The establishment and development of Haloxylon ammodendron promotes salt accumulation in surface soil of arid sandy land

YongZhong Su,TingNa Liu,JunQia Kong

Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences/Key Laboratory of Eco-Hydrology in Inland River Basin,CAS,Lanzhou,Gansu 730000,China

ABSTRACT Haloxylon ammodendron,a representative C4 succulent xerophyte and salt-secreting plant,is widely used in vegetation reestablishment programs to stabilize shifting sand, and is one of the dominant shrubs in the shelter belt used to control desertification in the desert-oasis ecotone in northwestern China. In this study, we collected soil samples in an age sequence of 0-,2-,5-,13-,16-,31-,and 39-year-old H.ammodendron plantations to assess the effects of the shrub on soil fertility and salinity. Results show that SOC and total N concentrations increased significantly with increasing plantation age and increased 5.95- (in the interspaces) to 9.05-fold (under the canopy) and 6.15- to 8.46-fold at the 0-5 cm depth at the 39-year-old plantation compared with non-vegetated sandy land. Simultaneously, H. ammodendron establishment and development resulted in significant salt accumulation in the surface layer.On average,total soil salt content at the 0-5 cm and 5-20 cm depth increased 16.8-fold and 4.4-fold,respectively,compared with non-vegetated sandy land.The increase of total salt derived mostly from the accumulation of, Ca2+ and Na+ with H. ammodendron development. The accumulation in salinity was more significant than the increase in fertility,suggesting that improved soil fertility did not limit the impact of salinization.The adverse effect of salt accumulation may result in H. ammodendron plantation degradation and impact community stability in the long run.

Keywords: Haloxylon ammodendron; soil salt and its component; soil organic carbon; plantation chronosequence; sandy land in desert-oasis ecotone

1 Introduction

Haloxylon ammodendron (C.A. Mey.) Bunge is a large xerophytic shrub in Chenopodiaceae,and its natural habitat is sandy desert, gravel desert, clay desert and saline land in Asian and African deserts (Tobe et al., 2000; Zhu and Jia, 2011). In China, H. ammodendronis is distributed mainly in the Junggar Basin, the northern edge of the Tarim Basin, the Gurbantonggut,Badain Jaran,Ulanbuh,and Tengger deserts,the western area of the Kubuqi Desert, and the Hexi Corridor of Gansu Province; it is a dominant species in deserts(Guo et al., 2005). H. ammodendron is remarkably tolerant of a variety of environmental stresses including drought, heat, cold, and high salt concentration in the soil. It is a C4plant, the seedlings can grow rapidly, and it is capable of surviving in any environment as long as it has a minimal supply of water (Zhu and Jia, 2011; Yang et al., 2014). H. ammodendron has commonly been used in windbreaks, sand-fixing projects, and vegetation restoration on desertified land due to its rapid growth characteristics, adaptability to wind and sand environmental conditions and drought stress. H. ammodendron plays an important role in reducing wind erosion and sandstorms, thus controlling and minimizing desertification (Su et al.,2007b;Yang et al., 2014). Currently, H. ammodendron has become the dominant shrub in the shelter belt to control desertification in arid regions of northwestern China(Zhu and Jia,2011;Yang et al.,2014).

Studies dealing with H. ammodendron have been continually undertaken due to the constant expansion of artificial H. ammodendron plantation areas in arid regions of northwestern China. Early studies focused on its ecological functions, water consumption and drought tolerance mechanisms, physiological and biochemical characteristics, and water source and soil water use characteristics (Tobe et al., 2000;Huang et al., 2003; Su et al., 2007a; Wei et al., 2007;Zhu and Jia, 2011). These studies also focused on soil, water, salt and nutrient characteristics of H. ammodendron plantations and the soil spatial heterogeneity induced by H. ammodendron individuals (Li et al., 2007; Liu et al., 2009). In recent years, the reasons for and mechanisms of H. ammodendron population degeneration, changes in the soil environment following establishment of H. ammodendron and its impacts on community stability have received much attention (Si et al., 2011; Wang et al., 2015; Cao et al., 2016; Zhang et al., 2016a; Zhang et al., 2016b).Several studies indicated that H. ammodendron establishment and development on sandy land enhanced soil nutrient accumulation and soil organic matter, with N and P nutrient concentrations generally higher with increasing plantation age (Wang et al.,2015;Zhang et al.,2016b).Improved soil fertility resulted in higher microbial diversity and biomass under H. ammodendron canopy than in the open interspaces (Cao et al., 2016), suggesting that H. ammodendron establishment and development may be beneficial to the improvement of the soil environment.However, H. ammodendron is a salt-secreting plant,absorbing substantial salts from the soil profile, and then returning them to surface soil via litterfall, indicating more salt accumulation in surface soil. Liu et al. (2009) and Zhang et al. (2016a) found that Na+,K+, Cl-, andconcentrations were significantly h ig he r on v eget a tion pa t ches be neath H. a m mod endron than in open land. Salt accumulation in surface soil after H. ammodendron establishment interfered with understory herbaceous performance and thus influenced vegetation restoration (Zhang et al.,2016a). The accumulation of salt in surface soil and the decrease of salt in root distribution layers may be one of the reasons for H. ammodendron degeneration.However, the dynamics and processes in soil salt following H. ammodendron establishment and development are largely unknown. Information about soil salt changes following the establishment of H. ammodendron is required for a better understanding of the soil environmental evolution, vegetation stability and the interactions between soil and vegetation.The objective of this study was to identify changes in soil salt following the establishment of artificial H.ammodendron plantations on sandy land in the desert-oasis ecotone in an arid region of northwestern China.

2 Materials and methods

2.1 Study sites

The study was carried out in a desert-oasis ecotone in Linze County in the middle of the Hexi Corridor region of Gansu Province, China, located between 39°09′N-39°19′N and 100°02′E-100°21′E,at the southern edge of the Badain Jaran Desert, with an altitude ranging from 1,368 to 1,380 m. Linze oasis is connected with dense moving and denuded residual dunes as well as gobi. The region has a typical temperate desert climate: dry and hot in summer, cold in winter, plenty of sunshine, very little precipitation and frequent strong winds. According to statistics of the Linze Weather Station, the annual mean air temperature is about 7.6°C,with an absolute maximum of 39.1 °C and an absolute minimum of -27 °C. Normal annual precipitation is 117 mm.Mean annual pan-evaporation is approximately 2,390 mm, 20 times greater than the annual precipitation. Mean annual wind velocity is 3.2 m/s, and the prevailing wind direction is from the northwest.Gales with wind velocities>17 m/s occur 15 or more days per year. The depth of the groundwater level ranges from 4 to 10 m (Su et al.,2007b).

The natural vegetation at the perimeter of the oasis is composed of desert shrubs including Calligonum mongolicum Turcz., Calligonum gobicum (Bunge ex Meisn.) Losinsk., and some small sub-shrubs such as Nitraria sphaerocarpa Maxim. and Reaumuria soongorica (Pall.) Maxim. Common annual species include Bassia dasyphylla, Salsola collina, Chloris virgata,Agriophyllum squarrosum, Halogeton arachnoideus,and Corispermum lehmannianum. Their growth periods are generally from June to September. The natural vegetation cover in the study area only ranges from 5%to 7%(Zhang et al.,2016a).

To control desertification around the oasis and to prevent drifting sands from encroaching into the oasis, H. ammodendron was introduced and planted on sandy land at the periphery of the oasis with the aid of straw checkerboards as sand binders beginning in the mid-1970s (Su et al., 2007b). Since the year 2000,ecological restoration and desertification control projects were implemented at the desert-oasis ecotone to maintain the ecological security of the oasis ecosystem. The planting of H. ammodendron has gradually extended from the fringe of the oasis toward the desert. To date, H. ammodendron plantations with ages from 2-39 years old were distributed in the desert-oasis ecotone, and it has become the dominant community in the study area.

2.2 Sampling and measurements

We adopted a chronological approach to study changes in soil salt characteristics in age sequences of 0-,2-,5-,9-,13-,16-,31-,and 39-year-old H.ammodendron plantations after being planted on shifting sand dunes. Previous analysis of soil properties from different periods indicated that these unstable shifting sand dunes showed no significant differences in soil texture and organic matter over time (Chen et al.,1998; Su et al., 2007b; Su et al., 2010), implying that relatively similar soil characteristics existed before planting. Investigation and soil sampling were carried out in August 2014.Three plots with an area of 10m×10m were chosen randomly in each plantation age sequence. Five H. ammodendron shrubs of similar growth habits were selected at each plot to record height and stem diameter. Due to natural death and shrub self-thinning process, the number of existing living individuals generally decreased with an increase in plantation years. After establishment of 16 years,the rate of existing living individuals were 28%and dead branches reached to 15.8%, and H. ammodendron growth appeared to be degenerative (Zhang et al.,2016b).

In the control area (age 0 years), three plots were established near the planted sites, and soil samples were collected from five random points within each plot.In the seven H.ammodendron plantations(age 2,5, 9, 13, 16, 31 and 39), five individual shrubs were chosen in each plot, and samples were collected from two different locations surrounding each selected H.ammodendron shrub: beneath the canopy at a distance of approximately 20 cm from the main stem (under the canopy), and from open land 50 cm outside the canopy (in the interspaces). At each location, a composite soil sample from two depths (0-5 and 5-20 cm) was collected from five sampling points. Soil samples were taken from the 0 to 5 cm depth using a shovel, and from the 5 to 20 cm depth using a 5-cm diameter soil auger.

Soil samples were air-dried and passed through a 2-mm sieve for pH and electrical conductivity (EC)analyses, and a <0.1 mm sieve was used for SOC, total N, and soil salinity analyses. Soil organic carbon(SOC) was determined by the Walkley-Black dichromate oxidation method (Nelson and Sommers, 1982),and total N was measured using an Elementar Analysensysteme (Vario MACRO CUBE, Germany). Soil electrical conductivity (EC) was measured using an electrical conductivity meter at a soil/water ratio of 1:2.5, and soil pH was measured using a pH meter at a soil/water ratio of 1:5.Soilandconcentrations were measured using the double indicator neutralization method, Cl-concentration was measured using AgNO3titration andby EDTA indirect titration, Ca2+and Mg2+were measured using EDTA titration, and Na+and K+were measured using a flame photometer (Institute of Soil Sciences, Chinese Academy of Sciences, 1978). Total salt content was obtained by calculating the sum of anions and cations.

2.3 Statistical analyses

Comparisons of soil parameters among the treatments were restricted by location and depth. One-way analysis of variance (ANOVA) and least significant difference (LSD) were carried out using the SPSS package. LSD values were reported at the 5% level of significance.

To identify differences in soil properties under the shrub canopy (A) and in the inter-shrub area (B), we used an enrichment ratio (E) where E=/A/B (Wezel et al., 2000; Su et al., 2012). The enrichment ratio was calculated as the average of ratios for each pair of samples analyzed. The value of E should reflect the effect of shrubs on the spatial distribution of soil properties.

3 Results

3.1 Changes in SOC, total N and pH following H. ammodendron establishment

The establishment and development of H. ammodendron improved SOC and total N accumulation(Figure 1). SOC and total N concentrations at the 0-5 cm surface layer 39 years after its planting increased 9.1-fold and 8.3-fold under the canopy and 2.8-fold and 3.5-fold in the interspaces, respectively, in comparison with the non-vegetated sandy land. In the planting chronosequence, SOC and total N concentrations, both under the canopy and in the interspace, increased significantly with increased plantation age.The increases at the 0-5 cm depth appeared earlier than those at the 5-20 cm depth. Significant change in SOC at the 0-5 cm depth was observed in plantations that where 5 years old,while that at the 5-20 cm depth was found in plantations that where 13 years old. With the development of H. ammodendron, SOC and total N concentrations were higher under the canopy than those in the interspaces. Soil pH increased under the canopy in the 5 year old H. ammodendron plantation. However, it did not vary significantly in the 9 year old plantation,either under the canopy or in the interspaces.

Figure 1 SOC,total N concentrations,and pH in the different H.ammodendron plantation ages.Bars represent standard deviation values;letters within the same sampling location show significant differences at P level<0.05(LSD)

3.2 Accumulation of soil salt following H.ammodendron establishment

The establishment and development of H. ammodendron resulted in a significant accumulation of soil salt in the sandy soils (Table 1).At the 0-5 cm depth,total salt content under the canopy increased by 1.6-,2.0-, 2.9-, 4.2-, 10.4- and 16.8-fold, respectively, and from the non-vegetated site (1.98 cmol/kg) after 5, 9,13,16,31,and 39 years of shrub occupancy.In the interspaces,this increase was 1.6-,2.0-,2.7-,2.9-,8.7-,and 16.8-fold, respectively. Total soil salt content at the 5-20 cm depth show a similar trend of variation as that in the surface soil, but the values of the increase were lower than those of the surface soil, with an increase of 1.3-4.3-fold and 1.3-4.5-fold under the canopy and in the interspaces, respectively. Similar to the total salt content, electrical conductivity (EC) increased 17.4-fold and 6.2-fold at the 0-5 cm and 5-20 cm depths under the canopy,and 12.7-fold and 8.5-fold in the interspaces, respectively, after 39 years of shrub occupancy.

Table 1 Soil salt component and electrical conductivity(EC)in H.ammodendron plantations of different establishment age

to be continued

Table 1 Soil salt component and electrical conductivity(EC)in H.ammodendron plantations of different establishment age

From the analysis of salt ion composition, with the increase of planting age,concentration show an exponential accumulation. After 39 years of shrub occupancy,concentration increased 78.5-80.6-fold at the 0-5 cm surface layer, and 6.5-7.1-fold at the 5-20 cm depth, and became the dominant anion(Table 1). Cl-andconcentrations show a similar variation to that ofin an age sequence of H.ammodendron in the plantations, but the increased rate was smaller than that of. Ca2+and Na+concentrations followed a similar trend in variation to that of, with an exponential increase in the time series of plantation age. Significant change in Mg2+concentration occurred in soils after 16 years of shrub occupancy, with the greatest values in the 31-year plantation under the canopy and in the interspaces.The sandy soils show a very low K+concentration.After 9 years of H.ammodendron occupancy,K+concentrations show a significant increase at the 5-20 cm soil layer in both sampling locations. At the 0-5 cm surface soil depth, the K+concentration in the 31-year and 39-year plantations under the canopy was significantly higher than that in other plantations and in the non-vegetated control area. With the development of H.ammodendron,accumulation of salt ions in the surface soil generally increased. After 13 years of shrub growth, salt ion concentrations show significant differences between the two soil depths, andand Ca2+had the greatest differences.

3.3 Enrichment ratios for soil parameters in H.ammodendronin plantations of different ages

The enrichment ratios (E) for soil fertility and salinity differed among the different H. ammodendron plantations. The E values for SOC and total N ranged from 1.05 to 1.89, and from 1.14 to 2.24 in the surface layer, respectively. At the 5-20 cm depth, the E values ranged from 1.00 to 1.80 for SOC, and from 1.04 to 1.84 for total N (Table 2). This indicated a clear accumulation effect for soil fertility under the canopies and increased spatial heterogeneity at the microhabitat scale induced by the shrubs. For total salt content, the E values ranged from 0.98 to 1.44 and from 0.89 to 1.26 at the 0-5 cm and 5-20 cm depth,respectively. With the exception of the 16-year and 31-year plantations,the E values for total anions,total cations, and total salt in other plantations were close to 1.00, indicating soil salt accumulation under the canopies and in the interspaces,simultaneously.

4 Discussion

This study indicates that the establishment and development of H. ammodendron on shifting sandy land in a desert-oasis ecotone in an arid region resulted in significant improvement in the SOC and total N of surface soil. The positive effects increased with plantation age.These results agree with studies from other regions (Su and Zhao, 2003; Li et al., 2007; Zhao et al., 2007). The improvement of SOC and total N induced by re-vegetation is a complicated ecological process that is simultaneously affected by many biotic and abiotic variables. First, shrub establishment and development not only offered an important safeguard against soil erosion, but shrubs trapped wind-blown fine materials and dust that are rich in nutrients and deposited in the surface soils (Wezel et al., 2000; Su et al., 2004). Re-vegetation on sandy land enhanced the deposition of silt and clay fractions in the soil surface layer which contributed to the improvement in SOC and nutrients(Su et al.,2007).In the same study site,Wang et al.(2015)and Zhang et al.(2016b)indicated that silt and clay content in surface soil increased with increasing age of an H. ammodendron plantation, and SOC and total concentrations were highly related to silt and clay content. Second, with the development of shrubs, litter input and root turnover contributed to SOC and total N accumulation.Because litter and fine materials trapped during physical transport accumulated mostly in the soils under the canopies, SOC and total N concentrations were significantly higher under the canopies than those in the interspaces, confirming the common characteristic of the heterogeneity pattern and islands of fertility induced by shrubs in many arid and semi-arid ecosystems (Schlesinger and Pilmanis, 1998; Su and Zhao,2003;Li et al.,2011;Li et al.,2014).

These results also indicate that the growth and development of H. ammodendron shrubs resulted in significant accumulation of soil salt, especially in the 0-5 cm surface soil. H. ammodendron is a succulent,halophytic plant that can absorb salt ions from the soil during its growth (Xi et al., 2004). Simultaneously, as a typical succulent xerophyte, H. ammodendron can absorb and accumulate a great quantity of Na+, Ca2+,K+, and Cl-from the soil as an important physiological osmoregulator which is efficiently transported to the leaves as well as its photosynthesizing branches to resist drought stress (Wang et al., 2004; Kang et al.,2013; Kang et al., 2017).Wang et al. (2014) observed that salt content in H. ammodendron tissues increased with increased growth years,and the salt content in assimilation branches and perennial branches of 10-year H. ammodendron reached 58.3-60.6 g/kg and 84.6-88.2 g/kg,respectively.Bai et al.(2012)found that Na+content in H. ammodendron leaves reached 6.9 g/kg, a number which was 7-10 times higher than that of other desert plants.Therefore,with the increase of H.ammodendron growth years, the input and accumulation of litter enriched in salt content resulted in salt accumulation in the surface soil (Xi et al., 2004). In addition, the salt ion migration in the soil was accompanied by the movement of soil water.With the increase of H. ammodendron growth years, water consumption through shrub evaporation increased and soil water in the deep layers was transported up to the surface layer, resulting in salt in deep soils moved upward and accumulated continuously in the surface soils (Liu et al., 2017). The observations of soil water and salt dynamics in H. ammodendron plantations shows that soil water content and EC values in the 50-70 cm depth were lowest in the soil profile, confirming the shrubs' absorption of soil water and salt and their upward movement (Liu et al., 2017). In the study area,annual precipitation is 117 mm and is only 5% of annual evaporation. Once soil salt accumulates in the surface layer, leaching and desalting processes do not occur.Salt accumulation in the surface soil and reduction in the root distribution (Liu et al., 2017) may be one of the mechanisms in H. ammodendron degeneration 13 years after its planting. Further studies on salt dynamics in soil profiles are required.

Table 2 Enrichment ratios(E)of soil properties for H.ammodendron plantations of different age

The increased rate of salt content was higher than that of SOC concentration (Figure 2), indicating that the effect of H. ammodendron on salt accumulation was more significant than the effect of fertility,reflecting the negative effect of H.ammodendron on the soil environment. Although the salt accumulation in the surface soil is propitious to sand surface stabilization by promoting the formation of soil crust and aggregates (Su et al., 2007b), excessive accumulation of soil salt interferes with seed accumulation and restrains the growth and development of their understory plants (Zhang et al., 2016). Therefore, artificial regeneration of shrubs is needed to curtail the excessive accumulation of soil salt. Additionally, H. ammodendron is the most extensively introduced sand-fixing plant in the study area which has been replacing native shrubs (e.g., C. mongolicum and N. sphaerocarpa) as the dominant species.This has resulted in a decrease of species diversity. Planting H. ammodendron on sandy land in arid region increases vegetation coverage,but the planting pattern with a single species allocation may produce some unpredictable impacts on vegetation composition and community stability in the long run.

Figure 2 The relationships of SOC concentration and total salt content at the 0-5 cm depth with plantation age

5 Conclusion

This study indicates that the establishment and development of H. ammodendron on shifting sandy land resulted in an improvement of SOC and total N, and their concentrations increased significantly with increasing plantation age.SOC and total N show significant enrichment under the shrub canopy, confirming the effect of fertility islands as reported in other arid and semi-arid zones. Additionally, the establishment of H. ammodendron resulted in a significant accumulation of soil salt. In the 0-39 age sequence of shrub plantations, the increase in salinity was more significant than the increase in fertility, suggesting that improved soil fertility did not limit the impact of salinization. The adverse effect of salt accumulation on the soil environment may produce some unpredictable impacts on vegetation composition and community stability in the long run.

Acknowledgments:

The study was supported by the National Key Research and Development Program of China (No.2017YFC0504304).