (significantly) Harbin
and Changchun, both of which are in the northeast,
Harbin being the furthest north of any site in the study.
In fact, Harbin presented a second bloom of the only
new species, Rhododendron dauricum and in three
Number of species/
sites/times (of all
species at all sites)
with the second
bloom
3/2/3
Forsythia viridissima
Lindl. (Shenyang: 1979;
Guiyang: 1979)
Magnolia denudata Desr.
(Chongqing: 1965)
6/8/13
Prunus salicina Lindl.
(Guilin: 1973, 1975,
1977)
Prunus persica Stockes.
(Guilin: 1974; Liuzhou:
1977)
Paulownia fortunei Hemsl.
(Liaocheng: 1973)
Cercis chinensis Bunge
(Yangzhou: 1977)
Forsythia suspensa Vahl
(Beijing: 1973, 1976,
1978; Xi’an: 1979)
Cercis chinensis Bunge
(Yangzhou: 1966)
Prunus persica Stockes.
(Yangzhou: 1967)
Species showing
second bloom
[Species (site:
year)]
1970s
1960s
Decade
Table 3 Plants with YSB and their spatial distribution by decade
Prunus triloba var. truncata Lindl. (Mudanjiang:
1987)
Prunus triloba var. plena
(Xi’an: 1982)
Pyrus betulaefolia Bunge
(Wuhan: 1982)
Pyrus communis L.
(Renshou: 1988)
Syringa oblata var. alba
(Mudanjiang: 1989)
15/11/36
Malus micromalus Makino (Guiyang: 1987)
Paulownia fortunei Hemsl.
(Guiyang: 1987)
Prunus persica Stockes.
(Nanchang: 1988; Ganxian: 1980, 1988; Liuzhou: 1981–1983,
1985–1988)
Prunus salicina Lindl.
(Renshou: 1988)
Malus halliana Koehne
(Yangzhou: 1984, 1986)
Forsythia suspensa Vahl
(Beijing: 1980; Luoyang:
1983, 1987–1989; Xi’an:
1980, 1982, 1984, 1985,
1988)
Forsythia viridissima
Lindl. (Guiyang: 1982,
1985)
Magnolia denudata Desr.
(Wuhan: 1986)
Cerasus tomentosa Thunb.
(Xi’an: 1984)
Cercis chinensis Bunge
(Yangzhou: 1984, 1989)
1980s
Rhododendron dauricum
L. (Harbin: 2003, 2005,
2006)
Syringa oblata Lindl.
(Changchun: 2003, 2004)
Syringa oblata var. Alba
(Mudanjiang: 1994;
Xi’an: 1991)
11/11/24
Magnolia liliflora Desr.
(Chongqing: 2005)
Michelia figo Spreng.
(Nanchang: 2004, 2006)
Paulownia fortunei Hemsl.
(Guiyang: 2003, 2004)
Prunus triloba var. Plena
(Xi’an: 1990, 1991, 1994)
Pyrus communis L.
(Renshou: 1990)
Syringa oblata Lindl.
(Beijing: 1995)
10/9/22
Magnolia denudata Desr.
(Chongqing: 2005)
Forsythia viridissima
Lindl. (Shenyang: 2004;
Shanghai: 2004, 2005)
Liriodendron chinense
Sarg. (Nanchang: 2005)
Forsythia suspensa Vahl
(Beijing: 2004–2006;
Hohhot: 2005; Xi’an:
2003, 2006)
Cerasus tomentosa Thunb.
(Xi’an: 2003)
Cercis chinensis Bunge
(Nanchang: 2003, 2005)
2000s
Prunus persica Stockes.
(Ganxian: 1992; Liuzhou: 1990, 1991,
1993–1995)
Prunus salicina Lindl.
(Renshou: 1990)
Malus micromalus Makino (Beijing, 1995)
Cerasus tomentosa Thunb.
(Xi’an: 1991, 1993)
Forsythia suspensa Vahl
(Hohhot: 1993; Luoyang: 1992, 1993; Xi’an:
1991)
Malus halliana Koehne
(Yangzhou: 1991)
1990s
719
720
different years between 2000 and 2006. Hohhot, in the
eastern part of northwest China, was again observed as
having a second bloom. Also worth mentioning is
Magnolia denudata, which was first observed in second
bloom in Chongqing (1965) and then again in Wuhan
(1986). Maintaining this bi-decadal pattern, it was again
observed, but back in Chongqing, which had not had an
observed second bloom in the 40 years prior to 2005.
Chongqing also presented the occurrence of second
bloom in a species, Magnolia liliflora, that had not
previously presented. In total, five new species were
observed in the 2000s, while Cerasus tomentosa presented for a third consecutive decade in Xi’an, and
Cersis chinensis reappeared in second bloom, this time in
Nanchang.
In total, of the 36 samples presenting a second bloom,
although only 7 were statistically significant, 24 showed
clearly observable increases in frequency. In contrast, of
the 12 samples that exhibited decreased frequency, only
1 was significant. The average trend of YSB for 36
samples was 0.0064, meaning that frequency increased
6.4% per decade. The increase was, however, much
larger (about 28%) over the 1963–2006 duration of the
study period.
Discussion
In the past 50 years, the annual mean surface temperature across China increased by 1.1°C, with a 0.40°C per
decade warming in the northeast and north regions,
which is larger than the warming trend in the southeast
and southwest regions (National Council on Climate
Change in China 2007). Such warming in the north is
consistent with the more pronounced FBD trends
observed in those regions in comparison with trends
observed in more southerly regions (Table 4, Fig. 2).
Significant correlations of FBD trend and that of temperature can be seen from the statistics of Table 4. FBD
trends correlate with temperatures of the former month
most significantly, with 31 data series of 46 (67.39%) at
a significance level of 0.01 (P < 0.01), and with 38 data
series of 46 (82.61%) at a significance level of 0.05
(P < 0.05), respectively. The relationship between FBD
trends and the average temperatures of April and May
were the second most significant correlation, with 17
data of 46 (36.96%) at significance level of 0.01
(P < 0.01), and with 26 data series of 46 (56.52%) at
significance level of 0.05 (P < 0.05) respectively. So the
FBD advance was caused by the advance of spring and
the temperature increase in spring in China. The four
northeast sites, for example, presented the greatest
overall significance between phenological advancement
and spring temperature of any region in the study.
Markedly, however, even in the two southern regions,
where delays were observed in 8 of 12 species, the overall
trend was toward advancement. Overall, the first bloom
of China’s plants in spring has advanced by approximately 5.3 days since 1963, or about 0.121 days per year
on average. Such phenological trends, with appreciable
increases in northern temperatures compared to slight or
no increases in the south, confirm previous, though more
regional, studies that indicated such latitudinal orientations affecting FBD advancements in China. Such trends
have also been confirmed in other regions of the world
(Menzel et al. 2006; Schwartz and Reiter 2000), demonstrating the truly global nature of the phenological
changes substantiated by this China-wide study.
The data for YSB as observed by CPON over the
course of the study period requires further, more controlled investigation, but several initial conclusions can
be advanced. According to the observational data (Table 5), a consistent pattern emerges across the study area
when warming trends are correlated with the occurrence
of YSB. Regardless of which 10-day period is considered
in the 50 days prior to an occurrence of YSB in a species, a trend emerges whereby warm temperature
anomalies result in YSB occurrences far more often than
when cooling anomalies are present, with northeast
China presenting the most apparent ratio of occurrence
(9:1). Interestingly, although the ratio in north China
and the eastern part of northwest China is the lowest of
all the regions, it had the highest total number (36) of
YSB occurrences. This is especially interesting since the
central southern and southwestern region had more sites
and species, implying that the increase of autumn temperatures for each site coincides with the increasing
occurrences of second bloom. This trend indicates that
temperature in the period before the onset of second
blooms plays a critical role in the occurrence of YSB. A
statistical connection between second bloom and sunshine duration is not conclusive, however, as the photoperiodism for most plants depends only on daytime
length and not on sunshine duration. This is a result
requiring further investigation.
The current warming trend, which researchers across
the Northern Hemisphere have observed since the early
1980s, first became empirically measureable in China in
1989. The results of this study suggest that increased
instances of YSB in China correspond with this trend,
with second blooms rising observably until the 1980s,
when their occurrence spiked sharply. The multi-decadal
trend of YSB is especially notable because, after the
sharp increase of occurrences in the 1980s, the number
of observed second blooms actually declined by 33%.
Even so, in the 1990s and 2000s, second blooms still
occurred at least 40% (and as much as 73%) more often
than in the 1960s and 1970s. According to the YSB
events occurring in China during the last few decades, it
can be speculated that this special phenological phenomenon might appear in other countries in near future.
Additionally, plants can produce almost all their
organs in autumn, but formation of their sexual cells
requires environments with low temperature, thus, the
plants usually bloom the following spring. But with the
increasing occurrence of abnormally hot weather in
autumn, plants react to this environment if to that of the
next spring, and, as a consequence, bloom in autumn in
Rhododendron dauricum L.
Prunus triloba Lindl.
Syringa oblata var. alba
Rhododendron dauricum L.
Prunus triloba var. Truncata
Syringa oblata var. alba
Syringa oblata Lindl.
Forsythia viridissima Lindl.
Syringa oblata Lindl.
Forsythia suspensa Vahl
Syringa oblata Lindl.
Malus micromalus Makino
Paulownia fortunei Hemsl.
Pyrus betulaefolia Bunge
Prunus persica Stockes.
Malus halliana Koehne
Cercis chinensis Bunge
Forsythia viridissima Lindl.
Magnolia denudata Desr.
Prunus persica Stockes.
Cercis chinensis Bunge
Michelia figo Spreng.
Liriodendron chinense Sarg.
Prunus persica Stockes.
Forsythia suspensa Vahl
Prunus davidiana Franch.
Forsythia suspensa Vahl
Forsythia suspensa Vahl
Cerasus tomentosa Thunb.
Prunus triloba var. Plena
Syringa oblata Lindl.
Magnolia denudata Desr.
Pyrus betulaefolia Bunge
Prunus salicina Lindl.
Pyrus communis L.
Magnolia denudata Desr.
Magnolia liliflora Desr.
Paulownia fortunei Hemsl.
Magnolia denudata Desr.
Prunus persica Stockes.
Forsythia viridissima Lindl.
Malus micromalus Makino
Paulownia fortunei Hemsl.
Prunus persica Stockes.
Prunus salicina Lindl.
Prunus persica Stockes.
Harbin
4–24
5–4
5–8
4–29
5–3
6–9
5–1
4–20
4–30
4–2
4–12
4–16
4–12
3–31
3–29
4–3
4–5
3–12
3–14
3–19
3–20
4–6
4–17
2–19
4–11
4–13
3–13
3–18
3–23
3–30
4–4
3–1
3–27
3–4
3–9
3–3
3–11
3–27
2–28
3–20
2–18
3–10
3–22
3–2
2–25
2–19
Average FBD
0.412
0.07
0.105
0.347
0.273
0.16
0.141
0.024
0.177
0.293
0.304
0.243
0.379
0.171
0.327
0.349
0.191
0.246
0.488*
0.657*
0.589*
0.141
0.056
0.706**
0.346
0.034
0.15
0.345
0.263
0.177
0.158
0.029
0.087
0.561*
0.52*
0.503**
0.661**
0.004
0.547*
0.538*
0.457*
0.6*
0.351
0.633**
0.649**
0.393
R1
0.796**
0.67**
0.493*
0.605*
0.585*
0.151
0.515
0.015
0.279
0.318
0.3
0.383*
0.059
0.385
0.645**
0.356
0.415*
0.837**
0.679**
0.655*
0.631*
0.133
0.236
0.623**
0.299
0.554**
0.562**
0.792**
0.727**
0.633**
0.376*
0.364
0.045
0.605**
0.77**
0.527**
0.396
0.353
0.427
0.621**
0.489*
0.767**
0.727**
0.744**
0.714**
0.323
R2
0.778**
0.676**
0.574*
0.703**
0.492*
0.101
0.488
0.33
0.659**
0.809**
0.694**
0.75**
0.255
0.075
0.678**
0.698**
0.697**
0.242
0.358
0.088
0.188
0.498
0.346
0.09
0.611*
0.523*
0.241
0.581**
0.732**
0.783**
0.702**
0.186
0.162
0.393
0.43
0.456**
0.709**
0.566*
0.149
0.395
0.448*
0.579*
0.642**
0.204
0.06
0.039
R3
0.864**
0.757**
0.667**
0.75**
0.734**
0.46*
0.697**
0.69**
0.745**
0.33
0.698**
0.691**
0.37
0.298
0.097
0.211
0.001
0.05
0.151
0.48
0.143
0.289
0.557*
0.148
0.525
0.482*
0.113
0.224
0.342
0.406*
0.56**
0.196
0.045
0.045
0.282
0.077
0.028
0.278
0.005
0.065
0.108
0.011
0.066
0.052
0.186
0.194
R4
0.295
0.405
0.289
0.444
0.21
0.278
0.297
0.076
0.001
0.182
0.336
0.264
0.433
0.107
0.253
0.083
0.151
0.078
0.123
0.045
0.131
0.202
0.385
0.092
0.522
0.242
0.098
0.046
0.171
0.275
0.563**
0.257
0.069
0.171
0.173
0.068
0.065
0.399
0.229
0.369
0.151
0.073
0.413
0.089
0.028
0.128
R5
0.917**
0.801**
0.703**
0.877**
0.788**
0.213
0.795**
0.638*
0.82**
0.624**
0.802**
0.821**
0.407
0.116
0.488*
0.517
0.545**
0.161
0.296
0.254
0.016
0.497
0.601*
0.167
0.799**
0.692**
0.222
0.47*
0.616**
0.696**
0.758**
0.027
0.072
0.344
0.495
0.361*
0.575**
0.566*
0.068
0.236
0.472*
0.594*
0.57*
0.107
0.047
0.124
R3–4
0.917**
0.801**
0.703**
0.877**
0.788**
0.213
0.795**
0.638*
0.82**
0.624**
0.802**
0.821**
0.407
0.116
0.488*
0.517
0.545**
0.161
0.296
0.254
0.016
0.497
0.601*
0.167
0.799**
0.692**
0.222
0.47*
0.616**
0.696**
0.758**
0.027
0.072
0.344
0.495
0.361*
0.575**
0.566*
0.068
0.236
0.472*
0.594*
0.57*
0.107
0.047
0.124
R4–5
0.89**
0.809**
0.674**
0.755**
0.732**
0.328
0.739**
0.641**
0.756**
0.558**
0.79**
0.778**
0.509*
0.039
0.369
0.413
0.387
0.148
0.268
0.21
0.061
0.347
0.683*
0.204
0.814**
0.689**
0.212
0.347
0.5*
0.62**
0.781**
0.078
0.08
0.273
0.475
0.315
0.531*
0.333
0.124
0.317
0.47*
0.573*
0.464*
0.057
0.034
0.077
R3–5
Average FBD Average FBD during 1963–2006 (month-day); R1–R5 correlation coefficient between FBD and temperature of January to May respectively; R3–4, R4–5, R3–5 correlation
coefficient between FBD and average temperature of March to April, April to May, and March to May respectively
*P < 0.05, ** P < 0.01
Liuzhou
Guilin
Guiyang
Changde
Changsha
Chongqing
Renshou
Wuhan
Luoyang
Xi’an
Ganxian
Hohhot
Nanchang
Shanghai
Liaocheng
Yancheng
Yangzhou
Beijing
Changchun
Shenyang
Mudanjiang
Species
Site
Table 4 Mean FBD of each species and its correlation with spring temperatures
721
98
60
38
59
39
58
40
58
40
61
37
33
25
8
23
10
21
12
20
13
18
15
19
7
12
12
7
10
9
8
11
10
9
36
19
17
15
21
19
17
21
15
23
13
10
9
1
9
1
8
2
9
1
10
0
Temperature anomaly in the 5th 10 days before the second bloom
Temperature anomaly in the 4th 10 days before the second bloom
Temperature anomaly in the 3rd 10 days before the second bloom
Temperature anomaly in the 2nd 10 days before the second bloom
Total second bloom occurrence
Temperature anomaly in the 1st 10 days before the second bloom
Occurrence
Occurrence
Occurrence
Occurrence
Occurrence
Occurrence
Occurrence
Occurrence
Occurrence
Occurrence
with
with
with
with
with
with
with
with
with
with
warming (+) anomaly
cooling ( ) anomaly
warming (+) anomaly
cooling ( ) anomaly
warming (+) anomaly
cooling ( ) anomaly
warming (+) anomaly
cooling ( ) anomaly
warming (+) anomaly
cooling ( ) anomaly
North China
and the eastern
part of Northwest
China
Northeast
China
Region
Table 5 Relationship between temperature variability and second flowering in China and regional differences
Southeast
China
Southwest and
South Central
China
Total
722
advance. So, a second bloom in autumn might be
explained by unusually high temperatures in autumn.
For example, variation in the original thermoperiodism
and photoperiodism in autumn might be a major factor
in triggering the second bloom of plants in China.
Again, further investigation is necessary to confirm this
hypothesis.
The data from this study clearly indicate that both
the phenological advance of FBD in spring and the
increased occurrence of YSB in autumn and early winter
are consistent with climate warming—a result that could
have significant implications if the current warming
trend continues. Each plant species has physiological
threshold temperatures that they can tolerate and,
although plants can adapt and survive within a certain
range of conditions, there are both maximum and minimum temperature thresholds beyond which advance or
delay of phenophases can lead to long-term developmental deviations that cause permanent changes to plant
physiologies. As indicated by Chuine and Beaubien
(2001), phenology is shown to be a major determinant of
plant species range and should therefore be used to
assess the consequences of global warming on plant
distribution and the spread of alien plant species. If this
trend continues, these thermophilic plants may begin to
demonstrate permanent patterns of spatial migration,
which is why further study into these phenomena,
especially using data collected from CPON, is both
necessary and warranted.
Acknowledgments We would very much like to thank Gregory
Pierce for his efforts in helping composing and editing the English
language presentation of this paper. This research project was
supported by National Natural Science Foundation of China
(NSFC, Project No.: 41030101, 40625002, and 40871033), and
project of Institute of Geographical Sciences and Natural
Resources Research, Chinese Academy of Sciences.
References
Chen X, Hu B, Yu R (2005) Spatial and temporal variation of
phenological growing season and climate change impacts in
temperate eastern China. Glob Change Biol 11:1118–1130
Chuine I, Beaubien EG (2001) Phenology is a major determinant of
tree species range. Ecol Lett 4:500–510
Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD
(2007) Shifting plant phenology in response to global change.
Trends Ecol Evol 22:357–365
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, Takahashi M, Katano I (2010) Genetic diversity increases
regional variation in phenological dates in response to climate
change. Glob Change Biol 16:373–379
Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in
British plants. Science 296:1689–1691
Gange AC, Gange EG, Sparks TH, Boddy L (2007) Rapid and
recent changes in fungal fruiting patterns. Science 316:71
Ibáñez I, Primack RB, Miller-Rushing AJ, Ellwood E, Higuchi H,
Lee SD, Kobori H, Silander JA (2010) Forecasting phenology
under global warming. Philos Trans R Soc B Biol Sci
365:3247–3260
723
Intergovernmental Panel on Climate Change (IPCC) (2007)
Climate change 2007: the physical science basis. Cambridge
University Press, New York
Li RP, Zhou GS, Guo CM et al (2008) Phenology characteristics of
Ulmus pumila, its simulation from 1981 to 2005 in Northeast
China (in Chinese). J Meteorol Environ 24:20–24
Li HM, Ma YS, Wang YL (2010) Influences of climate warming on
plant phenology in Qinghai Plateau (in Chinese). J Appl
Meteorol Sci 21:200–505
Luterbacher J, Liniger MA, Menzel A, Estrella N, Della-Marta
PM, Pfister C, Rutishauser T, Xoplaki E (2007) Exceptional
European warmth of autumn 2006 and winter 2007: historical
context, the underlying dynamics, and its phenological impacts.
Geophys Res Lett 34:L12704
Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, AlmKubler K, Bissolli P, Braslavska OG, Briede A, Chmielewski
FM, Crepinsek Z, Curnel Y, Dahl A, Defila C, Donnelly A,
Filella Y, Jatczak K, Mage F, Mestre A, Nordli O, Penuelas J,
Pirinen P, Remisova V, Scheifinger H, Striz M, Susnik A, Van
Vliet AJH, Wielgolaski F-E, Zach S, Zust ANA (2006) European phenological response to climate change matches the
warming pattern. Glob Change Biol 12:1969–1976
National council on climate change in China (2007) China’s
National Assessment Report on Climate Change (in Chinese).
Science Press, Beijing
Piao S, Ciais P, Friedlingstein P et al (2008) Net carbon dioxide
losses of northern ecosystems in response to autumn warming.
Nature 451:49–52
Schwartz MD, Chen X (2002) Examining the onset of spring in
China. Clim Res 21:157–164
Schwartz MD, Reiter BE (2000) Changes in North American
spring. Int J Climatol 20:929–932
Schwartz MD, Ahas R, Aasa A (2006) Onset of spring starting earlier
across the Northern Hemisphere. Glob Change Biol 12:343–351
Wan M, Liu X (1979) China’s national phenological observational
criterion (in Chinese). Science Press, Beijing
Zhang F, Jiang A (1996) A review of studies on the phenology in
China. Phenol Seas 1:71–78
Zheng J, Ge Q, Hao Z (2002) Impacts of climate warming on plants
phenophases in China for the last 40 years. Chin Sci Bull
47:1826–1831
Zheng JY, Ge QS, Hao ZX, Wang WC (2006) Spring phenophases
in recent decades over eastern China and its possible link to
climate changes. Clim Change 77:449–462