Ecol Res (2014) 29: 889–896 DOI 10.1007/s11284-014-1177-7
ORIGINAL ARTICLE
Yang Zhao • Xinrong Li • Zhishang Zhang Yigang Hu • Yongle Chen Biological soil crusts influence carbon release responses following rainfall in a temperate desert, northern China
Received: 3 February 2014 / Accepted: 19 June 2014 / Published online: 15 July 2014 The Ecological Society of Japan 2014
Abstract How soil cover types and rainfall patterns Keywords Arid regions Æ Biological soil crusts Æ influence carbon (C) release in temperate desert ecosys- Extreme rainfall event Æ Rainfall pattern Æ Tengger tems has largely been unexplored. We removed intact Desert crusts down to 10 cm from the Shapotou region, China, and measured them in PVC mesocosms, immediately Abbreviations after rainfall. C release rates were measured in soils with BSCs Biological soil crusts four cover types (moss-crusted soil, algae-crusted soil, C Carbon mixed (composed of moss, algae, and lichen)-crusted EPS Extracellular polysaccharide soil, and mobile dune sand). We investigated seven dif- MDS Mobile dune sand ferent rainfall magnitudes (0–1, 1–2, 2–5, 5–10, 10–15, Rs Soil respiration 15–20, and >20 mm) under natural conditions. C re- lease from all four BSCs increased with increasing SOC Soil organic carbon rainfall amount. With a rainfall increase from 0 to 45 mm, carbon release amounts increased from 0.13 ± 0.09 to 15.2 ± 1.35 gC m 2 in moss-crusted 2 soil, 0.08 ± 0.06 to 6.43 ± 1.23 gC m in algae-crus- Introduction ted soil, 0.11 ± 0.08 to 8.01 ± 0.51 gC m 2 in mixed- 2 crusted soil, and 0.06 ± 0.04 to 8.47 ± 0.51 gC m in Biological soil crusts (BSCs) are globally widespread mobile dune sand, respectively. Immediately following communities of diminutive organisms such as cyano- heavy rainfall events (44.9 mm), moss-crusted soils bacteria, green algae, lichens, mosses and other organ- showed significantly higher carbon release rates than isms. BSCs are closely integrated with surface soil algae- and mixed-crusted soils and mobile dune sands, particles, resulting in the formation of a cohesive thin- which were 0.95 ± 0.02, 0.30 ± 0.03, 0.13 ± 0.04, and 2 1 layer; they may constitute as much as 40 % of the living 0.51 ± 0.02 lmol CO2 m s , respectively. Changes cover in arid and semi-arid ecosystems. These soil in rainfall patterns, especially large rain pulses organisms can significantly improve soil stability and (>10 mm) affect the contributions of different soil cover fertility by alleviating soil erosion, contributing greatly types to carbon release amounts; moss-crusted soils to carbon (C) assimilation and nitrogen fixation, and sustain higher respiration rates than other biological creating favorable microhabitats for other organisms crusts after short-term extreme rainfall events. (Belnap and Lange 2003; Bowker et al. 2006;Li2012). BSCs are major players in the global C cycles, in terms of C uptake from and release to the atmosphere (Elbert et al. 2012). The high photosynthetic C fixation potential of BSCs, such as lichen crusts, makes them an important C uptake pathway (C sink) in desert ecosys- tems. Thus, researchers have recently become interested in studying BSCs, and their role in C cycling (Zaady Y. Zhao (&) Æ X. Li Æ Z. Zhang Æ Y. Hu Æ Y. Chen et al. 2000; Huxman et al. 2004a, b; Li et al. 2012). BSCs Shapotou Desert Research and Experimental Station, Cold and also contribute to C release in desert ecosystems; how- Arid Regions Environmental and Engineering Research Institute, ever, many studies neglect this role (Thomas et al. 2008; Chinese Academy of Sciences, 320 Donggang West Road, Lanzhou 730000, China Thomas and Hoon 2010; Gao et al. 2012; Li et al. 2012). E-mail: [email protected] Castillo-Monroy et al. (2011) found that BSC-domi- 890 nated sites accounted for 43 % of total C release by soil respiration (37 % from vegetation and 20 % from bare Materials and methods soil) in a semi-arid steppe ecosystem on the Iberian Peninsula. They concluded that BSC-dominated areas Study site are the main contributors to the total C release by soil respiration in desert ecosystems. Furthermore, the vast The Shapotou region is located on the southeast edge of BSC surface area on the Colorado Plateau has increas- the Tengger Desert in northern China (37 33¢N, 105 02¢E) at an elevation of 1,339 m AMSL. The area is ing CO2 release rates related to 2 C elevated soil tem- peratures and additional 2 and 30 mm summer rainfall a typical transitional zone between desert and desert oasis. The natural vegetation is dominated by Sweet- events. This enhanced CO2 flux in soils covered with BSCs indicates that the contribution of BSCs to atmo- vetch (Hedysarum scoparium) and Sand Rice (Agrio- phyllum squarrosum), with a cover of approximately spheric CO2 is projected to increase (Zelikova et al. 2012). Relatively few studies have assessed the role of 1 %. Most of the area is covered by high, dense, and BSCs in ecosystem C release; C release from soils cov- continuous reticulate barchan dunes. The soil substrate ered with different BSC types under natural conditions is is loose and impoverished mobile sand. The mean an- especially poorly understood (Thomas et al. 2008; Grote nual air temperature is 9.6 C, with extreme minimum et al. 2010; Coe et al. 2012;Li2012). and maximum temperatures of 25.1 and 38.1 C, respectively. Mean annual rainfall is 186.6 mm and Spatial and temporal patterns in water availability 1 limit biological processes in arid and semi-arid eco- mean annual wind velocity is 2.9 ms . To insure systems (Noy-Meir 1973). There is a growing appre- smooth operation of the Baotou-Lanzhou Railway in ciation that the magnitude of rainfall in these areas the sand dune area, a vegetation protective system was influences ecosystem processes, including C dynamics established along the railway line in 1956 by the Chinese (Bowling et al. 2011). The C release in desert BSCs is Academy of Sciences and related departments (Li et al. ultimately water-limited (Sponseller 2007;Groteetal. 2005). 2010). Because of low, unpredictable rainfall and their Establishment of the vegetation protective system proximity to the soil surface, desert BSCs are dry and involved an initial stage with a ‘‘sand barrier’’ made of inactive>90%ofthetime(Langeetal.1994). woven willow branches or bamboo to act as a wind- Therefore, they do not contribute to the C exchange break. Behind the sand barrier, straw checkerboards for much of the time (Wilske et al. 2008). Once wet- (1 m · 1 m) were established. The straw was inserted to a depth of 15–20 cm, so that it protruded approximately ted, BSCs immediately release CO2 through non- metabolic and metabolic pathways (Smith and Mo- 10–15 cm above the dune surface. These barriers re- lesworth 1973; Farrar and Smith 1976). Optimal wa- mained intact for 4–5 years, allowing time for xero- phytic plants to establish. During this period, a number ter levels can strongly stimulate CO2 release in BSCs (Belnap and Lange 2003;Huxmanetal.2004a, b). of native shrubs, including Peashrub Caragana korshin- Rainfall magnitudes and patterns in deserts also skii, Sagebrush Artemisia ordosica, and H. scoparium, influence C release (Huxman et al. 2004b). Responses were planted within the checkerboards. North of the of C release by desert plants (e.g., Sala and Lauren- railway line, a 500 m-wide protective belt was set up, roth 1982; Schwinning et al. 2002), soil microbial while on the south side, a 200 m-wide protective belt was communities (Austin et al. 2004), short grass steppes established; thus, the total length of the protective sys- (Munson et al. 2010), and hot desert ecosystems tem was 16 km. The vegetation in this system plays a (Sponseller 2007) to rainfall events are well docu- vital role in soil rehabilitation and production of this mented. However, there is still little information on desert ecosystem by stabilizing dune surfaces, preventing the effects of rainfall magnitude on C release from wind erosion and thus stabilizing the local desert eco- BSC-covered soil in temperate deserts (Belnap et al. system. In addition, surface BSCs have expanded to 2004;Lietal.2012). cover 60 % of the vegetation protection system during Inthere-vegetatedfixedsandduneareainthe the past 54 years (Li et al. 2005). Shapotou region of the Tengger Desert in China, moss, algal and mixed crusts are the three predomi- nant soil crust types. These crusts form a dense green Experimental design and carbon release measurements bio-carpet, covering large areas that amount to more than 95 % of the regional surface; they stabilize the We selected the four most frequent soil cover types in the mobile sand (Li et al. 2005, 2012). The present study 1956 re-vegetated area for measurement of C release rate was conducted in this region to answer three ques- from April to October in 2011 and 2012: (1) moss- tions: (1) How does C release amount vary with crusted soil (with more than 90 % moss crust cover), (2) different soil cover types? (2) How does rainfall algae-crusted soil (with more than 70 % algal crust), (3) magnitude influence C release amounts and patterns mixed (moss/algae/lichen)-crusted soil (with 45 % moss in different soil cover types? (3) How does C release crust, 45 % algal crust, and 10 % lichen crust), (4) from different soil cover types respond to extreme mobile dune sand (with no biological soil crust cover). rainfall events? Consistent with other deserts (Sala and Laurenroth 891
1982; Lauenroth and Bradford 2009), rainfall in this ration rate returned to the pre-rainfall level. Rainfall desert is small and brief ( £ 10 mm). Rainfall events of distribution in the Shapotou region during these exper- less than 10 mm magnitude account for 85 % of the imental periods is shown in Fig. 1. total annual rainfall frequency and 49 % of the annual To assess temporal variation in C release rates after rainfall amount; while 10–20 mm rainfall events account rainfall, we compared the rates measured at 9:00–10:00 for 11 % of the annual rainfall frequency and 30 % of am on different days. Additionally, a temperature cor- the annual rainfall amount, and rainfall events exceeding rection algorithm was used to standardize all measure- 20 mm account for 4 % of the total annual rainfall ments to 20 C, according to Parkin and Kaspar (2003): frequency and 21 % of the annual rainfall amount (Li et al. 2010). Thus, we defined seven rainfall magnitudes CO2 release rate at 20 C ¼ Rs Q ðÞ20 T =10 ð1Þ in this study: 0–1, 1–2, 2–5, 5–10, 10–15, 15–20, and where Rs was the measured CO2 release at a specific >20 mm. hour, T was the soil temperature at 5 cm-soil depth at the time Rs was measured, while Q was the Q10 obtained from laboratory incubations of different soil types at Sample collection and carbon release measurements different temperatures (5–35 C). For moss-, algae- and mixed-crusted soils, and MDS, these Q10 values were To avoid terrain and vegetation influences on crust determined to be 2.20, 1.88, 1.93, and 1.32, respectively. development, all samples were randomly collected from We first calculated the daily and hourly mean values undisturbed soil in the spaces between shrubs. Samples of C release amount during the measurement period, were collected in October 2010 using PVC tubes, with and then added these values to obtain the total C release 10.4 cm-inner diameter, and a height of 12 cm. All sam- amount from moss, algae, and mixed-crusted soils, and 2 ples had a surface area of 85 cm and a thickness of MDS for each rainfall magnitude. To avoid the effects of approximately 10 cm to ensure that active rhizines and continuous rainfall on cumulative C release calculations, organisms, as well as most of the surface soil organic we only used data from rainfall events when C release matter layer in the crust were included. The samples were rates returned to baseline before subsequent rainfall. taken to the nearby experimental station and randomly This resulted in 36 events (0–1 mm, n = 13; 1–2 mm, buried in soil (still in the PVC tubes), keeping the BSC n = 7; 2–5 mm, n = 6; 5–10 mm, n = 3; 10–15 mm, surfaces at the same level as the local soil surface. To keep n = 3; 15–20 mm, n = 2; and > 20 mm, n = 2). the test conditions close to those in the natural environ- Chlorophyll a and b concentrations were estimated ment, we maintained natural soil water and air cycles, and after sample collection in 2010. Pigments were extracted we kept the base of the PVC tubes open for drainage. with 98 % ethanol in a dimly lit room. The absorptions Post rainfall CO2 release rate in collected samples was of the extracted solutions were measured at wavelengths measured between April and October in 2011 and 2012, of 649 and 665 nm using a spectrophotometer (UV-1700 using a Li-6400-09 Soil Chamber (LI-COR, Lincoln, PharmaSpec, Japan). Concentrations were calculated NE, USA). Measurements were taken immediately after according to the following relationships (Chappelle et al. rainfall and repeated daily between 9:00 to 10:00, 14:00 1992; Hui et al. 2013): to 15:00 and 20:00 to 21:00 (GMT + 8) until the C re- ÀÁ lease rate returned to the pre-rainfall level. For each Chlorophyll a concentration lgcm 2 measurement, soil respiration rates were recorded at 4 s ¼ 12:7A665 þ 2:69A649 ÀÁ ð2Þ intervals over a 40 s period, once steady state conditions Chlorophyll b concentration lgcm 2 were achieved within the chamber. If the rainfall mag- ¼ 22:9A 4:68A ð3Þ nitude was less than 2 mm, then measurements were 649 665 taken immediately after rainfall, and repeated hourly where A649, and A665 were the absorption values at 649 (because sample surfaces dried rapidly) until the respi- and 665 nm, respectively.
Fig. 1 Rainfall distribution during the experimental periods from April to October in 2011 and 2012 in the Shapotou region of the Tennger Desert, northern China 892
Soil organic carbon (SOC) was measured using the fall magnitude. However, when the rainfall magnitude K2Cr2O7 method, which is described in the Agriculture exceeded 15 mm, C release amounts did not increase Chemistry Specialty Council, Soil Science Society of further in algae- or mixed-crusted soils. Similarly, no China (1983). difference in C release amount was observed between the 15–20 and >20 mm rainfall magnitudes in algae-crusted soil and MDS (Fig. 2; Table 4). Hence, there were dif- Statistical analysis ferences in C release amounts among crust types for different rainfall magnitudes. To test for significant effects of different soil cover type and rainfall magnitude on C release, we used a two-way ANOVA. The Duncan post hoc test was conducted when Temporal variation in carbon release amounts variances were equal, while Tamhane’s T2 test was car- ried out when variances were not equal. Nonlinear Following small (4.8 mm) to moderate (13.7 mm) rain- regression analyses were used to examine the relation- fall events, C release rates in all four types of BSCs ships between C release in soils with different cover types showed similar trends; namely a high C release rate and after different rainfall magnitudes. All of the AN- immediately following rainfall, followed by a gradual OVA and regression analyses were performed using the decrease. However, immediately following heavy rainfall SPSS 16.0 statistical software (SPSS Inc., Chicago, IL, events (44.9 mm), moss-crusted soils had higher C re- 2 1 USA). lease rates (0.95 ± 0.02 lmol CO2 m s ) than algae- and mixed-crusted soils, and MDS, with rates of 0.30 ± 0.03, 0.13 ± 0.04, and 0.51 ± 0.02 lmol CO2 Results m 2 s 1, respectively. The C release rate for moss-crus- ted soils showed a gradually decrease after heavy rainfall Carbon release amount in the four soil cover types events. Algae- and mixed-crusted soils, on the other hand, first showed a gradual increase and then decrease Contributions to mean C release amount differed sig- in C release after heavy rainfall. The highest C release nificantly among soil cover types: it was highest for rates from algae- and mixed-crusted soils occurred on moss-crusted soil, and lowest for MDS. The C release the sixth day following heavy rainfall. Hence, for all amount ranged from 0.13 ± 0.09 to 15.2 ± 1.36 gC rainfall magnitudes, different soil crust types can be m 2 in moss-crusted soil, which was significantly higher ordered from highest to lowest C release rates, as fol- than in all other soil cover types. While the C release lows: moss-crusted soils > mixed-crusted soils > amounts ranged from: 0.08 ± 0.06 to 6.43 ± 1.23 gC algae-crusted soils > MDS (Fig. 3). m 2 in algae-crusted soil; 0.11 ± 0.08 to 8.01 ± Using the two-way ANOVA, the model variables ex- 0.50 gC m 2 in mixed-crusted soil; and 0.06 ± 0.04 to plained 98.9 % of the variation in C release rate. Both soil 8.47 ± 0.51 gC m 2 in MDS. The C release amounts cover type and rainfall magnitude had significant effects from all soil cover types increased with increasing rain- on the C release amount (FBSC = 497.756, p < 0.001; FRainfall = 616.552, p < 0.001; FBSC · Rainfall = 26.375, p < 0.001; Table 1). Nonlinear regression analyses sug- gested significant correlations between rainfall magnitude and C release. The fitted models accounted for a sub- stantial part of the variation in soil respiration rates (rainfall magnitude explained more than 95 % of C re- lease in moss-crusted soils and MDS, more than 90 % in algae-crusted soils, and more than 85 % in mixed-crusted soils; Table 2).
Chlorophyll a + b concentration and SOC content
Our study showed that moss-crusted soil had signifi- cantly higher chlorophyll a and b concentration (3.81 ± 0.42 lgcm 2) than algae- and mixed-crusted soils, with concentrations of 2.07 ± 0.31 and 2.90 ± Fig. 2 The contribution of rainfall magnitudes (0–1 mm, n = 13; 0.22 lgcm 2, respectively. Moss-crusted soil also had 1–2 mm, n = 7; 2–5 mm, n = 6; 5–10 mm, n = 3; 10–15 mm, significantly higher SOC content (9.53 ± 1.52 g kg 1) n = 3; 15–20 mm, n = 2; >20 mm, n = 2) to carbon release rate 2 than and mixed-crusted soils, and MDS, with contents (gC m ; mean ± SE) in different soil cover types: moss- (MOCS), 1 algae- (ACS), and mixed-crusted soils (composed of moss, algae, of 5.74 ± 0.81, 6.61 ± 1.07, and 3.24 ± 0.73 g kg , and lichen; MICS), and mobile dune sand (MDS), respectively respectively (Table 3). 893