全 文 ：Received 9 Jan. 2004 Accepted 22 May 2004
Supported by the Knowledge Innovation Program of The Chinese Academy of Sciences (KSCXI-08-02).
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Acta Botanica Sinica
植 物 学 报 2004, 46 (10): 1170-1177
Differential Responses to Simulated Precipitation Exhibited by a Typical
Shrub and a Herb Coexisted in Hunshandak Sandy Land
NIU Shu-Li, PENG Yu, JIANG Gao-Ming*, LI Yong-Geng, GAO Lei-Ming,
LIU Mei-Zhen, CUI Hong-Xia, DING Li
(Laboratory of Quantitative Vegetation Ecology, Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, China)
Abstract: To assess the ecophysiological responses and adaptive strategies to rainfall exhibited by
different plant functional types, we compared gas exchange, leaf water potential (Yleaf) and PSⅡ photo-
chemical efficiency (Fv/Fm) between Hedysarum fruticosum Pall. (shrub) and Salsola collina Y. L. Chang
(herb) under a series of simulated rainfalls. The experiment was conducted in Hunshandak Sandy Land,
North China. The values of net photosynthetic rate (Pn), transpiration rate (E), stomatal conductance (gs),
Fv/Fm and Yleaf always elevated with the increasing amount of simulated rainfall. Whereas water use
efficiency (WUE) maintained constant in H. fruticosum while always decreased in S. collina. Both species
fully recovered their Pn and Fv/Fm 3 d after rainfall, while gs and Yleaf recovered only within 2 d. However,
the response patterns were obviously different. H. fruticosu promote its physiological traits within 5-15
mm rainfall but no further positive enhancement was noted when rainfall was larger than 15 mm. In S.
collina, however, the enhancement continued with more water applied. We inferred that H. fruticosum and
S. collina responded similarly to rainfall in time courses but differential to simulated precipitation change.
S. collina was likely to be physiologically sensitive to instant increasing soil water, that can be regarded as
a prodigal water use type; whilst H. fruticosum was a conservative water user.
Key words: gas exchange; leaf water potential (Yleaf); Hedysarum fruticosum ; Salsola collina ;
Hunshandak Sandy Land
Precipitation is one of the major factors determining net
primary production (NPP) in arid and semiarid zones (Noy-
Meir, 1973; Boyer, 1982; Nobel, 1997). For plants growing
under limited water conditions, an efficient water use has
been proposed either through increasing biomass produc-
tion (Clifton-Brown and Lewandowski, 2000) or supporting
drought tolerance (Sobrado, 2000). However, species with
different plant functional types (PFTS) differ dramatically
both in water use efficiency (WUE), the ability in resisting
drought (McCarron and Knapp, 2001; McDowell, 2002),
and relieving from drought threatening (Williams, 2000).
Similarly, it has been suggested that different water use
strategies by plants allows the coexistence of different PFTs
in habitats where water shortage is predominate (Brown et
al., 1997; Sala et al., 1997). For example, grasses utilizing
short-term water availability have their roots occurring in
upper soil layers, while shrubs rely on a deeper soil water
resource that is more stable in the long term (Burgess, 1995;
Schwinning et al., 2002). This can be realized as the way of
water resource niche separation. The drought response
patterns and their recovery times after re-watering might be
dissimilar between shrubs and grasses coexisted together.
However, there are still few reports about the physiological
mechanisms for the coexistence of different species with
differential adaptive strategies in arid or semi-arid areas.
The focus of this study, therefore, was to characterize
the differential responses of species with different PFTs in
responding to the instantaneous rainfall that often hap-
pens in semi-arid area. Our hypothesis is that shrubs and
grasses vary spatially and temporally in their response pat-
terns to the amount of rainfall. Such a pattern is specifically
useful in understanding the ecophysiological significance
for the coexistence of shrubs and grasses.
1 Materials and Methods
1.1 Study area
Measurements were taken in the Hunshandak Sandy
Land Ecosystem Research Station of The Chinese Acad-
emy of Sciences, that is located (42º23 N, 112º23 E) in the
middle of Xilingel League of Inner Mongolia (Nei Mongol)
Autonomous Region of China. The woody species compo-
sition at the site is dominated by Ulmus pumila var.
sabulosa L., Salix gordejevii Y. L. Chang, Hedysarum
fruticosum Pall. While for herbs, Corispermum
NIU Shu-Li et al.: Differential Responses to Simulated Precipitation Exhibited by a Typical Shrub and a Herb Coexisted in
Hunshandak Sandy Land 1171
heptapotamicum Iljin, Salsola collina Pall., Leymus
chinensis Tzvel., and Agriophyllum squarrosum L. are
common. Such ecosystem is most sensitive to precipita-
tion that leads to a series of ecological problems. For
example, in summer if precipitation is less than 250 mm,
decrease in NPP is frequently reported (Bai et al., 2001).
Besides, overgrazing leads to further degradation of the
grasslands. Hunshandak is now recognized as one of the
seriously degraded sandlands in China (Jiang, 2002).
The prevailing climate is of cold-temperate arid and semi-
arid type. The average annual temperature is about 1.7 ℃,
with the monthly maximum (July) and minimum (January)
being 16.6 ℃ and -24.1 ℃, respectively. The accumulative
temperature (>10 ℃) varies from 2 000 ℃ to 2 600 ℃. The
frostless period is approximately 100 d. This area receives
annual precipitation about 250-350 mm, fluctuate yearly
from 150 mm to 400 mm. For certain months, the maximum
monthly precipitation (30 mm/month) was observed from
June to August and the minimum one (1 mm/month) from
March to May. The annual potential evaporation, however,
is 2 000-2 700 mm, about 10 folds of the annual precipitation.
1.2 Plants materials
Hedysarum fruticosum Pall. is a sub-shrub distributing
in the stabilized or semi-stabilized sand dune in Hunshandak
Sandy Land. It is about 1.5-2.0 m in height, with odd plu-
mose compound leaves and maximum rooting depth of 4.
6-6.0 m. It adapts to dry habitat well and easily germinate
(Chen, 1986). Its seedling grows faster in the first year of
development and spreading stem reaches to 18 cm. However,
Salsola collina Pall. is an annual xeromorphic herb which
has a root system of about 30 cm in depth. It belongs to a
fibrous root system with thin branch roots (Chen, 1986). Its
stems spread as much as or more horizontally than vertically.
The leaves are alternate, 2-5 cm long and fleshy. The
growth period for both species is from mid-May to late
September.
1.3 Experimental design
In the early summer of 2002, 36 circular plots (F 100 cm)
were put either on H. fruticosum or S. collina plants pro-
tected by an aluminous frame (50 cm× 50 cm× 50 cm,
length× width× depth). Each plot was centered by a
single plant and contained no other plants except the tar-
get species. The treated individuals had the similar height
and width, being kept at least 100 cm apart from each plot.
All treatments were assigned randomly with three replicates.
Six rainfall treatments, i.e. 0 mm (control plant), 5 mm, 10
mm, 15 mm, 20 mm and 25 mm rainfall were applied to each
species. The total experimented plants for each species had
18 individuals. To avoid artificial effect, on 15 July, water
was supplied for all individuals with a handheld sprinkler
as uniformly and slowly as possible. The soil water status
before watering was moderate drought. The days follow-
ing the simulated precipitations were all sunny with tem-
perature changing from 26 ℃ to 37 ℃ during mid-day time.
1.4 Gas exchange measurement
Gas exchange, fluorescence, leaf and soil water poten-
tial were measured prior to rainfall, 1, 2, 3 and 4 d after
rainfall, respectively. Net photosynthetic rate (Pn), transpi-
ration rate (E), stomatal conductance (gs) and internal CO2
concentration (Ci) were measured using a LCA-4 Portable
Photosynthetic System (ADC, Hoddesdon, England). All
the measurements started from 9:00 am when photosyn-
thetic photon flux density (PPFD) was above light satu-
rated point and stopped at 11:00 am (to avoid high radia-
tion stress) on clear days of July 15-19, 2002. Conditions
for measurements were: ambient CO2 concentration (Ca)
350 mmol/mol, vapour pressure deficit (2.0 ± 0.4) kPa, leaf
temperature (35.00 ± 0.26) ℃ and photon flux density (2 100 ±
42) mmol.m-2.s-1. WUE was calculated as Pn/E. Leaf areas
for calculating gas exchange variables were measured by
an Area Meter (AM100, ADC, Hoddesdon, England). Dur-
ing operation, air was collected from 6 m above the floor
and dried (by passing through “drier”) to 20% relative hu-
midity before being pumped into the analyzer. The full-
expanded functional leaves in upper shoots were selected
for the gas exchange measurement. Three replications, each
from a separate plant, were done.
1.5 Chlorophyll fluorescence
Chlorophyll fluorescence was measured using a por-
table plant efficiency analyzer (PEA, Hansatech, King’s
Lynn, UK). Fo (minimal fluorescence), Fm (maximal
fluorescence), Fv (variable fluorescence) and Fv/Fm
(maximal photochemical efficiency of PSⅡ) were measured
shortly after keeping the leaf for 30 min in the dark. A red
irradiance of 2 000 mmol.m -2. s -1 was used for
measurements. The fully-expanded leaves near those for
gas exchange measurement were sampled to measure. Three
replicates were done.
1.6 Leaf water potential (Y leaf)
The Y leaf was measured with a WP4 Dewpoint Potential
Meter (Decagon Devices, Inc., Pullman Washington, USA),
from fully expanded leaves with few twigs that were sampled
from around the top parts of the plants. The details of Y leaf
measurement are available in another report (Liu et al., 2003).
1.7 Soil water contents (SWCs)
SWCs were measured 2 d after watering when water
was infiltrate into the deep soil and each soil layer kept
steady water condition. It was investigated with a Delta-T
Acta Botanica Sinica 植物学报 Vol.46 No.10 20041172
Device Moisture Meter (Profile Probe, Type PR1/6, USA).
Four probes were buried around one of the each target
plant in four separate directions. Measurement was taken
at 20 cm depth intervals, beginning from 0 cm to 80 cm of
the soil layer.
1.8 Data analysis
Analyses of variance (ANOVA) of treatment as main
factors were conducted to reveal the impact of amount of
precipitation on physiological characteristics. Analysis of
variance of leaf traits was made on each measurement and
the significance of plant mean square determined by test-
ing against the error (species× replicate) mean square.
The least significant differences (LSD) between the means
were estimated at 95% confidence level. All the statistical
analyses were performed using the SPSS 10.0 package
(SPSS 10.0 Inc., Chicago, USA).
2 Results
2.1 Changes in SWC
Simulated precipitation increased SWC of each layer of
the soils where the target plants distributed. For example,
compared with the control plant (0 mm “rainfall” was
applied), SWC of soils at the layer of 20, 40, 60 and 80 cm,
where the target plants received 25 mm “rainfall”, were re-
spectively 5, 5, 3 and 3 folds of those without rainfall
treatment. Vertically, SWC elevated in the soil from 20 to 60
cm depth at any water amount treatment, but kept steady
when the soil layer was deeper than 60 cm (Fig.1).
2.2 Time courses of recovery
All the ecophysiological variables were elevated after
rewatering. However, the fully recovery times (reach the
maximal values of characteristics) were remarkably different.
The maximum gs and Yleaf occurred 2 d after rainfall while
Pn and Fv/Fm recovered 3 d after rainfall (Fig.2). After the
ultimate recovery, all variables remained at a plateau status
with the longer time. On the contrary, the controlled plant
encountered a further depression in photosynthesis dur-
ing experimental times. As for the whole time course’s
response, S. collina had a similar trend with that of H.
fruticosum.
2.3 Ecophysiological changes along rainfall treatments
Ecophysiological variables showed different response
patterns to the water treatment at 3 d after rainfall when the
two species reached constant status. Pn of H. fruticosum
was enhanced by 16%-64% from 5 to 15 mm rainfall treat-
ments and then kept constant when the simulated precipi-
tation exceeded 15 mm. While in S. collina, Pn was always
increased (P<0.05) (Fig.3A). E, gs, Fv/Fm, Yleaf and WUE
changed similarly as the way of Pn in both species, i.e. the
ecophysiological traits of H. fruticosum were found to be
saturated under 15 mm rainfall treatment, while those of S.
collina could not saturate during the water treatment (Fig.
3). Compared with H. fruticosum, S. collina had signifi-
cantly higher E, Yleaf and lower Pn at any water treatments.
It was worthily noted that the responses of WUE in
both species differed from the above-mentioned ecophysi-
ological traits. H. fruticosum had a constant higher WUE at
any water treatment, while S. collina always decreased the
value with the increasing of simulated precipitation (Fig.
3F).
2.4 Photosynthetic limitations by stomata
The best fit of the net photosynthesis, transpiration
rate and intercellular CO2 concentration versus stomatal
conductance (Fig.4) displayed a positive linear relation-
ship in both species, indicating strong dependence of the
assimilation rate on stomatal aperture. At the same sto-
matal opening, H. fruticosum had significantly higher as-
similation rate but relatively lower E compared with S.
collina, which also reflected the higher WUE in H.
fruticosum.
3 Discussion
Although there have been a number of researches fo-
cusing on the responses of plant growth to water gradient
in arid and semi-arid habitats (Ehleringer, 1991; Alder et al.,
1996; Schwinning et al., 2002), a series of ecophysiological
responses during their water stress and drought relief have
been seldom reported. In this study, we chose two species
with different functional types to seek their particular strat-
egies to environmental stress from ecophysiological point
Fig.1. Changes of soil water content (SWC) in 20 cm, 40 cm,
60 cm and 100 cm layers below soil surface among different
amount of simulated rainfall in Hunshandak Sandland. Error
bars are ± SE.
NIU Shu-Li et al.: Differential Responses to Simulated Precipitation Exhibited by a Typical Shrub and a Herb Coexisted in
Hunshandak Sandy Land 1173
Fig.2. Changes in net photosynthesis rate (Pn), stomatal conductance (gs), leaf water potential (Yleaf) and photochemical efficiency
(Fv/Fm) with the development of drought relief in Hedysarum fruticosum, a shrub species (A-D) and Salsola collina, a herb (E-H). Error
bars are ± SE.
of view, H. fruticosum (a typical shrub) and S. collina (a
herb) widely distributed in the semi-arid areas of
Hunshandak Sandland, North China. Both species received
the same amount of water through simulated precipitation.
Along the created water gradient, both H. fruticosum and
S. collina showed significant increases of gs, E and Pn
Acta Botanica Sinica 植物学报 Vol.46 No.10 20041174
(Fig.3). Such patterns suggest stomata controlled gas ex-
change is triggered by variations of soil water, which is
commonly found in arid environments (Prior et al., 1997;
Medrano et al., 2002). The strategy that stomata respond-
ing to soil water availability should be superior to a non-
responsive behavior, because it minimizes the probability
of complete soil dying which might cause death of plants
(Cowan, 1982; Abril and Hanano, 1998). The exhibition of
Pn, E and Ci to gs (Fig.4) demonstrates that it might be
strong stomatal regulation for both H. fruticosum and S.
collina. The ability to regulate stomatal conductance may
determine species persistence on a changing environment.
Strong stomatal regulation abilities in both H. fruticosum
and S.collina express their high adaptation ability to
drought.
The gs had an effect on CO2 diffusion into the leaf
mesophyll, as we found in H. fruticosum and S.collina (Figs.
2, 3). However, the results do not necessarily imply that gs
is the primary factor regulating Pn. The fully recovery of gs
and Pn after rewatering was not synchronous. Pn recov-
ered to the maximum value 3 d after rewatering while gs and
Ci 2 d after water supplying (Fig.2). Therefore, we
Fig.3. Net photosynthesis rate (Pn) (A), transpiration rate (E) (B), stomatal conductance (gs)(C), photochemical efficiency (Fv/Fm) (D),
leaf water potential (Yleaf) (E) and water use efficiency (WUE) (F) of Hedysarum fruticosum and Salsola collina in response to the
different simulated rainfall. Error bars are ± SE
NIU Shu-Li et al.: Differential Responses to Simulated Precipitation Exhibited by a Typical Shrub and a Herb Coexisted in
Hunshandak Sandy Land 1175
suggested that the non-stomatal factors also limited pho-
tosynthesis under drought status in our experiments. The
lag recovery of Pn and Fv/Fm took place at the same time,
implying photochemical and carboxylation efficiency were
depressed also during drought and lasted longer time than
gs (Flexas et al., 2001; Parry et al., 2002). So, the depression
and recovery of Pn might be explained by both stomatal
and non-stomatal dependence.
The two species with different PFTs exhibited differen-
tial response patterns to simulated precipitation. Photo-
synthesis of S. collina responded sensitively to variance
of water irrigation, non-saturation in Pn being recorded even
“rainfall” was up to 25 mm (Fig.3A). Lower WUE was also
noted in it (Fig.3F). Such response pattern reflected the
opportunistic growth of S. collina in resilienting its assimi-
lation ability after the environmental changes. It is a well-
known adaptive response to water deficit, which was also
observed in a Mediterranean native Lupinus albus
(Rodrigues et al., 1995). Although both Pn and E in S. collina
increased with gs, E changed more relative to Pn (Fig.4A,
B), leading to decreased WUE (Fig.3F). On the contrary, H.
fruticosum might be considered as a species with conser-
vative water use strategy. Although small amount of rain-
fall could satisfy its need for photosynthesis (Fig.3A), it
did not open stoma further for the sake of stopping water
losses from transpiration (Fig.3B). The rebundant rainfall
might be conserved in deeper soils for potentially extend-
ing growth into later drought period. Such species could
have stronger drought resistance, which is reflected by
lowerYleaf (Fig.3E).
In conclusion, we induced that H. fruticosum and S.
collina responded differently to the changes of simulated
precipitations. S. collina might be prodigal water use type
which is stomata dependence with high carbon gain, while
H. fruticosum could be conservative water use type that
had higher WUE. The differential physiological adaptations
to water condition especially their water use strategies may
be the mechanism of their coexistence in the sand dune
ecosystems.
Acknowledgements: We thank Mr. R.T. Wu, Herisitai
Village, Zhenglanqi Banner of Inner Mongolia for provid-
ing aids in field work.
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