cover in northern Iran

cover in northern Iran

Acta Ecologica Sinica 39 (2019) 328–333 Contents lists available at ScienceDirect Acta Ecologica Sinica journal homepage: www.elsevier.com/locate/ch...

696KB Sizes 0 Downloads 83 Views

Acta Ecologica Sinica 39 (2019) 328–333

Contents lists available at ScienceDirect

Acta Ecologica Sinica journal homepage: www.elsevier.com/locate/chnaes

Evaluating soil biochemical/microbial indices as ecological indicators of different land use/cover in northern Iran Negar Moghimian, Seyed Mohsen Hosseini ⁎, Yahya Kooch, Behrouz Zarei Darki Faculty of Natural Resources & Marine Sciences, Tarbiat Modares University, 46417-76489 Noor, Mazandaran, Iran

a r t i c l e

i n f o

Article history: Received 27 June 2018 Received in revised form 4 January 2019 Accepted 17 May 2019 Available online 25 May 2019 Keywords: Natural forest Plantation Microbial indices Soil respiration

a b s t r a c t The objective of the study was to examine changes in microbial parameters have been used to monitor changes in soil quality under different land uses in north of Iran. The microbial parameters included microbial respiration (MR), substrate induced respiration (SIR), carbon availability index (CAI), microbial biomass carbon (MBC), microbial biomass nitrogen (MBN), ratio of MBC/MBN, metabolic quotient (qCO2) and microbial ratio were determined under different land use/cover, i.e. virgin natural forest (VNF), degraded natural forest (DNF), alder plantation (AP), sequoia plantation (SP), improved fallow (IF) and home garden (HG) areas in northern Iran. Five composed samples per land use/cover were taken from the top 10 cm of the soil. MR and SIR (0.45 and 1.66 mg CO2-C g−1 day−1, respectively) were found to be significantly higher under AP land uses than in the other areas. CAI did not differ for the land uses; MBC (591 and 590 mg kg−1, respectively) had higher significantly under SP and VNF land uses than in the other areas. MBN (64.25 and 62.33, respectively mg kg−1) was significantly higher in AP and VNF land uses, ratio of MBC/MBN (17.02) was higher in SP land use than other areas, HG had significantly higher qCO2 (0.0012 μg CO2-C mg−1 MBC day−1) and finally microbial ratio was significantly higher under IF (599.16) in comparison with HG N AP ≈ DNF N VNF N SP areas. Overall, our results indicate that AP land use (Alnus subcordata C. A. Mey.) increase of soil quality and alder plantation is suitable for rehabilitation of degraded natural forests. © 2019 Published by Elsevier B.V. on behalf of Ecological Society of China.

1. Introduction Changes in land use and inappropriate land management practices, that affect the environment often lead to severe soil deterioration and loss of soil quality especially microbial indicators [1–3]. The concentration of C and N may be positively or negatively related to soil microbial activities under different land uses [4]. Soil respiration as a key ecosystem process that releases C as CO2 from soil is affected by changing land use [5]. Liu et al. [6] has shown that the conversion of a natural forest into another land use such as plantation leads to a net accretion of soil respiration. By contrast, Mohanty and Panda [7] noted that natural forest conversion reduces soil respiration. Soil microbial biomass plays a critical role in nutrient retention and soil fertility in terrestrial ecosystems [8]. Soil microbial population size as represented by microbial biomass C (MBC) is one of the most frequently analyzed biological parameters for studying soil quality, because it is both a source of labile nutrients and an agent for the transformation of soil nutrients. Soil MBC together with metabolic quotient, microbial entropy and C availability index are recognized as sensitive indicators of changes in soil quality; these properties are ultimately affected by different land

⁎ Corresponding author. E-mail address: [email protected] (S.M. Hosseini).

https://doi.org/10.1016/j.chnaes.2019.05.006 1872-2032/© 2019 Published by Elsevier B.V. on behalf of Ecological Society of China.

covers and are considered to be quantitative indicators for C dynamics in soils [2]. Different cover influence on the soil microbial biomass N (MBN) and mineralization process can regulate overall nutrient cycling in land uses, which may occur through their effects on substrate quality, soil physico-chemical properties and microbial community [6]. As microbial parameters the soil metabolic quotient (qCO2, CO2 emission to microbial biomass ratio) are sensitive to disturbance [9]. This ratio is related to the microbial energy demand. Soil quality is a combination of soil properties that are able to readily change in response to variations in soil conditions [10].The importance of using indices to assess soil quality has been recently emphasized. In the last few years, a variety of soil quality indices has been proposed, several based upon biochemical and microbiological features [1]. We tested the following hypotheses: (1) forest degradation decreases microbial indices, and (2) alder plantation improve soil quality compared to needle-leaved plantation and non-forest covers. The present study aimed to evaluate different land use/ cover in northern Iran, also selecting and prioritize the appropriate species in this area.

N. Moghimian et al. / Acta Ecologica Sinica 39 (2019) 328–333

2. Objects and methods 2.1. Site location The objective of the study was to assess the effect of six land use systems, i.e. (I) intact natural stand (INS), (II) degraded natural stand (DNS) covered by Common hornbeam and Ironwood species, (III) alder plantation (AP), (IV) sequoia plantation (SP), (V) improved fallow (IF) and (VI) Agroforestry type of home garden (HG) areason soil biochemical/microbial indicators of soil quality in top soil. We hypothesized that i) land use and management practices affect biochemical/ microbial properties and ii) broad leaf plantation improve soil quality compared other land uses followed by increasing nutrient elements. To test our hypotheses, we determined soil microbial biomass-C, \\N and soil microbial respiration (MR), we also determined the substrate induced respiration (SIR), Carbon availability index (CAI), metabolic quotient (qCO2) and microbial ratio. This research carried out in Tilekenar district of Salmanshahr in Mazandaran province, northern Iran (between 36°39′36″ N–36°40′01″ N and 51°09′55″ E–51°10′18″ E; Fig. 1) with elevation of 250 m above sea level and a slope b 5%. Annual mean rainfall is 1300 mm with wet months between September and February and a dry season between May and August. Average annual temperature is 17 °C at the Noushahr city metrological station, which is 5 km away from the study area (Fig. 2). According to the USDA Soil Taxonomy, soils can be classified as silty-clay-loam Alfisols, developed on dolomite lime stones belonging to the upper Jurassic and lower Cretaceous period. The study area was previously covered by native species (i.e. Quercus castaneifolia C. A. M. macranthera F. & M., Zelkova carpinifolia (Pall.) Dippel, Parrotia persica C.A.Mey., Carpinus betulus L., Diospyros lotus. L. and Buxus hyrcana Pojark.), following unproductive exploits and destruction of the forest, about 27 years ago, reforestation has been done within 3 × 3 m spaces in this area, with Caucasian alder (Alnus subcordata C. A. Mey.), velvet maple (Acer insigne Boiss.), as well as exotic species of sequoia or redwood (Sequoia sempervirens (D. Don) Endl.) and mixed stand (Acer velutinum Boiss.(maple) and Sequoia sempervirens (D. Don) Endl.) in different areas. The stands were never fertilized. However, some areas were not afforested in 1989 and are now covered by degraded natural stand of Carpinus betulus-Parrotia persica, and improved fallow and home garden areas [11].

329

soil samples of each transect were mixed together in order to obtain a homogeneous sample and from each land use/cover 5 mixed soil samples, totally thirty (6 land uses/covers × 5 replicate), were transferred to laboratory in spring (in favorable conditions of moisture and temperature). On soil samples, physical (water content), chemical (pH, organic carbon, total nitrogen, available P, K, Ca and Mg contents) and biological (microbial respiration, substrate induced respiration, microbial biomass carbon/ nitrogen, metabolic quotient and microbial ratio parameters were analyzed. Soil water content was measured by weighing method and pH meter was employed to determine the soil pH. The WalkleyBlack technique was used to determine soil organic carbon. The total N was measured using a semi Micro - Kjeldhal technique. The available P was determined with spectrophotometer by using Olsen method. The available K, Ca, and Mg (by ammonium acetate extraction at pH 9) were determined with Atomic absorption spectrophotometer [12]. Soil microbial respiration (MR) was determined by trapping and measuring the evolved CO2 over a 5-day period. Substrate induced respiration (SIR), was determined using glucose (1%) as the substrate and the evolved CO2 was measured after 72 h incubation. The evolved CO2 was adsorbed in NaOH and measured by HCI titration. MBC and MBN were measured by fumigation-extraction method [13]. 2.3. Calculations and statistical analyses The soil metabolic quotient, qCO2 (MR: MBC), microbial ratio (MBC: Corg) and C availability index (MR:SIR) were calculated based on the values of organic C, MR, SIR and MBC [13]. The normality of the variables was checked by the Kolmogorov-Smirnov test and Levene's test was used to examine the equality of the variances. One-way analysis of variance (ANOVA) was used to compare soil properties data among the land uses. Duncan test was further employed to test for differences at the P = .05 level. All statistical analyses were conducted using the SPSS v. 20 statistical software packages. Factor analysis is a statistical tool for exploring complex relationships among variables. For this purpose, we used principal component analyses (PCA) to examine relationships in the multivariate data. Multivariate correlations were used to identify significant relationships among variables and principal components using PC-Ord version 5.0. 3. Results

2.2. Sampling and laboratory analysis

3.1. Soil physico-chemical properties

In each sampling site soil was collected in three soil profiles (25 × 25 cm) were dug along (at the beginning, the middle and the end) the five parallel transects in the central part of land use/cover, resulting in 15 soil samples for each site at a depth of 0–10 cm. Three

Water content was lowest under IF ≈ HG than in AP land use. Significantly highest soil pH was found under AP and IF ≈SP land uses had the lowest values, jointly. A significantly higher content of organic C was found under SP and for total N was found under AP among between land uses. A greater amount of the C/N ratio was found under SP area. Available P in the AP type showed significantly higher values when

Fig. 1. Location of the study area in the Mazandaran province, Northern Iran.

Fig. 2. Embrotermic curve of the study area, based on meteorological data.

330

N. Moghimian et al. / Acta Ecologica Sinica 39 (2019) 328–333

compared with other land uses. A greater amount of available K, Ca and Mg were detected under AP ≈ VNP than other land uses (Table 1). 4. Soil microbial and biochemical activities Soil BR and SIR were found to be significantly highest under AP than in other land uses. Soil CAI was not significantly different among land uses. Significantly higher amounts of soil MBC were found under VNP ≈ SP compared with the other studied land uses. A greater amount of the soil MBN was found under AP ≈ VNP land uses. MBC/MBN ratio was significantly higher under SP than in DNF ≈ IF ≈ VNF N AP N HG land uses. Soil qCO2 was higher under HG than in AP N IF N HG N VNF ≈ DNF ≈ SP land uses. Soil microbial ratio was significantly different among the land covers, IF ≈ HG had the highest value, jointly and SP had least value (Fig. 3). From the PCA output, explained N90% of variance in soil features under studied land uses. The right PC1 shows the condition with good quality, high values of water content, accumulation of macro element nutrients and high values of microbial fraction (BR, SIR, CAI, qCO2 and MBN) and this can be attributed to AP, VNF and HG land uses, while the left PC1 presented positions with less macro elements nutrients, and MBC, microbial ratio imposed by DNF, SP and IF land uses (Fig. 4). 5. Discussion The highest values of soil respiration (MR and SIR) were found under AP land use than natural forest. Different values of soil respiration in this study indicate that the substrate quality, humic substances, is very variable under different land uses [14]. Among this, presence of broadleaved species in natural mixed stands increased soil respiration, as compared with the other land uses that is accordance with the report of Fang et al. [4]. SP land use had lower soil respiration than AP land use at paired sites reviewed by Wang et al. [5]. Our results showed significant positive correlations between soil respiration and soil pH and water content in land uses. Maximum soil respiration occurs in the middle of the soil water range [15]. Our data is parallel to previous research [16] confirming that soil pH close to 7.0 is most suitable for microbial respiration. The C/N ratios tended to be higher under plantations, especially SP land use, suggesting that soil microbes would be more limited by nutrients than by substrate (C) availability in that situation. Soil nutrient contents are as a major factor controlling the variability in soil microbial respiration [17]. The high soil respiration under AP, VNF and HG respectively can be explained by an increase in the contents of soil nutrients (i.e. N, P, K, Ca and Mg), which would stimulate microbial activity thus leading to an increase in respiration from soil [17]. According to the findings of Kooch et al. [18], the soil total N content is one of the main factors that affect decomposition of plant litter, and litter decomposition rate is a major source of soil CO2 emission. Based on the results of the current study, greater values of total N were found under alder plantation, which includes higher microbial respiration as compared to sequia

plantation and IF. Parallel to this study, Cao et al. [19] reported that the soil N content promoted the release of CO2 from the soil. The metabolic quotient, qCO2 (MR per unit of microbial biomass) is considered as the most straight forward index widely used to evaluate ecosystem development, disturbance or system maturity and has a great potential for improving our understanding of the development of microbial communities in the ecosystem that they inhabit (20). However, qCO2 must be interpreted carefully because higher qCO2 indices are also correlated with the availability of easily degradable organic substrates and do not necessarily indicate stressful conditions [14]. In our study, the lower metabolic quotient, showed under SP land use, indicated higher efficiency of microbial function in soil. In contrast, for HG and after that AP land uses, the higher metabolic quotient indicated that important quantities of carbon per unit biomass [21], also similar our result Dinesh and Chaudhuri [22] represent qCO2 levels increase in the plantations land use. Enhanced qCO2 levels in the plantations, therefore, suggested greater maintenance demand suggesting that the conversion of total carbon into microbial carbon is less efficient leading to lower SMBC [20]. The variation in qCO2 can indicate that different microbial community structures occurred according to the different land use [23]. Changes in metabolic quotient can be attributable mainly to soil moisture, pH, organic C, total N and nutritional status of the soil under different land covers [24], some of which are similar to our results. Liu and Wang [25] pointed that higher soil microbial quotient, as an important indicator of soil quality, indicated carbon accumulation in the soil, and the microbial number and population structure in the soil changed with the land use/cover change. Based our data in this study, the C availability index (MR/SIR), isn't seen significant between land uses. Gorobtsova et al. [26] claimed that CAI the development of soils and the course of ecological succession and depends on the type of cultivated lands. The soil microbial entropy (ratio of MBC to total organic C) is used to reflect the balance of soil ecosystem, it is an index of the mineralization rate of soil microbes on organic matter, the higher value represents higher mineralization rate and could induce higher soil nutrient utilization rate. Similar our result decrease of microbial ratio under sequoia plantation (SP land use), It is due to the reduction of soil pH than other land uses [24,27]. Soil MBC is an important component in most terrestrial ecosystems and a small change in microbial biomass could have a major impact on plant nutrient availability [3]. Our data showed significant changes in soil MBC in natural forest and SP plantations. The increase in soil MBC in two land uses were probably a result of increased C input from the litter products. When C was supplied to soil in the form of residue, the microbial biomass increased in size. The microbial growth due to organic input is mainly dependent on the increased availability of C in the soil. Although the quantity of microbial biomass is mainly related to C inputs, other mitigating factors can regulate the growth and activity of the native micro flora [19]. Such as MBC, MBN decrease with change land use due to declining C input (i.e.by plant residues in IF) [3]. Decline in microbial biomass after conversion is also linked to tillage practices i.e. IF. Regular tillage in croplands changes the soil physicochemical environment, which affects microbial biomass [3,28]. After SP land use, VNF increases

Table 1 Mean values of the soil variable analyzed. Soil features

VNF

DNF

AP

SP

IF

HG

F test

p value

Water content (%) pH (1:2.5 H2O) Organic C (g kg−1) Total N (g kg−1) C/N ratio Available P (mg kg−1) Available K (mg kg−1) Available Ca (mg kg−1) Available Mg (mg kg−1)

28.18ab 6.90b 2.18b 0.22b 9.76b 12.61b 285a 280.3a 56.5a

27.85ab 6.83c 1.82c 0.19c 9.69c 6.51d 192b 254.1d 51.40ab

30.94a 7.06a 1.48d 0.32a 4.55d 13.01a 292a 286.3a 58.2a

28.20ab 6.15e 2.69a 0.12d 23.45a 6.26d 218ab 267.3bc 46.7b

26.35b 6.19e 0.51f 0.11d 4.50e 6.23d 207b 261.8 cd 46.60b

26.63b 6.25d 0.93e 0.21b 4.50e 8.56c 225ab 277.4ab 52.3ab

2.321 600.268 257.129 111.762 562,618.616 978.658 3.025 11.561 4.788

0.007 0.000 0.000 0.000 0.000 0.000 0.030 0.000 0.004

Results from the ANOVAs are included (F test and p value). Different letters in each line indicate significant differences (p b .05 by Duncan test) between land uses/covers. (VNF = virgin natural forest; DNF = degraded natural forest; AP = Alder plantation; SP=Sequoia plantation; IF=Improved fallow; HG = Home garden).

N. Moghimian et al. / Acta Ecologica Sinica 39 (2019) 328–333

0.5

a

b

d

0.3

DNF

AP

ns

0.35 0.3 0.25 0.2 0.15 0.1 0.05 0

IF

VNF

ns

ns MBC

DNF

AP

SP

IF

a

a

50

d

40

HG

(d)

e

30 20 10

(e) 0 VNF

DNF

AP

SP

IF

0.0014

HG

b

SP

IF

HG

a

b

DNF

AP

SP

d

d

IF

HG

a

b

b

b c d

DNF

AP

SP

IF

HG

a

700

c

d

0.0006

20 18 16 14 12 10 8 6 4 2 0

AP

c

VNF

Microbial ratio

d

a

DNF

600

0.001 qCO 2

(f)

a

0.0012

700 600 500 400 300 200 100 0

VNF

b

c

60

e

0.0004 0.0002

(g)

b

1

HG

ns

ns

ns

VNF

MBN

SP

MBC/ MBN

CAI

VNF

0.0008

b

(b) 0

0

70

b

0.5

0.1

(c)

b

1.5

d

0.2

(a)

a

ab SIR

MR

2

c

c

0.4

331

500 400

cd

bc

b

bc

300

d

200 100

0

(h) VNF

DNF

AP

SP

IF

HG

0 VNF

DNF

AP

SP

IF

HG

Land use/ cover

Land use/ cover

Fig. 3. Mean values (±SE) of soil microbial respiration(mg CO2-C g-1 day-1) (a), substrate induced respiration (mg CO2-C g-1 day-1) (b), CAI (Carbon availability index) (c), microbial biomass carbon(mg kg-1) (d), microbial biomass nitrogen (mg kg-1) (e), microbial biomass carbon/microbial biomass nitrogen (f), metabolic quotient(μg CO2-C mg-1 MBC day-1) (g) and microbial ratio (h) under different land uses/covers (VNF = virgin natural forest; DNF = degraded natural forest; AP = Alder plantation; SP = Sequoia plantation; IF = Improved fallow; HG = Home garden).

soil microbial biomass content in soil under systems with high plant diversity and also vegetation quality [29]. IF and HG land uses significantly lower microbial biomass, soil organic C. IF land use has been shown to strongly decrease the biomass and diversity of soil microbial communities, thus impacting on soil functions [25]. Our observations are concomitant with other studies which have demonstrated that plant inputs have an influencing role in soil microorganism diversity and biomass, as a result of the different quantities and qualities of litter fall and root exudates [27] that could be a hint of either stress or disturbance [30]. In this study, the correlations between microbial biomass N with soil moisture were positive that is accordance with Bolat [30] report. Also Wen et al. [27] found similar relationships between soil water content and microbial biomass in forest ecosystem. This result may be due to high soil moisture, to less exposure to sunlight and to the superior quality of the litter in the former stand, favoring the growth of microbes. The increased levels of soil microbial N under AP and VNF land uses could be explained by the higher nutrient concentrations (particularly total N) and pH as compared to IF [31]. MBN increased with increasing total N [25]. It appears that microbial biomass can replace soil organic C

and total N to evaluate soil quality.This suggests that variation in soil MBC and MBN in this study could largely be explained by the levels of soil total C, N and these results also indicate that soil microbial properties should be addressed to assess the effects of land use management practices on forestland quality [31]. Significant and positive correlation between soil microbial biomass and available nutrients could also be attributed to significant and positive correlation between soil properties [8]. Differences in the type and amount of organic matter added to soils under different land uses can affect microbial biomass and microbial activities [24]. 6. Conclusions Soil biochemical/microbial distinguished between land-use types and are therefore useful for monitoring changes in soil quality. It appears that the type of land use following forest conversion is important in determining the amount of microbial properties losses from forest ecosystems. Among different kinds of land use/cover, AP improved the soil fertility (greater amounts of total N and available nutrients

332

N. Moghimian et al. / Acta Ecologica Sinica 39 (2019) 328–333

Fig. 4. PCA based on the correlation matrix of the land covers, soil chemical and microbial features. The studied land covers were the VNF = virgin natural forest; DNF = degraded natural forest; AP = Alder plantation; SP = Sequoia plantation; IF = Improved fallow; HG = Home garden. WC = Water content; pH, C = Carbon content; N = Total nitrogen; P = Available phosphorus, K = Available potassium; Ca = Available calcium; Mg = Available; magnesium; BR = Basal respiration; SIR = Substrate induced respiration; MBC = Microbial biomass of carbon; qCO2 = Metabolic quotient; MR = Microbial ratio.

including P, K, Ca and Mg) and biological activities (higher values of soil MR, SIR and MBN) but under IF, MBN is reduced due to the reduction of carbon and nitrogen and other soil fertility elements. This is a result of the role of Alnus subcordata as N-fixing species with good quality of litter, and suitable native broadleaved species is proposed to rehabilitate degraded natural forests. Acknowledgement We are grateful to Mr. J. Froghi and Mr. S. Boor for help with field sampling and laboratory analyses. This research was done by financial supports of Tarbiat Modares University, Tehran, Iran. References [1] E.C. Ruiz, A.C. Ruiz, R. Vaca, P. Aguila, J. Lugo, Assessment of soil parameters related with soil quality in agricultural systems, Life Sci J. 12 (2015) 154–161. [2] M. Maharjan, M. Sanaullah, B. Razavi, Y. Kuzyakov, Effect of land use and management practices on microbial biomass and enzyme activities in subtropical top-and sub-soils, Appl. Soil Ecol. 113 (2017) 22–28. [3] K.Z. Mganga, B.S. Razavi, Y. Kuzyakov, Land use affects soil biochemical properties in Mt. Kilimanjaro region, Catena. (2016) 22–29. [4] H. Fang, S. Cheng, Yu G. WangY, M. Xu, X. Dang, L. Wang, Changes in soil heterotrophic respiration, carbon availability, and microbial function in seven forests along a climate gradient, Ecol. Res. (2014) 1077–1086. [5] Q. Wang, F. Xiao, T. He, S. Wang, Responses of labile soil organic carbon and enzyme activity in mineral soils to forest conversion in the subtropics, Ann. For. Sci. (2013) 579–587. [6] J. Liu, P. Jiang, H. Wang, G. Zhou, J. Wu, F. Yang, X. Qian, Seasonal soil CO2 efflux dynamics after land use change from a natural forest to Moso bamboo plantations in subtropical China, For. Ecol. Manag. (2011) 1131–1137. [7] R.B. Mohanty, T. Panda, Soil respiration and microbial population in a tropical deciduous forest soil of Orissa, India, Flora-Morphology, Distribution, Functional Ecology of Plants. (2011) 1040–1044. [8] R.S. Yadav, B.L. Yadav, B.R. Chhipa, S.K. Dhyani, M. Ram, Soil biological properties under different tree based traditional agroforestry systems in a semi-arid region of Rajasthan, India, Agro.System. (2011) 195–202. [9] T. Anderson, Domestic. The metabolic quotient for CO2 (qCO2) as a specific activity parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils, Soil Biol. Biochem. (1993) 393–395.

[10] R. Marzaioli, R. D'Ascoli, R.A. De Pascale, F.A. Rutigliano, Soil quality in a Mediterranean area of southern Italy as related to different land use types, Appl. Soil Ecol. (2010) 205–212. [11] N. Moghimian, S.M. Hosseini, Y. Kooch, B. Zarei Darki, Impacts of changes in land use/cover on soil microbial and enzyme activities, Catena. (2017) 407–414. [12] J. Ghazanshahi, Soil and Plant Analysis, Hooma Publications, 2006 272p (In Persian). [13] N. Ali Asgharzad, Laboratory Methods in Soil Biology, Tabriz University Publications, 2010 (522 p In Persian). [14] K. Singh, B. Singh, R. Singh, Changes in physico-chemical, microbial and enzymatic activities during restoration of degraded sodic land: ecological suitability of mixed forest over monoculture plantation, Catena. (2012) 57–67. [15] C. Liao, Y. Luo, C. Fang, B. Li, Ecosystem carbon stock influenced by plantation practice: implications for planting forests as a measure of climate change mitigation, PLoS One 5 (2010), e10867. [16] Y. Kooch, B. Samadzadeh, S.M. Hosseini, The effects of broad-leaved tree species on litter quality and soil properties in a plain forest stand, Catena. (2017) 223–229. [17] V. Tardy, O. Mathieu, J. Lévêque, S. Terrat, A. Chabbi, P. Lemanceau, P.A. Maron, Stability of soil microbial structure and activity depends on microbial diversity, Environ. Microbiol. Rep. (2014) 173–183. [18] Y. Kooch, F. Rostayee, S.M. Hosseini, Effects of tree species on topsoil properties and nitrogen cycling in natural forest and tree plantations of northern Iran, Catena. (2016) 65–73. [19] Y.S. Cao, Y.B. Lin, Fu S.L. RaoXQ, Effects of artificial nitrogen and phosphorus depositions on soil respiration in two plantations in southern China, J. Trop. For. Sci. (2011) 110–116. [20] T.H. Anderson, K.H. Domsch, Soil microbial biomass: the eco-physiological approach, Soil Biol. Biochem. (2010) 2039–2043. [21] A. Fterich, M. Mahdhi, M. Mars, The effects of Acacia tortilis subsp. raddiana, soil texture and soil depth on soil microbial and biochemical characteristics in arid zones of Tunisia, Land Degrad. Dev. (2014) 143–152. [22] R. Dinesh, S. Chaudhuri, Soil biochemical/microbial indices as ecological indicators of land use change in mangrove forests, Ecol. Indic. (2013) 253–258. [23] S. Sinha, R.E. Masto, L.C. Ram, V.A. Selvi, N.K. Srivastava, R.C. Tripathi, J. George, Rhizosphere soil microbial index of tree species in a coal mining ecosystem, Soil Biol. Biochem. (2009) 1824–1832. [24] Z. Zeng, S. Wang, C. Zhang, H. Tang, X. Li, Z. Wu, J. Luo, Soil microbial activity and nutrients of evergreen broad-leaf forests in mid-subtropical region of China, J. For. Res. (2015) 673–678. [25] S. Liu, C. Wang, Temporal and spatial patterns of soil microbial carbon and nitrogen in five types of temperate forests, J. Ecol. (2010) 3135–3143. [26] O.N. Gorobtsova, F.V. Gedgafova, T.S. Uligova, R.K. Tembotov, Eco physiological indicators of microbial biomass status in chernozem soils of the Central Caucasus (in the territory of Kabardino-Balkaria with the Terek variant of altitudinal zonation), Russ. J. Ecol. (2016) 19–25.

N. Moghimian et al. / Acta Ecologica Sinica 39 (2019) 328–333 [27] L. Wen, P. Lei, W. Xiang, W. Yan, S. Liu, Soil microbial biomass carbon and nitrogen in pure and mixed stands of Pinus massoniana and Cinnamomum camphora differing in stand age, For. Ecol. Manag. (2014) 150–158. [28] R. Lai, A. Lagomarsino, L. Ledda, P.P. Roggero, Variation in soil C and microbial functions across tree canopy projection and open grassland microenvironments, Turk. J. Agric. For. (2014) 62–69. [29] D.K. Da Silva, A.S. Araujo, L.C. Maia, Soil microbial biomass and activity under natural and regenerated forests and conventional sugarcane plantations in Brazil, Geoderma. (2012) 257–261.

333

[30] I. Bolat, The effect of thinning on microbial biomass C, N and basal respiration in black pine forest soils in Mudurnu, Turkey, Eur. J. For. Res. (2014) 131–139. [31] Y. Huang, S.L. Wang, Z.W. Feng, Z.Y. Ouyang, X.K. Wang, Z. Feng, Changes in soil quality due to introduction of broad leaf trees into clear felled Chinese fir forest in the mid subtropics of China, Soil Use Manag. (2004) 418–425.