Trees (2005) 19: 711–720

DOI 10.1007/s00468-005-0435-2

ORIGINAL ARTICLE

Chun-Wang Xiao · Osbert J. Sun ·

Guang-Sheng Zhou · Jing-Zhu Zhao · Gang Wu

Interactive effects of elevated CO2 and drought stress on leaf water

potential and growth in Caragana intermedia

Received: 3 November 2004 / Accepted: 7 April 2005 / Published online: 5 May 2005


C Springer-Verlag 2005

Abstract We studied the responses of leaf water poten- Introduction

tial (
w ), morphology, biomass accumulation and alloca-
tion, and canopy productivity index (CPI) to the combined Atmospheric carbon dioxide concentration has been
effects of elevated CO2 and drought stress in Caragana predicted to double its current level before the end of
intermedia seedlings. Seedlings were grown at two CO2 this century as a result of human activities (Bazzaz 1990;
concentrations (350 and 700 µmol mol−1 ) interacted with Watson et al. 1990; Keeling et al. 1995; Morison and Lawlor
three water regimes (60–70%, 45–55%, and 30–40% of 1999; Houghton et al. 2001). A doubling of the atmospheric
field capacity of soil). Elevated CO2 significantly increased CO2 and rises in other greenhouse gases, such as methane,

w , decreased specific leaf area (SLA) and leaf area ratio nitrous oxide, and CFCs, could increase the average
(LAR) of drought-stressed seedlings, and increased tree global temperature by 1.4–5.8◦ C and change precipitation
height, basal diameter, shoot biomass, root biomass as well patterns in the next 100 years (Houghton et al. 2001).
as total biomass under the all the three water regimes. Global warming and altered precipitation patterns due to
Growth responses to elevated CO2 were greater in well- increases in atmospheric CO2 concentrations are of major
watered seedlings than in drought-stressed seedlings. CPI international concerns for both policy-makers and scientific
was significantly increased by elevated CO2 , and the in- communities (Ottman et al. 2001). Further, the elevated
crease in CPI became stronger as the level of drought stress CO2 may bring about increased aridity in some areas of the
increased. There were significant interactions between el- planet (Gregory et al. 1997; Houghton et al. 2001). There-
evated CO2 and drought stress on leaf water potential, fore, it is of great importance to elucidate the effects of
basal diameter, leaf area, and biomass accumulation. Our elevated CO2 in conjunction with drought stress on plants.
results suggest that elevated CO2 may enhance drought In the past decades, the effects of elevated CO2 on
avoidance and improved water relations, thus weakening plants have been documented in numerous papers and
the effect of drought stress on growth of C. intermedia review articles, and the consensus of most of these reports
seedings. is that elevated CO2 increases plant growth (Ceulemans
and Mousseau 1994; Poorter et al. 1996; Drake and
Keywords Biomass allocation . Canopy production Gonzalez-Meler 1997; Jach and Ceulemans 1999; Norby
index . Morphology . Specific leaf area . Caragana et al. 2001; Calfapietra et al. 2003; Janssens et al.
intermedia 2005). However, only relatively few investigations have
considered the direct consequences of soil water deficits
imposed on plants that are exposed to elevated CO2
atmospheres (Serraj et al. 1999). In studies concerned with
C.-W. Xiao (
) · O. J. Sun · G.-S. Zhou the interactive effects of elevated CO2 and water stress,
Laboratory of Quantitative Vegetation Ecology, Institute of some found that elevated CO2 significantly increased plant
Botany, The Chinese Academy of Sciences, growth (Kimball et al. 1995; Centritto et al. 1999; Serraj
Beijing 100093, P.R. China et al. 1999; Ottman et al. 2001; Wall et al. 2001), possibly
e-mail: cwxiao@ibcas.ac.cn
Tel.: +86-10-62836289 because plants growing in elevated CO2 improved water
Fax: +86-10-82595962 relations under drought stress and were able to withstand
the drought stress better (Grant et al. 1999; Wall 2001;
J.-Z. Zhao · G. Wu Wall et al. 2001; Wullschleger et al. 2002). However, there
Department of Systems Ecology, Research Center For
Eco-Environmental Sciences, The Chinese Academy of were also studies finding no positive effects of elevated
Sciences, CO2 on plant growth under drought-stressed conditions
Beijing 100085, P.R. China (Mo et al. 1992; Ward et al. 1999; Derner et al. 2003).
712

Maowusu sandland is located in the middle of the north- Experimental design

ern China with a semi-arid climate (37◦ 30 –39◦ 20 N;
107◦ 20 –113◦ 30 E). Caragana intermedia Kuanget H.C. The experiment consisted of two CO2 concentrations
Fu is a dominant desert shrub of the region, occurring interacting with three levels of watering regimes. On
mainly in the semi-fixed and fixed dunes of Maowusu sand- 2 June 2001, seedlings of similar size were transferred into
land. The plant is used by local people as feed for livestock, two identical greenhouse compartments (6 m×3 m×3 m):
and as shelter for protection of soils against desertifica- one with elevated CO2 that doubled the current level
tion (Zhang 1994). At present, desertification, coupled with (700±10 µmol mol−1 for day and night), and another with
rapid soil erosion, is becoming a critical issue in Maowusu ambient CO2 (350±5 µmol mol−1 for day and night). Pure
sandland. As water is often a limiting resource for plant re- CO2 was supplied from storage tanks with vaporization
cruitment, growth, physiology, nutrient dynamics, and net facilities. A slight airflow was maintained with fans that
ecosystem productivity in the semi-arid area (Zhang 1994; provided an outgoing air stream in each compartment. The
Danin 1996), most of the previous researches on desert concentrations of CO2 inside the chambers were contin-
plants in Maowusu sandland have been mainly concerned uously monitored with infrared gas analyzer (Fuji ZSB,
with drought stress tolerance (Xiao and Zhou 2001; Xiao Japan) and controlled by a computer.
et al. 2002). However, with the perception of decreasing Each CO2 treatment contained 60 seedlings randomly di-
precipitation with the global climate change scenarios in vided into groups of 20 and subjected to three soil water
much of the semi-arid regions (Fu and An 2002), the in- regimes. Pots in both compartments were placed on racks
teractive effects between elevated CO2 and drought stress to ensure proper drainage and to avoid interference from
may be more detrimental to changes in vegetation than the groundwater. The pots were spaced 20 cm apart in all di-
effect of either elevated CO2 or drought stress alone. rections to minimize competition for light, and rows were
In order to determine if exposure to elevated CO2 would oriented in a north-south direction.
allow desert plants to better withstand drought stress, we The three water regimes were 60–70%, 45–55%, and
investigated the effects of elevated CO2 on leaf water po- 30–40% of soil water content soil at field capacity, simu-
tential, morphology, biomass accumulation and allocation, lating well-watered (WW), moderate-watered (MW), and
and canopy productivity index of C. intermedia with vary- drought-stressed (DS) conditions. The soil water contents
ing soil moisture. Our study was carried out in the context were determined by weighing the pots daily and calculated
of scientifically predicting the changes of dominant plant based on the pot weight, soil dry weight, and the expected
community and effectively preventing desertification in soil water holding capacity. Water was added following at
Maowusu sandland as part of ecosystem restoration project the time of weighing to maintain the predetermined water
of arid and semi-arid lands of north-western China (Zhang content in each pot. Additionally, in the last stage of the
et al. 2000). experiment, the wet weight per seedling was estimated and
added to the pot weight.
The photosynthetic photon flux density (PPFD) in both
Materials and methods compartments was measured with a LCA-4 portable photo-
synthesis system (ADC, Hoddesdon, UK) at the start of the
Plant species and growth conditions experiment, and was not found to differ between the two
compartments. Due to light interception by the greenhouse
Caragana intermedia Kuanget H.C. Fu belongs to the fam- covers, PPFD inside the compartments was reduced to ap-
ily of Fabaceae, and is a deciduous shrub that occurs in proximately 90% of the level outside. No artificial light
Inner Mongolia, Ninxia, and Shanxi in China. The shrub is was used in the experiment. Temperature and relatively hu-
typically about 0.7–3.0 m tall and has odd, plumose, com- midity in both compartments were recorded continuously
pound leaves. It is one of the dominant shrubs that fix soil with WHM3 thermo-hygrograph (Tianjin, China), and were
and reduce wind speed, thus actively mitigating desertifi- found to be similar between the two compartments. There-
cation in Maowusu sandland. fore, the climatic conditions in both compartments were
Seeds of C. intermedia were collected from a single tree at assumed to be identical.
Maowusu sandland (39◦ 29.66 N and 110◦ 11.47 E, altitude
1295 m) in 2000. In April 2001, seeds were germinated
in sand and seedlings were transplanted individually into Measurements of leaf water potential
black plastic pots (10 cm in diameter and 10 cm in height)
filled with sand. The volume of the pot was sufficient to Leaf water potential (
w ) was determined with a mod-
avoid pot-binding effects. The pots remained in the open ified HR-33T dewpoint microvoltmeter (Wescor, Logan,
field under natural environmental conditions until the start UT, USA). Three uppermost fully expanded sunlit leaves
of the experiment. A slow releasing fertilizer (14% N, 14% within each treatment were collected for
w measure-
P,14% K) was added to the sand at the rate of 1 g per pot ment at 2-h intervals from 7:00 to 17:00 on 7 September
in end May. 2001.
 713

Fig. 1 Diurnal change of leaf −2.0

water potential (
w ) for C.
intermedia seedlings exposed to
ambient and elevated CO2 (350
and 700 µmol mol−1 ) under −2.1
well-watered (WW), b
ab
moderate-watered (MW), and ab b b
ab b
drought-stressed (DS) −2.2 ab ab ab
a c
conditions on 7 September a c c d c
bc

ψw (Mpa)
2001. Boxes represent treatment b b cd c bc bc
means − standard error. −2.3 a bc
b b b
Treatments with different letters b b b
b a
are significantly different
a
(P<0.05) according to
post-ANOVA Duncan’s test −2.4 a

350, WW 350, MW 350, DS

−2.5
700, WW 700, MW 700, DS

−2.6
7:00 9:00 11:00 13:00 15:00 17:00
Time of day (h)

Growth measurements water potential, and with two-way ANOVA, using CO2
concentrations and water regimes as main effects for growth
At the end of the experiment (17 September 2001), basal characteristics. Interactions among the effects were also
diameter, height, and number of leaves ≥ 5 mm in length analyzed. All statistical tests were considered significant at
were measured on each seedling. Twelve seedlings of each P≤0.05 and Duncan’s post-ANOVA pairwise analysis was
treatment were randomly chosen and used for measure- used to determine significant differences between means.
ments of leaf area and dry mass. Leaf area was measured
with an automatic leaf area meter (Hayashi-Denkoh
AAM-8, Tokyo, Japan). Leaves, shoots, and roots were Results
separated and dried at 85◦ C for 48 h and weighed. Leaf
area ratio (LAR: leaf area to total biomass, cm2 g−1 ), root Leaf water potential
mass ratio (RMR: root biomass to total biomass, g g−1 ),
root:shoot ratio (RSR: total root biomass to total stem and The diurnal patterns of
w were similar among the treat-
branches biomass, g g−1 ), and specific leaf area (SLA: leaf ments:
w was highest in morning, and decreased until
area to leaf biomass, cm2 g−1 ) were calculated according reaching its minimum at midday, and then increased in the
to Beadle (1993). Also, canopy productivity index (CPI: afternoon (Fig. 1). The
w varied significantly with time
total growth per unit leaf area, g cm−2 ) was estimated (P<0.001; Table 1). Seedlings exposed to elevated CO2
according to Sigurdsson et al. (2001). had less negative
w under all three water regimes, espe-
cially at midday, but significant effects were only observed
under drought-stressed conditions (Fig. 1). Drought de-
Statistical analysis creased
w significantly in both ambient CO2 and elevated
CO2 (Fig. 1). There was a significant interaction between
Data management and statistical analyses were performed sample time and water, and between CO2 and water in the
using SPSS software (SPSS, Chicago, IL). The data were effect on
w (P<0.01; Table 1), but not between sample
analyzed with three-way ANOVA, using sample times, CO2 time and CO2 , and sample time, CO2 , and water on
w
concentrations, and water regimes as main effects for leaf (P>0.05; Table 1).

Table 1 F-values of three-way ANOVA for leaf water potential water regimes of well-watered, moderate-watered, and drought stress
(
w ) of C. intermedia seedlings measured at six sample times (time), conditions (water)
two CO2 concentrations of 350 and 700 µmol mol−1 (CO2 ), and three
Source Time CO2 Water Time × CO2 Time × Water CO2 × Water Time × CO2 × Water
df 5, 72 1, 72 2, 72 5, 72 10, 72 2, 72 10, 72

w 139.1*** 50.1*** 107.5*** 1.6NS 2.6** 6.9** 0.2NS
Significance level: NS: not significant P>0.05. *P<0.05, **P<0.01, ***P<0.001
714

Fig. 2 Tree height, basal 50

diameter, number of leaves, leaf WW MW DS
area, and specific leaf area a
40
(SLA) of C. intermedia

Tree height (cm)

b
seedlings exposed to ambient bc
and elevated CO2 (350 and 30 c c
700 µmol mol−1 ) under d
well-watered (WW), 20
moderate-watered (MW), and
drought-stressed (DS) 10
conditions. Boxes represent
treatment means + standard
error. Treatments with different 0
letters are significantly different
(P<0.05) according to 3
post-ANOVA Duncan’s test
a

Basal diameter (mm)

b
bc
2 c c
d

60
a
Number of leaves

40 b
b
bc bc
c
20

80
a
Leaf area (cm2)

60
b
b
40 b
c
c
20

250
a a a a a
200 b
SLA (cm2 g-1)

150

100

50

0
350 700
CO2 concentration ( µmol mol-1)
 715

Morphology CO2 , there was no significant effect of drought stress on

CPI (Fig. 5). There was no significant interaction between
Elevated CO2 significantly increased the seedling height CO2 and water on CPI (P>0.05; Table 2).
and basal diameter under the three water regimes (Fig. 2).
Elevated CO2 only increased number of leaves and leaf
area under the well-watered condition and decreased SLA Discussion
under the drought-stressed condition (Fig. 2). Drought
significantly decreased the seedling height, basal diameter, In this study, we found that elevated CO2 led to lower inter-
number of leaves, and leaf area at both ambient and nal water deficits as the soil-water content became depleted,
elevated CO2, but only deceased SLA at elevated CO2 indicating improved plant water relations at elevated CO2 .
(Fig. 2). There was a significant interaction between CO2 This finding is consistent with other studies examining the
and water in the effect on basal diameter and leaf area interaction between elevated CO2 and water stress in the
(P<0.05; Table 2), but not for tree height, number of effect on plant water relations (e.g. Wall et al. 2001). Our
leaves, and SLA (P>0.05; Table 2). finding of increased
w by elevated CO2 under varying wa-
ter regimes is consistent with results for many other species
Biomass accumulation (Sionit et al. 1980; Bhattacharya et al. 1990; Kirkham et al.
1991; Prior et al. 1991; Wall et al. 2001). Moreover, a sig-
Elevated CO2 significantly increased shoot biomass, root nificant interaction between elevated CO2 and drought in
biomass, and total biomass under the three water regimes, the effect on
w was observed in our study. Our results in-
but increased the leaf biomass significantly only under the dicate that elevated CO2 would enhance drought avoidance
well-watered condition (Fig. 3). Elevated CO2 increased and improve water relations for C. intermedia seedings in
total biomass by 79% under the well-watered condition, future climate. Improved water relations would alleviate
by 61% under moderate-watered condition, and by 53% the deleterious effects of water stress on physiological pro-
under drought-stressed condition. Drought significantly cess, such as photosynthesis, and enhance growth during
decreased the leaf biomass, shoot biomass, root biomass, a drought (Hsiao and Jing 1987; Nelson and MacAdam
and total biomass at both ambient and elevated CO2 1989).
(Fig. 3). There was a significant interaction between CO2 Idso (1988) suggested that elevated CO2 would have
and water in the effect on leaf biomass, shoot biomass, and more beneficial effects on plants experiencing non-lethal
total biomass (P<0.05, P<0.01, and P<0.01, respectively; drought conditions than when they were well watered.
Table 2), but not on root biomass (P>0.05; Table 2). In the present study, elevated CO2 significantly increased
shoot biomass, root biomass, and total biomass under
three different water regimes, and total biomass responses
Biomass allocation to elevated CO2 were greater in well-watered plants
than under drought stress. This finding contradicts the
Elevated CO2 only significantly decreased the LAR under work of Idso (1988). In our study there was a significant
the drought-stressed condition (Fig. 4). Drought decreased interaction between elevated CO2 and drought stress in
LAR at elevated CO2 , and significantly increased RMR the effect on seedling height, basal diameter, number of
and RSR at both ambient and elevated CO2 (Fig. 4). There leaves, leaf area, and biomass of the plant tissues. These
were no significant interactions between CO2 and water on are in agreement with several similar studies (Townend
LAR, RMR, and RSR (P>0.05; Table 2). 1993, 1995; Guehl et al. 1994; Tschaplinski et al. 1995).
However, some studies with crop plants demonstrated
Canopy productivity index that growth responses to elevated CO2 were greater in
drought-stressed plants than in well-watered plants (Sionit
CPI was significantly increased by elevated CO2 (P<0.01; et al. 1980; Morison and Gifford 1984; Marks and Strain
Table 2; Fig. 5). The CO2 -induced increase in CPI became 1989; Clifford et al. 1993; Kimball et al. 1995; Pinter
stronger as drought stress increased (Fig. 5). At the ambient et al. 1996; Clark et al. 1999; De Luis et al. 1999).

Table 2 F-values of two-way ANOVA for tree height, basal di- productivity index (CPI) of C. intermedia seedlings measured at two
ameter, number of leaves, leaf area, specific leaf area (SLA), leaf CO2 concentrations of 350 and 700 µmol mol−1 (CO2 ) and three wa-
biomass, shoot biomass, root biomass, total biomass, leaf area ratio ter regimes of well-watered, moderate-watered, and drought-stressed
(LAR), root mass ratio (RMR), root:shoot ratio (RSR), and canopy conditions (water)
Source df Tree Basal Number Leaf SLA Leaf Shoot Root Total LAR RMR RSR CPI
height diameter of leaves area biomass biomass biomass biomass
CO2 1, 66 30.1*** 35.5*** 13.1*** 11.8*** 0.4NS 15.6*** 56.5*** 57.6*** 62.0*** 13.2*** 1.4NS 0.5NS 9.5**
Water 2, 66 27.4*** 33.7*** 19.7*** 31.8*** 1.6NS 37.5*** 40.1*** 20.3*** 45.2*** 1.7NS 9.2*** 6.6** 4.2*
CO2 × 2, 66 1.2NS 3.2* 0.9NS 3.4* 1.0NS 3.6* 5.4** 2.9NS 5.0** 1.5NS 0.8NS 0.01NS 2.3NS
Water
Significance level: NS: not significant P>0.05, *P<0.05, **P<0.01, ***P<0.001
716

Fig. 3 Leaf biomass, shoot 0.4

biomass, root biomass, and the
total biomass of C. intermedia WW MW DS
seedlings exposed to ambient a
0.3

Leaf biomass (g)

and elevated CO2 (350 and
700 µmol mol−1 ) under
well-watered (WW), b b
moderate-watered (MW), and b
0.2
drought-stressed (DS)
conditions. Boxes represent c
treatment means + standard c
error. Treatments with different 0.1
letters are significantly different
(P<0.05) according to
post-ANOVA Duncan’s test 0

0.4

a
Shoot biomass (g) 0.3

b
0.2 c
c c
0.1 d

0.4
a a
0.3
Root biomass (g)

0.2 b b b
c
0.1

1.2

a
0.9
Total biomass (g)

b
0.6 c c
c

0.3 d

0
350 700
CO2 concentration (µmol mol-1)
 717

Fig. 4 Leaf area ratio (LAR), 120

root mass ratio (RMR), and
root:shoot ratio (RSR) of C. WW MW DS
intermedia seedlings exposed to a
ambient and elevated CO2 (350 a a

LAR (cm2 g-1)

80 a
and 700 µmol mol−1 ) under ab
well-watered (WW), b
moderate-watered (MW), and
drought-stressed (DS)
conditions. Boxes represent 40
treatment means + standard
error. Treatments with different
letters are significantly different
(P<0.05) according to post 0
ANOVA Duncan’s test
0.6
a
ab
bc ab
c bc
RMR (g g-1)
0.4

0.2

a
ab bc ab
RSR (g g-1)

2
bc c
1

0
350 700
CO2 concentration ( µmol mol-1)

Fig. 5 Canopy productivity 0.03

index (CPI) of C. intermedia
seedlings exposed to ambient WW MW DS a
and elevated CO2 (350 and
700 µmol mol−1 ) under
well-watered (WW),
CPI (g cm-2)

moderate-watered (MW), and 0.02 b b

b b
drought-stressed (DS) b
conditions. Boxes represent
treatment means + standard
error. Treatments with different
letters are significantly different 0.01
(P<0.05) according to post
ANOVA Duncan’s test

0.00
350 700
CO2 concentration ( µmol mol-1)
718

Drought adapted tissue generally has lower SLA because Acknowledgements The work was financially supported by the
of xeromorphic features such as thicker cuticles, mesophyll, Knowledge Innovation Project of the Chinese Academy of Sci-
and epidermal cells, or higher trichome density (Hsiao and ences (KZCX1-SW-01-12) and the Project was sponsored by SRF for
ROCS, SEM. The authors are very grateful to Prof. Xin-Shi Zhang,
Acevedo 1974; Turner and Kramer 1980; Kramer 1983; Prof. Lian-Min Wang, and Dr. Zhen-Zhu Xu for their constructive
Fernández et al. 2002; Marron et al. 2003; Zhang et al. comments and help with the research.
2004). No significant drought effects were observed in
SLA at ambient CO2 in this study. This may be because
C. intermedia is a desert plant species and preadapted to References
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