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Fine-root distribution, production, decomposition, and effect on soil organic carbon of three revegetation shrub species in northwest China
Forest Ecology and Management 359 (2016) 381–388
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Fine-root distribution, production, decomposition, and effect on soil organic carbon of three revegetation shrub species in northwest China q Zongrui Lai a, Yuqing Zhang a,b,⇑, Jiabin Liu c, Bin Wu a,b, Shugao Qin a,b, Keyu Fa a a
Yanchi Research Station, School of Soil and Water Conservation, Beijing Forestry University, Beijing 100083, China Key Laboratory of Soil and Water Conservation and Desertification Combating, Beijing Forestry University, Ministry of Education, Beijing 100083, China c School of Natural Resources and Environment, Northwest A & F University, Yangling, Shaanxi 712100, China b
a r t i c l e
i n f o
Article history: Received 21 December 2014 Received in revised form 16 April 2015 Accepted 23 April 2015 Available online 16 May 2015 Keywords: Artemisia ordosica Carbon sequestration Decomposition Hedysarum mongolicum Light fraction soil organic carbon Salix psammophila
a b s t r a c t Revegetation with xerophilous shrubs is an effective approach to combat desertification in northwestern China; however, evaluation studies on fine-root properties of shrubs and soil organic carbon are limited. To gain a better understanding of revegetation practices, we investigated the vertical distribution of fine-root biomass, necromass, production, and effect on soil organic carbon (SOC) content in three shrub species (Salix psammophila, Hedysarum mongolicum, and Artemisia ordosica). In addition, we also estimated the fine root decomposition rate with litterbag techniques. The results showed that revegetation practices resulted in a significant increase in SOC content. Over a 10 year period of revegetation, the SOC content in S. psammophila, H. mongolicum, and A. ordosica plots increased by 0.87, 1.07, and 1.82 times, respectively, more than that in bare-land plot. Increase in total SOC content was mainly due to increase in light-fraction SOC, except for the A. ordosica plot. Variations in the short-term increase of SOC content after revegetations with the three shrubs on sand land might be explained by fine root decomposition rates, at least in part. A. ordosica may be a better species for SOC accumulation and sequestration in the study site. Additionally, fine-root biomass and production were not associated with more SOC content increase in shrub plots. The results suggest the mechanism of SOC accumulation and sequestration differed among shrub plots and highlight the effectiveness of different shrub species as revegetation materials in terms of SOC accumulation and sequestration. Ó 2015 Elsevier B.V. All rights reserved.
1. Introduction China has been severely impacted by desertification, which is widely recognized as a significant environmental problem that increasingly threatens human survival and development (Gao et al., 2012). Revegetation that has been used extensively in northwestern China since the 1980’s, is one of the most effective and sustainable means to control desertification and rehabilitate degraded land (Zhang et al., 2009). Salix psammophila, Hedysarum mongolicum, and Artemisia ordosica are considered as excellent fixed-dune species due to their high adaptability to arid and infertile areas affected by wind erosion. Currently, these three shrub species are dominant in desert plant communities of northwestern China, particularly in the Mu Us Desert. Although their distribution patterns (Chen et al., 2002), water-use efficiency (Yang et al., q
This article is part of a special section entitled ‘‘Forests, Roots and Soil Carbon’’.
⇑ Corresponding author at: School of Soil and Water Conservation, Beijing Forestry University, 35 Qinghua Eastroad, Haidian District, Beijing 100083, China. Tel.: +86 10 62336172; fax: +86 10 62338689. E-mail address: [email protected] (Y. Zhang). http://dx.doi.org/10.1016/j.foreco.2015.04.025 0378-1127/Ó 2015 Elsevier B.V. All rights reserved.
2008), effects on soil nutrients, and other environmental benefits (Gao et al., 2014) have been studied extensively, information on their root properties and effects on soil carbon (C) is limited. Root systems fulfill important functions in nutrient uptake and C exchange in terrestrial ecosystems, thus they play an important role in biogeochemical cycling (Trumbore and Gaudinski, 2003). The belowground part of plants is considered to be a major C pathway to soil and significantly contributes to belowground C cycle (Chapin III and Ruess, 2001). In addition, it is known that the root system influences soil microbial activity and decomposition processes (Janssens et al., 2002). Fine roots (<2 mm) are an ephemeral part of the root system and have faster turnovers, as well as higher metabolic activity compared to lower-order roots (Pregitzer et al., 2002; McCormack et al., 2013). Although fine roots constitute a small proportion (<5%) of total standing root biomass in many terrestrial ecosystems (Gill and Jackson, 2000), it is estimated that 33% of global net primary production is consumed for fine-root growth, respiration, and turnover (Jackson et al., 1997). Fine roots are also the major sites of infection by mycorrhizal fungi, which affect a wide
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range of soil physicochemical and biological properties, including soil structure and nutrient content (Strand et al., 2008). Although mycorrhizal colonization, root exudation, and soil properties significantly affect soil organic carbon (SOC) content (Matamala et al., 2003), fine roots are the dominant pathways through which C enters the soil organic matter (SOM) pool (Jackson et al., 1997), and their structure and functional processes have an impact on SOC stocks and dynamics (Ferguson and Nowak, 2011). Therefore, information on the properties and dynamics of fine roots is essential for understanding the biogeochemical processes in terrestrial ecosystems (Pregitzer et al., 2002; Strand et al., 2008; Upson and Burgess, 2013). Fine-root properties and dynamics may play a key role in nutrient cycle and soil C sequestration (Chang et al., 2012; Upson and Burgess, 2013) in forest ecosystems (Matamala et al., 2003); for instance, fine-root biomass and vertical distribution potentially influence long-term changes in SOC content (Ferguson and Nowak, 2011; Asaye and Zewdie, 2013), while higher rates of fine-root production lead to higher C inputs to soil (Stover et al., 2010). Recent studies showed that spatial heterogeneity of SOC was positively correlated with the vertical distribution of fine roots (Beniston et al., 2014) and also soil C with fine-root biomass and C across all depth intervals (Liao et al., 2014). In addition, it is known that fine-root production and turnover directly impact biogeochemical cycle of C in terrestrial ecosystems (Matamala et al., 2003), while fine-root productivity may be similar in magnitude to foliar productivity (Norby et al., 2004). The presence of root scars indicates that fine roots are ephemeral root modules, which shed like leaves and serve as source of C for soil (Pregitzer et al., 2002). Previous studies showed that approximately 30–80% of SOC content is provided through the rapid turnover and decomposition of fine roots (Ruess et al., 2003) and variation in SOC stocks mainly depends on fine-root decomposition rates influenced by genetic and environmental factors (Lemma et al., 2007; Hobbie et al., 2010). Therefore, a study of fine-root properties is essential for a detailed understanding of their role as a source of litter and C storage in soil. Compared to the moist ecosystems, fine roots comprise a higher proportion of total plant biomass in the drylands (Jackson et al., 1997; Zhang et al., 2009), probably because of the increased allocation of C to root system due to relatively low nutrient availability in soil (Clark et al., 2010). Fine roots, which act as a conduit for the transport of C into the SOM pool (Strand et al., 2008), may play a key role in the accumulation of SOC in the drylands (Nosetto et al., 2006); therefore, additional information on fine-root properties is critical for a better understanding of the belowground C cycle. Previous studies focused either on fine roots (Huang et al., 2008; Cheng et al., 2009) or on SOC content (Li et al., 2012) in revegetation areas of northwest China; however, few studies have assessed the fine-root properties and dynamics, total SOC content and its fractions following revegetation. In this study, we investigated the vertical distribution of the fine root biomass, necromass, production, and SOC content in three shrub species (A. ordosica, H. mongolicum, and S. psammophila) in order to gain a better understanding of revegetation practices. Our specific objectives were to (1) estimate fine-root properties, including fine root biomass, distribution, production and decomposition; and (2) detect the effect of fine roots on SOC content; and (3) elucidate the variation in SOC stocks based on fine-root properties rate in three revegetation shrub species. 2. Materials and methods 2.1. Study site description The study was conducted at the Yanchi Research Station (37°6 80 N–37°730 N, 107°200 E–107°260 E; 1530 m a.s.l), in Ningxia
Province, northwestern China. The study site is located at the south edge of the Mu Us Desert and has a semiarid continental monsoon climate. The average annual temperature is 8.1 °C (1954–2014) and the frost-free period lasts from April to November and is 156 days on average (Feng et al., 2013). Rainfall occurs mainly from July through September with average annual precipitation being approximately 287 mm (Jia et al., 2014). The soil texture of the study area is sandy in the 0–1-m profile and average soil bulk density is 1.5 g m3. In 2001, H. mongolicum and A. ordosica were randomly established with aerial seeding and S. psammophila was planted using cuttage (row spacing of 4 m) on stabilized sand dunes. After revegetation, shrub plots were fenced, grazing was prohibited, and no fertilizer was applied since then. Although S. psammophila was planted using cuttage, disturbances were limited to plot preparation. Overall, human and wild-animal disturbances in shrub plots were rare. Soil type and micro-physiographic conditions were similar among shrub plots (Table 1). Plots were relatively flat with a slope of 1.0–3.0°. 2.2. Fine-root biomass and necromass determination Fine roots were sampled with a steel bucket-type soil auger (8.5-cm-diam. bucket auger with 25 cm height) with T-handle in September 2011. Three plots of 30 m 30 m were established at the research area, one for each species (S. psammophila, H. mongolicum, and A. ordosica). Each plot of A. ordosica and H. mongolicum was divided into 36 subplots of 5 m 5 m and a total of 72 randomly selected soil cores (36 subplots 2 shrub species) were collected. The distance between cores and shrubs ranged approximately from 0.1 to 0.5 m and 0.05 to 0.2 m, respectively, in A. ordosica and H. mongolicum plots, and were 0.5, 1.0, 1.5 and 2.0 m from shrubs in S. psammophila plots. Fine-root samples were collected at depth intervals of 0–20, 20–40, 40–60 and 60–80 cm. The uppermost 0–20 cm layer consisted of humus in all cases and the thickness of organic layers ranged from 0 to 0.5 cm. Four soil cores collected at the same depth were mixed in order to ensure a good representation of fine roots in each sample. In total 52 soil cores were collected to create 13 soil samples for the determination of fine-root biomass. All soil samples were sieved through a three metal-sieve stack with different pore sizes (2, 1, and 0.5 mm from top to bottom) and all roots and root nodules were manually collected. All sieved soil samples were stored based on depth interval for measuring fine-root production with ingrowth cores. Roots were stored in zip polythene bags and transported to laboratory within 30 min from collection, where they were stored in a freezer at 10 °C. Dead fine roots (fine-root necromass) were separated from live (fine-root biomass) based on their color and lustre, elasticity, toughness, smell, and the appearance of phloem (Brassard et al., 2013). To determine fine-root biomass, all root samples were sorted. Roots with a diameter more than 2 mm and grass roots were discarded. Both live and dead fine-root samples were washed with distilled water and then dried at 70 °C until a constant weight for determine root dry weight. 2.3. Measurement of SOC content Approximately 100 g of sieved soil was collected from each of four depth intervals (0–20, 20–40, 40–60, and 60–80 cm) in three shrub plots. Soil samples were collected with a 10-cm bucket-type auger at depth intervals of 0–20, 20–40, 40–60, and 60–80 cm in each subplot. To have a good representation of SOC in each sample, 3 soil cores collected at the same depth were mixed in order to ensure a good representation of three shrub plots. To identify the effect of shrub planting on SOC content, we chose a bare land plot (30 m 30 m), in which 12 soil cores were
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Z. Lai et al. / Forest Ecology and Management 359 (2016) 381–388 Table 1 Characteristics of the plots and soil properties (mean ± S.D., n = 6). Plot traits and soil properties
S. psammophila plot
A. ordosica plot
H. mongolicum plot
Sand land
Plot area (m m) Forestation technique Soil crust species Plant density (stem ha1)
30 30 Cuttage Algal and lichen 1804 (clusters) 1923.06 ± 100.93 2.45 ± 0.18 80 Sandy soil 1.49 ± 0.14 8.43 ± 0.66 5.92 ± 0.58 1.4 ± 0.10 8.74 ± 0.12 18.92 ± 2.32 0.62 ± 0.04 0.16 ± 0.01 1.93 ± 0.23 1.62 ± 0.11
30 30 Aerial seedings Moss and lichen 2747 (clusters) 205.98 ± 18.90 0.58 ± 0.09 75 Sandy soil 1.51 ± 0.12 8.65 ± 0.81 5.78 ± 0.63 1.5 ± 0.11 8.79 ± 0.11 18.73 ± 3.34 0.67 ± 0.03 0.16 ± 0.02 1.91 ± 0.28 1.65 ± 0.17
30 30 Aerial seeding Algal and lichen 73,219 (individuals) 392.53 ± 28.84 0.75 ± 0.12 85 Sandy soil 1.51 ± 0.16 8.8 ± 0.73 6.06 ± 0.49 1.5 ± 0.08 8.83 ± 0.18 19.05 ± 2.89 0.74 ± 0.07 0.18 ± 0.02 2.06 ± 0.21 1.68 ± 0.14
30 30 – – – – – – 0 Sandy soil 1.53 ± 0.14 8.5 ± 0.59 5.7 ± 0.37 1.5 ± 0.05 8.99 ± 0.15 19.68 ± 4.02 0.55 ± 0.03 0.17 ± 0.03 1.81 ± 0.18 1.63 ± 0.20
Aboveground biomass (g m2) Mean height (m) Canopy coverage (%) Soil type Soil bulk (g cm3) <0.05 in grain diameter (%) Silt (%) Clay (%) pH Electrical conductivity (ls cm1) Total N (g kg1) Total P (g kg1) Available N (mg kg1) Available P (mg kg1)
Note: soils from the upper 30 cm of soil profile were analyzed in this study.
randomly collected and then divided into four depth intervals (0–20, 20–40, 40–60 and 60–80 cm). A total of 192 soil samples ((3 shrub plots + 1 bare-land plot) 4 depth intervals 12 replicates) were collected and placed at room temperature for a week. Then they were sieved (pore size < 2 mm), milled ground, and stored in zip polythene bags until analysis. Soil bulk density was determined for each depth interval using a cutting ring (volume of 100 cm3) and calculated as the ratio of oven-dry soil weight to cutting ring volume. Total SOC content was determined using the dichromate oxidation method (Walkley and Black, 1934). Heavy-fraction SOC (HF-SOC) and light-fraction SOC (LF-SOC) were analysed using the Gregorich and Ellert (1993) method. In our study, we used 1.8 g ml1 NaI solution to separate LF-SOC from HF-SOC. LF-SOC content was determined by Elementar CHNS analyzer model Vario EL III (Elementar Analyser Systeme, GmbH, Hanau, Germany) and HF-SOC was also determined using the classic dichromate oxidation method (Walkley and Black, 1934).
length 0.4 m depth). All fine roots were washed with deionized water, sorted into less than 2-cm fractions and then dried at 70 °C until a constant weight was obtained. Nylon mesh bags (length 10 cm, diameter 10 cm, pore size 50 lm) were used for determining root decomposition. Approximately 5 g of fine-root samples were placed into mesh bag and heat-sealed. A total of 225 mesh bags (3 shrubs 5 replicates 15 collection times) were deployed on 28 March 2012 at a randomly selected site dominated by H. mongolicum and S. psammophila and collected once a month during two growth periods (28 April to 28 October 2012 and 28 March to 28 October 2013). Upon collection, fine roots were removed from bags, dried at 70 °C until a constant weight was obtained, weighted, milled ground, and analysed for total C. Total C in fine-root samples were analysed using Elementar CHNS analyser (Vario EL III, Elementar Analyser Systeme, GmbH, Hanau, Germany).
2.4. Fine-root production determination
Statistical analyses was conducted using SPSS 18.0 statistical software package (SPSS Inc., Chicago, IL, USA). The differences of the fine-root biomass, fine-root necromass, fine-root production, SOC content, and its fractions among soil layers were compared by the LSD test. The t-test was used to compare the effect of revegetation practices on fine root parameters and SOC content. Two way analysis of variance (ANOVA) accompanied by Holm’s test was applied for examining statistical differences among the mass loss and C release of standardized fine root litter at different time intervals. Mean differences were considered significant at p < 0.05.
Fine-root production was estimated using ingrowth cores. In September 2011, sieved soil samples were placed in nylon mesh bags (length 80 cm, diameter 8.5 cm, and pore size 0.5 mm) and then bags were placed into the ground holes, which had created from soil-core sampling, to the corresponding depth interval and shrub plot. A total of 72 ingrowth cores (36 subplots 2 shrub plots) were placed in both H. mongolicum and A. ordosica plots and a total of 52 ingrowth cores were placed in S. psammophila plot. Mesh bags were collected 12 months later in September 2012. Each of them were divided into four depth intervals (0–20, 20–40, 40–60, and 60–80 cm), then sieved through a three metal-sieve stack with different pore sizes (2, 1, and 0.5 mm from top to bottom) and all fine roots were manually collected to determine annual fine-root production of shrub species. In the laboratory, all roots were washed with distilled water and then dried at 70 °C until a constant weight for determine root dry weight. 2.5. Mesh-bag experiment for root decomposition determination We established a fine root decomposition experiment using fine roots of three shrub species collected in 2012 from 12 trenches near the plots (3 shrub plots 4 directions; 0.5 m width 1 m
2.6. Statistical analysis
3. Results 3.1. Fine-root biomass A. ordosica had the highest fine-root mean diameter (0.90 mm), followed by H. mongolicum (0.76 mm) and S. psammophila (0.46 mm). Fine-root biomass of H. mongolicum and A. ordosica was 21.58 ± 2.30 g m2 and 41.09 ± 3.84 g m2, respectively, while that of S. psammophila was 189.96 ± 10.27 g m2. Fine-root biomass of S. psammophila in the top soil down to was significantly greater than that of H. mongolicum or A. ordosica (p < 0.001; Fig. 1). No significant differences in fine-root biomass distribution of H. mongolicum and A. ordosica were observed, except for the
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Fig. 1. Vertical distributions of fine-root biomass and necromass among shrub species (A. ordosica, H. mongolicum, and S. psammophila). Bars indicate the standard error of the means (H. mongolicum and A. ordosica: 36, S. psammophila: 13). Lowcase and capital letters indicate the significant difference of mean values of fine root biomass and necromass, respectively, among the treatments. Bars with the same letter indicate a non-significant difference (p = 0.05).
Fig. 3. Vertical distribution of fine root production and necromass among different shrub species (A. ordosica, H. mongolicum, and S. psammophila). Bars indicate standard error of the means (H. mongolicum and A. ordosica: 36, S. psammophila: 13). Low-case and capital letters indicate the significant difference of mean values of fine root production and necromass, respectively, among the treatments. Bars with the same letter indicate a non-significant difference (p = 0.05).
35.48 ± 2.80 g m2, respectively. Mean diameter of fine roots in the ingrowth cores were 0.45 mm for S. psammophila, 0.59 mm for H. mongolicum and 0.51 mm for A. ordosica. The fine-root production of H. mongolicum and A. ordosica was not significantly different in any depth interval, while the fine-root production of S. psammophila was significantly higher than that of H. mongolicum and A. ordosica in all depth intervals (p < 0.001; Fig. 3). The 0–40 cm depth intervals contained 48% and 45% of fine-root production of H. mongolicum and A. ordosica, respectively. Fine-root production of S. psammophila at the same depth intervals was 57% and had a decreasing tendency with depth (Fig. 3). Mortality rate of newly grown fine roots was higher at the 0–40 cm depth intervals than that at the 40–80 cm depth intervals (Fig. 3). Fine-root mortality rate of S. psammophila was significantly higher (over 5% of total fine-root production) than that of H. mongolicum and A. ordosica. 3.3. Fine-root decomposition Fig. 2. Cumulative fine root carbon content of different shrub species with soil depth (A. ordosica, H. mongolicum, and S. psammophila). Bars indicate standard error of the means (H. mongolicum and A. ordosica: 36, S. psammophila: 13).
0–20 cm. Approximately 69% of fine roots of A. ordosica and S. psammophila were concentrated at the 0–40 cm depth intervals; the proportion of fine roots of H. mongolicum at the same depth intervals was 40%. Fine-root necromass of S. psammophila (approximately 20% of the total fine-root biomass) was significantly higher than that of H. mongolicum (approximately 7% of total fine-root biomass) or A. ordosica (approximately 12% of total fine-root biomass) as shown in Fig. 1. Approximately 70% of fine-root necromass occurred at the 0–40 cm depth intervals (Fig. 1), indicating that fine-root turnover mostly occurred close to surface. Greater proportion of fine-root C of S. psammophila was concentrated at the 0–40 cm depth intervals compared to H. mongolicum or A. ordosica (Fig. 2). 3.2. Fine-root production Fine-root production densities of S. psammophila, H. mongolicum, and A. ordosica were 310.22 ± 23.30 g m2, 37.54 ± 3.31 g m2 and
Fine-root necromass loss of S. psammophila was slower than that of H. mongolicum and A. ordosica (p < 0.5; Fig. 4a). Fine-root necromass loss of A. ordosica experienced an initial slow period (0–30 days), later fast period (30–150 days and slow period (150–360 days), and a final fast period (360–450 days), fine-root necromass loss during the slow periods was not significant. Fine-root mass of H. mongolicum and S. psammophila was gradually lost during 540 days of decomposition. However, fine-root mass showed different decomposition rates between the two growth periods in three shrub species (Fig. 4a). After 180 days, the remaining fine-root biomass of A. ordosica was 76.9 ± 1.9%, of S. psammophila was 80.7 ± 1.6%, and of H. mongolicum was 78.7 ± 2.1%, while after 540 days, the corresponding percentages were 60.8 ± 0.9% for A. ordosica, 76.2 ± 0.6% for S. psammophila, and 73.6 ± 0.9% for H. mongolicum. Fine-root C loss rate of A. ordosica was the highest among shrub species (Fig. 4b). During the initial 30 days, fine-root C loss was not significant in any shrub species (Fig. 4b). Thereafter, A. ordosica and S. psammophila had a fast period of C loss (30–60 days) and a slow period of C loss (60–180 days), while fine-root C of H. mongolicum decreased gradually (Fig. 4b). During the second growth period, H mongolicum had a slow period (330–450 days) and a fast period
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Fig. 5. Vertical distributions of light-fraction soil organic carbon and heavy-fraction soil organic carbon among the different shrub (A. ordosica, H. mongolicum, and S. psammophila) plots and the bare land plot. Low-case and capital letters indicate the significant difference of mean values of light-fraction and heavy-fraction soil organic carbon, respectively, among the treatments. Bars with the same letter indicate a non-significant difference (p = 0.05).
Fig. 4. Percent dry mass (a) and carbon (b) remaining of fine roots of different shrub species (A. ordosica, H. mongolicum, and S. psammophila) during 540 days of decomposition. Bars indicate standard error of the means (n = 5). Break days represent frost periods in the study site.
(450–540 days) of C loss, while A. ordosica had a fat period (330–450 days) and a slow period (450–540 days). After 180 days, fine-root C loss of A. ordosica was 18.1 ± 1.1%, of S. psammophila was 16.6 ± 1.0%, and of H. mongolicum was 14.9 ± 1.3%, while after 540 days, the corresponding percentages were 33.6 ± 0.3% for A. ordosica, 19.7 ± 0.4% for S. psammophila, and 21.4 ± 0.2% for H. mongolicum.
depth in bare land plot. However, it was observed that depth had an effect on LF-SOC and HF-SOC contents (Fig. 5) and LF-SOC content had a decreasing tendency with depth in shrub plots (Fig. 5). At the 0–40 cm depth intervals, vertical distributions of LF-SOC and HF-SOC in A. ordosica plot were significantly higher than those in S. psammophila and H. mongolicum plots (p < 0.001), and vertical distribution of LF-SOC in the S. psammophila plot was significantly higher than that in the H. mongolicum plot (p < 0.05; Fig. 5). At 40–80 cm depth intervals, LF-SOC content was significantly different in all shrub plots, while HF-SOC content in S. psammophila plot was higher than that in H. mongolicum plot (p < 0.05). Compared to total SOC content, a higher LF-SOC content was found in A. ordosica (68 ± 4.8%) and S. psammophila (67 ± 3.2%) plots at the 0–40 cm depth intervals (p < 0.05), while there was no significant change in H. mongolicum plot (Fig. 5).
3.4. SOC content and its fractions
4. Discussion
Down to a depth of 80 cm soils, the SOC content were 1387.8 g m1 for A. ordosica plot, 1019.2 g m1 for H. mongolicum plot, 922.8 g m1 for S. psammophila, and 492.5 g m1 for bare-land plot. SOC content was significantly higher in shrub plots than that in bare land plot (p < 0.001; Fig. 5). SOC content in A. ordosica plot was significantly higher than that in S. psammophila or H. mongolicum plots, while SOC content of H. mongolicum plot in the all soil layers was significantly greater than that of S. psammophila plot (p < 0.01; Fig. 5). Although no significant differences were observed in three shrub plots within the 20–80 cm soil layer, the SOC content showed a decreasing tendency with depth. More than 50% of SOC content in shrub plots was concentrated at the 0–40 cm depth intervals. Specifically, these percentages were 58.1 ± 2.0% in A. ordosica plot, 55.8 ± 2.0% in S. psammophila plot, and 54.1 ± 1.8% in H. mongolicum plot (Fig. 5). A significantly higher SOC content was observed in A. ordosica (37.0%) and S. psammophila (32.6%) plots at the 0–20 cm depth interval compared to that in H. mongolicum plot (25.4%). At the 0–20 cm depth interval, the LF-SOC content was higher than HF-SOC content in shrub plots (p < 0.05), although at deeper depth intervals results were reversed (Fig. 5). The proportion of LF-SOC and HF-SOC contents did not change significantly with
4.1. Vertical patterns of fine root biomass and production in three shrub species Despite the similar plot conditions, vertical patterns of fine-root biomass and production varied significantly among shrub species (Figs. 1 and 2). The fine root biomass of S. psammophila was significantly higher than that of H. mongolicum and A. ordosica, and the highest proportion was concentrated at the 0–40 cm depth intervals (Fig. 1). Although fine roots of A. ordosica were mostly concentrated at the 0–20 cm depth interval, no significant differences were observed among the 20–80 cm depth intervals. Fine-root distribution patterns of S. psammophila and A. ordosica were similar to those in many drylands, showing that depth intervals close to surface generally have a higher content of fine roots (Oppelt et al., 2005; Cheng et al., 2009; Gwenzi et al., 2011; Chang et al., 2012). In drylands, a high fine-root biomass close to surface might increase the ability of plants to absorb soil resources (particularly water) and adapt to drought periods (Gwenzi et al., 2011; Chang et al., 2012), while it might decrease their C investment (Huang et al., 2008). A comparison among shrub species showed a significant difference in fine-root biomass, which might be attributed to genetic differences (Oppelt et al., 2005). In addition, the fine-root
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biomass of some desert trees is relatively low close to surface (Chang et al., 2012), something that is in agreement with the low proportion of fine-root biomass at the 0–20 cm depth interval in H. mongolicum plot (Fig. 1). Previous studies have indicated that it is possible some shrubs with intense and shallow root systems, as well as others with deep root systems, to coexist and interact with neighbouring shrubs when resources are scarce in drylands (Ward et al., 2013). In our study, differences in vertical distribution of fine roots among shrub species suggested that they might have different adaption mechanisms when resources are limited. Fine-root production varied among different shrub plots (Fig. 3). Fine-root production of S. psammophila was significantly higher than that of H. mongolicum or A. ordosica (Fig. 1b). In addition, aboveground biomass of S. psammophila was strikingly greater than that of the other two shrubs (Table 1). These results may suggest that C investment to fine roots varies among shrub species. The highest amount of necromass occurred close to surface (Figs. 1 and 3), which may be attributed to the fact that in semi-arid and arid regions the topsoil is generally or periodically dry (Zhang et al., 2009). Nevertheless, the fine roots of different plant species respond to temporal changes of the topsoil in different ways (Ward et al., 2013). Fine-root production of S. psammophila was mostly concentrated in the 0–20 cm depth interval; however, fine root productions of H. mongolicum and A. ordosica in all soil layers were evenly distributed (Fig. 3). Some studies showed that fine-root production had different vertical patterns in different soil profiles due to heterogeneity of soil nutrients and water (Wang et al., 2014). Zhang et al. (2009) revealed that soil moisture in sandy soils increases with depth, which may suggest that plants with a higher proportion of fine roots at deeper depths can use water that is stored there and adapt better in drylands (Gwenzi et al., 2011). Overall, our results indicated that shrub species have different root foraging strategies. In this study, ingrowth core technique might overestimate fine root production. First, root growth of some plants were stimulated by some light damage and roots were generally damaged by using augers during soil core sampling. Second, the homogenized sandy soil habitat of reconstructed ingrowth core will present a less competitive environment. Finally, the ingrowth bags were collected after 1 year, fine root turnover was not estimated inside this period. However, there was not a better alternative method that can be used as a quick and less expensive method of estimating fine root production. Despite limitations, the results are helpful for assessing the effect of shrub species on fine root production and the differences of root forage strategies among different shrubs. 4.2. SOC stock and distribution SOC stocks down to 80 cm soil depth ranged from 922.8 to 1387.8 g m1 after revegetation on stabilized sand dunes (Fig. 5). Our study generated generally lower values than those in previously reported studies in semi-arid or desert regions (Jeddi et al., 2009). For instance, Yüksek and Yüksek (2011) reported that revegetation on bare sand improved SOC stocks at the 0–20 cm interval, ranging from 1610 to 9420 g m1, while Liu et al. (2010) showed that SOC content ranged from 8.2 to 10.5 Mg ha1 at the same depth interval in semi-arid regions. A probable explanation is that in our study the time period for SOC accumulation after revegetation was relatively short, Additionally, it is known that SOC stocks increase with precipitation (Jobbágy and Jackson, 2000; Wang et al., 2014), thus, in our study, low precipitation (287 mm) was a major limiting factor for plant production and litter decomposition that subsequently affected SOC content. More than 50% of SOC content in shrub plots was concentrated at the 0–40 cm depth intervals (Fig. 5). Our results are in agreement with previous studies that also reported a high SOC content
close to surface (Wang et al., 2004), which was mostly attributed to litter (leaf and root) input (Upson and Burgess, 2013) and soil crust (Feng et al., 2013). However, most of the studies have focused only on depths close to surface, neglecting vertical distribution (Upson and Burgess, 2013). As a result, collected data on SOC spatial heterogeneity were insufficient or estimation of SOC content was inaccurate (Wang et al., 2014). In any case, SOC stocks in large regions with high heterogeneity remain to be investigated. 4.3. Effects of revegetation on SOC stocks and fractions SOC stock and distribution varied significantly in shrub plots (Fig. 5). A. ordosica had the highest SOC stocks (1387.8 g m1), followed by H. mongolicum (1019.2 g m1) and S. psammophila (922.8 g m1). Compared to the bare land plot (492.5 g m1), our results suggested that revegetation improved SOC stocks significantly (Fig. 5) and they are in agreement with previous reported studies (Nosetto et al., 2006; Yüksek and Yüksek, 2011; Zhang et al., 2014). In degraded drylands, revegetation with shrubs generally increased C input to soil through litter production (Yüksek and Yüksek, 2011). Our results indicated that SOC stocks were higher after revegetation (Fig. 5). Specifically, SOC stocks in A. ordosica, S. psammophila, and H. mongolicum plots increased 1.82, 1.07, and 0.87 times, respectively, more than those in the bare land plot. Variation in SOC stock increase among shrub species may be attributed to different mechanisms of C input to soil and litter composition (Hiltbrunner et al., 2013). Additionally, soil microbial communities, which control the decomposition of litter and thus regulate C mineralization, are primarily affected by vegetation types (Clemmensen et al., 2013). Different vegetation practices may lead to different microclimatic conditions, which significantly affect organic matter decomposition (Kellman et al., 2007). LF-SOC content was more variable among different depth intervals (Fig. 5) than that of HF-SOC (Fig. 5) and its content was more easily affected by soil depth (Liu et al., 2010). One possible explanation may be that LF-SOC is controlled by the amount of litter input, which differs among plant species (Puget et al., 2000). Increase in total SOC content was mainly due to increase in LF-SOC (Fig. 5), except for A. ordosica plot, indicating that this change was unstable. LF-SOC content primarily derives from plant residues, roots, and fungal hypha at different decomposition stages (Kimetu and Lehmann, 2010) and is generally sensitive to land-use changes, while HF-SOC is not (Puget et al., 2000; Liu et al., 2010) due to its slow formation (Six et al., 2004). In our study, the highest increase in HF-SOC content was observed in the A. ordosica plot compared to the H. mongolicum and S. psammophila plots (Fig. 5), indicating that mechanisms of SOC accumulation differ among different revegetation practices. These results indicated that A. ordosica might be a better species for revegetation in terms of SOC sequestration. Although increased HF-SOC and LF-SOC were affected by the amount and quality of litter (Liu et al., 2010), the mechanisms of SOC accumulation were strongly controlled by SOC dynamics and turnover (Asaye and Zewdie, 2013). SOC dynamics and turnover remain to be studied under different revegetation practices in order to better understand the mechanisms that underlie SOC accumulation. 4.4. Effects of fine roots on SOC content Our results showed that C content from fine-root litter might be low in shrub plots (Fig. 1). Compared to the H. mongolicum (0.5 g C m2 years1) and A. ordosica (0.4 g C m2 years1) plots, the S. psammophila plot (8.1 g C m2 years1) had the highest C content derived from fine-root necromass. Our results showed that a high content of fine-root biomass and production supported the return of organic mass and nutrients through fine-root turnover
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(Yang et al., 2004); however, higher fine-root biomass and production did not represented greater SOC (LF-SOC and HF-SOC) content in shrub plots (Figs. 1, 2 and 5). Similarly, SOC stocks did not respond to high fine-root biomass (Ferguson and Nowak, 2011) and soil C accretion was not dependent on the amount of standing fine-root biomass and production (Asaye and Zewdie, 2013). A possible explanation could be that in addition to fine root litter, leaf and branch litter, insoluble organic matter from roots, refractory microbial biomass, and live root exudates mostly contribute to SOC accumulation at deeper soil depths in some regions (Matamala et al., 2003; Uselman et al., 2007). For example, some studies have indicated the importance of SOC originating from live roots as root exudates (Uselman et al., 2007). Another study showed that leaf litter decomposition, rather than root litter, was the major contributor to soil fertility (Tang et al., 2013). These results suggested that the fine-root litter of different shrub plots contributes to SOC accumulation at different rates and the mechanisms of SOC accumulation varies among shrub plots. Our results showed that the fine roots of A. ordosica had the fastest decomposition rate compared to the other two shrub species (Fig. 4), which might be an explanation of SOC stocks variation among shrub plots. An increase in SOC stocks mainly depends on the rate of fine-root decomposition, which is affected by genetic and environmental factors (Hobbie et al., 2010). Some studies demonstrated that fine-root decomposition was important for C input to soil (Lemma et al., 2007; Hobbie et al., 2010). A root-litter decomposition experiment showed that the initial root-mass and C decomposition of S. psammophila and H. mongolicum were slow (Fig. 4), indicating that fine-root litter C was more slowly released to soil compared to A. ordosica, even though fine-root turnover occurred in soil. These results indicated that A. ordosica might be a better species for improving SOC accumulation in the study site and a possible explanation of the reason that A. ordosica plot had the highest increase in SOC storage. It should be pointed out that we did not measure any seasonal dynamics or the turnover of fine roots, which could have resulted in an underestimation of C input from fine roots. Fine-root mortality and dieback are possible to occur across all seasons (Matamala et al., 2003). Thus, we might have underestimated the contribution of fine-root litter to SOC accumulation. Further, the mesh-bag experiment showed that most of the initial materials remained for more than 2 years. Simultaneously, the changes in soil properties of ingrowth cores might result in an overestimation on fine-root production. Therefore, our results on fine roots may only allow us to make comparisons among shrub species. In future studies, fine-root turnover should be monitored for to obtain a more accurate estimate of the effect of fine-root litter on SOC accumulation after revegetation. 5. Conclusions Revegetation with xerophilous shrubs is an effective approach to combat desertification in northwestern China. Our study showed that the development of S. psammophila, H. mongolicum, and A. ordosica significantly improved SOC compared to bare-land plots. Increase in total SOC content was mainly due to an increase in LF-SOC, except for the A. ordosica plot. Although S. psammophila had the highest fine-root biomass and production among shrub species, the highest increase in SOC was observed in the A. ordosica plot, followed by the H. mongolicum and S. psammophila plots. The effect of fine-root litter on SOC accumulation varied significantly among different shrub plots. Therefore, A. ordosica may be a better species for SOC accumulation and sequestration in the study site. Overall, the results suggested that the mechanism of SOC accumulation and sequestration differed among shrub plots.
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Acknowledgements This study was funded by the National Science and Technology Support Program in the margin of the 12th Five-Year Plan (No. 2012BAD16B02) and the Fundamental Research Funds for the Central Universities (BJFU-TD2011-04). We would like to thank the staff of the Yanchi Research Station. Special thanks go to Su Lu, Bao Wei, and Liwei Wei for their help with sampling and measurements in the field and laboratory. References Asaye, Z., Zewdie, S., 2013. Fine root dynamics and soil carbon accretion under thinned and un-thinned Cupressus lusitanica stands in, Southern Ethiopia. Plant Soil 366, 261–271. Beniston, J.W., DuPont, S.T., Glover, J.D., Lal, R., Dungait, J.A.J., 2014. Soil organic carbon dynamics 75 years after land-use change in perennial grassland and annual wheat agricultural systems. Biogeochemistry 120, 37–49. Brassard, B., Chen, H.Y.H., Cavard, X., Laganière, J., Reich, P.B., Bergeron, Y., Paré, D., Yuan, Z., 2013. 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Fine-root distribution, production, decomposition, and effect on soil organic carbon of three revegetation shrub species in northwest China q Zongrui Lai a, Yuqing Zhang a,b,⇑, Jiabin Liu c, Bin Wu a,b, Shugao Qin a,b, Keyu Fa a a
Yanchi Research Station, School of Soil and Water Conservation, Beijing Forestry University, Beijing 100083, China Key Laboratory of Soil and Water Conservation and Desertification Combating, Beijing Forestry University, Ministry of Education, Beijing 100083, China c School of Natural Resources and Environment, Northwest A & F University, Yangling, Shaanxi 712100, China b
a r t i c l e
i n f o
Article history: Received 21 December 2014 Received in revised form 16 April 2015 Accepted 23 April 2015 Available online 16 May 2015 Keywords: Artemisia ordosica Carbon sequestration Decomposition Hedysarum mongolicum Light fraction soil organic carbon Salix psammophila
a b s t r a c t Revegetation with xerophilous shrubs is an effective approach to combat desertification in northwestern China; however, evaluation studies on fine-root properties of shrubs and soil organic carbon are limited. To gain a better understanding of revegetation practices, we investigated the vertical distribution of fine-root biomass, necromass, production, and effect on soil organic carbon (SOC) content in three shrub species (Salix psammophila, Hedysarum mongolicum, and Artemisia ordosica). In addition, we also estimated the fine root decomposition rate with litterbag techniques. The results showed that revegetation practices resulted in a significant increase in SOC content. Over a 10 year period of revegetation, the SOC content in S. psammophila, H. mongolicum, and A. ordosica plots increased by 0.87, 1.07, and 1.82 times, respectively, more than that in bare-land plot. Increase in total SOC content was mainly due to increase in light-fraction SOC, except for the A. ordosica plot. Variations in the short-term increase of SOC content after revegetations with the three shrubs on sand land might be explained by fine root decomposition rates, at least in part. A. ordosica may be a better species for SOC accumulation and sequestration in the study site. Additionally, fine-root biomass and production were not associated with more SOC content increase in shrub plots. The results suggest the mechanism of SOC accumulation and sequestration differed among shrub plots and highlight the effectiveness of different shrub species as revegetation materials in terms of SOC accumulation and sequestration. Ó 2015 Elsevier B.V. All rights reserved.
1. Introduction China has been severely impacted by desertification, which is widely recognized as a significant environmental problem that increasingly threatens human survival and development (Gao et al., 2012). Revegetation that has been used extensively in northwestern China since the 1980’s, is one of the most effective and sustainable means to control desertification and rehabilitate degraded land (Zhang et al., 2009). Salix psammophila, Hedysarum mongolicum, and Artemisia ordosica are considered as excellent fixed-dune species due to their high adaptability to arid and infertile areas affected by wind erosion. Currently, these three shrub species are dominant in desert plant communities of northwestern China, particularly in the Mu Us Desert. Although their distribution patterns (Chen et al., 2002), water-use efficiency (Yang et al., q
This article is part of a special section entitled ‘‘Forests, Roots and Soil Carbon’’.
⇑ Corresponding author at: School of Soil and Water Conservation, Beijing Forestry University, 35 Qinghua Eastroad, Haidian District, Beijing 100083, China. Tel.: +86 10 62336172; fax: +86 10 62338689. E-mail address: [email protected] (Y. Zhang). http://dx.doi.org/10.1016/j.foreco.2015.04.025 0378-1127/Ó 2015 Elsevier B.V. All rights reserved.
2008), effects on soil nutrients, and other environmental benefits (Gao et al., 2014) have been studied extensively, information on their root properties and effects on soil carbon (C) is limited. Root systems fulfill important functions in nutrient uptake and C exchange in terrestrial ecosystems, thus they play an important role in biogeochemical cycling (Trumbore and Gaudinski, 2003). The belowground part of plants is considered to be a major C pathway to soil and significantly contributes to belowground C cycle (Chapin III and Ruess, 2001). In addition, it is known that the root system influences soil microbial activity and decomposition processes (Janssens et al., 2002). Fine roots (<2 mm) are an ephemeral part of the root system and have faster turnovers, as well as higher metabolic activity compared to lower-order roots (Pregitzer et al., 2002; McCormack et al., 2013). Although fine roots constitute a small proportion (<5%) of total standing root biomass in many terrestrial ecosystems (Gill and Jackson, 2000), it is estimated that 33% of global net primary production is consumed for fine-root growth, respiration, and turnover (Jackson et al., 1997). Fine roots are also the major sites of infection by mycorrhizal fungi, which affect a wide
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range of soil physicochemical and biological properties, including soil structure and nutrient content (Strand et al., 2008). Although mycorrhizal colonization, root exudation, and soil properties significantly affect soil organic carbon (SOC) content (Matamala et al., 2003), fine roots are the dominant pathways through which C enters the soil organic matter (SOM) pool (Jackson et al., 1997), and their structure and functional processes have an impact on SOC stocks and dynamics (Ferguson and Nowak, 2011). Therefore, information on the properties and dynamics of fine roots is essential for understanding the biogeochemical processes in terrestrial ecosystems (Pregitzer et al., 2002; Strand et al., 2008; Upson and Burgess, 2013). Fine-root properties and dynamics may play a key role in nutrient cycle and soil C sequestration (Chang et al., 2012; Upson and Burgess, 2013) in forest ecosystems (Matamala et al., 2003); for instance, fine-root biomass and vertical distribution potentially influence long-term changes in SOC content (Ferguson and Nowak, 2011; Asaye and Zewdie, 2013), while higher rates of fine-root production lead to higher C inputs to soil (Stover et al., 2010). Recent studies showed that spatial heterogeneity of SOC was positively correlated with the vertical distribution of fine roots (Beniston et al., 2014) and also soil C with fine-root biomass and C across all depth intervals (Liao et al., 2014). In addition, it is known that fine-root production and turnover directly impact biogeochemical cycle of C in terrestrial ecosystems (Matamala et al., 2003), while fine-root productivity may be similar in magnitude to foliar productivity (Norby et al., 2004). The presence of root scars indicates that fine roots are ephemeral root modules, which shed like leaves and serve as source of C for soil (Pregitzer et al., 2002). Previous studies showed that approximately 30–80% of SOC content is provided through the rapid turnover and decomposition of fine roots (Ruess et al., 2003) and variation in SOC stocks mainly depends on fine-root decomposition rates influenced by genetic and environmental factors (Lemma et al., 2007; Hobbie et al., 2010). Therefore, a study of fine-root properties is essential for a detailed understanding of their role as a source of litter and C storage in soil. Compared to the moist ecosystems, fine roots comprise a higher proportion of total plant biomass in the drylands (Jackson et al., 1997; Zhang et al., 2009), probably because of the increased allocation of C to root system due to relatively low nutrient availability in soil (Clark et al., 2010). Fine roots, which act as a conduit for the transport of C into the SOM pool (Strand et al., 2008), may play a key role in the accumulation of SOC in the drylands (Nosetto et al., 2006); therefore, additional information on fine-root properties is critical for a better understanding of the belowground C cycle. Previous studies focused either on fine roots (Huang et al., 2008; Cheng et al., 2009) or on SOC content (Li et al., 2012) in revegetation areas of northwest China; however, few studies have assessed the fine-root properties and dynamics, total SOC content and its fractions following revegetation. In this study, we investigated the vertical distribution of the fine root biomass, necromass, production, and SOC content in three shrub species (A. ordosica, H. mongolicum, and S. psammophila) in order to gain a better understanding of revegetation practices. Our specific objectives were to (1) estimate fine-root properties, including fine root biomass, distribution, production and decomposition; and (2) detect the effect of fine roots on SOC content; and (3) elucidate the variation in SOC stocks based on fine-root properties rate in three revegetation shrub species. 2. Materials and methods 2.1. Study site description The study was conducted at the Yanchi Research Station (37°6 80 N–37°730 N, 107°200 E–107°260 E; 1530 m a.s.l), in Ningxia
Province, northwestern China. The study site is located at the south edge of the Mu Us Desert and has a semiarid continental monsoon climate. The average annual temperature is 8.1 °C (1954–2014) and the frost-free period lasts from April to November and is 156 days on average (Feng et al., 2013). Rainfall occurs mainly from July through September with average annual precipitation being approximately 287 mm (Jia et al., 2014). The soil texture of the study area is sandy in the 0–1-m profile and average soil bulk density is 1.5 g m3. In 2001, H. mongolicum and A. ordosica were randomly established with aerial seeding and S. psammophila was planted using cuttage (row spacing of 4 m) on stabilized sand dunes. After revegetation, shrub plots were fenced, grazing was prohibited, and no fertilizer was applied since then. Although S. psammophila was planted using cuttage, disturbances were limited to plot preparation. Overall, human and wild-animal disturbances in shrub plots were rare. Soil type and micro-physiographic conditions were similar among shrub plots (Table 1). Plots were relatively flat with a slope of 1.0–3.0°. 2.2. Fine-root biomass and necromass determination Fine roots were sampled with a steel bucket-type soil auger (8.5-cm-diam. bucket auger with 25 cm height) with T-handle in September 2011. Three plots of 30 m 30 m were established at the research area, one for each species (S. psammophila, H. mongolicum, and A. ordosica). Each plot of A. ordosica and H. mongolicum was divided into 36 subplots of 5 m 5 m and a total of 72 randomly selected soil cores (36 subplots 2 shrub species) were collected. The distance between cores and shrubs ranged approximately from 0.1 to 0.5 m and 0.05 to 0.2 m, respectively, in A. ordosica and H. mongolicum plots, and were 0.5, 1.0, 1.5 and 2.0 m from shrubs in S. psammophila plots. Fine-root samples were collected at depth intervals of 0–20, 20–40, 40–60 and 60–80 cm. The uppermost 0–20 cm layer consisted of humus in all cases and the thickness of organic layers ranged from 0 to 0.5 cm. Four soil cores collected at the same depth were mixed in order to ensure a good representation of fine roots in each sample. In total 52 soil cores were collected to create 13 soil samples for the determination of fine-root biomass. All soil samples were sieved through a three metal-sieve stack with different pore sizes (2, 1, and 0.5 mm from top to bottom) and all roots and root nodules were manually collected. All sieved soil samples were stored based on depth interval for measuring fine-root production with ingrowth cores. Roots were stored in zip polythene bags and transported to laboratory within 30 min from collection, where they were stored in a freezer at 10 °C. Dead fine roots (fine-root necromass) were separated from live (fine-root biomass) based on their color and lustre, elasticity, toughness, smell, and the appearance of phloem (Brassard et al., 2013). To determine fine-root biomass, all root samples were sorted. Roots with a diameter more than 2 mm and grass roots were discarded. Both live and dead fine-root samples were washed with distilled water and then dried at 70 °C until a constant weight for determine root dry weight. 2.3. Measurement of SOC content Approximately 100 g of sieved soil was collected from each of four depth intervals (0–20, 20–40, 40–60, and 60–80 cm) in three shrub plots. Soil samples were collected with a 10-cm bucket-type auger at depth intervals of 0–20, 20–40, 40–60, and 60–80 cm in each subplot. To have a good representation of SOC in each sample, 3 soil cores collected at the same depth were mixed in order to ensure a good representation of three shrub plots. To identify the effect of shrub planting on SOC content, we chose a bare land plot (30 m 30 m), in which 12 soil cores were
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Z. Lai et al. / Forest Ecology and Management 359 (2016) 381–388 Table 1 Characteristics of the plots and soil properties (mean ± S.D., n = 6). Plot traits and soil properties
S. psammophila plot
A. ordosica plot
H. mongolicum plot
Sand land
Plot area (m m) Forestation technique Soil crust species Plant density (stem ha1)
30 30 Cuttage Algal and lichen 1804 (clusters) 1923.06 ± 100.93 2.45 ± 0.18 80 Sandy soil 1.49 ± 0.14 8.43 ± 0.66 5.92 ± 0.58 1.4 ± 0.10 8.74 ± 0.12 18.92 ± 2.32 0.62 ± 0.04 0.16 ± 0.01 1.93 ± 0.23 1.62 ± 0.11
30 30 Aerial seedings Moss and lichen 2747 (clusters) 205.98 ± 18.90 0.58 ± 0.09 75 Sandy soil 1.51 ± 0.12 8.65 ± 0.81 5.78 ± 0.63 1.5 ± 0.11 8.79 ± 0.11 18.73 ± 3.34 0.67 ± 0.03 0.16 ± 0.02 1.91 ± 0.28 1.65 ± 0.17
30 30 Aerial seeding Algal and lichen 73,219 (individuals) 392.53 ± 28.84 0.75 ± 0.12 85 Sandy soil 1.51 ± 0.16 8.8 ± 0.73 6.06 ± 0.49 1.5 ± 0.08 8.83 ± 0.18 19.05 ± 2.89 0.74 ± 0.07 0.18 ± 0.02 2.06 ± 0.21 1.68 ± 0.14
30 30 – – – – – – 0 Sandy soil 1.53 ± 0.14 8.5 ± 0.59 5.7 ± 0.37 1.5 ± 0.05 8.99 ± 0.15 19.68 ± 4.02 0.55 ± 0.03 0.17 ± 0.03 1.81 ± 0.18 1.63 ± 0.20
Aboveground biomass (g m2) Mean height (m) Canopy coverage (%) Soil type Soil bulk (g cm3) <0.05 in grain diameter (%) Silt (%) Clay (%) pH Electrical conductivity (ls cm1) Total N (g kg1) Total P (g kg1) Available N (mg kg1) Available P (mg kg1)
Note: soils from the upper 30 cm of soil profile were analyzed in this study.
randomly collected and then divided into four depth intervals (0–20, 20–40, 40–60 and 60–80 cm). A total of 192 soil samples ((3 shrub plots + 1 bare-land plot) 4 depth intervals 12 replicates) were collected and placed at room temperature for a week. Then they were sieved (pore size < 2 mm), milled ground, and stored in zip polythene bags until analysis. Soil bulk density was determined for each depth interval using a cutting ring (volume of 100 cm3) and calculated as the ratio of oven-dry soil weight to cutting ring volume. Total SOC content was determined using the dichromate oxidation method (Walkley and Black, 1934). Heavy-fraction SOC (HF-SOC) and light-fraction SOC (LF-SOC) were analysed using the Gregorich and Ellert (1993) method. In our study, we used 1.8 g ml1 NaI solution to separate LF-SOC from HF-SOC. LF-SOC content was determined by Elementar CHNS analyzer model Vario EL III (Elementar Analyser Systeme, GmbH, Hanau, Germany) and HF-SOC was also determined using the classic dichromate oxidation method (Walkley and Black, 1934).
length 0.4 m depth). All fine roots were washed with deionized water, sorted into less than 2-cm fractions and then dried at 70 °C until a constant weight was obtained. Nylon mesh bags (length 10 cm, diameter 10 cm, pore size 50 lm) were used for determining root decomposition. Approximately 5 g of fine-root samples were placed into mesh bag and heat-sealed. A total of 225 mesh bags (3 shrubs 5 replicates 15 collection times) were deployed on 28 March 2012 at a randomly selected site dominated by H. mongolicum and S. psammophila and collected once a month during two growth periods (28 April to 28 October 2012 and 28 March to 28 October 2013). Upon collection, fine roots were removed from bags, dried at 70 °C until a constant weight was obtained, weighted, milled ground, and analysed for total C. Total C in fine-root samples were analysed using Elementar CHNS analyser (Vario EL III, Elementar Analyser Systeme, GmbH, Hanau, Germany).
2.4. Fine-root production determination
Statistical analyses was conducted using SPSS 18.0 statistical software package (SPSS Inc., Chicago, IL, USA). The differences of the fine-root biomass, fine-root necromass, fine-root production, SOC content, and its fractions among soil layers were compared by the LSD test. The t-test was used to compare the effect of revegetation practices on fine root parameters and SOC content. Two way analysis of variance (ANOVA) accompanied by Holm’s test was applied for examining statistical differences among the mass loss and C release of standardized fine root litter at different time intervals. Mean differences were considered significant at p < 0.05.
Fine-root production was estimated using ingrowth cores. In September 2011, sieved soil samples were placed in nylon mesh bags (length 80 cm, diameter 8.5 cm, and pore size 0.5 mm) and then bags were placed into the ground holes, which had created from soil-core sampling, to the corresponding depth interval and shrub plot. A total of 72 ingrowth cores (36 subplots 2 shrub plots) were placed in both H. mongolicum and A. ordosica plots and a total of 52 ingrowth cores were placed in S. psammophila plot. Mesh bags were collected 12 months later in September 2012. Each of them were divided into four depth intervals (0–20, 20–40, 40–60, and 60–80 cm), then sieved through a three metal-sieve stack with different pore sizes (2, 1, and 0.5 mm from top to bottom) and all fine roots were manually collected to determine annual fine-root production of shrub species. In the laboratory, all roots were washed with distilled water and then dried at 70 °C until a constant weight for determine root dry weight. 2.5. Mesh-bag experiment for root decomposition determination We established a fine root decomposition experiment using fine roots of three shrub species collected in 2012 from 12 trenches near the plots (3 shrub plots 4 directions; 0.5 m width 1 m
2.6. Statistical analysis
3. Results 3.1. Fine-root biomass A. ordosica had the highest fine-root mean diameter (0.90 mm), followed by H. mongolicum (0.76 mm) and S. psammophila (0.46 mm). Fine-root biomass of H. mongolicum and A. ordosica was 21.58 ± 2.30 g m2 and 41.09 ± 3.84 g m2, respectively, while that of S. psammophila was 189.96 ± 10.27 g m2. Fine-root biomass of S. psammophila in the top soil down to was significantly greater than that of H. mongolicum or A. ordosica (p < 0.001; Fig. 1). No significant differences in fine-root biomass distribution of H. mongolicum and A. ordosica were observed, except for the
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Fig. 1. Vertical distributions of fine-root biomass and necromass among shrub species (A. ordosica, H. mongolicum, and S. psammophila). Bars indicate the standard error of the means (H. mongolicum and A. ordosica: 36, S. psammophila: 13). Lowcase and capital letters indicate the significant difference of mean values of fine root biomass and necromass, respectively, among the treatments. Bars with the same letter indicate a non-significant difference (p = 0.05).
Fig. 3. Vertical distribution of fine root production and necromass among different shrub species (A. ordosica, H. mongolicum, and S. psammophila). Bars indicate standard error of the means (H. mongolicum and A. ordosica: 36, S. psammophila: 13). Low-case and capital letters indicate the significant difference of mean values of fine root production and necromass, respectively, among the treatments. Bars with the same letter indicate a non-significant difference (p = 0.05).
35.48 ± 2.80 g m2, respectively. Mean diameter of fine roots in the ingrowth cores were 0.45 mm for S. psammophila, 0.59 mm for H. mongolicum and 0.51 mm for A. ordosica. The fine-root production of H. mongolicum and A. ordosica was not significantly different in any depth interval, while the fine-root production of S. psammophila was significantly higher than that of H. mongolicum and A. ordosica in all depth intervals (p < 0.001; Fig. 3). The 0–40 cm depth intervals contained 48% and 45% of fine-root production of H. mongolicum and A. ordosica, respectively. Fine-root production of S. psammophila at the same depth intervals was 57% and had a decreasing tendency with depth (Fig. 3). Mortality rate of newly grown fine roots was higher at the 0–40 cm depth intervals than that at the 40–80 cm depth intervals (Fig. 3). Fine-root mortality rate of S. psammophila was significantly higher (over 5% of total fine-root production) than that of H. mongolicum and A. ordosica. 3.3. Fine-root decomposition Fig. 2. Cumulative fine root carbon content of different shrub species with soil depth (A. ordosica, H. mongolicum, and S. psammophila). Bars indicate standard error of the means (H. mongolicum and A. ordosica: 36, S. psammophila: 13).
0–20 cm. Approximately 69% of fine roots of A. ordosica and S. psammophila were concentrated at the 0–40 cm depth intervals; the proportion of fine roots of H. mongolicum at the same depth intervals was 40%. Fine-root necromass of S. psammophila (approximately 20% of the total fine-root biomass) was significantly higher than that of H. mongolicum (approximately 7% of total fine-root biomass) or A. ordosica (approximately 12% of total fine-root biomass) as shown in Fig. 1. Approximately 70% of fine-root necromass occurred at the 0–40 cm depth intervals (Fig. 1), indicating that fine-root turnover mostly occurred close to surface. Greater proportion of fine-root C of S. psammophila was concentrated at the 0–40 cm depth intervals compared to H. mongolicum or A. ordosica (Fig. 2). 3.2. Fine-root production Fine-root production densities of S. psammophila, H. mongolicum, and A. ordosica were 310.22 ± 23.30 g m2, 37.54 ± 3.31 g m2 and
Fine-root necromass loss of S. psammophila was slower than that of H. mongolicum and A. ordosica (p < 0.5; Fig. 4a). Fine-root necromass loss of A. ordosica experienced an initial slow period (0–30 days), later fast period (30–150 days and slow period (150–360 days), and a final fast period (360–450 days), fine-root necromass loss during the slow periods was not significant. Fine-root mass of H. mongolicum and S. psammophila was gradually lost during 540 days of decomposition. However, fine-root mass showed different decomposition rates between the two growth periods in three shrub species (Fig. 4a). After 180 days, the remaining fine-root biomass of A. ordosica was 76.9 ± 1.9%, of S. psammophila was 80.7 ± 1.6%, and of H. mongolicum was 78.7 ± 2.1%, while after 540 days, the corresponding percentages were 60.8 ± 0.9% for A. ordosica, 76.2 ± 0.6% for S. psammophila, and 73.6 ± 0.9% for H. mongolicum. Fine-root C loss rate of A. ordosica was the highest among shrub species (Fig. 4b). During the initial 30 days, fine-root C loss was not significant in any shrub species (Fig. 4b). Thereafter, A. ordosica and S. psammophila had a fast period of C loss (30–60 days) and a slow period of C loss (60–180 days), while fine-root C of H. mongolicum decreased gradually (Fig. 4b). During the second growth period, H mongolicum had a slow period (330–450 days) and a fast period
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Fig. 5. Vertical distributions of light-fraction soil organic carbon and heavy-fraction soil organic carbon among the different shrub (A. ordosica, H. mongolicum, and S. psammophila) plots and the bare land plot. Low-case and capital letters indicate the significant difference of mean values of light-fraction and heavy-fraction soil organic carbon, respectively, among the treatments. Bars with the same letter indicate a non-significant difference (p = 0.05).
Fig. 4. Percent dry mass (a) and carbon (b) remaining of fine roots of different shrub species (A. ordosica, H. mongolicum, and S. psammophila) during 540 days of decomposition. Bars indicate standard error of the means (n = 5). Break days represent frost periods in the study site.
(450–540 days) of C loss, while A. ordosica had a fat period (330–450 days) and a slow period (450–540 days). After 180 days, fine-root C loss of A. ordosica was 18.1 ± 1.1%, of S. psammophila was 16.6 ± 1.0%, and of H. mongolicum was 14.9 ± 1.3%, while after 540 days, the corresponding percentages were 33.6 ± 0.3% for A. ordosica, 19.7 ± 0.4% for S. psammophila, and 21.4 ± 0.2% for H. mongolicum.
depth in bare land plot. However, it was observed that depth had an effect on LF-SOC and HF-SOC contents (Fig. 5) and LF-SOC content had a decreasing tendency with depth in shrub plots (Fig. 5). At the 0–40 cm depth intervals, vertical distributions of LF-SOC and HF-SOC in A. ordosica plot were significantly higher than those in S. psammophila and H. mongolicum plots (p < 0.001), and vertical distribution of LF-SOC in the S. psammophila plot was significantly higher than that in the H. mongolicum plot (p < 0.05; Fig. 5). At 40–80 cm depth intervals, LF-SOC content was significantly different in all shrub plots, while HF-SOC content in S. psammophila plot was higher than that in H. mongolicum plot (p < 0.05). Compared to total SOC content, a higher LF-SOC content was found in A. ordosica (68 ± 4.8%) and S. psammophila (67 ± 3.2%) plots at the 0–40 cm depth intervals (p < 0.05), while there was no significant change in H. mongolicum plot (Fig. 5).
3.4. SOC content and its fractions
4. Discussion
Down to a depth of 80 cm soils, the SOC content were 1387.8 g m1 for A. ordosica plot, 1019.2 g m1 for H. mongolicum plot, 922.8 g m1 for S. psammophila, and 492.5 g m1 for bare-land plot. SOC content was significantly higher in shrub plots than that in bare land plot (p < 0.001; Fig. 5). SOC content in A. ordosica plot was significantly higher than that in S. psammophila or H. mongolicum plots, while SOC content of H. mongolicum plot in the all soil layers was significantly greater than that of S. psammophila plot (p < 0.01; Fig. 5). Although no significant differences were observed in three shrub plots within the 20–80 cm soil layer, the SOC content showed a decreasing tendency with depth. More than 50% of SOC content in shrub plots was concentrated at the 0–40 cm depth intervals. Specifically, these percentages were 58.1 ± 2.0% in A. ordosica plot, 55.8 ± 2.0% in S. psammophila plot, and 54.1 ± 1.8% in H. mongolicum plot (Fig. 5). A significantly higher SOC content was observed in A. ordosica (37.0%) and S. psammophila (32.6%) plots at the 0–20 cm depth interval compared to that in H. mongolicum plot (25.4%). At the 0–20 cm depth interval, the LF-SOC content was higher than HF-SOC content in shrub plots (p < 0.05), although at deeper depth intervals results were reversed (Fig. 5). The proportion of LF-SOC and HF-SOC contents did not change significantly with
4.1. Vertical patterns of fine root biomass and production in three shrub species Despite the similar plot conditions, vertical patterns of fine-root biomass and production varied significantly among shrub species (Figs. 1 and 2). The fine root biomass of S. psammophila was significantly higher than that of H. mongolicum and A. ordosica, and the highest proportion was concentrated at the 0–40 cm depth intervals (Fig. 1). Although fine roots of A. ordosica were mostly concentrated at the 0–20 cm depth interval, no significant differences were observed among the 20–80 cm depth intervals. Fine-root distribution patterns of S. psammophila and A. ordosica were similar to those in many drylands, showing that depth intervals close to surface generally have a higher content of fine roots (Oppelt et al., 2005; Cheng et al., 2009; Gwenzi et al., 2011; Chang et al., 2012). In drylands, a high fine-root biomass close to surface might increase the ability of plants to absorb soil resources (particularly water) and adapt to drought periods (Gwenzi et al., 2011; Chang et al., 2012), while it might decrease their C investment (Huang et al., 2008). A comparison among shrub species showed a significant difference in fine-root biomass, which might be attributed to genetic differences (Oppelt et al., 2005). In addition, the fine-root
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biomass of some desert trees is relatively low close to surface (Chang et al., 2012), something that is in agreement with the low proportion of fine-root biomass at the 0–20 cm depth interval in H. mongolicum plot (Fig. 1). Previous studies have indicated that it is possible some shrubs with intense and shallow root systems, as well as others with deep root systems, to coexist and interact with neighbouring shrubs when resources are scarce in drylands (Ward et al., 2013). In our study, differences in vertical distribution of fine roots among shrub species suggested that they might have different adaption mechanisms when resources are limited. Fine-root production varied among different shrub plots (Fig. 3). Fine-root production of S. psammophila was significantly higher than that of H. mongolicum or A. ordosica (Fig. 1b). In addition, aboveground biomass of S. psammophila was strikingly greater than that of the other two shrubs (Table 1). These results may suggest that C investment to fine roots varies among shrub species. The highest amount of necromass occurred close to surface (Figs. 1 and 3), which may be attributed to the fact that in semi-arid and arid regions the topsoil is generally or periodically dry (Zhang et al., 2009). Nevertheless, the fine roots of different plant species respond to temporal changes of the topsoil in different ways (Ward et al., 2013). Fine-root production of S. psammophila was mostly concentrated in the 0–20 cm depth interval; however, fine root productions of H. mongolicum and A. ordosica in all soil layers were evenly distributed (Fig. 3). Some studies showed that fine-root production had different vertical patterns in different soil profiles due to heterogeneity of soil nutrients and water (Wang et al., 2014). Zhang et al. (2009) revealed that soil moisture in sandy soils increases with depth, which may suggest that plants with a higher proportion of fine roots at deeper depths can use water that is stored there and adapt better in drylands (Gwenzi et al., 2011). Overall, our results indicated that shrub species have different root foraging strategies. In this study, ingrowth core technique might overestimate fine root production. First, root growth of some plants were stimulated by some light damage and roots were generally damaged by using augers during soil core sampling. Second, the homogenized sandy soil habitat of reconstructed ingrowth core will present a less competitive environment. Finally, the ingrowth bags were collected after 1 year, fine root turnover was not estimated inside this period. However, there was not a better alternative method that can be used as a quick and less expensive method of estimating fine root production. Despite limitations, the results are helpful for assessing the effect of shrub species on fine root production and the differences of root forage strategies among different shrubs. 4.2. SOC stock and distribution SOC stocks down to 80 cm soil depth ranged from 922.8 to 1387.8 g m1 after revegetation on stabilized sand dunes (Fig. 5). Our study generated generally lower values than those in previously reported studies in semi-arid or desert regions (Jeddi et al., 2009). For instance, Yüksek and Yüksek (2011) reported that revegetation on bare sand improved SOC stocks at the 0–20 cm interval, ranging from 1610 to 9420 g m1, while Liu et al. (2010) showed that SOC content ranged from 8.2 to 10.5 Mg ha1 at the same depth interval in semi-arid regions. A probable explanation is that in our study the time period for SOC accumulation after revegetation was relatively short, Additionally, it is known that SOC stocks increase with precipitation (Jobbágy and Jackson, 2000; Wang et al., 2014), thus, in our study, low precipitation (287 mm) was a major limiting factor for plant production and litter decomposition that subsequently affected SOC content. More than 50% of SOC content in shrub plots was concentrated at the 0–40 cm depth intervals (Fig. 5). Our results are in agreement with previous studies that also reported a high SOC content
close to surface (Wang et al., 2004), which was mostly attributed to litter (leaf and root) input (Upson and Burgess, 2013) and soil crust (Feng et al., 2013). However, most of the studies have focused only on depths close to surface, neglecting vertical distribution (Upson and Burgess, 2013). As a result, collected data on SOC spatial heterogeneity were insufficient or estimation of SOC content was inaccurate (Wang et al., 2014). In any case, SOC stocks in large regions with high heterogeneity remain to be investigated. 4.3. Effects of revegetation on SOC stocks and fractions SOC stock and distribution varied significantly in shrub plots (Fig. 5). A. ordosica had the highest SOC stocks (1387.8 g m1), followed by H. mongolicum (1019.2 g m1) and S. psammophila (922.8 g m1). Compared to the bare land plot (492.5 g m1), our results suggested that revegetation improved SOC stocks significantly (Fig. 5) and they are in agreement with previous reported studies (Nosetto et al., 2006; Yüksek and Yüksek, 2011; Zhang et al., 2014). In degraded drylands, revegetation with shrubs generally increased C input to soil through litter production (Yüksek and Yüksek, 2011). Our results indicated that SOC stocks were higher after revegetation (Fig. 5). Specifically, SOC stocks in A. ordosica, S. psammophila, and H. mongolicum plots increased 1.82, 1.07, and 0.87 times, respectively, more than those in the bare land plot. Variation in SOC stock increase among shrub species may be attributed to different mechanisms of C input to soil and litter composition (Hiltbrunner et al., 2013). Additionally, soil microbial communities, which control the decomposition of litter and thus regulate C mineralization, are primarily affected by vegetation types (Clemmensen et al., 2013). Different vegetation practices may lead to different microclimatic conditions, which significantly affect organic matter decomposition (Kellman et al., 2007). LF-SOC content was more variable among different depth intervals (Fig. 5) than that of HF-SOC (Fig. 5) and its content was more easily affected by soil depth (Liu et al., 2010). One possible explanation may be that LF-SOC is controlled by the amount of litter input, which differs among plant species (Puget et al., 2000). Increase in total SOC content was mainly due to increase in LF-SOC (Fig. 5), except for A. ordosica plot, indicating that this change was unstable. LF-SOC content primarily derives from plant residues, roots, and fungal hypha at different decomposition stages (Kimetu and Lehmann, 2010) and is generally sensitive to land-use changes, while HF-SOC is not (Puget et al., 2000; Liu et al., 2010) due to its slow formation (Six et al., 2004). In our study, the highest increase in HF-SOC content was observed in the A. ordosica plot compared to the H. mongolicum and S. psammophila plots (Fig. 5), indicating that mechanisms of SOC accumulation differ among different revegetation practices. These results indicated that A. ordosica might be a better species for revegetation in terms of SOC sequestration. Although increased HF-SOC and LF-SOC were affected by the amount and quality of litter (Liu et al., 2010), the mechanisms of SOC accumulation were strongly controlled by SOC dynamics and turnover (Asaye and Zewdie, 2013). SOC dynamics and turnover remain to be studied under different revegetation practices in order to better understand the mechanisms that underlie SOC accumulation. 4.4. Effects of fine roots on SOC content Our results showed that C content from fine-root litter might be low in shrub plots (Fig. 1). Compared to the H. mongolicum (0.5 g C m2 years1) and A. ordosica (0.4 g C m2 years1) plots, the S. psammophila plot (8.1 g C m2 years1) had the highest C content derived from fine-root necromass. Our results showed that a high content of fine-root biomass and production supported the return of organic mass and nutrients through fine-root turnover
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(Yang et al., 2004); however, higher fine-root biomass and production did not represented greater SOC (LF-SOC and HF-SOC) content in shrub plots (Figs. 1, 2 and 5). Similarly, SOC stocks did not respond to high fine-root biomass (Ferguson and Nowak, 2011) and soil C accretion was not dependent on the amount of standing fine-root biomass and production (Asaye and Zewdie, 2013). A possible explanation could be that in addition to fine root litter, leaf and branch litter, insoluble organic matter from roots, refractory microbial biomass, and live root exudates mostly contribute to SOC accumulation at deeper soil depths in some regions (Matamala et al., 2003; Uselman et al., 2007). For example, some studies have indicated the importance of SOC originating from live roots as root exudates (Uselman et al., 2007). Another study showed that leaf litter decomposition, rather than root litter, was the major contributor to soil fertility (Tang et al., 2013). These results suggested that the fine-root litter of different shrub plots contributes to SOC accumulation at different rates and the mechanisms of SOC accumulation varies among shrub plots. Our results showed that the fine roots of A. ordosica had the fastest decomposition rate compared to the other two shrub species (Fig. 4), which might be an explanation of SOC stocks variation among shrub plots. An increase in SOC stocks mainly depends on the rate of fine-root decomposition, which is affected by genetic and environmental factors (Hobbie et al., 2010). Some studies demonstrated that fine-root decomposition was important for C input to soil (Lemma et al., 2007; Hobbie et al., 2010). A root-litter decomposition experiment showed that the initial root-mass and C decomposition of S. psammophila and H. mongolicum were slow (Fig. 4), indicating that fine-root litter C was more slowly released to soil compared to A. ordosica, even though fine-root turnover occurred in soil. These results indicated that A. ordosica might be a better species for improving SOC accumulation in the study site and a possible explanation of the reason that A. ordosica plot had the highest increase in SOC storage. It should be pointed out that we did not measure any seasonal dynamics or the turnover of fine roots, which could have resulted in an underestimation of C input from fine roots. Fine-root mortality and dieback are possible to occur across all seasons (Matamala et al., 2003). Thus, we might have underestimated the contribution of fine-root litter to SOC accumulation. Further, the mesh-bag experiment showed that most of the initial materials remained for more than 2 years. Simultaneously, the changes in soil properties of ingrowth cores might result in an overestimation on fine-root production. Therefore, our results on fine roots may only allow us to make comparisons among shrub species. In future studies, fine-root turnover should be monitored for to obtain a more accurate estimate of the effect of fine-root litter on SOC accumulation after revegetation. 5. Conclusions Revegetation with xerophilous shrubs is an effective approach to combat desertification in northwestern China. Our study showed that the development of S. psammophila, H. mongolicum, and A. ordosica significantly improved SOC compared to bare-land plots. Increase in total SOC content was mainly due to an increase in LF-SOC, except for the A. ordosica plot. Although S. psammophila had the highest fine-root biomass and production among shrub species, the highest increase in SOC was observed in the A. ordosica plot, followed by the H. mongolicum and S. psammophila plots. The effect of fine-root litter on SOC accumulation varied significantly among different shrub plots. Therefore, A. ordosica may be a better species for SOC accumulation and sequestration in the study site. Overall, the results suggested that the mechanism of SOC accumulation and sequestration differed among shrub plots.
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