沙漠研究 22-1, 77 -82 (2012 )"ICAL 1 / DT X"

Journal of Arid Land Studies－Refereed Paper－

Seasonal Dynamics of Asiatic Desert C3/C4 Species Related to LandscapePlanning and Rehabilitation of Salt Affected Lands
Elena SHUYSKAYA*1), Toshpulot RAJABOV2), Naoko MATSUO3), Kristina TODERICH2),
Liliya GISMATULLINA2), Pavel VORONIN1) and Norikazu YAMANAKA4)
Abstract: This paper considers how salt and drought tolerant C3/C4 arid/semiarid plants in pure or mixed stands can control salinity,
improve rangelands productivity and reverse desertification in Central Asian arid and semiarid zones. Spatial distribution of C3/C4
photosynthetic types within different desert vegetation plant communities differs by seasons and along the soil salinity gradient. The
ratio of C3:C4 species was represented as 10:1, 10:2 and 10:9 for xero-, xerohalo-, haloxerophyte plant communities from non-saline tosaline habitats, respectively. During summer season insignificantly increased values of C4 species (in 1.5-3.7 times) were found forinvestigated plant communities. More than 90% of biomass proportion of xerophyte plant community is represented by C3 species.
The total productivity of xerohalophyte plant community is 1000 kg/ha of which 15% belongs to C3 species and 85% to C4 species.
The productivity of haloxerophyte plant community is determined by C4 species, which consists of 87% of total biomass. Fromspring to autumn a decreasing trend of biomass of C3 and increasing of C4 plants in the vegetation cover of desert rangelands was
revealed. Optimal spatial combination of C3/C4 plants by considering their phenological rhythms and mechanisms of adaptation to
drought cycles and soil salinity guarantees high plant survival and biomass accumulation on salt affected rangelands. Coexistence ofC3/C4 species under wide range of salinization combined with limited content of water in the soil was considered as the essential
factor in the elaboration of optimal landscape planning and rehabilitation techniques of degraded rangelands affected by salinity.
Key Words: Agroforestry, C3/C4 types, Kyzylkum desert ecosystems, Salinity gradient, Vegetation dynamics

1. Introduction
Drought and salinity can have great effect on food security
in Central Asia. The inland Irano-Turanian cold desert
ecosystem under currently ongoing climate changes arecharacterized by reduced species-richness, especially trees andshrubs and, thus, by having a low resistance to climate
extinctions. Vegetation cover of sandy desert rangelands has
a complicated spatial structure determined mostly by impact ofheterogeneity of desert environment.
Replacement of
deep-rooted, perennial native vegetation by shallow-rooted,
annual and invasive non palatable species induced salinization,waterlogging and decreasing of rangelands productivity.
Frequency of climatic extremes (droughts) and changes in soil
salinity alter the plant functional group composition,
distribution and abundance of species, which significantly
reduce productivity of arid ecosystems and loss of biodiversity.
Considerable research has been done on soil-vegetation
relationship in coastal salt marshes saline soils (Pop, 1984;
Greaver and Sternberg, 2006). However, investigations
identifying the major environmental factors associated withvegetation patterns on inland saline desert areas are scarce andlimited to the descriptive botanic documentation of species(Akjigitova, 1982; Toderich et al., 2009). It is presumed thatthe virgin psammo- and xerophytic desert plant communities(with predominant of C3 species) available for grazing ofanimals are replaced by halophytic plant communities (C4species predominant) with less nutritional values andpalatability. As a rule C4-plants have twice as much the water
use efficiency (WUA) as C3 ones (Farguhar et al., 1989).
Meanwhile, the C4-plants input to Central Asia desert flora are
relatively low (Pyankov, 2001). Additionally, these species
colonize marginal areas and are more competitive towards
sensitive species (Toderich et al., 2007). However, many of
Asiatic C3/C4 are at the edge of disappearance due toovergrazing and may become an irreversible loss ofphytogenetic resources. Most of populations of the desert
halophytes within flora of the Uzbekistan are local and small,sometimes fragmented. They frequently have incomplete life
cycles with little ability to reproduce, low indices of renewal
and replacement. The present study aims to describe theseasonal variation of distribution and density/productivity of
C3/C4 species for different desert plant communities along thesalinity gradient. The δ13C data were used to assess the
responses of native plants to climate change and the effect of*Corresponding Author: evshuya@gmail.com
K.A. Timiryazev Institute of Plant Physiology RAS, Botanicheskaya st., 35, Moscow, 127276, Russia
1) K.A. Timiryazev Institute of Plant Physiology RAS

3) Graduate School of Bioresources, Mie University, Japan

2) Department of Desert Ecology and Water Resources Research, Samarkand Division of the Academy of Sciences of Uzbekistan. Uzbekistan

4)Arid Land Research Center, Tottori, Japansalinization on natural vegetation in Central Asian dryland
ecosystem.

2. Material and Methods
2.1. Description of the study sites
The study area is located at north-east part of Karakata
depression in the central part of Kyzylkum desert, Uzbekistan(mean annual temperature = 15.7°C, mean annual precipitation= 175 mm; Gintzburger et al., 2003). Geographically therangeland plots are located between the coordinates of 41°06’
13.7’’N; 064°50’55.5’’E and 41°03’36.4’’N; 064°53’52.6’’E
and elevation ranges of 100-130 m above the see level. The
climate of Karakata depression is typical for the condition of
Kyzylkum desert which is characterized by sharp fluctuationsof daily and seasonal temperatures.
The amount ofprecipitation is small and it is mostly occurred during thewinter-spring seasons. Spatial distribution (zonation) of
natural vegetation in relation to soil salinity was studied in a
distance of about 4 km, located between two artesian hot
springs. The most important factor for the zonation was soil
salinity (calculated for total dissolved salts values) and the salt
tolerance limits of species.
Based on geobotanicaldescriptions of vegetation cover (ratio of xerophilous andhalophilous species) and on level of soil salinization (ECvalues) 4 microlandscape sites were divided along the salinity
and relief gradients. These selected plant communities
belong to different vegetation types: xerophyte (1 site),
xerohalophyte (2 sites), haloxerophyte (1 site). The wet salt
depression was used as a benchmark of high soil salinization(according to total content of cations and anions) and specified
as “Solonchak”.
2.2. Calibration EM38
Electromagnetic conductivity devices were expressed atstandardized reference temperature of 250°C. The reason for
expressing at reference temperature is the fact that electrolytic
conductivity increases at a rate of approximately 1.9%
(Rhoades et. al.,1999). The formula provided in Sheets andHendrickx (1995), who fit the curve to conversion table given
in USDA (1954), we used as: EC25 = ECa * [0.4470 +
1.4034exp (T/26.815)], where EC25 is standardized ECa, ECa apparent electrical conductivity and T-soil temperature.
2.3. Plant samples
2.3.1. Vegetation surveys
Geobotanical descriptions were done using 2 m × 50 m
transect (in semi shrub plant communities) and 5 m × 50 m
transect (in shrub plant communities - Haloxylon aphyllum
associated), in three replications. Total numbers of shrubs ofeach species within the 100 m2 and 250 m2 were counted in 3
size classes (big, medium, small) based on plant height anddiameter. For each size class and each species one
representative plant was harvested and separated into woody,green and dead parts. The total biomass for each subplot wasdetermined by combining density data of each species present.
Cover of individual shrub species was determined from a
50m-line intercept along one edge of the 2 m × 50 m and 5 m ×
50 m plot.
2.3.2. Stable isotope analysis
Plant material for stable isotope analysis had been gatheredat natural vegetation of typical desert plant communities. The
leaves or photosynthetic shoots from 3-5 individuals of eachplant species were collected at each site. The photosyntheticorgan samples were oven-dried at 70°C for 48 h and finely
grounded. The δ13C in the organic samples was analyzed
using a continuous flow system of an elemental analyzer andan isotope ratio mass spectrometer (Flash2000 & Delta S,
Thermo Fisher Scientific) at Field Science Education andResearch Center, Kyoto University. Carbon isotope ratios
were expressed by the following equation: δ13C
value=((Rsam-Rstd)/Rstd)*1000 (‰), where Rsam and Rstd
represent the 13C/12C of the samples and standard.
2.3.3. Estimation dry biomass
The harvested material was packed in paper bags in thefield and then oven dried at 65°C for 72 hours in laboratory.
The dry weight of all the species was then combined to get the
total biomass estimates.

3. Results and Discussion
3.1. Soil and ground water salinity characteristics
Groundwater table fluctuates from 0.5 - 2.5 m (below soil
surface) during May-July at the dry solonchaks andexperimental agricultural plots and up to 8.0 - 20.0 m in thevirgin desert Artemisia pastures. Ground watermineralization at shallow water table level taken under
haloxerophyte and halophyte sites varies in the range of 2000 8200 mg l - 1 (Asian Development Bank, 2008).
Measurements of soil EC in early spring and at the end ofvegetation season (late autumn) shown slight to medium
salinity (30 - 150 mS m-1), although at the upper 40 cm horizon
at some points EC reached values of over 250 mS m-1. Soiltypes of surveyed area are light sandy and silt-sandy loam withlow organic matter (less than 1%) throughout the profile up to
the depth of 60 cm and cation exchange capacity in the rangeof 5.0 mmol g-1 and 10.0 mmol g-1. The soil lower layers arealso saline due to the presence of high content of gypsum.
Total nitrogen (N) and phosphorus (P) contents in salt affectedsoils are low, usually ranging between 0.7 - 5.5 mg kg-1

a)
120
%

100
80
60
40
20
0
Xerophyte

Xerohalophyte

Xerohalophyte

Haloxerophyte

Solonchak

Ca

Mg

Na

HCO3

Cl

SO4

cations

anionsb)500
y = 11.53x + 32.74
R2 = 0.89

450
400

Fig. 2. Ratio of species with С3 and С4 types of photosynthesis indifferent plant associations (a – xerophyte, b - xerohalophytes, c– haloxerophyte) during vegetation season.

mSm-1

350
300
250
200
150
100
50
0
0.00

10.00

20.00

30.00

40.00

Na, m m ol l-1

Fig. 1. a) Relative content of different cations and anions in soils
among studied zones (where the maximum content of ions
was taken as 100%); b) Linear regression between
estimated of soluble salts from electrical conductivity (EM38)
and Na + content across salinity gradient.

and 10.0 -18.26 mg kg-1, respectively. Available potassium(K+) content is classified as low or moderate. Chemical
analysis of soil showed that main type of mineralization is
calcium-sodium and hydrocarbonate-sulfate. The virgin
Artemisia pasture and gray brown stabilized sands (underxherophyte site) with the least content of salinity and soil
moisture is characterized by significantly amount of Ca2+,
HCO32- ions and the least content of Na+, Mg2+, Cl- comparewith other tested sites.
As shown on Figure 1 a,b, the ability of up-taking and/or
accumulation of sodium ion in the upper soils profile andelectric conductivity value detected by EM38 were graduallyrising accordingly to spatial changes in floristic composition
within investigated rangelands sites. Electric conductivity
values and Na+ content were graphed and a high positive (R2 =0.89) linear regression was observed as increasing the level ofsoil salinization, which mostly occurs on lowland saline
depression (less than 100 m above sea level) across desert
relief (Perelman et al., 2001). i.e. electric conductivity
value reflects the salinity characteristics at microrelief
level.
3.2. Plant communities structure
The seasonal dynamics of vegetation is related to inter-

specific and intra-specific plant species competition, carrying
capacity of rangeland and land use management. Desert
topographical features and salinity gradient are of primary
importance in determining the contribution of various planttaxons with different photosynthetic pathways to comprise coreecological plant associations or vegetation units. The main
criteria of differentiation of vegetation communities were theabundance of the individual species. Three types of
ecological plant associations on desert rangelands wereallocated and their botanical composition was identified: 1.
aboriginal xerohytes on sandy and grey-brown desert soils
represented by Ferula assa-foetida, Aellenia subaphylla,
Ammothamnus Lehmannii, Astragalus villosissimus, Artemisia
diffusa, Salsola praecox, Heliotropium sp., Calligonum
leucocladum, Stipa sp., Convolvulus hamadae, Mausolea
eriocarpa; 2. xerohalophytes plant communities consists ofArtemisia diffusa, Haloxylon aphyllum, Ammothamnus
Lehmannii, Peganum harmala, Alhagi pseudoalhagi; 3.
haloxerophytes on saline prone sandy soils dominated byannuals species of Salsola sp., Climacoptera sp., Suaeda sp.,
Halocharis hispida, and perennials Halimocnemum
strobilacea; Halostachys belangeriana; Aeluropus littoralis;
Limonium suffruticosa and others.
3.3. Plant density of С3- and С4 species
The highest density of xerophyte and xerohalophyte plantcommunities belongs to C3 species consisting of 89-94% and74-91%, respectively (Fig. 2). The ratio of C4 plants showedsmaller values than C3 plants for both plant communities. As
its name implies, the plant density of haloxerophyte
community represented considerably rapid changes during theseasons in term of the ratio of C3 and C4 plants. In spite of thedominancy character of C3 species in haloxerophyte

a)
3500

C4

3000

C3

Biomass, kg/ha

2500
2000
1500
1000
500
0
1

2

3

Xerophyt e

1

2

3

1

2

3

Xerohalophyt es Haloxerophyt e

b)
100
90

projective cover, %

80
70
60
50
40
30
20
10
0
s pring
Xerophytes um m er

autum nXerohalophytes

Haloxerophyte

Fig. 3. Biomass production of C3 and C4 species (a) and seasonal
projective cover of C4 species (b) in plant communities (where1, 2 and 3 corresponds to spring, summer and autumn
seasons).

community, the proportion of C4 species is noticeably
increased than in other plant communities. The contributionof C4 species in haloxerophyte community showed 19%, 70%
and 45% during spring, summer and autumn seasons,respectively. However, during the summer season relatively
increased values of C4 species were observed for all plantcommunities.
3.4. Plant biomass of natural rangelands along the salinity
gradient
Xerophyte plant community is characterized with thelowest value of rangeland productivity consisting of 300 kg of
biomass per hectare. More than 90% of biomass proportionof xerophyte plant community is represented by C3 species(Fig. 3a). The total productivity of all plants in xerohalophyte
plant communities is 1000 kg/ha of which 15% belongs to C3
species and 85% to C4 species. The ratio of C4 species is

considerably increased in productivity of haloxeropyte plantcommunity and covered 87% of total biomass. Only
8.6-18.4% of total biomass belongs to C3 species.
Haloxerophyte plant community is characterized with highest
biomass among other plant communities - 2600 kg/ha.
Seasonal dynamics of total biomass production ofvegetation communities is characterized by increased trend
during the vegetation period reaching the highest values inautumn season for the amount of C4 species (Fig. 3b).
However, there is opposite dynamics of biomass depending on
the photosynthesis type plants: decreased trend for C3 andincreased trend for C4 species during the seasons.
Result of this study showed that ratio of C3 and C4 plants invegetation communities differs both along the salinity gradientand on seasons of the year. Along the salinity gradient theratio of C3:C4 species (in average by all seasons) is represented
as 10:1, 10:2 and 10:9 for xero-, xerohalo-, haloxerophyte plantcommunities, respectively (Fig. 2). Regular prevalence of C3
species is observed, as proportion of С4 species in the flora ofdesert vegetation of Uzbekistan does not exceed than 4%(Pyankov et al., 2001, Toderich et al., 2007).
Nevertheless, proportion of C4 species is increased along
the salinity gradient and in haloxerophyte plant community its
amount becomes comparable to the proportion of C3 species.
С4 species occurs mostly on salt affected soils because Na+ isessential for C4 species (for the translocation of pyruvate acrossthe chloroplast envelope) where sodium ion functions as a
micronutrient and to some extent all Chenopodiaceae species(studied С4 chenopods) are halophytes (Akhani et al., 1997,
Toderich et al., 2007) Additionally, in case of vegetation coverof Karakum desert (Pyankov et al., 2002) and grasslands ofArgentina (Feldman et al., 2008) the increased amount of C4
species comparatively to C3 species has also shown along thegradient of deterioration of soil condition and soil salinization.
Significant dependence of C3 species on soil salinization
indicates about the reduction of carbon isotope discrimination(δ13C value) of studied C3 species along the salinity gradient(from -27.39‰ to -24.79‰) (Fig. 4a). A 2‰ differences inδ13C value of С3 plants indicates a difference in water-use
efficiency of about 30% (Ehleringer and Cooper, 1988;
Dawson, 1993). In this case, C4 species demonstrates
independence of δ13C value along the salinity gradient (Fig. 4b).
A positive correlation of total productivity of main plantcommunities along the gradient of salinity with vegetative
cover of C4 species, especially due to the perennial C4 tree andshrubs like Haloxylon aphyllum and Calligonum leucocladum
was identified. The dominance of C3 species in spring andearly summer seasons in the studied areas is determined byabundance of short-live species of ephemers and ephemeroids.
The high ratio of C4 species in summer is stipulated by annuals

a)Plant communities

-22
1

-23

2

Xerophyte

3
Xerohalophytes

4
Haloxerophyte

d13C, %o

-24
-25
-26
-27
-28
-29

b)
Plant communities

-10
-10.5

1

-11

Xerophyte

23
Xerohalophytes

4
Haloxerophyte

d13C, %o

-11.5
-12
-12.5
-13
-13.5
-14
-14.5
-15

Fig. 4. Leaf carbon isotope ratio of (a) С3 and (b) С4 species along
salinity gradient.

halophytes from genus Salsola, Halocharis, Gamanthus,
Climacoptera, Suaeda etc. (more than 40% among total C4
species of haloxerophytic plant community). The vegetationof majority of mentioned species is over at the end ofsummer-early autumn (Fig. 3b). Species with C4 type ofphotosynthesis with high transpiration efficiency are better
adapted to soil water deficit or physiological drought that isstrongly expressed in summer period, thus, the productivity of
C4 species within different desert plant communities do notmuch dependent on the regime of rainfall. There is not linear
relation between the biomass of plant communities andseasonal projective cover of C4 species due to the occurrenceof increased values of these plant parameters in different
seasons: high biomass in autumn and high projective cover insummer.

3.5. Landscape planning and Rehabilitation Technique
for salt affected Lands
A number of native and exotic halophytes both C3 and C4
plants suitable for reclamation of arid and semi-arid,

salt/affected and waterlogging areas have been proven very
useful in demonstration trials. Mixture of C3/C4 desert fodder
species planted within the inter-spaces of salt-tolerant
trees/shrubs plantations improves productivity of rangelands
degraded affected by soil salinization. Application of suchapproach solves the animal feed gaps in the lands degradedboth by overgrazing and salinity, and promotes to increase theincome for farmers. Agro-silvi-pastoral trials used forlandscape planning and rehabilitation of saline soils represent amodel of ecosystem function/services for agropastoral
communities as adaptation measures to climate change. The
coexistence of C3 and C4 species is facilitated because C3
species can colonize nutrient rich microsites, while C4 species
canopy nutrient poor microsites. Comparing different species
within a small scale habitat along a salinity gradient we foundthat short-lived annuals or herbaceous species had significantly
lower values of forage biomass than perennial species. The
selection for trees with low δ13C and, therefore, hightranspiration efficiency, has the potential to increase total tree
biomass growth in water-limited arid saline environments.
Results obtained in this study showed that the successful
performance of drylands afforestation technique is based onpartial overlapping of natural niches of C3/C4 species.
Therefore the optimal rehabilitation technique of saline prone
rangelands consists from 12% of tree cover, 20% wild
xerohalophytes, 38% of biannual and 30% annual forage crops,
which in mixture planting significantly increase theproductivity of rangelands by providing a satisfactory drainage- control and preventing accumulation of salts at the root zone
area.

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