全 文 ：Received 28 Jun. 2003 Accepted 29 Sept. 2003
Supported by the State Key Basic Research and Development Plan of China (G2000048704) and the National Natural Science Foundation of
China (90202015).
* Author for correspondence. E-mail: .
http://www.chineseplantscience.com
Acta Botanica Sinica
植 物 学 报 2004, 46 (3): 284-293
Ecophysiological Evidence for the Competition Strategy of Two
Psammophytes Artemisia halodendron and A. frigida
in Horqin Sandy Land, Nei Mongol
ZHOU Hai-Yan1,2, LI Sheng-Gong3, LI Xin-Rong2, ZHAO Ai-Fen4, ZHAO Ha-Lin2, FAN Heng-Wen2, WANG Gang1*
(1. State Key Laboratory of Arid Agro-Ecology of Lanzhou University, Lanzhou 730000, China;
2. Shapotou Station of Desert Experimental Research, Cold and Arid Regions Environmental and Engineering
Research Institute, The Chinese Academy of Sciences, Lanzhou 730000, China;
3. Department of Biology, University of Utah, Salt Lake City, UT84112, USA;
4. Department of Biological Science and Biotechnology, Yantai Normal University, Yantai 264025, China)
Abstract: Gas exchange, water relations and leaf chemical characteristics were examined of two
dominant psammophytes: Artemisia frigida Willd and A. halodendron Turcz. ex Bess in Horqin sandy land, Nei
Mongol, China under different water regimes. The measurements were conducted by submitting the plants
to five different irrigation levels. A. frigida was characterized by lower photosynthetic rate (Pn), lower
transpiration rate (TR) and lower shoot water potential (Yw) relative to A. halodendron. Foliage of A. frigida
had higher values of relative water deficit (RWD), bound water content (BWC), ratio of bound water content
to free water content (BWC/FWC) and integrated drought-resistant index (DI) than that of A. halodendron.
Water relations differed significantly between two species in response to soil water availability. Yw, BWC
and BWC/FWC ratio of A. halodendron exhibited large variation with gradual decrease of soil moisture.
However, in terms of these parameters, A. frigida was characterized by higher capacity of water holding and
drought tolerance relative to A. halodendron. Proline and total soluble sugar contents of A. frigida and A.
halodendron tended to increase with decrease of soil moisture and the former had a larger increase
amplitude than the latter. This shows that A. frigida has a higher osmotic regulation ability than A. halodendron.
Under the extreme drought conditions, Yw, RWD, BWC and BWC/FWC of two species were approximate,
but soluble proteins degraded largely. A large amount of accumulation of organic matter, proline and total
soluble sugars were observed in both A. halodendron and A. frigida. The increase in proline and total soluble
sugar contents and soluble protein degradation of A. frigida far exceeded those of A. halodendron. We
believe that the accumulated materials at this moment are mostly of nutrient substances available for the
recovery of plants after the drought. This is one of the reasons why A. halodendron plants died while A.
frigida plants survived under extremely drought condition. Our results suggest that these ecophysiological
features of A. frigida are favorable to its growth in the fixed sandy land compared with A. halodendron, which
often lost its dominance due to weak competition for water sources under lower soil water availability and
are major factors resulting in replacement of A. halodendron by A. frigida in the later stage of sandy
vegetation succession in Horqin.
Key words: Artemisia frigida ; A. halodendron ; water stress; gas exchange; plant water relations; leaf
chemical characteristic; adaptive strategy
The Horqin sandy land, located in the northeastern part
of China (42°41–45°15 N, 118°35–123°30 E, 180–650 m
above mean sea level), has undergone severe desertifica-
tion over the past several decades due primarily to over-
grazing and over-cultivation (conversion of grassland to
farmland) (Zhu and Wang, 1993). Efforts have been made
since the mid-1970s to recover vegetation on decertified
sandy land through growing indigenous plants adaptive
to sandy land (Li et al., 1994). Artemisia halodendron, a
dominant plant in the semi-fixed sand dune in the area (Li
and Zhang, 1991), was preferentially used for this purpose
because of its easy availability, good adaptability to sand
land, and little labor cost (Li et al., 1994). In the first 4–5 a
after planting, A. halodendron generally grows well and
plays a critical role in stabilizing sandy land against wind-
erosion (Li and Zhang, 1991). However, in the following
years, with further stabilization of the sandy land surface,
A. halodendron is limited with growth and finally will be
replaced by other plants with higher adaptability to drought
such as A. frigida (Li et al., 1997). Both A. halodendron
ZHOU Hai-Yan et al.: Ecophysiological Evidence for the Competition Strategy of Two Psammophytes 285
and A. frigida are regarded as indicator plants, the former
for the semi-fixed sandy land (Li and Zhang, 1991) and the
latter for the degraded grassland ecosystem in Horqin (Li,
1994; Wang et al., 2001). A. frigida communities are rarely
seen in Horqin sandy land except in some protected
grasslands, and are often replaced by A. halodendron com-
munities due to desertification (Zhao and Zhou, 1999). It is
expected that these two plants show characteristically dif-
ferent responses to environmental changes with sandy land
stabilization after re-vegetation. But such information is
not available now (Zhao, 1996). In present study, we exam-
ined ecophysiological features of these two plants under
controlled soil moisture conditions. We hypothesize that
water would be the dominant factor limiting growth of A.
halodendron after desertified sand land is fixed or stabi-
lized and meanwhile the stabilization creates favorable soil
conditions for recruitment of A. frigida. We also hypoth-
esize that A. frigida would have advantages over A.
halodendron for growth under water-limited conditions.
Therefore, characterization of responses of these two spe-
cies to different water regimes is the major topic of the
present study.
1 Materials and Methods
1.1 Study site and plant materials
The experiment was conducted at the Naiman Station of
Desertification Research, The Chinese Academy of Sciences
(42°58 N, 120°43 E, 350 m above mean sea level), in Naiman,
Nei Mongol, China. Naiman is located at the southwest
end of the Horqin sandy land and belongs to the continen-
tal semi-arid monsoon climate in the temperate zone, with
windy and dry winters and springs, and warm and com-
paratively rain-rich summers followed by short and cool
falls. According to the statistics (1961–2000) of the Naiman
Weather Station, the annual mean air temperature is about
6.8 ℃; the annual mean precipitation is 366 mm with strong
seasonal variability (Chang et al., 2000). Although around
90% of the total annual precipitation falls in the growing
season from April through September, frequent drought is
the limiting factor for growth of sandy land vegetation (Li,
1996). The annual mean pan-evaporation is 1 935 mm. The
annual frost-free period is 150 d. The zonal soils are charac-
terized by sandy substrate with light yellow color, coarse
texture and loose structure. The original vegetation is grass-
land (dominant species include Stipa grandis, Leymus
chinensis, and Agropyron cristatum) with sparsely scat-
tered woods (mainly Ulmus pumila). The sandy land veg-
etation is generally dominated by psammophytes includ-
ing some shrubs (e.g. Caragana microphyla, Salix
gordejevii), semi-shrubs (e.g. Artemisia halodendron, A.
frigida), forbs (e.g. Agriophyllum squarrosum, A. scoparia),
and grasses (e.g. Aristida adscensionis, Calamagrostis
pseudophragmites, Digitaria ciliaris, Leymus chinensis,
L. secalinus, Pennisetum centrasiaticum) (Li, 1996; Li et
al., 2002).
A. halodendron is a broadleaf deciduous shrub (semi-
shrub), about 50-100 cm tall, with extensive root system. It
grows well and dominates the semi-fixed and shifting sand
dunes in Horqin sandy land. In general, it degenerates when
sand dunes were entirely fixed or stabilized (Li and Zhang,
1991). A. frigida is widely distributed deciduous scrub with
extensive root system. It has small hairs on the leaves and
stems reducing its water loss from leaves by deflecting the
wind and insulating leave’s surfaces. It can grow 10-40 cm
tall. It also shows strong tolerance to drought and is one of
the dominant species on the fixed sand dunes of Horqin
sandy land. This plant generally increases under long-term
overgrazing (Zhao, 1996).
Growth and development conditions for A. frigida and
A. halodendron under soil water treatments are shown in
Table 1.
1.2 Water treatments
Seedlings of healthy A. frigida and A. halodendron were
taken directly from field in early summer (28 April 1998) for
the water stress experiment. They were transplanted imme-
diately in the pots (45 cm in depth ´ 35 cm in diameter) filled
with field sand soil. One seedling was planted in each pot.
The pots were placed in an experimental field at the Naiman
Station of Desertification Research and separated into five
groups (each group had six pots) for watering treatments.
The weight of each plot was measured before and after the
transplantation. To determine amount of irrigation water
and the time interval of irrigation, a blank pot test was made:
at first the pot was watered to the field capacity of water
holding (about 30% in volume) and then the weight of the
pot was measured. The pot weight was measured for sev-
eral times as soil volumetric water content (qv) decreased
to 20%, 10%, and 4%, respectively.
After the plants in the pots recovered to their normal
growth status, the following treatments were made from
June to July (Fig.1): A, well-watered with irrigation approach-
ing the field capacity of water holding (qv ~ 30%); B, no
water limiting (control), qv corresponded to 70% of the field
water holding capacity (qv ~20%); C, slightly water-stressed
(qv ~10%); D, no irrigation (qv < 4%); and E, no irrigation in
the first 18 d (qv < 4%), and then irrigated to qv reaching
about 20%. One month after the treatments, various physi-
ological parameters aforementioned were measured.
Acta Botanica Sinica 植物学报 Vol.46 No.3 2004286
1.3 Soil water content and gas exchange measurements
qv was monitored in each pot using Time Domain Re-
flectometry (TDR) sensors following the procedure of Wan
et al. (1993) with a TDR cable tester (Tektrooix 1502,
Tektronix, Beaverton, OR, USA). Stainless steel rods were
vertically installed to depths of 10, 20, and 30 cm in irrigated
plots.
In the peak growth period (June, July and August 1998),
a portable photosynthesis systems (Li-6200, Li-Cor Inc.,
Lincoln, Ne, USA) was used to measure leaf photosyn-
thetic characteristics of A. frigida and A. halodendron grow-
ing in the field, about 1 km away from the Naiman Station of
Desertification Research. Generally, sunlit, fully expanded
healthy leaves on the upper part of each species were used
for photosynthetic measurements (five replications) on a
clear day when their diurnal courses (600-1 800) were
monitored, leaves were enclosed in the cuvette with mini-
mal disturbance to their orientation. The Li-6200 was cali-
brated with the standard gases before measurements and
allowed the measurement of air temperatures (Ta), leaf tem-
perature (Tl), air relative humidity (RH) and photosynthetic
photon flux density (PPFD). It outputs net photosynthe-
sis (Pn), transpiration rate (TR) and stomatal conductance
(gs).
1.4 Water relations and leaf chemical characteristics
Water potential (Yw) from fully expanded current year
shoots was measured with a pressure chamber (Model ZLZ-
5, Lanzhou University, Lanzhou, China). Relative water
deficit (RWD), bound water content (BWC) and free water
content (FWC) under fully turgor conditions were derived
from the Pressure-Volume (PV) curves measured (Tyree et
al., 1972) with the ZLZ-5 pressure chamber and a balance
with the precision of 0.01 mg (Model AP 250, Precision
Weighing Balances, Bradford, MA, USA). The integrated
drought-resistant index (DI) was calculated using the
method described by Li et al. (1992) and Wang et al. (2002):
DI= ∑ ( )2 (1)
where DI is an integrative representation of Yp o (Yp when
i =1
Pi
Po
n
Table 1 Growth and development conditions for Artemisia frigida and A. halodendron under soil water treatments
Species Treatment
Tree height Canopy size Shoot length
Leaf feature Development condition
(cm) (cm2) (cm)
A. frigida A 22.1 21× 17 3.5 Normal Flowering and bearing fruit
B 34.2 30× 22 10.4 Normal Flowering and bearing fruit
C 29.1 25× 22 7.1 Normal Flowering and bearing fruit
D 19.4 15× 15 2.1 Wilting, yellowing or No flowering and bearing
shedding off，new leaves fruit
sprout in the next year
E 20.7 19× 18 2.2 Partly restored to Flowering and bearing fruit
normal condition
A. halodendron A 62.3 33× 30 9.4 Normal Flowering and bearing fruit
B 92.3 60× 47 15.0 Normal Flowering and bearing fruit
C 87.4 60× 24 12.3 Normal Flowering and bearing fruit
D 53.9 24× 24 7.9 Wilting, yellowing or No flowering and bearing
sheding off，died in fruit
the next year
E 62.7 35× 27 3.1 Partly restored to Flowering and bearing fruit
normal condition
Values shown are mean ± SE where n = 6. A, soil volumetric water content (qv) about 30%; B, qv about 20%; C, qv about 10%; D, qv was
less than 4%; and E, no irrigation in the first 18 d, and then irrigated to the qv reaching about 20%.
Fig.1. Soil water content from the plots used in the present
study (July 1998). A, soil volumetric water content (qv) about
30%; B, qv about 20%; C, qv about 10%; D, qv was less than 4%;
and E, no irrigation in the first 18 day, and then irrigated to the qv
reaching about 20%. One month after the treatments, various
physiological parameters were measured.
ZHOU Hai-Yan et al.: Ecophysiological Evidence for the Competition Strategy of Two Psammophytes 287
pressure potential (Yp) = 0);Yp100 (Yp100 when plant water
is saturated), BWC, BWCtlp (BWC when Yp = 0) and RWCtlp
(RWC when Yp = 0). Subscript i in equation (1) represents
above parameters. For Yp o、Yp100 and BWC, pi repre-
sents their observed values, and po represents their maxi-
mal values. For BWCtlp and RWCtlp, Pi = 1 – Pob, and Po=1-
Pmin, where Pob represents observed value, Pmin represent
the minimum observed value.
Determination of leaf chemical properties before the
sample collection, soil particles were removed from the leaf
samples. For each treatment, 30-50 leaves growing in mid-
canopy and fully expanded were collected on sunny days
in August 1998, from the same five plants, mixed together
and dried in oven at 50 ℃ or frozen in liquid nitrogen (N)
immediately after being separated into portions of 0.5 g
fresh weight (FW) for each sample, then taken to the labo-
ratory for relevant experiments.
Total soluble sugar content was determined colorimetri-
cally using aphenol-sulphuric acid assay technique (Dubois
et al., 1956). Nitrate N content of leaves was determined
according to Ye et al. (1979). Soluble protein content of
leaves was determined by the Bradford’s method (1976).
Nitrate reductase activity (NRA) was determined accord-
ingly to Radin (1973). Proline content was determined ac-
cording to Bates et al. (1973). Permeability (µS/cm) of cyto-
plasmic membrane was measured with a conductivity meter
(Cole-Parmer 19820, Cole-Parmer Inc., Vernon Hills, IL, USA).
Dry weight (DW) of leaf organic matter was determined
with the burning method in the Muffle furnace (Zhu et al.,
1990).
1.5 Statistical analysis
Analysis of the relationships between the gas exchange
characteristics and water relations was performed using
linear regression. The significance of the differences among
the five watering treatments and between two species was
analyzed by means of the standard two-way ANOVA with
significant level P = 0.05. Data points are the averages of
3-12 replicates and differences between the means were
analyzed by the Tuckey’s least significant differences test.
2 Results
2.1 Diurnal patterns of gas exchange and environmental
variables
Here, the gas exchange determined on 4 August 1998
was presented only because the changing patterns of gas
exchange and environmental variables measured on the
different dates were highly similar (Fig.2). qv was 6.3% dur-
ing the measurement period (TDR, depths 10, 20, 40, 60, 80
and 100 cm). Leaf-to-air vapor pressure deficit (VPD)
varied between 40 and 50 Pa KPa between 10:00 and 16:00
(Fig.2a). PPFD reached about 1 200 mmol.m-2.s-1 at around
600 h and varied between 1 950 and 2 050 mmol.m-2.s-1
between 10:00 and 16:00 (Fig.2b). The highest Tl was 40 ℃
for A. halodendron and 37 ℃ for A. frigida, respectively
(Fig. 2c).
Pn and TR were usually higher in the early morning and
in the late afternoon, varied little during the remainder of
the daytime (Fig.2d, e). The maximal Pn value was 17.4 mmol.
m-2.s-1 for A. halodendron (06:00) and 6.2 mmol.m-2.s-1
for A. frigida (18:00), respectively. Except for the early morn-
ing and late afternoon, Pn (1.07 mmol.m-2.s-1) of A.
Halodendron was similar in magnitude to that of A. frigida
(1.01 mmol.m-2.s-1) (P = 0.961). A. frigida and A.
halodendron displayed a similar pattern for diurnal varia-
tion of gs (Fig.2f). The gs was higher both in the early
morning and in the late afternoon, and varied little during
the rest of the day.
2.2 Plant water relations
The diurnal patterns of Yw differed significantly be-
tween these two species (Fig.2g). Yw of A. frigida was
significantly lower than that of A. halodendron through-
out the day (P < 0.001) (Table 2). The shoot water potential
(Yw) of A. frigida in various growing periods (June, July
and August) was usually lower than that of A. halodendron
(Table 2). Yw values of these two shrubs have different
responses to soil water availability (Table 3). Yw in A.
frigida was significantly greater in well-watered soil condi-
tions (treatment A) and decreased rapidly in treatment B.
No significant difference was found among the treatments
C, D (a.m.) and E for A. frigida. It seemed that extreme water
stress (treatment D) considerably decreased Yw in A.
haoldendron (Table 3). Irrigation after strong water-stressed
(treatment E) significantly increased Yw in A. haoldendron.
Therefore, A. frigida and A. haoldendron displayed quite
different responses to dry environmental conditions. Ex-
cept in the treatments A and D (p.m.), when no significant
differences in Yw were found between A. frigida and A.
haoldendron, A. frigida usually had significantly lower Yw
values than A. haoldendron (Table 3).
A. frigida exhibited higher BWC and higher BWC/FWC
ratio in various growing periods (Table 2). DI (Li et al.,
1992) was significantly higher for A. frigida than A.
halodendron (Table 2). Under the treatments A, B, C and E,
RWD, BWC and BWD/FWC in A. frigida were significantly
higher than those of A. halodendron (Table 3). After the
strong water-limited treatment (treatment E), irrigation made
the above three parameters return to their pre-treatment
levels (Table 3). Under extremely drought conditions
Acta Botanica Sinica 植物学报 Vol.46 No.3 2004288
Fig.2. Diurnal course of leaf-to-air vapour pressure deficit (VPD) (a); photosynthetic photon flux density (PPFD) at the leaf level (b);
leaf temperature (Tl) (c); net photosynthesis (Pn) (d); transpiration rate (TR) (e); stomatal conductance (gs) (f); shoot water potential
(Yw) (g) for Artemisia frigida and A. halodendron. Data expressed as mean ± SE; n = 3-6 leaves; each leaf from a different individual.
Measurements were made on 4 August 1998.
Table 2 Seasonal variations in shoot water potential (Yw), water relative deficit (RWD), bound water content (BWC), bound water to
free water ratio (BWC/FWC), and drought resistance index (DI) for Artemisia frigida and A. halodendron
Species Month Yw (MPa) RWD (%) BWC (%) BWC/FWC DI
A. frigida June -1.40 ± 0.02 Aa 12.2 ± 0.3Aa 29.0 ± 0.5Aa 1.73 ± 0.09Aa
July -1.85 ± 0.04 Ba 22.9 ± 0.6Ba 58.5 ± 0.6Ba 3.15 ± 0.33Ba 1.773a
August -1.75 ± 0.04Ca 17.7 ± 0.4Ca 50.0 ± 0.5Ca 1.55 ± 0.07Aa
A. halodendron June -0.91 ± 0.02 Ab 6.4 ± 0.3Ab 30.0 ± 0.5Aa 0.47 ± 0.05Ab
July -1.23 ± 0.03 Bb 18.2 ± 0.5Bb 10.0 ± 0.1Bb 0.14 ± 0.02 Bb 1.082b
August -1.30 ± 0.03Cb 12.3 ± 0.4Cb 37.0 ± 0.4Cb 0.73 ± 0.07 Cb
Values shown are mean ± SE where n = 6. Different upper- and lowercase letters indicate significant differences between the different seasons
of the same specie (P < 0.05) and different species of the same season (P < 0.05), respectively
(treatment D, a.m.), RWD of A. halodendron increased
rapidly, indicating loss of large amount of free water and
correspondingly a large increase in BWC, when A. frigida
and A. halodendron had similar values of RWD and BWC.
Both plants showed a large increase in RWD and a consid-
erable decrease in BWC in the mid afternoon (p.m.) relative
to the morning (a.m.) in the treatment D. Measurements of
conductivity for leaf cell membrane also indicates that these
two plants displayed substantially high membrane conduc-
tivity in the extremely water-limited conditions, e.g., the
ZHOU Hai-Yan et al.: Ecophysiological Evidence for the Competition Strategy of Two Psammophytes 289
membrane conductivity was 24.2 (25.1) µS/cm in the treat-
ment D (14:00) and 18.7 (9.3) µS/cm in the treatment D (14:00
h) for A. halodendron (A. frigida), respectively.
2.3 Leaf chemical characteristics
Chemical component of leaves differed significantly
between two species and in response to soil water
availability. Under the conditions of different soil moisture
contents, A. frigida had higher dry organic matter in leaves
than A. halodendron (Fig.3a). Dry organic matter of A.
frigida and A. halodendron increased rapidly in the treat-
ment D.
Regardless of the treatments, A. halodendron usually
displayed higher soluble protein concentration in leaves
than A. frigida (Fig.3b). A. frigida and A. halodendron pre-
sented reduction of soluble protein under the treatment D.
The amplitude of soluble protein concentration reduction
was particularly higher for A. frigida (62.3%) than for A.
halodendron (38.2%) (P < 0.001) (Fig.3b).
In the treatments A, B and C, the nitrate N content and
nitrate reductase activity (NRA) of A. frigida were hsigher
than those of A. halodendron （Fig.3c, d）. However, in
the treatment C both the nitrate N content and NRA of A.
frigida reached a noticeable peak values and in the treat-
ment D they reduced largely. In the treatment C, the nitrate
N content of A. halodendron increased but its NRA showed
no significant difference among different treatments.
The proline contents of A. frigida and A. halodendron
tended to increase with decreasing soil water content but
A. frigida had a larger increase amplitude than A.
halodendron (Fig.3e). In various treatments the proline con-
tent of A. frigida was higher than that of A. halodendron.
Under extreme drought condition, proline concentration in
A. frigida increased substantially, and reached as large as
7.1 mg/g, or 8.7 times the value of A. halodendron.
The total soluble sugar contents of A. frigical and A.
halodendron increased with the decrease in soil moisture
content and the former showed a higher increase amplitude
than the latter (Fig.3f). In the treatments A, B, C and E,
soluble sugar concentration of A. halodendron was usu-
ally higher than that of A. frigida. Under extreme water-
stress conditions, the soluble sugar concentration increased
by 1.3 times for A. frigida, and was significantly higher
than that for A. halodendron.
3 Discussion
Stomatal response is a primary mechanism for short-
term adjustment of carbon gain and water loss (Schulze,
1986). Increased stomatal closure, may reduce the ratio of
transpiration to water uptake from the soil, temporarily im-
proving plant water content, delaying the onset of the de-
hydration phase and therefore increasing survival. Stomatal
closure also results in a more efficient loss of water per
carbon (C) assimilated (Farquhar et al., 1988). There was a
strong linear relationship between CO2 exchange and tran-
spiration rates for A. frigida (Fig.4). Thus, the regulation of
stomatal opening of A. frigida in response to the large
changes in leaf-to-air VPD resulted in almost constant wa-
ter use efficiency (WUE) throughout the day and increas-
ing survival.
Regardless of growth seasons, time of the day, and un-
der no or slight water-limiting conditions, water potential
of A. halodendron was significantly higher than that of A.
frigida. For these two species, linear relations existed be-
tween Yw and gs (or Pn) (Fig.5). The relationship between
Table 3 Shoot water potential (Yw), water relative deficit (RWD), bound water content (BWC), and bound water to free water ratio
(BWC/FWC) for Artemisia frigida and A. halodendron under soil water treatments
Species Treatment
Yw (MPa) RWD (%) BWC (%) BWC/FWC
08:00 14:00 08:00 14:00 08:00 14:00 08:00 14:00
(h) (h) (h) (h)
A. frigida A -1.10 ± 0.02Aa 26.3 ± 1.4Aa 53.2 ± 1.4Aa 1.59 ± 0. 09Aa
B -1.43 ± 0.04Ba 32.4 ± 1.3Ba 38.2 ± 1.9Ba 1.30 ± 0.07Ba
C -1.43 ± 0.05Ba 32.0 ± 1.5Ba 42.5 ± 1.8Ca 1.67 ± 0.10 Aa
D -1.50 ± 0.05Ba -1.75 ± 0.05Ca 32.7 ± 1.5 Ba 45.3 ± 2.5Ca 47.3 ± 2.0Da 25.0 ± 1.9Ea 2.37 ± 0. 18Ca 0.84 ± 0.07Da
E -1.45 ± 0.03Ba 31.3 ± 1.3 Ba 37.2 ± 1.7Ba 1.18 ± 0.11Ba
A. halodendron A -0.95 ± 0.03Ab 8.7 ± 0.6ABb 40.2 ± 2.1Ab 0.79 ± 0.08Ab
B -0.73 ± 0.02Bb 10.0 ± 0.7Ab 23.0 ± 1.5Bb 0.34 ± 0.09Bb
C -0.95 ± 0.03Ab 25.6 ± 1.1Cb 33.5 ±1.8Cb 0.81 ± 0.11Ab
D -1.30 ± 0.03Cb -1.80 ± 0.05Da 35.0 ±1.5Da 43.0 ± 2.1Da 49.7 ± 2.4Da 28.0 ±1.9Ba 3.25 ± 0.23 Cb 0.97 ± 0.11Aa
E -1.05 ± 0.02 Ab 8.2 ± 0.6Bb 26.1 ± 1.7Bb 0.40 ± 0.09Bb
Values shown are mean ± SE where n = 6. Different upper-and lowercase letters indicate significant differences between the different soil water
content treatments of the same specie (P < 0.05) and different species of the same soil water content treatments (P < 0.05), respectively. A,
soil volumetric water content (qv) about 30%; B, qv about 20%; C, qv about 10%; D, qv was less than 4%; and E, no irrigation in the first 18
d, and then irrigated to the qv reaching about 20%
Acta Botanica Sinica 植物学报 Vol.46 No.3 2004290
Fig.3. Variation in dry organic matter concentration (a); soluble
protein concentration (b); nitrate nitrogen concentration (c); ni-
trate reductase activity (NRA) (d); proline concentration (e);
soluble sugar concentration (f) in leaves of Artemisia frigida and
A. halodendron under various soil water content treatments. Data
expressed as mean ± SE; n = 3; Different upper-and lowercase
letters indicate significant differences between the different soil
water content treatments of the same species (P < 0.05) and
different species of the same soil water content treatments (P <
0.05), respectively. A, soil volumetric water content (qv) about
30%; B, qv about 20%; C, qv about 10%; D, qv was less than 4%;
and E, no irrigation in the first 18 d, and then irrigated to the qv
reaching about 20%.
Fig.4. The relationship between net photosynthesis (Pn) and
transpiration (TR) for Artemisia frigida and A. halodendron. Data
from the diurnal courses described in Fig. 2. n = 84.
Fig.5. Stomatal conductance (gs) and net photosynthesis (Pn) as
affected by water potential (Yw) for Artemisia frigida and A.
halodendron. Data from the diurnal courses described in Fig.2. n
= 84.
Yw and gs (or Pn), was stronger in A. frigida (r2 = 0.73, 0.28)
than in A. halodendron (r2 = 0.66, 0.18). The slope in the
relationship between Yw and gs (or between Yw and Pn)
was significantly steeper in A. frigida than in A.
haoldendron.
The BWC and BWC/FWC ratio are often used as drought-
resistant indices of plants growing in water-stressed
ZHOU Hai-Yan et al.: Ecophysiological Evidence for the Competition Strategy of Two Psammophytes 291
conditions. During the peak growth period and under no or
slight water-limiting conditions, BWC and BWC/FWC ratio
in A. frigida were significantly higher than that of A.
halodendron, suggesting that tissues of A. frigida have
higher water-holding capacity than those of A.
halodendron. Yw , RWD, BWC and BWC/FWC ratio of two
species exhibited quite different responses to soil water
variations, A. halodendron presented higher amplitude of
variation in these parameters than A. frigida, suggesting
that water in plant tissues of A. halodendron is sensitive to
environmental conditions while A. frigida is more adaptive
to dry habitat. Above characters, coupling with high DI,
enable A. frigida to have larger competitive capacity than
A. halodendron under water stress condition.
A. frigida has the higher capacity of dry organic matter
production than A. halodendron under different soil water
conditions. The amplitude of soluble protein degradation
was particularly higher for A. frigida than for A.
halodendron under extremely drought condition. Higher
protein degradation is more favorable to proline accumula-
tion in plants under extremely drought condition. Water
stress can give rise to hydroxylation of protein and accu-
mulation of amino acid, enhance conversion of glutamine
into proline and proline compounds by restricting oxidiza-
tion and synthesis of the latter into protein (Blackman, 1991).
Under slight water stress conditions, A. frigida has higher
nitrate absorbability than A. halodendron and thereby fa-
voring protein synthesis. However, under extreme water
stress conditions, decrease of nitrate N content and NRA
in A. frigida is favorable to the degradation of protein.
Proline is an important osmoticum in higher plants. The
benefit of the accumulation of proline has been proposed
as a compatible osmotic solute（Handa et al., 1986), as a
protein-stabilizing or solubilizing factor under limited cell
water conditions (Blackman, 1992) and as a source of re-
duced N and C (Xie et al., 1997). Large accumulation of
proline can not only regulate osmotic potential of cells, but
be stored as non noxious materials being useful for the
growth under low water potential conditions (Liu, 1992).
Soluble sugars play an important role in osmotic regulation
of cells. Water stress may result in increase of soluble
sugars, which can be used for osmotic regulation to main-
tain turgor potential of cells and thus usually are thought
to be drought-resistant materials (Chen et al., 1990). In
addition, an increase in soluble sugars is one of important
survival strategies for temperate desert plants under sus-
tained water stress conditions (Shibata, 1993). Our mea-
sured results showed that the osmotic regulation abilities
of A. frigida and A. halodendron tended to increase with
the decrease in soil moisture content and the former had a
higher osmotic regulation ability than the latter.
The present study also showed that under extreme
drought condition (q v < 4% for a long time ) Yw , RWD and
BWC of A. frigida and A. halodendron had an approximate
final values. In such a case, the leaves of A. halodendron
became permanently withered, while A. frigida continuously
produced new shoots. In the next spring of this experiment
A. frigida grew well but A. halodendron entirely died. This
indicated that under the prolonged extremely drought
condition, the physiological functions of A. halodendron
were damaged seriously or even lost the ability of recovery,
while A. frigida suffered less serious disturbance in their
physiological processes and they could accumulate large
amount of organic materials such as proline, soluble sugar
and other nutrient substances, which are of vital impor-
tance to the energy storage and growth after drought. Our
field observations showed that in the normal rainfall years
both A. frigida and A. halodendron grew well but in the
dry years with sparse rainfall A. frigida exhibited a high
drought resistance and survival rate, while A. halodendron
gradually declined.
Investigation on microenvironmental changes after re-
vegetation on desertified sandy land indicates that with
stabilization of the sandy land and increase of vegetation
cover, the habitat become drier, unfavorable to the growth
of A. halodendron but favorable to invasion of more
drought-resistant plants (Li et al., 2002). In conclusion, the
examination on physiological characteristics, including gas
exchange, plant water relations, and leaf chemical charac-
teristics of A. frigida and A. haoldendron shows that our
hypotheses at the beginning of this paper are correct, i.e.,
water is the dominant factor limiting growth of A.
halodendron after sand dunes are fixed or stabilized;
meanwhile, due to its higher resistance capacity to water-
stress, A. frigida has advantages over A. halodendron for
growth under water-limited conditions and hence replaces
A. halodendron in dominance in late vegetation succes-
sion in Horqin sandy land.
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(Managing editor: HAN Ya-Qin)