Wc

YWa

b

c

a

ARRA

KGFWFE

1

(latiaewr2agf

tB

((Wz

0h

Field Crops Research 134 (2012) 193–199

Contents lists available at SciVerse ScienceDirect

Field Crops Research

jou rn al h om epage: www.elsev ier .com/ locate / fc r

arming impacts on winter wheat phenophase and grain yield under fieldonditions in Yangtze Delta Plain, China

unlu Tiana, Jin Chena, Changqing Chena, Aixing Dengb, Zhenwei Songb, Chengyan Zhengb,illem Hoogmoedc, Weijian Zhanga,b,∗

Institute of Applied Ecology, Nanjing Agricultural University, Nanjing 210095, ChinaInstitute of Crop Science, Chinese Academy of Agricultural Sciences/Key Laboratory of Crop Physiology & Ecology, Ministry of Agriculture, Beijing 100081, ChinaFarm Technology Group, Wageningen University, Wageningen 6700 AA, The Netherlands

r t i c l e i n f o

rticle history:eceived 27 March 2012eceived in revised form 31 May 2012ccepted 31 May 2012

eywords:lobal warming

a b s t r a c t

A five-year experiment with Free Air Temperature Increase facility was conducted to investigate the actualresponses of winter wheat phenophase and yield to warming in Yangtze Delta Plain, China. Air temper-ature increase of around 1.5 ◦C in wheat canopy advanced crop phenophases significantly, leading to areduction in length of the entire growth period by 10 days (P < 0.05). This reduction was mainly found inthe length of pre-anthesis phase, while the length of post-anthesis phase was prolonged slightly. Warm-ing increased grain yield by 16.3% (P < 0.05) whereas no significant effects were found on the aboveground

ood securityheat growth

ree air temperature increaseast China

biomass. Warming tended to increase the numbers of productive spike and filled grain and the harvestindex. The areas of flag leaf and total green leaf at anthesis and the 1000-grain weight were 36.0, 19.2 and5.9% higher in the warmed plots than the un-warmed control (P < 0.05), respectively. Warming stimu-lated the filling rate of inferior grain (P < 0.05), while the rate of superior grain stayed almost unchanged.The above evidences suggest that anticipated warming may facilitate winter wheat production in East

China.

. Introduction

More than 20% of the world’s food consumers depend on wheatTriticum aestivum L.) which is produced on an area of over 200 mil-ion hectares worldwide (Ortiz et al., 2008). And winter wheat areaccounts for more than 80% of this total, and it is typically grown inhe seasons of winter and spring where warming is mainly antic-pated. China is the largest country of winter wheat production,nd more than 70% of Chinese winter wheat is sown in the east-rn provinces. Meanwhile, the mean air temperature in the 2000sas about 1.5 and 0.7 ◦C higher than during the 1980s and 1990s,

espectively, and is expected to increase with about 1.2–2.0 ◦C by050 in China (Chavas et al., 2009). Thus, to learn the impacts of

nticipated warming on winter wheat growth in East China willreatly facilitate the development of strategies leading to futureood security in China and even in the world.

∗ Corresponding author at: Institute of Crop Science, Chinese Academy of Agricul-ural Sciences/Key Laboratory of Crop Physiology & Ecology, Ministry of Agriculture,eijing 100081, China. Tel.: +86 010 62156856, fax: +86 010 62156856.

E-mail addresses: tyunlu@126.com (Y. Tian), chenjin2004777@sina.comJ. Chen), c7450@263.net (C. Chen), dengaixing@163.comA. Deng), songzw@caas.net.cn (Z. Song), qdjmzcy@163.com (C. Zheng),

illem.Hoogmoed@wur.nl (W. Hoogmoed), zhangweij@caas.net.cn,wj@njau.edu.cn (W. Zhang).

378-4290/$ – see front matter © 2012 Elsevier B.V. All rights reserved.ttp://dx.doi.org/10.1016/j.fcr.2012.05.013

© 2012 Elsevier B.V. All rights reserved.

To date, our knowledge on the impacts of climatic changes onwheat remains quite uncertain in China. For example, Xiao et al.(2008) reported that the interaction of warming temperature andchanged rainfall might lead to an increase of 3.1% in wheat yieldsat a low altitude and of 4.0% at a high altitude in China by 2030.With a method of crop-specific panel data analysis, however, Youet al. (2009) found that a 1.0◦C increase in wheat growing seasonmight reduce grain yield by about 3–10%. Similarly, with a mod-eling approach, Chavas et al. (2009) reported that the aggregatepotential productivity of winter wheat might increase 24.9% if withCO2-fertilization effect and might decrease 2.5–12% if without CO2-fertilization effect in East China. Recently, models that link cropyields to weather indicated that China wheat production mightdecline by 5.5% (Lobell et al., 2011). Thus, further evidences fromfield observations are essential to decrease the uncertain in theassessment of warming impacts on wheat production.

Many experiments have been conducted on actual cropresponses to warming (Porter and Gawith, 1999; Ortiz et al.,2008; Aronson and McNulty, 2009). Most of the experiments,however, were performed at a plant or plant community scaleunder controlled conditions, rather than at a crop system scale

in situ (Aronson and McNulty, 2009). Moreover, exiting warmingexperiments mainly focused on low or high temperature stressduring crop key phenophases, only few were performed over anentire growth cycle with anticipated air temperature increase level

194 Y. Tian et al. / Field Crops Research 134 (2012) 193–199

F aily mt ) in th

(fiwtwoiItbfi

2

2

to1stsswTapssp0a

ig. 1. Diurnal air temperature variation in the jointing stage on 2008/3/6 (a) and dhe picture of FATI facility (c) and the variations of soil moisture at 0–20 cm layer (d

Nijs et al., 1996; Kimball and Conley, 2009). Evidences providedrom previous experiments might not fully represent the real-stic impacts of future warming, and further field experiments

ith an entire growth cycle at a crop system scale are essen-ial. Yangtze Delta Plain is one of the major regions of winterheat cropping area in China, and Nanjing city is a typical region

f this plain. We, therefore, conducted a five-year field warm-ng experiment since 2004 with a facility of Free Air Temperaturencrease (FATI) in Nanjing, Jiangsu province. Our objectives wereo investigate the actual responses of winter wheat phenophase,iomass production and grain yield to anticipated warming undereld conditions.

. Materials and methods

.1. Experiment site description

Field experiments were conducted from the winter of 2004 tohe summer of 2009 at the Experimental Station of Jiangsu Academyf Agricultural Sciences, Nanjing, Jiangsu Province, China (32◦02′N,18◦52′E, 11 m above the sea level). The station is situated in theubtropical monsoon climatic zone. The mean annual tempera-ure is 16.7 ◦C, and the annual precipitation is 1050 mm with 1900unshine hours and 237 frost-free days. The approximate time ofunrise in May is around 5:15 am. The precipitation is ample forinter wheat growth in normal years, thus, the field is not irrigated.

he cropping pattern of this winter wheat system has remainedlmost unchanged for over 1000 years. Its climate and croppingatterns are typical in East China. The soil at the experimentalite is a brunisolic silt loam soil (an Alfisols in USA-ST) with sand,

ilt, and clay respectively 0.5, 75.3 and 24.2%. Other relevant soilroperties are: soil organic C 8.2 g kg−1; total N 2.6 g kg−1; total P.6 g kg−1; total K 14.0 g kg−1; available P 166.2 mg kg−1 and avail-ble K 165.0 mg kg−1.

ean air temperature variation during the entire growth cycle (b) of wheat canopy,e growing season of 2008–2009.

2.2. Experimental design

The field warming system was constructed according to thedesign of FATI facility located at the Great Plain Apiaries, USA (Wanet al., 2002). The field experiment used a randomized block designwith three replicates of warmed with all-day time and un-warmedcontrol (Fig. 1). In each warmed plot, a single 180 cm × 20 cminfrared heater (Jiangsu Tiande special light source Co. Ltd., China)was suspended 1.5 m above the ground. In the un-warmed controlplot, a ‘dummy’ heater of the same shape and size was suspended atthe same height to simulate the shading effects of the heater (Fig. 1).Distance to adjacent plots was approximately 5 m to avoid heatingcontamination between treatments. The warming treatment wasstarted on the sowing date and maintained to the harvest date foran entire growth cycle. Although each plot was 6 m × 5 m in size,this FATI facility can only provide about a 2 m × 2 m sampling areawith uniform and reliable warming effects. All samples and fieldmeasurements were done in the 4 m2 area on a plot by plot basis.

2.3. Crop management

The cultivar of Yangmai 11 (Triticum aestivum L. cv Yang-mai 11) tested in this experiment is a major local cultivar withhigh yield potential. Standard agronomic practices commonly per-formed in this area were followed. Seeds were manually sownin November at a density of 225 plants m−2 with a row spaceof 20 cm. Crops were harvested in May or June in the next yearon a plot by plot basis depending on the maturity dates of eachtreatment. The fertilizer applications of N, P and K in each plotwere 225, 75 and 75 kg ha−1, respectively. The total P and K and

50% N were applied as basal dressing two days prior to sowing.The other 50% N was applied as side dressing at early tilleringin the beginning of March. In order to keep the same regimesof agronomic management between the treatments, all fertilizers

Y. Tian et al. / Field Crops Research 134 (2012) 193–199 195

Table 1Temperature differences between the warmed and un-warmed plots and percentages of time deviating from the 1.5 ◦C target increase in Tmean of the warmed plots duringwheat entire growth cycle.

Season Temperature differences (◦C) Percentages of time (%)

Tmax Tmin Tmean AT within ±1 ◦C within 2 ◦C ≥3 ◦C

2006–07 1.4 1.4 1.5 133.9 16.0 1.1 0.12007–08 1.8 1.4 1.7 207.3 9.1 7.2 0.52008–09 1.3 1.2 1.3 158.2 13.1 3.1 0.4Average 1.5 1.3 1.5 166.5 12.4 3.8 0.3

Tmax, Tmin, Tmean and AT mean the daily maximum temperature, minimum temperature, mean temperature and accumulated temperature (>0 ◦C) on wheat canopy, respec-tively. The temperatures were manually measured using thermometer in some key stages during the 2004–2005 and 2005–2006 seasons, the measurement was notc ital tep one wa

wup(3ttt

2

ombwisge

2

smtewHphatfdsoe

2

espgpwpps

ontinuous. Therefore, we just presented the temperature data monitored by a digeriod during the last three years. Since the temperatures were only monitored innalysis was conducted on the temperature data.

ere applied into each plot at the same date according to then-warmed control. Over the five-year experimental duration, therecipitation in the wheat entire growth cycle averaged 364.8 mm2004–2005: 365.4 mm; 2005–2006: 358.6 mm; 2006–2007:45.4 mm; 2007–2008: 396.9 mm; 2008–2009: 354.1 mm). Sincehe precipitation was ample, the fields were not irrigated duringhe experimental duration. There were no water and nitrogen limi-ations for winter wheat growth, which is a common in East China.

.4. Sampling method and measurement

Since wheat in the particular plot reached a particular devel-pment stage due to the warming effects, the sampling dates andeasured variables in this study were all done on a plot by plot

asis according to wheat development of each treatment. Mean-hile, the reliable sampling area of 2 m × 2 m was further divided

nto two equal sup-plots, one for plant sampling and variable mea-urement, and the other for plant population recording and actualrain yield determination almost without disturbance during thentire growth cycle.

.4.1. Temperatures and soil moistureDuring the first two years, air temperature in wheat canopy and

oil temperatures on the field surface and the 0–5 cm soil layer wereeasured manually using thermometer at crop key stages. During

he last three years, the temperatures were monitored automat-dly with an interval of every 20 min in each treatment for thehole growth season by a digital temperature monitor (ZDR241,angzhou Zheda Electronic Instrument Co. Ltd., China). Three tem-erature monitors were positioned in the plot center under theeater or the dummy heater on wheat canopy and field surfacend in the 5 cm soil layer, respectively. Since the monitoring sys-em was expensive, only two plots, one for warmed and the otheror un-warmed, were automatically monitored. Soil moisture wasetermined using the method presented by Bremner (1965). Soilamples were collected from the topsoil (0–20 cm) in wheat rowsf all replicates. Five cores (2.5 cm in diameter) were taken fromach replicate plot, and were mixed to form a composite sample.

.4.2. Plant phenophase, biomass growth and grain yieldThe dates of sowing, anthesis and maturity were recorded for

ach plot in every year. Anthesis date was recorded when 50% ofpikes flowered in a plot and maturity when most of the spikes in alot showed complete loss of green color. At maturity stage, above-round plant samples (15 plants) were taken from each plot. Thelants were separated into leaf plus culm and spike, and the spike

as further separated into vegetative part and grain. All plant sam-les were oven-dried at 80 ◦C for 24 h and weighed. After maturity,lant samples (1 m2 in area) were harvested from each plot to mea-ure the grain yield, in which fifteen spikes samples were taken to

mperature monitor with a time interval of every 20 min for wheat entire growtharmed plot and one un-warmed plot due to the high monitoring cost, no statistic

determine the yield components. The productive spike was definedas spike owing more than five filled grains when harvest.

2.4.3. Leaf area and photosynthetic rateAt the booting stage, 10 and 20 days post-anthesis (DPA), five

flag leaves from main stems were selected in each plot for thedetermination of net photosynthetic rate in the clear morning (at09:00–11:00, about 3–4 h after sunrise) using Li-Cor 6400 Open GasExchange System (Li-COR Inc., USA) in 2008 and 2009 (Turnbullet al., 2002). The average values of the photosynthetic rates of thefive leaves represented the rate for each plot. Fifteen plants fromeach plot were sampled at anthesis stage in 2008 and 2009. Theflag leaf and total green leaf areas were measured using a Li-3000Portable Area Meter (Li-COR Inc., USA). The average values of thefifteen plants were assumed to represent the leaf area of each plot.

2.4.4. Grain filling ratesAt anthesis stage, about 150 spikes were marked for the deter-

mination of the grain filling rate. Five spikes were taken andimmediately put into liquid nitrogen jars on 0, 8, 16, 24, 32 and 40DPA in 2008 and on 0, 7, 14, 21, 28 and 35 DPA in 2009 according towheat anthesis date of each plot. As soon as the jars were broughtin the laboratory on the sampling day, the spikes were stripped tograins and further separated into superior, inferior and the othergrains (Jiang et al., 2003). From the basal five to 12 spikelets onthe spikes, the first and second basal grains on each spikelet weredetached as superior grains whereas the most distal grain on thesame spikelet was detached as inferior grain. All grains were sep-arately oven-dried at 80 ◦C for 24 h to a constant weight for theinvestigation of grain filling rate.

2.5. Statistical analysis

Data were analyzed with Excel 2003 and the statistical packageSPSS 11.5. ANOVA with general linear models was used. Differenceswere considered significant at the level of P < 0.05.

3. Results

3.1. Wheat canopy temperatures and soil moisture

Temperature data presented in this paper were based on theautomatically monitoring in the last three years (Table 1). Forthe entire growth cycle, the daily maximum temperature (Tmax),minimum temperature (Tmin), mean temperature (Tmean) and accu-mulated temperature (AT, >0 ◦C) were 1.5, 1.3, 1.5 and 166.5 ◦Chigher in the warmed plots than those in the un-warmed control on

average across the last three years (Table 1). Although there werea few deviations of daily mean temperatures in the warmed plotsfrom the 1.5 ◦C target increase, the average percentages of timedeviating from the target increase within ±1.0, 2.0 and more than

1 Research 134 (2012) 193–199

3(iwfiipw

3

pwtapp

TttytWfi(n

yvm(eyaa

3

(bAfl

3

findg21c

4

4

gae

t

ph

enop

has

e,

biom

ass

pro

du

ctio

n, g

rain

yiel

d

and

its

com

pon

ents

in

the

war

med

and

un

-war

med

plo

ts

du

rin

g

the

five

year

s.

Trea

tmen

t

Dat

e

(mon

th/d

ay)

Prod

uct

ive

spik

en

o.

(pla

nt m

−2)

Gra

in

nu

mbe

r(g

rain

spik

e−1)

1000

-Gra

in

wei

ght

(g)

Abo

vegr

oun

dbi

omas

s

(g

m−2

)G

rain

yiel

d

(g

m−2

)

Har

vest

ind

ex(%

)

Sow

ing

An

thes

is

Mat

uri

ty

Un

-war

med

2004

Nov

embe

r

06

Ap

ril 1

3

May

27

606.

4

±

57.1

5a

38.8

±

1.72

a

44.8

±

0.20

a

1413

.2

±

176.

9a

606.

0

±

42.8

a

42.9

±

7.68

aW

arm

ed

Ap

ril 0

1

May

16

614.

4

±

45.2

1a

37.4

±

2.23

a

45.6

±

0.50

a

1412

.3

±

132.

6a

707.

8

±

102.

6a

50.1

±

7.52

aU

n-w

arm

ed

2005

Nov

embe

r

10

Ap

ril 1

4

May

28

409.

0

±

2.99

a

40.6

±

0.50

b

35.8

±

0.33

b

1398

.4

±

33.6

a

594.

0

±

5.0b

42.5

±

1.29

aW

arm

ed

Ap

ril 0

8

May

19

381.

3

±

50.0

0a

45.3

±

0.44

a

38.7

±

1.05

a

1500

.4

±

52.3

a

687.

6

±

32.1

a

45.8

±

1.07

aU

n-w

arm

ed

2006

Nov

embe

r

22

Ap

ril 1

5

Jun

e

02

537.

9

±

53.0

3a

35.6

±

2.30

a

48.6

±

0.37

b

1638

.3

±

187.

3a

709.

3

±

54.9

b

43.3

±

2.00

aW

arm

ed

Ap

ril 0

5

May

23

553.

0

± 37

.88a

38.0

±

1.05

a

51.1

±

0.95

a

1820

.7

±

109.

7a

863.

5

±

20.2

a

47.4

±

3.02

aU

n-w

arm

ed

2007

Nov

embe

r

15

Ap

ril 1

4

Jun

e

02

575.

0

± 15

.08a

39.5

±

0.43

a

39.3

±

0.20

b

1689

.7

±

75.5

a

635.

3

±

4.2b

37.6

±

1.53

aW

arm

ed

Ap

ril 0

4

May

21

621.

7 ±

13.6

4a

40.0

±

1.13

a

41.2

±

0.16

a

1814

.1

±

60.5

a

707.

4

±

10.4

a

39.0

±

0.76

aU

n-w

arm

ed

2008

Nov

embe

r

02

Ap

ril 1

0

May

24

583.

3 ±

14.8

1a

39.9

±

0.78

a

43.1

±

0.21

b

1592

.8

±

22.5

a

681.

2

±

21.1

b

42.8

±

1.21

aW

arm

ed

Mar

ch

23

May

14

623.

3

±

33.7

1a

41.2

±

1.51

a

47.7

±

0.04

a

1785

.6

±

54.6

a

785.

6

±

8.9a

44.0

±

1.58

aU

n-w

arm

ed

–

–

–

545.

7a

38.9

a

42.4

b

1546

.4a

645.

2b

41.8

aW

arm

ed

–

–

–

558.

7a

40.4

a

44.9

a

1666

.6a

750.

4a

45.3

a

ean

s

±

1

SE. V

alu

es

foll

owed

by

a

dif

fere

nt

lett

er

are

sign

ifica

ntl

y d

iffe

ren

t

betw

een

trea

tmen

ts

in

each

year

(P

<

0.05

).

96 Y. Tian et al. / Field Crops

.0 ◦C were only 12.4, 3.8 and 0.3% during the entire growth periodTable 1). And the seasonal and diurnal temperature variationsn the warmed plots were closely coupled with those in the un-

armed control (Fig. 1a and b), indicating a good simulation of theeld warming with the local temperature pattern. Although warm-

ng decreased the surface soil (0–20 cm) moisture by an averageercentage of 1.4%, the reduction was not significant as comparedith the un-warmed control (Fig. 1d).

.2. Crop phenophase, aboveground biomass and grain yield

Air temperature elevation significantly advanced wheathenophases (Table 2). The anthesis stage and the maturity stageere advanced by 11 and 10 days, respectively, leading to a reduc-

ion in length of the entire growth period by 10 days on averagecross the five years (Table 2, P < 0.05). The length of pre-anthesishase was shortened by 11 days (P < 0.05), while the post-anthesishase was prolonged slightly by one day.

Warming impacts on winter wheat growth are presented inable 2. The aboveground biomass production was 7.8% higher inhe warmed plot than the un-warmed control on average, thoughhe difference was not significant. Warming increased the grainield by 16.3% significantly (P < 0.05), resulting in an increment inhe harvest index by 8.4% as compared with the un-warmed control.

arming tended to increase the numbers of productive spike andlled grain on average by 13.0 spikes m−2 and 1.5 grains spike−1

Table 2). This warming increased the weight of 1000-grain sig-ificantly by 2.5 g on average.

Significant annual variation in wheat biomass, grain yield andield components was found between the five years (Table 3). Thisariation can be because of the great differences in the annual cli-ate pattern and crop sown date between the experimental years

Tables 1 and 2). However, there were no significant integratedffects on these measured variables between the treatment and theear (Table 3), suggesting that warming impacts on wheat growthre stable regardless of the differences in the annual climate patternnd sown date between the experimental years in the test site.

.3. Leaf area and photosynthetic rate

Warming significantly increased the flag leaf area by 36.0%Fig. 2a, P < 0.05) and the total area of green leaves at anthesis stagey 19.2% (Fig. 2b, P < 0.05) on average across the last two years.lthough warming tended to reduce the net photosynthetic rate ofag leaf, the decreases were not significant (Fig. 2c and d).

.4. Grain filling rate

There were significant differences in the responses of grainlling to warming between the grain types (Fig. 3). Warming sig-ificantly stimulated the filling rates of inferior grains (Fig. 3c and), while there were no significant effects on the rates of superiorrains (Fig. 3a and b). Over the experimental durations of 2008 and009, the average filling rates of inferior grains were respectively4.7 and 9.7% higher in the warmed plots than the un-warmedontrol.

. Discussion

.1. Warming impacts on winter wheat phenophase

It has been well established that warming can shorten croprowth period (Hodges, 1991; Porter and Gawith, 1999; Sadrasnd Monzon, 2006; Wang et al., 2008), however, the shortness ofach phenophase is expected to be different and needs to be further Ta

ble

2W

inte

r

wh

ea

Seas

on

2004

–05

2005

–06

2006

–07

2007

–08

2008

–09

Ave

rage

Val

ues

are

m

Y. Tian et al. / Field Crops Research 134 (2012) 193–199 197

0

10

20

30

40

50

20092008

Fla

g l

eaf

are

a (

cm

2 l

eaf

-1 )

Un-warmed

Warmed

(a)

0

30

60

90

120

150

20092008

To

tal

gre

en l

eav

es a

rea

( c

m 2 s

tem

-1 )

Un-warmed

Warmed

(b)

0

5

10

15

20

25

20 DPA10 DPABooting

2008

Net

ph

oto

syn

thet

ic r

ate

(m

mol

CO

2 m

-2 s

-1)

Un-warmed

Warmed

(c)

0

5

10

15

20

25

20 DPA10 DPABooting

2009

Net

ph

oto

syn

thet

ic r

ate

(m

mo

l C

O2 m

-2 s

-1)

Un-warmedWarmed

(d)

F otosyna

etast

Fd

ig. 2. Winter wheat flag leaf area (a), total green leaves area (b) and the flag leaf phre means ± 1 SE. DPA means the days post-anthesis.

videnced under field conditions. In this five-year field experimen-◦

al study, we found that anticipated warming (less than 1.5 C)

dvanced winter wheat phenophases, consequently resulting in aignificant reduction in wheat entire growth period. And this reduc-ion was mainly found in the length of pre-anthesis phase, on the

0

10

20

30

40

50

60

40 DPA32 DPA24 DPA16 DPA8 DPA0 DPA

Su

per

ior

gra

in w

eig

ht

(mg

gra

in -1

un-warmed

warmed

2008

(a)

0

10

20

30

40

50

60

40 DPA32 DPA24 DPA16 DPA8 DPA0 DPA

Infe

rio

r g

rain

wei

gh

t (

mg

gra

in -1 un-warmed

warmed

2008

(c)

))

ig. 3. Filling dynamics of superior (a and b) and inferior grains (c and d) in the warmedays post-anthesis.

thetic rate (c and d) in the warmed and un-warmed plots in 2008 and 2009. Values

contrary, length of post-anthesis phase was prolonged slightly. In

general, the length of crop pre-anthesis phase is mainly relatedto the accumulated temperature and the minimum temperature,while the length of post-anthesis phase is more related to the max-imum temperature (Hodges, 1991; Porter and Gawith, 1999). On

0

10

20

30

40

50

60

35 DPA28 DPA21 DPA14 DPA7 DPA0 DPA

Su

per

ior

gra

in w

eigh

t (m

g g

rain

-1

un-warmed

warmed

2009

(b)

0

10

20

30

40

50

60

35 DPA28 DPA21 DPA14 DPA7 DPA0 DPA

Infe

rior

gra

in w

eigh

t (m

g g

rain

-1 un-warmed

warmed

2009

(d)

))

and un-warmed plots in 2008 and 2009. Values are means ± 1 SE. DPA means the

198 Y. Tian et al. / Field Crops Resea

Table 3Significance values and freedom degrees of ANOVA analysis (two-way).

Source Year Warming Year × warming Error

df 4 1 4 20Aboveground biomass * ns nsGrain yield * * nsProductive spike number * ns nsGrain number * ns ns1000-grain weight * * nsHarvest index ns ns ns

“

toTaAsmparopw

atfhpnpbactntcwrwfwg

4

hwHcppiarfE

iti

ns” and “*” mean being insignificant and significant at 0.05 level, respectively.

he one hand, the air temperature is relative low, and frost/chillingccurs frequently during winter and spring seasons in East China.he length of wheat growth period, especially the length of pre-nthesis phase, is often prolonged by the low temperature weather.

slight increase of air temperature (less than 1.5 ◦C) can cause con-iderable increases in the accumulated temperature and the dailyinimum temperature. These increases can mitigate the low tem-

erature limitation to wheat plant development and growth anddvance the date reaching to the accumulated temperature valueequired for wheat anthesis. Consequently, a significant advantagef anthesis date and a great reduction in length of pre-anthesishase were found in the five-year field observations caused byarming.

On the other hand, the air temperature often increases quicklyfter wheat anthesis and reaches the heat stress level of 30 ◦C byhe end of May in East China. Thus, winter wheat is often suddenlyorced to early-maturing within a few days due to one or two strongot-dry winds, which can cause quick and serious drought on wheatlant and result in a large reduction in the grain weight. The short-ess of pre-anthesis phase length caused by warming can shift theost-anthesis phase forward into a relatively optimal temperatureackground (around 18–20 ◦C) than the un-warmed control (Slafernd Rawson, 1994, 1995). Although warming of less than 1.5 ◦Could significantly increase the Tmax, Tmin and Tmean compared tohe un-warmed control in this study site, these increments mightot lead to the heat stress level due to the relatively lower tempera-ure background of the warmed plots. Consequently, this warmingan not only mitigate the low temperature limitation but also helpinter wheat to avoid the hot-dry weather stress to grain matu-

ity. Therefore, a slightly prolonged length of post-anthesis phaseas found in this study site. Since most existing studies have been

ocused on the changes of crop entire growth period, our evidencesill help to enhance the understanding of warming impacts on crop

rowth.

.2. Warming impacts on winter wheat yield

Based on crop model and historical data analyses, several reportsave showed that future warming might cause large decrease ininter wheat yield in China (You et al., 2009; Chavas et al., 2009).owever, our observations showed that warming of less than 1.5 ◦Could increase wheat yield significantly. In most winter wheat crop-ing regions in East China, both frost/chilling in the pre-anthesishase and heat stress in the post-anthesis phase occur frequently

n one crop, often causing large decreases in grain yield (Shahnd Paulsen, 2003; Liu and Kang, 2006; Zhong et al., 2008). Ouresults indicate that anticipated warming may reduce both therost/chilling stress and the hot-dry stress to wheat growth inast China.

Firstly, anticipated warming less than 1.5 ◦C can directlyncrease the daily minimum temperature and the accumulatedemperature, so as to be beneficial for spike and terminal spikeletnitiation and growth through lowering the low temperature

rch 134 (2012) 193–199

limitation or even the frost/chilling stress. Evidence of this wasfound in the increases of the numbers of productive spike and filledgrain. Secondly, a moderate increase in air temperature can pro-mote crop leaf development and expansion (Porter and Gawith,1999), which was confirmed by the enlargements of the flag leaf andtotal green leaves areas (Fig. 2). These leaves are the most importantorgans for biomass production and grain filling (Austin et al., 1977;Bonnett and Incoll, 1992; Ntanos and Koutroubas, 2002). Althoughwarming tended to reduce leaf photosynthetic rate (Fig. 2), theenlargement of green leaves areas and prolonged stay-green dura-tion may increase light interception (Latiri-Souki et al., 1998; Liet al., 2008). Since there are no limitations of water and nitrogen inthis site, higher leaf area and light interception can greatly enhancecarbohydrate production and biomass accumulation. Thirdly,warming can advance the anthesis stage to shift the post-anthesisphase forward to a more optimal background temperature for grainfilling (Porter and Gawith, 1999; Lobell, 2007). Since the hot-dryweather often occurs suddenly by the end of May for a few days,a 10-day advantage of anthesis phase caused by warming can helpwheat avoiding the hot-dry stress. Although warming can increasethe temperature conditions, the increments are not high enough toreach to the heat stress level. Thus, the 1000-grain weight and thefilling rate of inferior grain were significantly higher in the warmedplots than the un-warmed control. Finally, warming-led enhance-ment of grain filling can promote dry matter translocation from thevegetative parts to the grain (Porter and Gawith, 1999), leading toa higher harvest index (Table 2). The above evidences can improvethe assessment certainty of warming impacts on wheat productionin China.

5. Conclusions

A common conclusion of many studies on anticipated warm-ing is that warming may cause a dramatic decrease in winterwheat yield as a result of a shorter length of growth period andof a higher heat stress expected in East China. Similar warming-led reduction in the length of wheat growth period was found inthis study, however, field warming of less than 1.5 ◦C increasedwheat grain yield significantly. The yield gains can be mainlyattributed to the mitigation of low temperature limitation duringpre-anthesis phase and to the avoidance of hot-dry stress duringthe post-anthesis phase due to the advantage of anthesis. Warmingcould directly increase the daily minimum temperature to pro-mote wheat plant development and growth, resulting in greaterincrements in green leaf area and productive spike and filled grainnumbers. Although warming resulted in a large reduction in theentire growth period of winter wheat, the main reduction occurredin the length of pre-anthesis phase, while the length of post-anthesis phase was prolonged slightly. Thus, warming can shiftthe post-anthesis phase forward to a more optimal backgroundtemperature situation for grain filling, resulting in higher 1000-grain weight and harvest index. Our results will give importantreferences to warming impact assessment on wheat productionin East China.

Acknowledgements

This work was supported by the National Basic Research Pro-gram of China (2010CB951501), the National Key TechnologySupport Program of China (2011BAD16B14), the Chinese Nature

Science Foundation (30771278) and New Century Excellent TalentsProgram, China (NCET-05-0492). We are grateful to Pro. GregoryVeeck, Western Michigan University, for his constructive sugges-tions and revision on this manuscript.

Resea

R

A

A

B

B

C

HJ

K

L

L

L

L

L

N

Y. Tian et al. / Field Crops

eferences

ronson, E.L., McNulty, S.G., 2009. Appropriate experimental ecosystem warmingmethods by ecosystem, objective, and practicality. Agric. Forest Meteorol. 149,1791–1799.

ustin, R.B., Edrich, J.A., Ford, M.A., Blackwell, R.D., 1977. The fate of the dry matter,carbohydrates and 14C lost from the leaves and stems of wheat during grainfilling. Ann. Bot. 41, 1309–1321.

onnett, G.D., Incoll, L.D., 1992. The potential pre-anthesis and post-anthesis con-tributions of stem internodes to grain yield in crops of winter barley. Ann. Bot.69, 219–225.

remner, J.M., 1965. Total nitrogen. In: Black, C.A. (Ed.), Methods of Soil Analysis,vol. 2. American Society of Agronomy, Madison, pp. 1149–1178.

havas, D.R., Izaurralde, R.C., Thomson, A.M., Gao, X., 2009. Long-term climatechange impacts on agricultural productivity in eastern China. Agric. Forest Mete-orol. 149, 1118–1128.

odges, H., 1991. Predicting Crop Phenology. CRC Press, Boston, USA.iang, D., Cao, W., Dai, T., Jing, Q., 2003. Activities of key enzymes for starch synthesis

in relation to growth of superior and inferior grains on winter wheat (Triticumaestivum L.) spike. Plant Growth Regul. 41, 247–257.

imball, B.A., Conley, M.M., 2009. Infrared heater arrays for warming field plotsscaled up to 5-m diameter. Agric. Forest Meteorol. 149, 721–724.

atiri-Souki, K., Nortcliff, S., Lawlor, D.W., 1998. Nitrogen fertilizer can increase drymatter, grain production and radiation and water use efficiencies for durumwheat under semi-arid conditions. Eur. J. Agron. 9, 21–34.

i, Q., Chen, Y., Liu, M., Zhou, X., Yu, S., Dong, B., 2008. Effects of irrigation and plantingpatterns on radiation use efficiency and yield of winter wheat in North China.Agric. Water Manage. 95, 469–476.

iu, H.J., Kang, Y., 2006. Regulating field microclimate using sprinkler misting underhot-dry windy conditions. Biosyst. Eng. 95, 349–358.

obell, D.B., 2007. Changes in diurnal temperature range and national cereal yields.Agric. Forest Meteorol. 145, 229–238.

obell, D.B., Schlenker, W., Costa-Roberts, J., 2011. Climate trends and global cropproduction since 1980. Science 333, 616–620.

ijs, I., Kockelbergh, F., Teughels, H., Blum, H., Hendrey, G., Impens, I., 1996. Freeair temperature increase (FATI): a new tool to study global warming effects onplants in the field. Plant Cell Environ. 19, 495–502.

rch 134 (2012) 193–199 199

Ntanos, D.A., Koutroubas, S.D., 2002. Dry matter and N accumulation and translo-cation for Indica and Japonica rice under Mediterranean conditions. Field CropRes. 74, 93–101.

Ortiz, R., Sayre, K.D., Govaerts, B., Gupta, R., Subbarao, G.V., Ban, T., Hodson, D., Dixon,J.M., Ortiz-Monasterio, J.I., Reynolds, M., 2008. Climate change: Can wheat beatthe heat? Agric. Ecosyst. Environ. 126, 46–58.

Porter, J.R., Gawith, M., 1999. Temperatures and the growth and development ofwheat: a review. Eur. J. Agron. 10, 23–36.

Sadras, V.O., Monzon, J.P., 2006. Modelled wheat phenology captures rising tem-perature trends: shortened time to flowering and maturity in Australia andArgentina. Field Crop Res. 99, 136–146.

Shah, N.H., Paulsen, G.M., 2003. Interaction of drought and high temperature onphotosynthesis and grain-filling of wheat. Plant Soil 257, 219–226.

Slafer, G.A., Rawson, H.M., 1995. Rates and cardinal temperatures for processes ofdevelopment in wheat: effects of temperature and thermal amplitude. Aust. J.Plant Physiol. 22, 913–926.

Slafer, G.A., Rawson, H.M., 1994. Sensitivity of wheat phasic development to majorenvironmental factors: a re-examination of some assumptions made by physi-ologists and modellers. Aust. J. Plant Physiol. 21, 393–426.

Turnbull, M.H., Murthy, R., Griffin, K.L., 2002. The relative impacts of daytime andnight-time warming on photosynthetic capacity in Populus deltoids. Plant CellEnviron. 25, 1729–1737.

Wan, S., Luo, Y., Wallace, L.L., 2002. Change in microclimate induced by exper-imental warming and clipping in tallgrass prairie. Global Change Biol. 8,754–768.

Wang, H.L., Gan, Y.T., Wang, R.Y., Niu, J.Y., Zhao, H., Yang, Q.G., Li, G.C., 2008. Pheno-logical trends in winter wheat and spring cotton in response to climate changesin northwest China. Agric. Forest Meteorol. 148, 1242–1251.

Xiao, G., Zhang, Q., Yao, Y., Zhao, H., Wang, R., Bai, H., Zhang, F., 2008. Impact ofrecent climatic change on the yield of winter wheat at low and high altitudes insemi-arid northwestern China. Agric. Ecosyst. Environ. 127, 37–42.

You, L., Rosegrant, M.W., Wood, S., Sun, D., 2009. Impact of growing season

temperature on wheat productivity in China. Agric. Forest Meteorol. 149,1009–1014.

Zhong, X., Mei, X., Li, Y., Yoshida, H., Zhao, P., Wang, X., Han, L., Hu, X., Huang, S.,Huang, J., Sun, Z., 2008. Changes in frost resistance of wheat young ears withdevelopment during jointing stage. J. Agron. Crop Sci. 194, 343–349.