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 46¢XN, 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

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 1¢XC 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 30¢XC in July.

The minimum monthly mean temperature decreases

greatly from south to north, which occurs in January, and

ranges from 7 to -12¢XC. 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 (Tai¡¦an 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 (Xi¡¦an) 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

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

25¢X0¡¬ 103¢X0¡¬

1922

14.6

993

1963-1988

Guiyang

26¢X42¡¬ 107¢X0¡¬

1050

15.3

1120

1963-1988

Hangzhou 30¢X5¡¬ 120¢X4¡¬

17

16.2

1317

1963-1988

Wuhan

31¢X0¡¬ 114¢X0¡¬

33

16.3

1169

1963-1988

Xi¡¦an

34¢X4¡¬ 109¢X4¡¬

437

13.4

563

1963-1988

Tai¡¦an

36¢X2¡¬ 116¢X55¡¬

137

12.7

683

1963-1988

Beijing

39¢X55¡¬ 116¢X18¡¬

50

11.7

578

1963-1988

Huhehaote 41¢X12¡¬ 111¢X43¡¬

1063

6.1

391

1963-1988

Shenyang

41¢X59¡¬ 123¢X11¡¬

44

8.2

681

1963-1988

Harbin

46¢X43¡¬ 126¢X42¡¬

149

3.7

523

1963-1988

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.

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 oblata¡¦s flowering to temperature ranged from

2.7 to 4.9 days/oC in the eastern low plain, including

Harbin, Shenyang, Beijing, Xi¡¦an, and Tai¡¦an (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

¡¾

is the length of the bar, i.e. the growing length.

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).

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 0¢XC

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 elements¡Xaltitude, latitude, and

longitude¡Xmay 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).

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.

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