The responses of soil respiration to environmental conditions have been studied extensively in various ecosystems. However, little is known about the impacts of temperature and moisture on soils respiration under biological soil crusts. In this study, CO2 efflux from biologically-crusted soils was measured continuously with an automated chamber system in Ningxia, northwest China, from June to October 2012. The highest soil respiration was observed in lichen-crusted soil (0.93±0.43 µmol m−2 s−1) and the lowest values in algae-crusted soil (0.73±0.31 µmol m−2 s−1). Over the diurnal scale, soil respiration was highest in the morning whereas soil temperature was highest in the midday, which resulted in diurnal hysteresis between the two variables. In addition, the lag time between soil respiration and soil temperature was negatively correlated with the soil volumetric water content and was reduced as soil water content increased. Over the seasonal scale, daily mean nighttime soil respiration was positively correlated with soil temperature when moisture exceeded 0.075 and 0.085 m3 m−3 in lichen- and moss-crusted soil, respectively. However, moisture did not affect on soil respiration in algae-crusted soil during the study period. Daily mean nighttime soil respiration normalized by soil temperature increased with water content in lichen- and moss-crusted soil. Our results indicated that different types of biological soil crusts could affect response of soil respiration to environmental factors. There is a need to consider the spatial distribution of different types of biological soil crusts and their relative contributions to the total C budgets at the ecosystem or landscape level.
Citation: Feng W, Zhang Y, Jia X, Wu B, Zha T, Qin S, et al. (2014) Impact of Environmental Factors and Biological Soil Crust Types on Soil Respiration in a Desert Ecosystem. PLoS ONE9(7): e102954. https://doi.org/10.1371/journal.pone.0102954
Editor: Xiujun Wang, University of Maryland, United States of America
Received: November 18, 2013; Accepted: June 25, 2014; Published: July 22, 2014
Copyright: © 2014 Feng et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This research was fund by the National Key Technology Research and Development Program of China for 12th Five-year Plan (2012BAD16B02) and the National Natural Science Foundation of China (31170666). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Soil respiration (Rs) accounts for the second largest carbon flux between terrestrial ecosystems and atmosphere, after gross primary productivity. Physical (e.g., soil temperature, moisture) and biological factors (e.g., microbial community) affecting Rs should be taken into consideration in order to accurately estimate global carbon balance . However, we have limited knowledge on the biophysical controls of Rs in dryland ecosystems. Drylands cover 41–47% of the terrestrial surface . Biological soil crusts (BSCs) as a biological factor commonly cover 70% of the inter-canopy earth in dryland and are found in all ecosystems around the world . BSCs consist of algae, lichen, moss, fungi, cyanobacteria, and bacteria and cover the top few millimeters of the soil surface , . However, knowledge about the role of BSCs as a modulator of Rs is still lacking –. It is important to study the effects of environmental factors, such as temperature and moisture, on Rs under BSCs. This knowledge can reduce bias in ecosystem-level estimation of Rs and can help us predict how climate changes will affect CO2 flux in desert ecosystems.
BSCs are an integral part of the soil system in arid regions worldwide . Rs studies in relation to BSCs have drawn much attention in the past decade . In the Gurbantunggute desert, the mean Rs of cyanobacteria/lichen-crusted soil is significantly higher than that of bare land after 15 mm rainfall . In Kalahari sand, the CO2 flux of cyanobacteria-crusted soil is lower than that of disturbed crusted soil . In the Iberian Peninsula, lichen-crusted soils are the main contributor to Rs . In the Mu Us desert, Rs does not differ between BSC-dominated areas and bare land . However, the limited knowledge about the role of BSCs as a modulator of Rs on C cycle merely focused on particular species or communities. Although those have provided valuable insights on the effects of BSCs on C fluxes, in-situ data remain rare and we have incomplete understanding of the impact of different types of BSCs on Rs.
Soil temperature (Ts) and soil water content (VWC) are the key environmental factors responsible for variation in Rs . Ts is the major control of Rs through its influence on the kinetics of microbial decomposition, root respiration, and the diffusion of enzymes and substrate . VWC controls the decomposition of soil organic matter, root respiration, and microbial actively , . Ts and VWC were been predicted to increase at global scales in the following decades . In order to assess the impact of the changing climate on ecosystem C flux, quantification of the effects of Ts and VWC on Rs is needed. Recent studies have shown that diurnal variations in Rs are usually highly correlated with temperature of the surface soil layers , . However, a few studies have reported a hysteresis effect and a decoupling between Rs and soil surface temperature during drought conditions in boreal forests , tropical forests , Mediterranean ecosystems , and desert ecosystems . Low water content may increase the degree of hysteresis between Rs and Ts , ,  or, in some cases, may reduce it . At the seasonal scale, Rs is also highly correlated with changes in Ts when water content is not limited , , . Strong inhibition of Rs has often been observed when soil water content is low . All those are mainly focused on shrub soils or bare-land soils. However, our ability to capture the effects of environmental factors on Rs in biologically-crusted soil is still lacking.
Understanding of how biologically-crusted soil types and environmental factors influence Rs in a desert ecosystem, we measured Rs in algae-, lichen-, and moss-crusted soil in the Mu Us Desert, northwestern China. The specific objectives of this study were: (1) to examine and compare the temporal variability of Rs in three crusted soils; (2) to determine seasonal and diurnal patterns of Rs; and (3) to assess the contributions of the three crusted soils to the amount of C released by Rs at the ecosystem level.
Materials and Methods
2.1 Ethics Statement
The study site is owned by Beijing Forestry University. The field work did not involve any endangered or protected species, and did not involve destructive sampling. Specific permits were required for the described study.
2.2 Site description
The research was conducted at the Yanchi Research Station (37°04′ to 38°10′ N and 106°30′ to 107°41′ E, 1550 m a.s.l.), Ningxia, northwest China. The area is located in the mid-temperate zone and characterized by a semiarid continental monsoon climate. The mean annual temperature is 8.1°C, the mean annual rainfall is 292 mm, 62% of which falls between July and September. The mean annual potential evaporation is 2100–2500 mm. All meteorological data were provided by the meteorological station of Yanchi County and represent 51 year averages (1954–2004). The vegetation in the area is dominated by Artemisia ordosica. The soil surface of inter-canopy is commonly covered by algae, lichen, and moss crusts, which are mainly composed of Microcoleus vaginatus, Oscillatoria chlorine, Collema tenax, and Byumargenteum, respectively , . The physical and chemical characteristics of the three crusted soils are shown in Table 1. The soil of the area is aripsamment with 1.61 g cm−3 in soil bulk density.
2.3 Soil respiration measurements
Continuous measurements of soil surface CO2 efflux (Rs) were made in an open area at Artemisia ordosica shrub land with intact algae, lichen and moss crusts between June and October in 2012. An automated soil respiration system (Model LI 8100A fitted with a LI-8150 multiplexer, LI-COR, Nebraska, USA) was used to measure Rs. Three permanent PVC collars (20.3 cm in diameter, 10 cm in height, inserted ∼7 cm) were separately installed in intact algae-, lichen- and moss-crusted soil in March 2012, three months before the start of measurements. A permanent opaque chamber (model LI-104, LI-COR, Nebraska, USA) was set on each collar. The measurement time for each chamber was 3 min and 15 s, including a 30 s pre-purge, a 45 s post-purge, and a 2 min observation period. Hourly Ts and VWC at 5-cm depth were measured near the chamber using an 8150-203 temperature sensor and an ECH2O soil moisture sensor (Li-COR, Nebraska USA), respectively. During observation, any plants re-growing within collars were manually removed. Rainfall was measured near the chamber by a manual rain gauge and a tipping-bucket rain gauge (model TE525MM, Campbell Scientific, UT, USA). Half-hourly incident photosynthetically active radiation (PAR) was measured using a quantum sensor (PAR-LITE, Kipp & Zonen, The Netherlands) near the chambers.
2.4 Data treatment and analysis
The CO2 efflux values greater than 15 µmol m2 s−1 or less than -1 µmol m2 s−1 were considered abnormal and removed from the dataset. Instrument failure, sensor calibration, and poor-quality measurements together resulted in the loss of 4% to 5.4% of the values for three chambers from June to October 2012 (Fig. 1).
To avoid including the impacts of photosynthesis and Birch effects on the seasonal responses of Rs to Ts and VWC, certain observations were removed from the dataset. (1) Daytime (photosynthetically active radiation, PAR >5 µmol m−2 s−1) CO2 efflux values were removed to ensure that no photosynthesis effects were included. (2) Measurements recorded immediately (within 30 min) after a rain event were excluded because they were potentially affected by the rewetting of the upper soil layers, which could stimulate respiration , . The daily mean nighttime value (Rs, Ts, and VWC) was computed as the average of the hourly values when PAR was below 5 µmol m−2 s−1. Daily mean nighttime values were used to examine the seasonal responses of Rs to Ts and VWC. The seasonal relationships between Rs and Ts were estimated using four common models: Exponential (Q10), Arrhenius, Quadratic, and Logistic (see Table 2). The four models were fitted separately for each crusted soil. Root mean square error (RMSE) and the coefficient of determination (R2) were used to evaluate model performance. Temperature-normalized daily mean nighttime Rs (RsN), calculated as the ratio of the observed nighttime Rs to the value predicted by the Q10 model, was used to analyze the seasonal dependence of daily mean nighttime Rs on VWC. Three bivariate models with Ts and VWC as independent variables were developed to show the combined effect of both variables (Table 3).
To ensure that the measurements of diurnal responses of Rs to Ts and VWC were not affected by photosynthesis, CO2 flux measurements taken within two days after a significant rain event (>10 mm) were removed from the dataset. Field observation revealed that the water content of BSCs layers decreased to the water compensation point of photosynthesis within two days after the last significant rain event (>10 mm) in all three crusted soils , . The mean diurnal courses of Rs, Ts, and VWC were computed for each month by averaging the hourly means for each time of day. Cross-correlation analysis was used to detect hysteresis between Rs and Ts at the diurnal scale. Correlation analysis was used to evaluate the relationship between Rs and Ts (Table 4). All analyses were processed in Matlab 7.11.1 (R2010b, the Mathworks Inc., Natick, MA, USA).
To examine whether daily mean nighttime Rs, Ts, and VWC differed among biologically-crusted soils, we used a two-way (biologically-crusted soil types and time) ANOVA, with repeated measures of one of the factors (time). The environmental factors show relatively small variation within three days. Thus, we selected consecutive three-day periods as the three replication for statistical requirements. When significant biologically-crusted soils effects were found (P<0.05), the Tukey HSD post hoc test was employed to evaluate differences between biologically-crusted soil types. Prior to these analyses, data were tested for assumptions of normality and homogeneity of variances and were log-transformed when necessary. All the ANOVA analyses were performed using the SPSS 15.0 statistical software (SPSS Inc., Chicago, Illinois, USA).
3.1. Hysteresis between Rs and Ts
Over the course of the diurnal period, Rs (µmol m−2 s−1) reached its minimum at 6:00 and peaked at around 10:00–11:00 (Fig. 2), and Ts arrived at its minimum at 7:00–8:00 and peaked at 16:00 in the three crusted soils. The diurnal variation of Rs was out of phase with Ts, causing hysteresis between Rs and Ts. The maximum mean lag time between Rs and Ts was 5 h in June in moss-crusted soil, and the minimum mean lag time was 1 h in August in lichen-crusted soil, with Rs peaking earlier than Ts (Table 4). The degree of hysteresis was small in lichen-crusted soil, and large in moss-crusted soil (Table 4). The lag time between Rs and Ts was negatively and linearly correlated with VWC in crusted soil (Fig. 3). The lag time was reduced as VWC increased. The r values, derived from the data set with synchronized Rs and Ts, were higher than that without synchronization (Table 4).
Each point is the monthly mean for a particular time of day.
3.2. Seasonal variation in Rs, Ts, and VWC
Similar changes in daily mean Ts, VWC, and CO2 flux (including both daytime and nighttime data) were detected in algae-, lichen-, and moss-crusted soils (Fig. 1). Daily mean Ts was high from June to August, after which it gradually declined (Fig. 1A). No differences were observed in the daily mean nighttime Ts between algae- (18.15±5.61°C, mean ± standard deviation, SD) and lichen-crusted soil (18.14±7.13°C). However, daily mean nighttime Ts in moss-crusted soil (17.45±5.56°C) was significantly lower than that in algae- and lichen-crusted soil (df = 2, F = 11.92, P = 0.013). Daily mean VWC sharply increased after each precipitation pulse (Fig. 1B). Daily mean nighttime VWC ranged from 0.049 to 0.14 m3 m−3, 0.057 to 0.16 m3 m−3, and 0.046 to 0.19 m3 m−3 in algae-, lichen-, and moss-crusted soil, respectively. Daily mean nighttime VWC was significantly higher in lichen-crusted soil (0.104±0.026 m3 m−3) than in algae- and moss-crusted soils (0.083±0.015 m3 m−3 and 0.089±0.026 m3 m−3, respectively) (df = 2, F = 251.91, P<0.001). Daily mean CO2 flux varied markedly following the changes in Ts and VWC, especially after a rain pulse. Daily mean CO2 flux peaked in late July and then generally declined following the decrease in Ts (Fig. 1C). The limiting effect of VWC on CO2 flux was clear as CO2 flux reached its highest value in a quick, sharp response to each rain event and then decreased to pre-rain values (Fig. 1B, C). Daily mean nighttime Rs was significantly different in three crusted soils (df = 2, F = 56.69, P<0.001) with the highest values in lichen-crusted soil (0.93±0.43 µmol m−2 s−1) and lowest values in algae-crusted soil (0.73±0.31 µmol m−2 s−1).
Daily mean nighttime Rs was positively related to Ts when VWC was higher than 0.075 m3 m−3 in moss-crusted soil and 0.085 m3 m−3 in lichen-crusted soil (Fig. 4). There were no differences among the four temperature-response models examined (Table 2). Ts at the5-cm depth explained 82%, 74%, and 51% of the seasonal variation of daily mean nighttime Rs when VWC was not a limiting factor in algae-, lichen-, and moss-crusted soil, respectively (Table 2). In algae-crusted soil, however, Rs was controlled by Ts below the VWC threshold value (Table 2). As no differences were observed among the temperature-response models, the remainder of the analysis was performed using the Q10 model. Over the study period, daily mean nighttime Rs normalized using the Q10 model with Ts at 5 cm depth (RsN) increased with VWC, except in algae-crusted soil (Fig. 5).
RsN is the ration of the observed soil respiration (Rs) value to the value predicted by the Q10 function. The solid line is fitted using linear regression.
The seasonal sensitivity of Rs to Ts (parameter b from the Q10 model in Table 2) were 2.01, 2.13, and 1.97 in algae-, lichen-, and moss-crusted soil, respectively. The long-term basal respiration rate at 10°C (Rs10, parameter a from the Q10 model in Table 2) for these same soils was 0.38, 0.46, and 0.55 µol m−2 s−1.
The bivariate model Q10-hyperbolic with Ts and VWC as independent variables produced higher R2and lower RMSE values than the other models in lichen- and moss-crusted soil (Table 3). There was no significant difference observed between the temperature-only and the bivariate model in algae-crusted soil (Table 3), and the estimated total C release calculated with the Q10 model and gap-filled Ts was 123.22 g C m−2 in algae-crusted soil (Table 3). The estimated total Rs, as computed using theQ10-hyperbolic model and gap-filled Ts and VWC, was 165.39 and 147.08 g C m−2 over the study period in lichen- and moss-crusted soils, respectively. Lichen-crusted soil was the main contributor to this flux among crusted soils during the study period.
4.1. Interactive effects of Ts and VWC on Rs
Over the course of the diurnal cycle, there was a significant hysteresis between Rs and Ts (Table 4, Fig. 2). Diurnal hysteresis has been observed in many other ecosystems –, ,  and is affected by many physical and biological processes, such as mismatch between the depth of temperature measurement and the depth of CO2 production, photosynthetic carbon supply for diurnal Rs , wind-induced pressure pumping , and different responses of autotrophic and heterotrophic respiration to environmental factors . We observed that the lag time between Rs and Ts was negatively related to VWC in the three crusted soils, which is consistent with the finding from the Mu Us desert . The increased lag time at low VWC in crusted soils was mainly due to the decoupling of Rs from Ts when VWC is low, and which indicate the sensitivity of root and microbial activity to soil moisture. The timing of the diurnal Rs peak is highly sensitive to VWC, with progressively earlier peaks as the VWC reduces. At low VWC, Rs peaks in the early morning due to root and microbial activity may strongly increased with condensation water, resulting to significant hysteresis between Ts and Rs (Fig. 2, Table 4) .
The seasonal changes in daily mean nighttime Rs were mainly controlled by Ts (Table 2, Fig. 4). The four temperature-only models performed well with the same R2. Ts explained 74% and 53% of the variation in Rs when VWC was above 0.085 and 0.075 m3 m−3 in lichen- and moss-crusted soil, respectively, but it was uncorrelated with Rs when VWC fell below those thresholds (Table 2). Our observations are in line with those of previous studies in many other ecosystems , , , . Wang et al.  reported that Ts explained 76% of the variation in Rs for VWC values above 0.08 m3 m−3, but it was uncorrelated with Rs when VWC fell below 0.08 m3 m−3. Castillo-Monroy et al.  found that Rs was controlled by Ts when soil moisture was higher than 11% in microsites dominated by BSCs. Below this level, Rs was driven by soil moisture alone. The decreased Rs under low VWC was limited by reduced microbial contact with the available substrate, dormancy and/or death of microorganisms, and substrate supply, which was affected by reduced photosynthesis and drying out of the litter in the surface layer , .
RsN increased with VWC and did not show a threshold value in moss- and lichen-crusted soils during the seasonal cycle. Our observation contrasts with the results of previous studies that found a distinct VWC threshold . The difference mainly resulted from low VWC (0.04–0.16 m3 m−3) and high soil porosity did not limit CO2 transport out of soil and CO2 production due to a lack of O2.
4.2. Differences in Rs among biologically-crusted soil types
Daily mean nighttime Rs was significantly different in three types of crusted soils (algae-, lichen- and moss-crusted soil) (df = 2, F = 56.69, P<0.001) with the highest values in lichen-crusted soil and lowest values in algae-crusted soil. This result contrasts with those of other studies in desert ecosystems. Su et al.'s  study of Gurbantunggute Desert reported no differences in carbon flux between moss- and lichen/cyanobacteria-crusted soil. The differences in the present study can be explained by the following aspects. It is possible that the lowest Rs in algae-crusted soil resulted from the differences in soil fertility induced by BSCs, total N was significantly lower in algae-crusted soil (0.17±0.09 g kg−1) than in lichen- (0.23±0.08 g kg−1) and moss-crusted soil (0.28±0.13 g kg−1) (unpublished data). In addition, the assemblage of microbial and microfaunal organisms varied in the three crusted soils , . The observation of the highest values occurred in lichen-crusted soil was in line with the result conducted in dry condition in the Mu Us desert. The highest values in lichen-crusted soil is mainly due to highest water content and total porosity of lichen layer .Ts was significantly lower in moss-crusted soil than in algae- and lichen-crusted soil (Fig. 1). This result is attributed to the darkening of the surface by cyanobacteria and lichens, resulting in greater absorption of solar radiation and a higher surface temperature . VWC in lichen-crusted soil was consistently significantly higher than in moss- and algae-crusted soils (Fig. 1). The difference may be attributed to higher dew deposition (soil moisture input by dewfall can be an important mechanism in dryland environment) and water infiltration in lichen-crusted soil than in moss- and algae-crusted soil .
The lag time between Rs and Ts differed depending on the type of crusted soil, suggesting that the response of species in biologically-crusted soils to VWC was different among crusted types. The timing of the diurnal Rs peak is highly sensitive to VWC, with progressively earlier peaks as the soil VWC declines . Moss crusts need more VWC than lichen and algae crust to achieve metabolic activity . In water stressed ecosystems, algae and lichen can utilize dew and light rainfall that moss are unable to use , . Thus the diurnal Rs in moss-crusted soil peaks earlier than algae- and lichen-crusted soils, which lead to significant hysteresis between Rs and Ts in moss-crusted soil. Hysteresis had a smaller impact on lichen-crusted soil than on algae-crusted soil. The result may be partly attributed to the higher water level in lichen- than in algae-crusted soil.
The average Q10 of 1.83 from three biologically-crusted soil types from June to October is at the lower end of the range of 1.28 to 4.75 from alpine, temperate, and tropical ecosystems across China . The low Q10 value is attributed to their low levels of soil organic matter, small microbial community, and dry soil conditions , , .The Q10 of algae-, lichen-, and moss-crusted soil was 1.98, 1.98, and 1.54, respectively. The majority of C associated with BSCs, in the forms of microbial biomass or their secretions , , is close to or at the soil surface and is directly in contact with small precipitation or dew captured by algae and lichen crusts. However, small amounts of hydration cannot directly reach the soil surface because the soil is covered with moss. The relatively small amounts of hydration in moss-crusted soils result in the lower Q10 , , , .
The effects of VWC and Ts on Rs should be considered in carbon cycle models in moss- and lichen-crusted soils. However, we did not find any effect of VWC on daily mean nighttime Rs in algae-crusted soil from June to October 2012 (Tables 2, 3). This observation coincided with the result that RsN was independent of VWC in algae-crusted soil. The independence of VWC from Rs in algae-crusted soil may be attributed to the low water requirement of algae for active metabolism , . Even a very small hydration event, such as water vapor and dew in the early morning, is sufficient to allow algae to achieve microbial metabolism. Further examination is needed to justify our conclusion regarding the role of VWC on algae-crusted soil due to the dew data gap. We used the Q10-hyperbolic model, with Ts and VWC as independent variables, to predict changes in Rs. Using Q10-hyperbolic model to predict Rs was also reported in a boreal trembling aspen stand .
Using temperature-only and Q10-hyperbolic model, we obtained an approximate estimate of the total amount of C released at each crusted soil via soil respiration of 123.2, 165.4, and 147.1 g C m−2 over 5 months studied in algae-, lichen- and moss-crusted soils, respectively. Lichen-crusted soil was the main contributor to the total C released by Rs. We found that total C released by Rs in lichen-crusted soil was 2.5% higher than the mean total C released by Rs (161.4 g C m−2, unpublished data) over 5 months, whereas total C released by Rs in algae- and moss-crusted soil were 23.65% and 8.87% smaller than the mean total C released by Rs, respectively. Our results show the importance of BSCs as modulators of Rs in the C release and indicate that we should not ignore their relative contributions to the total C budgets in desert ecosystems.
Our study showed that Rs was significantly different in three crusted soils with highest values in lichen-crusted soil and lowest values in algae-crusted soil. Lichen-crusted soil was the main contributor to the total C released by Rs. Over the diurnal cycle, Ts exerted dominant control over Rs in the three crusted soils. There was a significant lag between Ts and Rs over the diurnal cycle, and that the lag time increased as VWC decreased. Over the seasonal scale, the response of Rs to Ts was regulated by VWC, and Rs was uncorrelated with Ts when VWC dropped below 0.075 and 0.085 m3 m−3 in lichen- and moss-crusted soils, respectively. However, VWC was not a limiting factor on Rs in algae-crusted soil. Our results indicated that different types of BSCs may affect response of Rs to environmental factors. There is a need to consider the spatial distribution of different types of BSCs and their relative contributions to the total C budgets at the ecosystem or landscape level.
We thank Su Lu, Huishu Shi, Yuming Zhang, Xuewu Yang for their assistance with the field measurements and instrumentation maintenance. We are grateful to the anonymous reviewers and the Academic Editor for providing insightful comments and suggestions. We also thank language service company for their help with language revision, and valuable comments to the manuscript.
Conceived and designed the experiments: WF YZ BW TZ SQ XJ CS. Performed the experiments: SQ WF BW KF. Analyzed the data: WF SQ XJ BW. Contributed reagents/materials/analysis tools: YZ BW TZ XJ BW JL KF. Wrote the paper: WF YZ BW XJ SQ. Designed the software used in analysis: XJ.
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