Effects of afforestation on microbial biomass C and ...

Journal of Sustainable Forestry

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Effects of afforestation on microbial biomass C and respiration in eroded soils of Turkey Omer Kara, Emre Babur, Lokman Altun & Mustafa Seyis To cite this article: Omer Kara, Emre Babur, Lokman Altun & Mustafa Seyis (2016): Effects of afforestation on microbial biomass C and respiration in eroded soils of Turkey, Journal of Sustainable Forestry, DOI: 10.1080/10549811.2016.1190759 To link to this article: http://dx.doi.org/10.1080/10549811.2016.1190759

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Date: 27 June 2016, At: 02:00

JOURNAL OF SUSTAINABLE FORESTRY, 2016 http://dx.doi.org/10.1080/10549811.2016.1190759

Effects of afforestation on microbial biomass C and respiration in eroded soils of Turkey Omer Karaa, Emre Baburb, Lokman Altunb, and Mustafa Seyisa a

Department of Watershed Management, Faculty of Forestry, Karadeniz Technical University, Trabzon, Turkey; Department of Soil Science and Ecology, Faculty of Forestry, Karadeniz Technical University, Trabzon, Turkey

Downloaded by [Indira Gandhi Krishi Vishwavidyalaya ] at 02:00 27 June 2016

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ABSTRACT

KEYWORDS

Soil erosion is a major socioeconomic and environmental problem in Turkey. Almost 86% of the land in Turkey has suffered various degrees of soil erosion. The objective of this study was to determine whether differences in tree species affect soil characteristics and microbial activity in degraded soils. Results from this study showed that organic C (Corg) was highest in the black locust soil at 0–20 cm depth and lowest in the bare land. Microbial biomass C (Cmic) increased in the order black locust > Scotch pine > bare land at two soil depths. One-way ANOVA demonstrated that afforested soils contain significantly higher microbial biomass C than those in the bare land soils. Microbial quotient (Cmic/Corg) of soils are positively influenced by afforestation as the bare land soils exhibited lower microbial quotient than the associated Scotch pine and black locust soils. Microbial communities in black locust soils were energetically more efficient—had a lower metabolic quotient (qCO2)—with a higher Cmic/Corg compared to those in Scotch pine soils. However, the microbial quotient in our study was still below range and cannot reach equilibrium again 15 yr after afforestation. Restoration of degraded lands could be a long-term process from microbial activity in the observed regions.

Afforestation; black locust; microbial biomass; Scotch pine; soil erosion

Introduction Forests in Turkey cover 21.6 million ha, equal to 27% of the total land mass of the country. However, Turkey is one of the most erosion-prone countries in the world. Climatic features; steep slopes; large-scale forest fires; and socioeconomic factors such as land misuse, overgrazing, and illegal forest activities lead to an increase in soil erosion as well as environmental problems. Currently, the Turkish Ministry of Forestry and Water Affairs is implementing nationwide reforestation or afforestation with a goal of increasing forestland to cover 30% of total Turkish area by the end of 2023. The most common tree species used for erosion control in Turkey are Scotch pine and black locust, because of their high tolerance against drought and poor soil conditions (Turkish Ministry of Forestry and Water Affairs, 2008). The on-site and off-site impacts of water erosion are very serious environmental problems for the sustainable management of soils and watersheds in Turkey, since they CONTACT Omer Kara [email protected] Department of Watershed Management, Faculty of Forestry, Karadeniz Technical University, 61080 Trabzon, Turkey. Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/WJSF. © 2016 Taylor & Francis


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can lead to reduced soil fertility, sedimentation, pollution, and increased flooding. Due to the climatic and topographic conditions, reduction of plant cover, and excessive grazing, almost 86% of the land is suffering from some degree of soil erosion (Kara & Baykara, 2014). In some bare land of Turkey, where soil erosion is particularly severe, afforestation can be an important tool to rehabilitate the capacity of ecosystems. Afforestation of bare land to forest plantations has been carried out for timber demands, soil erosion and flood control, and the potential for forests to sequester atmospheric carbon dioxide (CO2). In order to expand site specific afforestation programs, matching the appropriate tree species to the soil characteristics needs special attention (Goel, Behl, & Singh, 2007). Many studies have found that the size of microbial biomass is mainly controlled by the soil physico-chemical properties (Singh, Munro, Potts, & Millard, 2007; Wakelin et al., 2008), but other studies suggest a strong effect of vegetation type on microbial biomass and its activity (Bezemer et al., 2006; Lamb, Kennedy, & Siciliano, 2011). Changes in ecosystem properties following afforestation are also likely to have positive effects on microbial biomass and activity. Previous studies from afforested ecosystems indicate that vegetation enhances soil-forming processes, leading to the buildup of organic matter and development of microbial communities (Fernández-Ondoño et al., 2010; Korkanç Yaşar, 2014; Prescott & Grayston, 2013). Soil microorganisms affect soil function and productivity in a variety of ways and provide an early sign of soil improvement or an early warning of soil degradation (Kara & Bolat, 2009; Muscolo, Panuccio, Mallamaci, & Sidari, 2014). Surface horizons are serving as a reservoir for soil microbial biomass also important for decomposition and nutrient cycling. The loss of topsoil can cause the diverse living organisms comprising the soil microflora to be carried away with the eroded soil. The loss of soil microflora through accelerated erosion can have detrimental effects on soil properties and cause a substantial decline in land value (Mabuhay, Nakagoshi, & Isagi, 2004). The breakdown of soil aggregates on eroded sites may be responsible for increased microbial mineralization and CO2 content of atmosphere, enhancing the greenhouse effect (Lal, 2005). Previous studies of afforestation in the Eastern Black Sea region of Turkey have focused on soil physicochemical characteristics. There is a need for research to determine the effect of land use change from bare land to forest plantation on microbial biomass C and activity in eroded soils. This study tested the hypothesis that soil microbial biomass C and activity were altered when bare land is afforested with either Robinia pceudoacacia L. or Pinus silvestris L. We also tested whether microbial biomass and activity were correlated to changes at two depths of 0–20 and 20–40 cm in the afforested soils.

Materials and methods Study sites The study was conducted in the Gümüşhane Province located on the south-facing slope of the Northeast Black Sea mountainous region of Turkey (40° 34′ N, 39° 17′ E; Figure 1). The elevation is approximately 1,300 m, with a west-southwest aspect. The region occupies a semi-arid and semi-humid zone of a continental climate. According to the climatological data for the past 30 yr, the area has mean annual temperature of 9.4°C and mean annual


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Figure 1. Location of the study site.

precipitation of 461 mm, with about 54% of rainfall occurring in the growing season between April and September. The mean temperature of the hottest month (July) is 39.5°C and the mean temperature of the coldest month (February) is −19.0°C. Soils in the studied area are classified as Entisol that show little horizon development in the profile. This study was conducted in autumn 2013, in Scotch pine (Pinus silvestris L.) and black locust (Robinia pseudoacacia L.) afforestation sites planted between 1995 and 2000 by the General Directorate of Afforestation. The plantation was established in four different locations within Gumushane and covered a total area of 346 ha. The sites were mechanically prepared with an excavator. Irrigation and fertilization were applied for the first 5 yr after planting. The bare land specified as the control area was considerably degraded grassland (density of plant cover in this area was < 5%) exposed to erosion and not fertilized.

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Soil sampling This experiment was conducted in a completely randomized design. Soil samples were taken at the 0–20 and 20–40 cm depths in each afforested area (Scotch pine and black locust) and the bare land used as a control. Stones, plants, and root debris were removed. Soil subsamples were sieved (< 2 mm) and stored at 4°C until they were destructively sampled during the following 3 days; other soil subsamples were air-dried, ground, and sieved (< 2 mm) as well. A total of 300 soil samples were collected from 25 different points of each land use types.


Physical and chemical properties of soils Soil physical and chemical properties were determined by the appropriate method: soil particle size distribution by the hydrometer method, pH of a 1:2.5 soil/water suspension with a pH meter, electrical conductivity (EC) in a 1:5 soil/water suspension with an EC meter, soil organic C by the Walkley-Black wet oxidation method, and CaCO3 content by the Scheibler calcimeter method (Rowell, 1994). Microbial biomass C (Cmic) Soil microbial biomass C (Cmic) was estimated by extracting 30-g oven-dry equivalents of field-moist mineral soil samples in 0.5 M K2SO4 (1:4 w/v) by the chloroform-fumigationextraction method described by Brookes et al. (1985) and Vance et al. (1987). Cmic was calculated from the difference in extractable organic C between fumigated and unfumigated soil samples as follows: biomass C = 2.64 EC, where EC refers to the difference in extractable organic C between the fumigated and unfumigated treatments; 2.64 is the proportionality factor for biomass C released by fumigation extraction (Vance et al., 1987). The microbial quotient (Cmic/Corg) was calculated by expressing Cmic as a percentage of total soil Corg. Basal respiration Basal respiration was determined by placing 50-g soil samples into 50-mL beakers and incubating them in the dark at 25°C in 1-L airtight, sealed jars along with 25 mL 0.05 M NaOH. After 7 days, the generated CO2 was measured by titration of excess NaOH with 0.05 M HCl (Alef, 1995). The metabolic quotient (qCO2) was calculated as the basal respiration rate (μg CO2-C h−1) per mg of microbial biomass C (Dilly & Munch, 1998). Statistical analyses This study was conducted with a completely randomized design. The effects of afforestation on physical, chemical, and microbial characteristics of soil were analyzed by ANOVA, and mean separations were computed using Duncan’s multiple range tests. Bivariate analysis was also performed with Pearson’s linear correlation between soil variables. Discriminant analysis (DA) is used to analyze the differences between two or more groups of multivariate data using one or more discriminant functions in order to maximally


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separate the identified groups. Therefore, DA was employed to find the difference between the tree species along with the soil variables. Statistical analyses were carried out using the Statistical Package for the Social Sciences Version 11.00 (SPSS Inc., Chicago, IL, USA) software package.

Results and discussion


Soil physical and chemical properties Selected physicochemical properties of the soil showed substantial differences between Scotch pine, black locust, and bare land (Table 1). The percentage of sand, silt, and clay, as well as CaCO3, pH, organic carbon, and available water were differed significantly by land use type. Soils collected in Black locust showed a significantly higher sand content at both depths (0–20 and 20–40 cm) in comparison to pine and bare land. In the mineral subsoils, the mean clay content was higher on average by 10.6–17.49% than the corresponding topsoil in the three land use types. It should be pointed out that in the soils of the research area, clay particles percolated through the soil, and accumulated in the subsoil. Bockheim and Hartemink (2013) show that a clay-enriched horizon is recognized in soil taxonomy at some level in 10 of the 12 soil orders. As we expected, high relative surface soil organic C changes was determined compared with subsoil following afforestation (Table 1). The percentage of organic C was highest in the black locust soil at 0–20 cm depth and lowest in the bare land (Table 1). Compared to the value (1.37%) for the surface soil under bare land, the contents of organic C increased 1.35-fold for black locust soil. Afforestation changes the quality and quantity of soil organic C through many pathways, including species-specific effects on litter production (Berthrong, Jobbagy, & Jackson, 2009; Paul, Polglase, Nyakuengama, & Khanna, 2002), root exudates (Grayston, Vaughan, & Jones, 1996), microbial community structure (Kara & Bolat, 2007), and variation of microclimate (Oke, 1987) would be expected to result in differential availability of various C sources in degraded soils. Increased organic C in the surface soils of black locust may be attributed to high rates of leaf fall (White, 1986). The use of N2 fixing black locust may increase leaf production and hence the amount of organic C input to soil. Previous studies show that following afforestation, the increase in Table 1. Comparison of some soil characteristics for the three land uses at the two depths.

Soil characteristics Sand (%) Silt (%) Clay (%) Soil texture CaCO3 (%) pH in water EC (dS m−1) SOC (%) AW (%)

Scotch Pine

Black locust

Bare land

Soil depth (cm)

Soil depth (cm)

Soil depth (cm)

0–20 69.98 ± 8.5a 9.40 ± 3.8a 20.60 ± 8.8a Sandy clay loam 1.68 ± 0.6a 7.65 ± 0.3a 0.12 ± 0.0a 1.49 ± 0.2a 8.81 ± 3.4a

20–40 68.20 ± 8.7A 9.70 ± 2.5A 22.08 ± 8.1A Sandy clay loam 1.55 ± 0.5A 7.50 ± 0.5A 0.10 ± 0.0A 1.20 ± 0.2A 8.86 ± 4.2A

0–20 77.19 ± 6.5b 8.81 ± 2.6a 13.98 ± 5.7a Sandy loam 1.39 ± 0.3b 7.68 ± 0.3a 0.16 ± 0.0a 1.85 ± 0.8b 8.16 ± 3.0ab

20–40 75.27 ± 4.6B 9.04 ± 1.9A 15.67 ± 4.1B Sandy loam 1,34 ± 0.4A 7.45 ± 0.5A 0.11 ± 0.0A 1.24 ± 0.5A 8.57 ± 3.9A

0–20 73.33 ± 4.8a 12.54 ± 2.6b 14.12 ± 3.4a Sandy loam 1.63 ± 0.1ab 7.75 ± 0.1a 0.15 ± 0.0a 1.37 ± 0.2a 6.59 ± 2.4b

20–40 71.04 ± 5.3A 12.35 ± 2.8B 16.59 ± 4.3B Sandy loam 1.54 ± 0.2A 7.76 ± 0.2B 0.12 ± 0.0A 1.14 ± 0.3A 7.59 ± 3.7A

Note. Values are the mean of 25 samples ± standard deviation. Within rows, the same lowercase letters indicate no significant differences (p > .05) for 0–20 cm and the same uppercase letters indicate no significant differences (p > .05) for 20–40 cm. EC = electrical conductivity, SOC = soil organic carbon, AW = available water.

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soil organic C was greater under plantations of N2-fixing species than in plantations of non-N2-fixing species (Bolat, Kara, Sensoy, & Yüksel, 2015; Nilsson, Schopfhauser, Hoen, & Solberg, 1995; Resh, 1999). Our results also indicated that increased organic C observed in the black locust soils was probably due to its higher litter quality. Black locust leaves decompose faster than Scotch pine needle and thus increase transformation of plant residues to soil organic C through enhancing microbial activity.


Soil microbial biomass carbon (Cmic) and microbial quotient (Cmic/Corg) The mean values for microbial biomass C were 165.8, 211.2, and 99.9 μg g−1 at 0–20 cm depth in the Scotch pine, black locust, and bare land soils, respectively; whereas these values were 167.7, 194.5, and 51.6 μg g−1 at 20–40 cm depth. Cmic increased in the order black locust > Scotch pine > bare land at both soil depths. One-way ANOVA demonstrated that afforested soils contained significantly higher microbial biomass C than those in the bare land soils (Figure 2a). This result clearly shows that afforestation improved microbial biomass C during the 15 yr after establishment. In the understory of the afforested area, organic matter inputs were large and arose from litter and fine roots, and exudation of organic compounds from roots may favor the accumulation of C in microbial biomass at the soil surface (Kara, Bolat, Cakıroglu, & Senturk, 2014; Stevenson, Sarmah, Smernik, Hunter, & Fraser, 2016; Wang, Fu, Lu, & Chen, 2011; Zhu, Li, Li, Liu, & Xue, 2010). Black locust plantations were more successful in rehabilitation of eroded soils compared to Scotch pine in the research area, due to its rapid growth rate and soilimproving properties. These results are consistent with those of previous studies showing that black locust is a valuable tree species for rehabilitation of eroded land, in that its impact on the soil creates favorable conditions, thus promoting the recovery of the soil microorganisms (Bolat et al., 2015; Lukić et al., 2015; Wang, Liu, & Xue, 2012). Soil microbial biomass did not decrease significantly with increasing soil depth in the afforested soils compared to bare land (Figure 2a). This could be explained by the fact that soil tillage may increase loosening which improves aeration and infiltration of water, and creates a greater volume for the development of roots and microorganisms following afforestation.

Figure 2. Changes in microbial biomass C (a) and Microbial quotient (Cmic/Corg) (b) with afforestation in two soil depths. Different letters above the bars indicate significant differences at p < .05 among the land use types.



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Microbial quotients (Cmic/Corg) of surface soils (0–20 cm) under Scotch pine and black locust, 1.10 and 1.14%, respectively, were significantly higher than those under bare land, 0.72% (Figure 2b). At the 20–40 cm soil depth, microbial quotient (Cmic/Corg) for scotch pine and black locust, as 1.39 and 1.56%, respectively, were 3.0–3.4 times (p < .05) larger than those for bare land (0.45%). It is clear that the microbial quotient of soils in terms of production of more labile organic substrates is positively influenced by afforestation as the bare land soils exhibited a lower microbial quotient than did the associated Scotch pine and black locust soils. These results agree with several previous studies that found afforestation on barren degraded soil leads improvement of soil microbiological characteristics (Chodak, Pietrzykowski, & Niklinska, 2009; Rong Mao & Zeng, 2010), thus supporting a relatively higher microbial quotient. The comparatively low ratio in bare land soil can, therefore, be ascribed to the more recalcitrant substrates maintained in both soil depths. The microbial quotient in agricultural and forest soils at neutral pH is very similar and in the range between 2.0 and 4.4% (Anderson, 2003). That average values (between 0.45 and 1.56%) in our study were still below this range and were unable to reach equilibrium 15 yr after afforestation of eroded land.

Microbial basal respiration (MR basal) and metabolic quotient (qCO2) Basal respiration (µg CO2-C g−1 h−1) ranged between 0.78 and 0.91 at 0–20 cm and 0.75 and 0.85 at 20–40 cm in the research area (Figure 3a). There was no significant effect of afforestation on basal respiration rates (p > 0.05) at the two soil depths. The low values of basal respiration recorded for these soils overall probably reflect their low total C content due to the frequent soil erosion events. Metabolic quotient (qCO2) has been widely used to assess soil development, substrate quality, response to stress and management practices (Anderson & Domsch, 1993; MartínLammerding, Navas, Albarrán, Tenorio, & Walter, 2015). Increases in qCO2 have been related with environmental stress and recalcitrant substrate (Killham, 1985; Spohn, 2015), while decreases in qCO2 have been associated with plant succession and high efficiency of substrate utilization (Sinsabaugh, Manzoni, Moorhead, & Richter, 2013). Values of qCO2 for neutral soils in a range from 0.5 to 2.0 μg CO2-C mg Cmic−1 h−1 were reported by Anderson (2003). In this study, qCO2 ranged from 0.47 to 1.45 μg CO2-C mg Cmic−1 h−1,

Figure 3. Changes in microbial basal respiration (a) and metabolic quotient (qCO2) (b) with afforestation in two soil depths. Different letters above the bars indicate significant differences at p < .05 among the land use types.

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with bare land soils having higher levels compared to afforested soils (p < .05). We determined the lowest values of qCO2 in black locust at depths of 0–20 cm and 20–40 cm (0.47 and 0.57 μg CO2-C mg Cmic−1 h−1, respectively; Figure 3b). The high metabolic quotient in the bare land indicated a low efficiency of the substrate utilization by the soil microbial community. In generally, soils with higher diversity are able better utilize the substrate what leads to lower values of metabolic quotient (Makova, Javorekova, Medo, & Majercikova, 2011). These results indicate that high microbial diversity in afforested soil are energetically more efficient (lower qCO2) with a corresponding higher Cmic/Corg percentage (increased biomass) compared to those in bare land.

Discriminant analysis Discriminant analysis (DA) was able to separate Scotch pine, black locust, and bare land from each other, for the topsoil as well as for the subsoil (Figure 4a and 4b). The soil variables that contributed to the classification and the values of the two canonical functions are shown in Table 2. A score above 0.3 is considered significant (Hair, Anderson, Tatham, & Black, 1992). At the topsoil (0–20 cm), the eigenvalues for the first 2 axes were 1.185 and 0.679, respectively; and they captured 63.6 and 36.4% of the total variance (Figure 4a). Correlation coefficients indicate that DA axis 1 is most strongly correlated with sand, clay, available water and microbial biomass C; and that DA axis 2 is mainly correlated with clay, available water, basal respiration, pH, organic carbon, microbial biomass C, Cmic/Corg and qCO2 (Table 2). At the subsoil (20–40 cm), two functions were obtained with eigenvalues, respectively, being 3.087 and 0.445. These functions could explain, respectively, 87.4 and 12.6% of the total variance (Figure 4b). The first axis was positively correlated with sand, clay, available water, basal respiration and microbial biomass C, while negatively correlated with pH. The second axis was positively correlated with organic C, sand, microbial biomass C and qCO2, while negatively correlated with lime and basal respiration (Table 2).

Figure 4. Scatter plot of the first two discriminant function values in 0–20 (a) and 20–40 cm depths (b).


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Table 2. Standardized coefficients of the canonical discriminant functions. Function Soil variables (0–20 cm) pH SOC Sand Clay AW MBS Cmic Cmic/Corg qCO2

1 −0.148 0.100 1.541 1.562 0.418 −0.202 0.586 0.020 −0.153

Function

2 −0.529 −0.402 0.299 1.228 0.476 0.433 −0.505 −0.330 −0.374

Soil variables (20–40 cm) pH SOC Sand Clay AW AS CaCO3 MBS Cmic qCO2

1 −0.553 −0.142 1.300 1.251 0.423 0.407 −0.244 0.409 0.710 −0.274

2 0.114 0.550 0.977 0.036 −0.262 −0.109 −0,356 −0.669 0.505 0.306


Note. SOC = soil organic carbon, AW = available water, MBS = microbial basal respiration,Cmic = microbial biomass carbon, AS = aggregate stability.

Percentage correct (range of 68 to 92%) indicate that 80.0% of the scotch pine, black locust and bare land were the most reliably classified with respect to soil properties (Table 3) at two soil depths.The accuracy of classification for Scotch pine, black locust, and bare land was, respectively, 80, 76, and 84% in topsoil (0–20 cm) and 68, 80, and 92% in subsoil (20–40 cm). The classification matrix indicates that all soils considered as Scotch pine, 80% in topsoil and 68% in subsoil which were classified as belonging to the same group, while the remaining 20 and 31%, respectively, showed characteristics similar to those of the black locust and bare land. On the other hand, the soils considered to be under black locust, 24% in topsoil and 20% in subsoil presented characteristics similar to those of soils under Scotch pine and bare land, respectively. The soils considered as bare land, 84% in topsoil and 92% in subsoil were classified as belonging to this group, while the remaining 16 and 8%, respectively, and showed characteristics similar to those of the Scotch pine and black locust (Table 3). Microbial biomass and activity may responsible for the separation of the Scotch pine, black locust, and bare land by DA, because afforested soils offer more sites and substrate for microbial community, thus promoting microbial quotient (higher Cmic/Corg percentage) and metabolic quotient (lower qCO2). These results provide strong evidence that different soil properties and microbial community occurred in the areas afforested with Scotch pine and black locust compared to those in bare land.

Conclusions This study demonstrated that afforestation leads to changes in soil properties, notably increases in organic carbon and improved microbial biomass and activity in these types of Table 3. Classification matrix after the discriminant analysis of soil properties at the two depths. Predicted classification Percentage correct* Original group Scotch pine Black locust Bare land

Scotch pine

Black locust

Bare land

0–20 cm

20–40 cm

0–20 cm

20–40 cm

0–20 cm

20–40 cm

0–20 cm

20–40 cm

80 76 84

68 80 92

20 2 3

17 5 1

3 19 1

8 20 1

2 4 21

0 0 23

Note. *Percentage correct indicates the percentages of cases that were correctly classified, while the fourth to ninth columns show the number of cases that were correctly and incorrectly classified by the discriminant analysis.

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degraded land, especially in the top soils. Black locust was more efficient than Scotch pine for soil rehabilitation in the research area. Microbial communities in black locust soils were energetically more efficient (had a lower qCO2) with a higher Cmic/Corg compared to those in Scotch pine soils.The selection of tree species can affect the success of afforestation in land degraded by water erosion, especially in arid and semiarid areas. Therefore, the choice of appropriate tree species for afforestation may help forest land managers to achieve success in the control of soil erosion.


Acknowledgments The authors are grateful to Dr. Kenneth A. Sudduth and Dr. Robert J. Kremer at the University of Missouri for their helpful advice and valuable comments that have greatly improved the quality of the manuscript.

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