Impact of forest degradation and reforestation with Alnus and Quercus species on soil quality and function in northern Iran

Ecological Indicators 112 (2020) 106132

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Impact of forest degradation and reforestation with Alnus and Quercus species on soil quality and function in northern Iran

T

Razie Sanjia, Yahya Koochb, , Ana Reyc ⁎

a

Faculty of Natural Resources & Marine Sciences, Tarbiat Modares University, 46417 76489 Noor, Mazandaran, Iran Faculty of Natural Resources & Marine Sciences, Tarbiat Modares University, 46417 76489 Noor, Mazandaran, Iran c Department of Biogeography and Global Change, National Museum of Natural History (MNCN), Spanish Scientific Council (CSIC), C/ Serrano 115bis, E 28006 Madrid, Spain b

ARTICLE INFO

ABSTRACT

Keywords: N-fixing species Litter quality C use efficiency Microbial activity C and N mineralization

Forest degradation causes soil carbon losses and affects soil C and N cycling. However, it is not clear how reforestation of degraded areas with different species affects soil and ecosystem restoration, particularly in northern Iran. The aim of this study was to evaluate the effect of forest degradation and reforestation with two contrasting species: Alnus and Quercus as N2-fixing and non N2-fixing tree species, respectively, on soil quality and function after 30 years in the northern Iran region. We selected four forest stands: Carpinus betulus-Parrotia persica natural forest (NF), Alnus subcordata (AP) and Quercus castaneifolia (QP) plantations as rehabilitated areas, and a degraded natural forest (DNF). We examined the main litter and soil chemical properties and soil C and N microbial fractions. Litter and soil physico-chemical properties and microbial activity differed among land covers. As expected, deforestation caused a decrease in most soil C and N fractions as well as in soil microbial activity with an increase in metabolic quotient-qCO2. The plantation with Quercus spp. improved substrate induced respiration, as well as microbial biomass carbon and dissolved organic carbon compared to the Alnus plantation, whereas mineral N was similar in the natural site and the Alnus plantation. Although forest plantations had not reached the same values of microbial activity as the natural forest soils, soil C and N fractions were similar to the natural site after 30 years. The findings of this study support the importance of preserving natural forests for soil conservation. In addition, employing of N2 fixing trees such as Alnus spp. or, Quercus spp., suitable native broadleaved species, is proposed for the rehabilitation of degraded natural forests. Although both forest plantations led to soil recovery after 30 years, Quercus plantations were more efficient in restoring microbial communities than Alnus plantations indicating that litter quantity is more important than litter quality for soil recovery.

1. Introduction There has been increasing concern in recent years about the impact of land use change on the global carbon (C) and nitrogen (N) cycles (Zeng et al., 2009; Wang et al., 2013). Deforestation is a major land use change resulting from changes in socio-economic and environmental conditions across the world (Raiesi and Beheshti, 2015). As a consequence, the area covered by native forests has declined by 5.2 million ha annually between 2000 and 2010 (Zamorano-Elgueta et al., 2015). Today, the loss of soil fertility following forest degradation is a severe ecological problem globally. In forest ecosystems, soil C and N contents are sensitive to deforestation and soil erosion (Atucha et al., 2013). Moreover, large amounts of greenhouse gases (i.e. CO2, CH4 and N2O) are often emitted to the atmosphere (Silva et al., 2011). The importance ⁎

of maintaining forest areas as part of the portfolio of measures to address climate change is also increasingly recognized (Sloan and Sayer, 2015). For this reason, afforestation and reforestation have been proposed as measures to combat climate change and land degradation (Tavakoli et al., 2018), by controlling soil degradation and improving soil fertility (Albert, 2015). As a result, planted forests are expanding worldwide with 7% increase in the total forest area (FAO, 2011). Today, planting trees in degraded areas has become common across many parts of the world (Parsapour et al., 2018) as forests improve ecosystem services such as water regulation, nutrient cycles, C and N stocks in soils, and different soil properties, and thus soil quality and function (Humpenoder et al., 2014). The direction and magnitude of change in soil quality often depends on historical land-use, climate, and soil and vegetation type (Zeng et al.,

Corresponding author. E-mail address: [email protected] (Y. Kooch).

https://doi.org/10.1016/j.ecolind.2020.106132 Received 21 February 2019; Received in revised form 17 January 2020; Accepted 22 January 2020 1470-160X/ © 2020 Elsevier Ltd. All rights reserved.

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Fig. 1. Location of the study area in the Mazandaran Province, Northern Iran (a, b). Schematic representation of the experimental design adopted for each land cover and soil sample size (figure not to scale) (c).

2009; Yuan et al., 2012; Wang et al., 2013). Plant species can have significant impacts on soil function and substrate quality through litter fall, accretion and decomposition of soil organic matter (Kooch et al., 2017a,b). Some researchers argue that planting local dominant species is more effective for recovering ecosystem function (Mcnamara et al., 2006; Hayden et al., 2010; Lu et al., 2017), while others demonstrate that the natural recovery of vegetation without human disturbance is an effective approach for soil nutrient cycling (Zheng et al., 2004). However, limited studies have associated the re-establishment of soil nutrients with alterations in specific microbial functional groups during reforestation. Many plantations of endemic and exotic species, including N2-fixing and non N2-fixing trees in degraded forest areas, improve soil fertility (Haghdoost et al., 2011; Kooch et al., 2016). Among different soil properties, soil organic matter is often used as a proxy of soil quality and productivity. However, soil organic matter alone does not adequately reflect changes in soil quality and function (Kara and Bolat, 2008) and other microbial indices such as microbial biomass and activity (i.e. soil metabolic quotient or qCO2, C availability index) can provide useful information on microbial activity and efficiency (Nannipieri et al., 2003). Soil microbes are involved in biochemical processes such as soil organic matter decomposition, humification, transformation and nutrient cycling (Ye et al., 2009) and are sensitive to land use changes (Zhao et al., 2012). Litter quality varying with tree species is one of the several factors determining the extent and speed of soil recovery after reforestation (Vesterdal et al., 2008). The concentration of C and N may be positively or negatively related to soil microbial activities under different tree species (Fang et al., 2014). Despite the existence of extensive afforested areas, especially alder (Alnus subcordata C. A. M.) and oak (Quercus castaneifolia C. A. M.) in vast areas of northern Iran (Sagheb-Talebi et al., 2014), few studies offer a critical overall examination of the development and ecological consequences of afforestation in the Hyrcanian region (Haghdoost et al., 2011), especially those related to soil properties. Previous studies from afforested ecosystems indicate that vegetation enhances soilforming processes, leading to the buildup of soil organic matter and development of microbial communities (Silva et al., 2011; Wang et al., 2013), but how long it takes for soils to recover is not clear nor how different tree species affect soil quality and function. In this study, we investigated: (1) the extent to which forest degradation affects soil quality and function and, (2) to what extent reforestation with Alnus, a nitrogen fixing species, and Quercus, is effective for soil recovery, in

particular, how reforestation with these contrasting species affects soil C and N cycles and (3) how these species affect soil C and N fractions and microbial communities after 30 years of reforestation. Specifically, we measured some of the most important soil C fractions [total organic C, microbial biomass of C (MBC), particulate and dissolved organic C (POM-C and DOM-C], and N fractions [NH4+, NO3−, microbial biomass of N (MBN), particulate and dissolved organic N (POM-N and DOM-N)], and soil microbial activity [basal respiration (BR) or C mineralization, soil induced respiration (SIR), qCO2 or metabolic quotient, microbial quotient, C availability index (CAI) and N mineralization]. We hypothesize that: (1) forest degradation as well as leading to significant soil fertility (i.e. POM-C, DOM-C, POM-N and DOM-N) losses, also reduces microbial activities related to soil C and N cycles (i.e. BR, SIR, MBC, microbial quotient, CAI, N mineralization and MBN) while the efficiency of soil microbes to process C (qCO2), decreases; (2) rehabilitating degraded natural forests with Alnus subcordata, a N fixing species, will improve soil quality increasing the concentration of soil mineral nitrogen (i.e. NH4+ and NO3−) more than with Quercus castaneifolia plantation since their litter quality differs between both species. However, the fact that: (3) higher litters inputs are expected with Quercus than Alnus trees, may positively affect C cycling more than N cycling in these areas. 2. Materials and methods 2.1. Study area: location and history The study area is located in the Galandrood district of the city of Noshahr (Mazandaran province in northern Iran; Fig. 1a, b) at 36° 30′ 40″ and 36° 37′ 30″ latitude, 51° 28′ 25″ and 51° 26′ 30″ longitude. The study stands are located at 300 m in altitude with a mild slope ranging between 0 and 5%. The region has a sub-Mediterranean climate with mean annual precipitation of 1043.6 mm, falling mostly between September and February with minimum and maximum monthly values in July (36 mm) and November (120 mm). The dry season (but without a real drought period) is from April to August, when monthly rainfall averages are less than 40 mm. Average daily temperatures range from 11.7 °C in February to 29.5 °C in August, with 20.6 °C on average (Tavakoli et al., 2018). According to the USDA Soil Taxonomy, soils are classified as silty-clay-loam Alfisols, developed on dolomite limestones belonging to the upper Jurassic and lower Cretaceous periods. This area 2

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is dominated by temperate natural forests containing native tree species (Carpinus betulus and Parrotia persica) and some individual trees of Caspian zelkova (Zelkova carpinifolia (Pall.) Dipp.) and Caspian locust (Gleditschia caspica Desf.). In the 1980s, this forest was divided into several parcels by the Forests and Rangelands Organization of Iran (FROI) that were partially destroyed because of extensive exploitation carried out by local residents. Consequently, in 1985 these plots were ‘‘clear-cut’’, stumps eradicated, and then afforested by the FROI in 1987. The dominant forest types, which were planted at a spacing of 2 × 2 m, included alder (Alnus subcordata) with 8.23 ha and oak (Quercus castaneifolia) with 7.82 ha. The stands were never fertilized. Therefore, in a relatively small homogeneous natural area, reforested and degraded plots could be found. This land is covered by herbaceous species including Asperula odorata L., Euphorbia amygdaloides L., Hypericum androsaemum L., and Polystichum sp (Tavakoli et al., 2018).

absorption spectrophotometer (Bower et al., 1952). POM-C and POM-N were determined by physical fractionation (Cambardella and Elliott, 1992; Handayani et al., 2009). DOM-C and DOM-N were measured using a Shimadzu TOC-550A total organic carbon (TOC) analyzer. DOM-N was calculated as the difference between the total dissolved N reading and the combined NH4+ and NO3− concentrations (Jones and Willett, 2006). Soil NH4+ and NO3− were extracted with a 2 M KCl solution (soil: solution, 1:5) and then filtered through a 0.45 µm filter. The extracted solutions were measured via colorimetric techniques at 645 and 420 nm to determine NH4+ and NO3− concentrations, respectively (Li et al., 2014). N mineralization was measured using a laboratory incubation procedure under controlled conditions (Robertson et al., 1999).

2.2. Experimental design

Soil BR was determined by measuring the CO2 evolved in a 3-day incubation experiment at 25 °C (Alef, 1995). The SIR measurement was performed using glucose 1% as the substrate; after 72 h, the evolved CO2 trapped in NaOH was measured by HCl titration (Anderson and Domsch, 1990). MBC and MBN were measured with the fumigationextraction method (Brookes et al., 1985).

2.4. Soil microbial biomass and activity

Plantations of alder and oak are common in northern Iran, but plots are very scattered and irregular and cover small areas. Therefore, it was difficult to find replicated areas of afforested species. In order to investigate the effect of forest degradation and reforestation on soil properties, after an extensive field trip, we selected four land cover types including a virgin natural forest (dominated by Carpinus betulus and Parrotia persica as a control plot), two reforested areas, one with alder and one with oak trees, and a degraded forest all nearby, no more than 500 m distance from each other with similar soil texture and topographical features (e.g., elevation, slope position, and aspect). In this study, one sample plot of 4 ha (200 × 200 m; Fig. 1c) was selected in each site (Kooch et al., 2018a,b,c; Kooch et al., 2019): NF = Natural forest; AP = Alnus subcordata plantation; QP = Quercus castaneifolia plantation; DNF = Degraded natural forest. In order to decrease border effects, surrounding rows of land covers were not considered during sampling, which was carried out during the summer of 2017 using a random systematic method (Kooch et al., 2019).

2.5. Calculations and statistical analysis The soil qCO2 (BR: MBC; Anderson and Domsch, 1990), microbial quotient (MBC: Corg; Jia et al., 2005) and CAI (BR: SIR; Cheng et al., 1996) were calculated based on the values of organic C, BR, SIR and MBC. One-way analysis of variance (ANOVA) was used to compare litter and soil properties among land covers. Difference between land cover was found by using the Duncan multiple range tests and Bonferroni correction was applied to adjust p-values for multiple comparisons (Chandra et al., 2016; Nishi and Sato, 2019). Prior to ANOVA, the normality of the variables was checked by the Kolmogorov-Smirnov test and Levene’s test was used to examine the homogeneity of variances. Variables without normal distribution and equal variance (i.e. soil pH, C/N ratio, available P, SIR and NH4+) were subjected to a Box-Cox power transformation to obtain approximately normal distributions and to stabilize the variances (Salek-Gilani et al., 2013). Simple linear correlation (i.e., Pearson's correlation coefficient) and regression analyses were used to characterize the relationship between soil C and N fractions and microbial activities with litter and soil properties across different land covers. All statistical analyses were conducted using the SPSS v. 20 statistical software package. Because each land cover occupies only a single plot, the design of this experiment thus suffers from pseudo-replication (see Hurlbert, 1984). Nevertheless, because such long-term experiments are rare, we felt that use of inferential statistics in this experiment would provide useful estimates of the effects of land covers on litter and soil properties (Menyailo et al., 2002). 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 (Mc Cune and Mefford, 1999). Pearson correlation analyses were performed to correlation of litter and soil characters with PCA components.

2.3. Litter and soil physico-chemical analyses Four soil profiles (25 × 25 cm) were dug along four parallel transects in the central part of each land cover plot, resulting in 16 soil samples for each site at a depth of 0–15 cm (Fig. 1c). Litter and soil samples were collected and litter thickness was measured with an accuracy of millimeters from each stand. Litter total C and N contents were determined in quadruplicate using dry combustion with an elemental analyzer (Fisons EA1108, Milan, Italy) calibrated by the BBOT [2, 5-bis-(5-tert-butyl-benzoxazol-2-yl)-thiophen] standard (ThermoQuest Italia S.p.A.). Litter phosphorus (P) concentration was determined spectrophotometrically (Novák et al., 2014). An atomic absorption spectrophotometer was used to determine total litter potassium (K) concentration by flame emission (Novozamsky et al., 1983). A soil subsample was stored in polyethylene bag for biological analysis at 4 °C until processed. Other subsamples were air-dried and passed through a 2-mm sieve (aggregates were broken). Bulk density was measured by the clod method (Plaster, 1985). Soil texture was determined by the Bouyoucos hydrometer method (Bouyoucos, 1962). Soil water content was measured by drying soil samples at 105 °C for 24 h. Soil pH was determined using an Orion Ionalyzer Model 901 pH meter in a 1:2.5, soil: water solution. EC (electrical conductivity) was determined using an Orion Ionalyzer Model 901 EC meter in a 1:2.5 soil: water solution. Soil organic C was determined using the WalkeyBlack method (Allison, 1975) and total N using a semi Micro-Kjeldahl method (Bremner and Mulvaney, 1982). Soil C and N stocks were calculated using the bulk density data and C and N concentrations for each site. Available P was determined with a spectrophotometer using the Olsen method (Homer and Pratt, 1961), and available K, Ca, and Mg (by ammonium acetate extraction at pH 9) were determined with an atomic

3. Results 3.1. Litter properties The litter layer was significantly (Bonferroni-adjusted p-value < 0.005) thicker under the Quercus plantation (11.80 ± 0.75 cm) than in the natural forest (8.11 ± 0.76 cm) and the Alnus plantation (6.69 ± 0.48 cm) plots. Litter C concentration did not vary significantly (Bonferroni-adjusted p-value > 0.005) between tree species. However, litter N and K concentrations varied among forest types with 3

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soil water content and chemical properties as soils in the natural forest, but lower C/N ratio and greater amount of available Ca than soils in the Quercus plantation (Table 1). Soil EC varied among sites as degraded forest (0.22 ± 0.01 ds m−1), Alnus (0.21 ± 0.01 ds m−1), Quercus (0.18 ± 0.00 ds m−1) and natural forest (0.16 ± 0.02 ds m−1) land covers, respectively (Table 1). 3.3. Soil C and N fractions and microbial activities As a consequence of lower litter input and soil quality, all C and N fractions were significantly [Bonferroni-adjusted p-value < 0.005 in all cases; except for N mineralization (Bonferroni-adjusted p-value > 0.005)] lower in the degraded soils than in those in the reforested and natural sites (Table 2). The concentrations of soil POM-C, DOM-C, microbial biomass, CAI, NH4+ and NO3– and DOM-N, in degraded sites were half those measured in the natural forest soils. The BR and SIR decreased by 64% and 28%, respectively. The microbial quotient was 69% lower than in the natural forest. As a result, the qCO2 was 67% higher than in soils in the degraded forest. The reforested sites had regained nutrient concentrations to levels similar as the natural forest. However, soils in the Quercus plantation had significantly more MBC, POM-C and DOM-C and significantly less N fractions including NH4+, NO3– and POM-N than the Alnus plantation. Soils in the Alnus plantation had the same concentrations of C and N fractions than soils in the natural forest (Table 2). Microbial activity was also significantly affected by afforestation and varied between species (Table 2). The qCO2 was not significantly different between forest species, but there was a trend of higher C efficiency in soils under Quercus than under Alnus trees. This was consistent with higher C in microbial biomass in soils under Quercus trees that reached similar values as those determined in the natural forest soils. Although there were no differences in the CAI, values measured in reforested soils have not recovered to values measured in the natural forest soils. Changes in N mineralization were not significant between forest sites. Reforestation with both species improved microbial activity as most indices were similar to those determined in soils in the natural forests. However, soils in the Quercus plantation had more MBC and thus, higher microbial quotient than the Alnus plantation and natural forests. Although BR was similar in all soils, SIR was higher in those from the Quercus plantation than in the other forest soils (Table 2). Based on Pearson correlation and regression analyses, the characters of SIR with litter thickness (r = 0.58), MBC with litter thickness (r = 0.62) and litter K (r = 0.55), DOM-C with litter thickness (r = 0.52), nitrate with litter C/N (r = -0.53), MBN with litter thickness (r = 0.52) and litter K (r = 0.55), POM-N with litter K (r = 0.66) and water content (r = 0.51) and DOM-N with litter K (r = 0.53) had high and significant correlation (r > 0.50; Bonferroni-adjusted p-value < 1.6 × 10-4) with litter and soil properties across different land covers (Fig. 3). Whereas, the correlation between the other studied soil C and N fractions and microbial activities with litter and soil properties were low (r < 0.50) and also non-significant (Bonferroni-adjusted p-value > 1.6 × 10-4) (See Appendix 1). Litter and soil properties in the land covers presented different locations in the PCA output. The first and second axes explained more than 85 and 11% of the variance, respectively. Soil quality and fertility decreased in the degraded natural forest site while the soil qCO2 was increased. Natural forest and Alnus plantation presented a good condition of soil fertility than soils in the Quercus site. Quercus plantation with lower soil fertility had enhanced C microbial fractions such as SIR, MBC and DOM-C (Fig. 4; Appendix 2).

Fig 2. Mean values ± standard error (SE) of the litter properties across different land covers. Results from the ANOVAs are included F test and *significant at the Bonferroni-adjusted p-value < 0.005. Different letters indicate significant differences between land covers. NF = Natural forest; AP = Alnus subcordata plantation; QP = Quercus castaneifolia plantation; DNF = Degraded natural forest. The DNF is showed with white bar to distinguish from the other treatments with black bars.

significantly (Bonferroni-adjusted p-value < 0.005) lower content in the degraded site (1.25 ± 0.10% and 1.31 ± 0.02%, respectively) than in the other land covers. As a result, litter C/N ratio was significantly (Bonferroni-adjusted p-value < 0.005) different among land covers with higher values in litter in the degraded site (34.11 ± 1.42) than in the other forest sites. There were significant differences (Bonferroni-adjusted p-value < 0.005) between litters from both tree species. Litter C/N ratio was higher in the Quercus plantation (32.62 ± 1.18) than in the Alnus plantation (26.27 ± 1.13) and the natural forest (27.68 ± 1.19) sites (Fig. 2). 3.2. Soil physico-chemical properties Soil compaction in the degraded site resulted in higher bulk density (1.53 ± 0.04 g cm−3) than in soils of the Quercus (1.40 ± 0.04 g cm−3) and Alnus (1.37 ± 0.05 g cm−3) plantations and natural forest site (1.34 ± 0.06 g cm−3) (Table 1). Soils in the degraded plots, with loam texture, had higher sand content (21%) and lower clay content (22%) than soils in the other forest types with clay loam soils. As a consequence, soil water content was significantly (Bonferroni-adjusted p-value < 0.005) lower (ca. 35%) in the degraded soil compared to the natural forest soils. Soil chemical properties were also affected by deforestation. Soil organic C and N concentrations and stocks were significantly reduced (by ca. 40%) in the degraded forest site compared to the natural forest site. Soil fertility was also lower in the deforested stands with significantly lower concentrations of available Mg and Ca (Bonferroni-adjusted p-value < 0.005), than soils in the natural forest (about 35%). Afforestation resulted in soil recovery with most soil physico-chemical variables reaching values similar to the original natural forest soils but to different extent depending on forest species. Planting Alnus improved soil quality to nearly original values, with similar bulk density, soil texture,

4. Discussion Because all of the land studied had similar soil texture and topographical features, the experiment provided a useful design for elucidating cause-and-effect relationships between tree species, litter and soil properties. However, the Galandrood land covers experiment 4

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Table 1 Mean values and standard error (SE) (sixteen replications in all case) of the soil variable analyzed. NF = Natural forest; AP = Alnus subcordata plantation; QP = Quercus castaneifolia plantation; DNF = Degraded natural forest. Soil properties

NF

AP

QP

DNF

F test

Mean

SE

Mean

SE

Mean

SE

Mean

SE

Physical properties

Bulk density (g cm−3) Sand (%) Silt (%) Clay (%) Water content (%)

1.34 28.68 42.06 29.25 42.48a

0.06 2.49 2.64 2.78 2.61

1.37 25.50 43.87 31.62 39.25a

0.05 2.69 2.45 2.26 1.48

1.40 27.87 44.12 28.00 42.58a

0.04 1.63 2.00 1.31 2.81

1.53 34.87 42.25 22.87 27.55b

0.04 3.29 3.14 1.00 1.66

2.63 2.77 0.17 3.49 10.27*

Chemical properties

pH (1:2.5 H2O) EC (ds m−1) Organic C (%) C stocks (Mg ha−1) Total N (%) N stocks (Mg ha−1) C/N ratio Available P (mg kg−1) Available K (mg kg−1) Available Ca (mg kg−1) Available Mg (mg kg−1)

6.20 0.16 3.47 50.42 0.22 3.21 14.69 11.96 188.56 167.43a 33.00a

0.18 0.02 0.69 12.52 0.03 0.65 0.80 2.240 26.55 19.72 3.85

6.51 0.21 3.74 52.06 0.25 3.54 14.80 14.35 244.81 178.43a 37.75a

0.18 0.01 0.38 5.93 0.01 0.34 1.02 1.06 18.51 10.13 1.23

6.26 0.18 4.02 57.68 0.23 3.20 17.59 13.35 195.14 126.22b 35.84a

0.07 0.00 0.43 7.34 0.01 0.33 0.87 0.78 11.13 9.64 2.33

6.67 0.22 2.09 32.80 0.14 2.18 14.33 11.02 185.93 110.28b 22.03b

0.12 0.01 0.32 5.79 0.01 0.29 0.86 0.45 12.22 8.23 1.94

2.16 3.70 3.16 1.65 3.82 1.85 2.83 1.24 2.32 6.49* 7.69*

Results from the ANOVAs are included F test and * significant at the Bonferroni-adjusted p-value < 0.005. Different letters in each line indicate significant differences between land covers. Table 2 Mean values and standard error (SE) (sixteen replications in all case) of the soil C and N fractions and microbial activities across different land covers. NF = Natural forest; AP = Alnus subcordata plantation; QP = Quercus castaneifolia plantation; DNF = Degraded natural forest; BR = Basal respiration (mg CO2 g−1 day−1); SIR = Substrate induced respiration (mg CO2 g−1 day−1); MBC = Microbial biomass carbon (mg kg−1); Metabolic quotient or qCO2 = BR: MBC (μg CO2-C mg−1 MBC day−1); Microbial quotient = MBC: Corg; C availability index (CAI) = BR: SIR; POM-C = Particulate organic carbon (g kg−1); DOM-C = Dissolved organic carbon (g kg−1); Ammonium = NH4 (mg kg−1); Nitrate = NO3 (mg kg−1); N mineralization = Nitrogen mineralization (mg N kg soil−1); MBN = Microbial biomass nitrogen (mg kg−1); POM-N = Particulate organic nitrogen (g kg−1); DOM-N = Dissolved organic nitrogen (g kg−1). Soil C and N fractions and microbial activities

NF

AP

QP

DNF

F test

Mean

SE

Mean

SE

Mean

SE

Mean

SE

Soil C fractions and microbial activities

BR SIR MBC qCO2 Microbial quotient C availability index POM-C DOM-C

0.39a 1.16b 503.19b 0.83b 223.75a 0.35a 2.84a 53.40b

0.15 0.23 126.12 0.09 35.82 0.04 0.43 4.92

0.31a 1.06b 460.75b 0.73b 137.76b 0.29a 2.41a 53.49b

0.10 0.17 137.70 0.08 14.22 0.02 0.25 4.74

0.37a 1.32a 660.00a 0.58b 188.44ab 0.28a 3.16a 71.36a

0.16 0.19 116.27 0.07 19.02 0.03 0.36 6.38

0.14b 0.84c 115.75c 1.39a 69.96c 0.17b 1.01b 17.29c

0.06 0.22 32.08 0.22 9.07 0.02 0.15 2.31

12.76* 14.72* 68.14* 6.76* 9.24* 5.48* 8.74* 22.20*

Soil N fractions and microbial activities

Ammonium Nitrate N mineralization MBN POM-N DOM-N

22.11a 21.75a 30.37 43.79a 0.41a 27.72a

2.56 2.05 3.42 3.22 0.05 2.02

27.69a 25.75a 31.87 43.55a 0.41a 28.33a

1.59 1.71 2.96 2.25 0.03 2.15

19.97ab 16.25b 29.49 47.09a 0.30a 26.49a

4.02 1.38 2.98 3.03 0.03 3.17

13.69b 10.33c 21.81 16.83b 0.19b 12.26b

1.33 0.33 2.18 0.98 0.00 0.30

4.93* 19.60* 2.35 30.88* 16.17* 12.40*

Results from the ANOVAs are included F test and * significant at the Bonferroni-adjusted p-value < 0.005. Different letters in each line indicate significant differences between land covers.

includes pseudo-replication, a problem in many large-scale experiments in ecology (see Hurlbert, 1984). Thus, the interpretation of the results should be based on the assumption that at the study site there are no other factors influencing litter and soil properties (Menyailo et al., 2002). The results provide evidence that the deforestation and subsequent reforestation of forest stands planted with Alnus and Quercus species caused species-specific changes in litter and soil properties, which could be ascribed to organisms such as mycorrhizae or protists (Perry et al., 1987; Turbé et al., 2010; Liu et al., 2019), after 30 years.

losses of nutrients (Boyle, 1975). As expected, in this study deforestation strongly decreased soil quality. Course texture soils in the degraded site allow rapid water infiltration and increase dissolved exchangeable base cations losses (Ashman and Puri, 2002), so the main effect of deforestation was the loss of soil quality leading to lower soil moisture holding capacity and higher soil bulk density than in natural forest soils. In particular, land degradation caused a loss of organic C resulting in lower C concentrations, C stocks and thinner A and B horizons, and loss of soil fertility (i.e., total N, available Ca and Mg). Decreases in soil fertility as a result of deforestation are common effects (Khresat et al., 2008) that are seen in our data (Table 1), too. Litter layer thickness increased following reforestation but the effect on soil fertility differed between forest species. According to Nsabimana et al. (2008), clay content and soil pH are two factors that explain nutrient levels in soils under different tree species. Small differences in soil texture between forest species and litter quality led to differences in soil mineral nutrient

4.1. Effect of forest degradation and reforestation on litter and soil physicochemical properties Deforestation has several strong negative effects on forest soils, including soil compaction, changes in soil texture components, nutrient removal with harvested material, increased erosion and/or percolation 5

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Fig 4. PCA based on the correlation matrix of the land covers, litter, soil physico-chemical and microbial properties (a, b). The studied land covers were the NF = Natural forest; AP = Alnus subcordata plantation; QP = Quercus castaneifolia plantation; DNF = Degraded natural forest. Litter C = Litter carbon; Litter N = Litter nitrogen; Litter P = Litter phosphorus; Litter K = Litter potassium; Bd = Bulk density; WC = Water content; C stocks = Carbon stocks; N stocks = Nitrogen stocks; AP = Available phosphorus, AK = Available potassium; ACa = Available calcium; AMg = Available magnesium; BR = Basal respiration; SIR = Substrate induced respiration; MBC = Microbial biomass of carbon; qCO2 = Metabolic quotient; Microbial q. = Microbial quotient; CAI = Carbon availability index; POM-C = Particulate organic carbon; DOMC = Dissolved organic carbon; NH4 = Ammonium; NO3 = Nitrate; Nmin = Nitrogen mineralization; MBN = Microbial biomass of nitrogen; POMN = Particulate organic nitrogen; DOM-N = Dissolved organic nitrogen. Fig. 3. Linear regressions between soil C and N fractions and microbial activities [SIR = Substrate induced respiration; MBC = Microbial biomass carbon; DOM-C = Dissolved organic carbon; Nitrate = NO3; MBN = Microbial biomass nitrogen; POM-N = Particulate organic nitrogen; DOM-N = Dissolved organic nitrogen] with litter and soil properties across different land covers. Regression equation, line of best fit, regression coefficients (r) and *significant at the Bonferroni-adjusted p-value < 1.6 × 10-4 are provided.

4.2. Effect of forest degradation and reforestation on soil C and N fractions Forest degradation also reduced all soil C and N fractions. The most common factors affecting soil-N cycling in forest ecosystems are substrate quality and quantity, size of microbial biomass pool, availability of soil C, and soil moisture content (Yang et al., 2013). Although C and N were similarly reduced by almost 40%, the reduction in C mineralization was stronger than in N mineralization indicating the C cycling is more sensitive to deforestation. Indeed, the strong reduction in the microbial quotient indicates that microbial communities were substrate limited in the degraded site. Differences in soil microbial properties between the plantations and natural forests were in parallel with differences in soil chemical properties, including total soil C and N fractions. The quality and quantity of forest litter indirectly control the transformations of soil N (Kooch et al., 2016). Other studies have also reported that the proportion of NH4+ and NO3− in the inorganic N pool is associated with land cover type (Wei et al., 2011; Li et al., 2014). The residues that have high C/N ratios produce strong competition for available N in soils, by leading the competition for available NH4+, thereby decreasing its concentration. Tree species cause significant changes in soil N transformation by modifying soil C and N contents (Yang et al., 2013). For example, the use of N-fixing tree species in forest restoration greatly affects the rates of N transformations (Kooch et al., 2016). Enhanced NO3− leaching after harvesting has been attributed to increased N mineralization and nitrification and reduced nitrogen uptake by vegetation (Arslan et al., 2010). In agreement, N addition under the N-fixing species Alnus increased soil NO3− concentrations. Nitrate accumulation is often negatively associated with

in soils under both species. We observed an increase (although nonsignificant) in the C/N ratio of soils under Quercus, indicating changes in the quality of organic matter to more recalcitrant litter than that of Alnus, an N fixing species (Llorente et al., 2010). Furthermore, the higher content of polyphenols in Quercus leaves may inhibit microbial activity and in turn, slow down litter decomposition (Williams et al., 2012). Aerts and Heil (1994) proposed C/N ratio, as an excellent predictor of litter decomposition in forest ecosystems. Although litter quality did not differ much between forest plantations, the concentration of P was enhanced in soils under Alnus plantations. This effect of an increased P concentration in Alnus litter may be a new finding of the effect of N2-fixing tree species, such as Alnus. The level of litter P concentration under Alnus trees depends on stand age (Radwan et al., 1984) whereas changes in soil available P can be more affected by tree density (Giardina et al., 1995). In our study, soil mineral concentration was similar to those in the natural forest soils so planting forest species such as Alnus and Quercus allowed soil recovery after 30 years. However, slight differences in soil texture components between forest species, with higher clay and lower sand content led to a tendency for higher concentrations of all nutrients in soils under Alnus trees.

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litter C/N ratio (Kooch et al., 2016). Soil C/N ratios between 22 and 24 have been suggested as a critical threshold for the onset of NO3− leaching in Europe and North America (Ollinger et al., 2002). In our study, soil C/N ratios were lower than this range, which would explain the net production of NO3− (Satti et al., 2003). POM-C and POM-N may provide a sensitive indicator reflecting impacts of short-term land cover change on soil quality (Su, 2007). POM-C is a labile intermediate in the soil organic matter continuum from fresh organic materials to humified soil organic C (Sreekanth et al., 2013), suggesting the dominance of POM was only partially supported by the results of this study, since this fraction accounted for just over half of the total soil organic matter. According to Tavakoli et al. (2018), the soil POM fractions (i.e. POM-C and N) can be mainly affected by the quantity and quality of litter inputs. So the annual accumulation of litters in soils under natural forest and plantations, and the increase of soil POM could be expected. In addition, Kooch and Bayranvand (2017) pointed out that the leaching of freshly fallen litter and the decomposition of forest floor organic matter are thought to be major sources of DOM-C and N in forest soils. In this study, litter thickness and litter K concentration were positively correlated with DOM-C and DOM-N. Thus, the observed increase in litter quantity as well as soil organic matter in Quercus plantations compared to Alnus plantations may explain greater amounts of C in the form of DOM. The increase was concomitant with an increase in MBC and higher C mineralization rates. In agreement with previous studies (e.g. Gao et al., 2014), forest degradation also reduced DOM-C, probably as a consequence of poor litter quality of leaves and roots. The large concentrations of POM-N in soils of reforested plantations can be attributed to improved soil physical conditions (Scharenbroch and Catania, 2012), total N and nutrient elements (Cheng et al., 2015). The findings of Witt et al. (2000) and Rahn and Lillywhite (2002) showed that the type of land cover was associated with differences in the litter quality and quantity as well as soil water content, which finally resulted in significant differences in the concentration of soil POM-N. We found high correlation between soil POM-N with litter K and water content across different land covers.

of soil organic matter (Gorobtsova et al., 2016). In agreement with previous studies (Singh et al., 2012; Li et al., 2015), we found a reduction in microbial biomass in the degraded site. Low soil organic C availability, quantity, quality and poor microbial community composition or growth conditions for micro flora after forest conversion are common (Raiesi and Beheshti, 2015). Substrate quantity and quality under different land covers causes shifts in microbial population altering microbial biomass and composition (Singh et al., 2012). This is attributed to the observed high correlation between soil MBC and MBN with litter thickness and litters K. Typically, soil microbial biomass increases with plant diversity including native forest or regenerated lands (Hackl et al., 2004). Reforestation with Quercus caused a considerable increase (Bonferroni-adjusted p-value < 0.005) in microbial biomass of carbon, 30% more than under Alnus plantation. The greater C retained in microbial biomass per unit of organic C under Quercus, demonstrated greater C use efficiency, in reference to MBC values (See Table 2). This higher microbial activity under Quercus may explain why we did not observe differences in N mineralization or major N fractions compared to soils under Alnus, despite higher N inputs in the later. Low microbial biomass can be indicative of either stress or disturbance, both of which can induce a rise in qCO2 (Cheng and Xia, 2012). 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 (Bini et al., 2013). In our study, the high qCO2 in the degraded site indicated that important quantities of carbon per unit biomass were lost through carbon mineralization, which reflects poor rhizosphere health (Bolat et al., 2015). A reduction in C use efficiency by microbes in degraded soils has been observed in other studies (Chen et al., 2005; Zeng et al., 2009) and results from the progressive loss of soil aggregates and soil organic matter quality, in particular the most labile soil organic C fraction (Raiesi and Beheshti, 2015). Forest plantation, with both species, decreased the qCO2 in rehabilitated areas indicating an improvement in soil microbial function after 30 years of reforestation. Even though there were not significant differences between Quercus and Alnus plantations, soils under Quercus had lower qCO2 indicating more efficient microbial communities in these soils. The microbial quotient (MBC: Corg) can be useful as a soil quality indicator to allow comparisons across soils with different organic matter content (Kara and Bolat, 2009). Generally, in degraded soils, the microbial C pool declines at a faster rate than soil organic matter, and the microbial quotient decreases (Kara and Bolat, 2009), reflecting low substrate availability (Xu et al., 2007). In this study, the highest microbial quotient was found in soils in the natural forest and the lowest in the degraded forests. Reforestation with both species reversed this trend, and increased microbial biomass and soil fertility were followed by a rise in this proportion of C held in microbial biomass. However, the proportion of organic C in microbial biomass was still lower than in the natural forest, suggesting that it may take longer for microbes to recover and/or reflect differences between forest species as natural forests present local species. Overall, soils under Quercus had more carbon in microbial biomass, which together with more efficient microbial communities (lower metabolic quotients) suggests that plantation with Quercus was more efficient in soil recovery. In order to further understand the state of the microbial communities, we calculated C availability index (Gorobtsova et al., 2016). This index allows us to understand whether the microbial community is substrate limited. A decrease in this index could be explained by an increase of microbial biomass with added substrate (SIR), by a decrease in basal respiration or both. The strong decline in deforested areas was probably the result of strong reductions in microbial populations, activity and reduced substrate availability with fertility loss. The soil recovery after reforestation was also reflected by the increase in this index almost to the values observed in the natural forests.

4.3. Effect of forest degradation and reforestation on microbial activities As expected, less favorable conditions of degraded soils also reduced soil CO2 emissions. Forest degradation often leads to reduced soil quality, soil activity and thus, soil respiration (Kooch and Bayranvand, 2017). This strong reduction in soil respiration in the degraded site was partly due to the highly reduced leaf litter input while the increased litter inputs over the years in the rehabilitated areas led to increases in soil respiration. There was significant and positive correlation between SIR and litter thickness implying that litter quantity controls changes in soil microbial respiration. In line with previous studies (Bárcena et al., 2014; Allen et al., 2015), our data revealed that the changes in land cover and management types could have significant effects on different soil characteristics causing altered levels of microbial properties in the topsoil. Different values of soil microbial respiration in this study, based on both basal and substrate-induced respiration, suggest that the influence of land covers on soil respiration is complex and is contingent upon substrate quality, humic substances (Singh et al., 2012), and different soil properties (Gorobtsova et al., 2016). Chodak and Niklińska (2010) claimed that the sites with greater amounts of litter inputs have higher soil microbial respiration. Accordingly, our findings indicated a significant increase in microbial respiration of the soil in natural forest soils and plantations, compared to deforested sites with the lack of organic C input in the soil (Saurette et al., 2006). On the other hand, García-Orenes et al. (2010) and Tardy et al. (2014) pointed that soil nutrient contents are a major factor controlling soil respiration. In our study area, the decrease in soil fertility following deforestation suppressed soil microbial respiration in the degraded natural forest site. Microbial biomass represents the living, actively metabolizing part 7

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5. Conclusion

support that protecting natural forest is essential for soil conservation in the Caspian region as deforestation rapidly degrades forest soils in this region. In addition, employing N2-fixing forest species, such as Alnus, and suitable native broadleaved species, such as Quercus, rapidly improves soil quality and function and thus, we recommend these species to rehabilitate degraded natural forests.

Our study clearly shows that the main negative effect of forest degradation was a decrease in soil quality that leads to a reduction in most microbial activities related to soil C and N cycles as a result of less efficient microbial communities. Interestingly, soil C mineralization was more affected than N mineralization in this forest, so forest degradation not only reduced soil C and N stocks but altered C and N cycling. In addition, rehabilitation of degraded natural forests with Alnus subcordata enhanced soil mineral nitrogen availability, while following Quercus castaneifolia plantation, the most positive effect was found on soil carbon microbial fractions. Contrary to our hypothesis, reforestation with Quercus was more efficient than Alnus in recovering soil function, as all microbial indexes reflected more efficient soil microbial communities. Higher litter inputs in Quercus plantations and thus, soil organic matter quantity, were more important than lower litter quality for soil recovery. The findings of this study strongly

CRediT authorship contribution statement Razie Sanji: Investigation, Writing - original draft. Yahya Kooch: Software, Supervision. Ana Rey: Writing - review & editing. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Appendix 1 Pearson correlation coefficients (r) of soil C and N fractions and microbial activities with litter and soil properties across different land covers. Litter and soil physical features Soil C fractions and microbial activities

Soil N fractions and microbial activities

L. thickness

L. C

L. N

L. C/N

L. P

L. K

Bulk density

Sand

Silt

Clay

Water content

BR SIR MBC qCO2 Microbial quotient C availability index POM-C DOM-C

0.47 0.58* 0.62* −0.28 0.30

0.21 0.22 0.23 0.16 0.02

0.35 0.34 0.45 −0.08 0.32

−0.08 −0.07 −0.15 0.26 −0.28

0.10 −0.04 0.10 −0.04 −0.04

0.41 0.47 0.55* −0.33 0.31

−0.31 −0.20 −0.28 0.11 −0.40

−0.11 −0.22 −0.28 0.35 −0.05

−0.02 0.00 0.06 −0.18 0.09

0.17 0.28 0.29 −0.23 −0.04

0.32 0.33 0.47 −0.31 0.25

0.24

0.12

0.27

−0.11

0.18

0.21

−0.24

−0.01

−0.02

0.05

0.21

0.30 0.52*

0.13 0.09

0.31 0.37

−0.13 −0.24

0.13 0.29

0.48 0.42

−0.19 −0.23

−0.14 −0.14

0.07 0.04

0.09 0.12

0.40 0.45

Ammonium Nitrate N mineralization MBN POM-N DOM-N

0.04 0.16 0.08

0.04 −0.12 −0.15

0.23 0.36 0.11

−0.16 −0.53* −0.30

0.05 0.28 0.10

0.35 0.35 0.28

−0.20 −0.20 −0.08

−0.15 −0.30 −0.09

−0.09 0.08 −0.00

0.31 0.29 0.12

0.26 0.23 0.12

0.52* 0.16 0.38

0.09 0.13 0.03

0.42 0.47 0.27

−0.30 −0.28 −0.23

0.22 0.28 0.23

0.55* 0.66* 0.53*

−0.28 −0.23 −0.18

−0.20 −0.23 −0.12

0.11 −0.04 −0.07

0.13 0.35 0.24

0.42 0.51* 0.26

pH

EC

Organic C

C stocks

Total N

N stocks

C/N ratio

Available P

Available K

Available Ca

Available Mg

BR SIR MBC qCO2 Microbial quotient C availability index POM-C DOM-C

−0.33 −0.03 −0.27 −0.00 −0.45

−0.17 −0.02 −0.25 0.15 −0.47

0.04 0.26 0.35 −0.35 −0.39

−0.01 0.21 0.25 −0.31 −0.42

0.09 0.25 0.26 −0.27 −0.38

0.02 0.19 0.16 −0.23 −0.43

0.01 0.14 0.35 −0.34 −0.20

0.05 0.30 0.07 −0.07 −0.26

−0.09 0.10 0.00 −0.11 −0.33

−0.03 0.20 0.14 −0.23 −0.13

0.06 0.33 0.33 −0.40 −0.16

−0.34

−0.16

−0.05

−0.09

0.00

−0.05

−0.04

−0.07

−0.14

0.09

−0.04

−0.28 −0.32

−0.38 −0.31

0.21 0.22

0.15 0.16

0.16 0.20

0.10 0.15

0.20 0.15

−0.06 0.09

−0.13 0.00

0.03 0.04

0.26 0.21

Ammonium Nitrate N mineralization MBN POM-N DOM-N

0.06 −0.16 −0.00

−0.08 −0.02 0.02

0.26 0.06 0.10

0.16 0.02 0.09

0.26 0.14 0.16

0.17 0.08 0.13

0.16 −0.09 −0.05

0.14 0.06 0.16

0.01 0.09 0.26

0.14 0.22 0.19

0.28 0.22 0.28

−0.29 −0.02 −0.06

−0.27 −0.14 −0.16

0.24 0.32 0.36

0.17 0.26 0.29

0.27 0.41 0.41

0.18 0.32 0.33

0.09 0.00 0.09

0.12 0.09 0.15

0.08 0.06 0.09

0.20 0.30 0.16

0.21 0.33 0.33

Soil chemical features Soil C fractions and microbial activities

Soil N fractions and microbial activities

*Significant at the Bonferroni-adjusted p-value < 1.6 × 10−4. Appendix 2 Correlation of litter, soil physico-chemical properties, C and N microbial indices with PCA components. Litter and soil physico-chemical properties Litter Litter Litter Litter Litter

thickness C N C/N P

Axis 1

Axis 2 ns

−0.79 −0.45ns −0.96* 0.66ns −0.63ns

ns

−0.58 −0.80ns 0.22ns −0.72ns −0.71ns

8

Soil C and N microbial indices

Axis 1

Axis 2

BR SIR MBC qCO2 Microbial quotient

−0.97* −0.87ns −0.94* 0.95* −0.87ns

−0.15ns −0.48ns −0.31ns 0.13ns −0.24ns

Ecological Indicators 112 (2020) 106132

R. Sanji, et al. Litter K Bulk density Sand Silt Clay Water content pH EC Organic C C stocks Total N N stocks C/N ratio Available P Available K Available Ca Available Mg

−0.96* 0.95* 0.89ns −0.48ns −0.88ns −0.98* 0.82ns 0.71ns −0.96* −0.96* −0.95* −0.94* −0.47ns −0.70ns −0.36ns −0.69ns −0.94*

0.25ns −0.20ns −0.33ns −0.05ns 0.44ns −0.13ns 0.40ns 0.38ns −0.09ns −0.17ns 0.24ns 0.27ns −0.75ns 0.28ns 0.72ns 0.70ns 0.14ns

C availability index POM-C DOM-C Ammonium Nitrate N mineralization MBN POM-N DOM-N

−0.92ns −0.96* −0.93* −0.95* −0.94* −0.96* −0.99** −0.92ns −0.98*

0.12ns −0.27ns −0.28ns 0.57ns 0.62ns 0.26ns −0.05ns 0.35ns 0.15ns

*P < 0.05. **P < 0.01. ns = not-significant.

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