Co-elevated CO2 and temperature and changed water availability do not change litter quantity and quality of pine and oak

Agricultural and Forest Meteorology 280 (2020) 107795

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Co-elevated CO2 and temperature and changed water availability do not change litter quantity and quality of pine and oak

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Park Hyun-Jina,1, Lim Sang-Sunb,1, Yang Hye Ina, Lee Kwang-Seungc, Park Se-Ina, ⁎ Kwak Jin-Hyeobd, Kim Han-Yonge, Oh Seung-Wonf, Choi Woo-Junga, a

Department of Rural & Biosystems Engineering, Chonnam National University, Gwangju 61186, Republic of Korea Bio R&D Center, CJ Cheiljedang, Suwon, Gyeonggi-do 16495, Republic of Korea c National Instrumentation Center for Environmental Management, Seoul National University, Seoul 08826, Republic of Korea d Department of Rural Construction Engineering, Chonbuk National University, Jeonju, Jeollabukodo 57896, Republic of Korea e Department of Applied Plant Science, Chonnam National University, Gwangju 61186, Republic of Korea f Department of Statistics, Chonnam National University, Gwangju 61186, Republic of Korea b

A R T I C LE I N FO

A B S T R A C T

Keywords: Global warming Lignin Litter decomposition Microbial respiration Stable carbon isotope Stable nitrogen isotope

Elevated CO2 concentration ([CO2]) and air temperature (Tair) as well as changed soil water availability (Wsoil) may affect quantity, chemistry, and microbial decomposability of tree leaf litter. However, our understanding is limited mainly to the effect of elevated [CO2]. This study investigated the effects of elevated [CO2] and Tair in combination with two Wsoil regimes on the quantity and chemistry including the ratio of lignin to nitrogen (lignin/N) of litter produced by Pinus densiflora and Quercus variabilis saplings, and microbial respiration of the soils amended with the litters. Either elevated [CO2] or high Wsoil alone increased litter production; meanwhile elevated Tair alone decreased litter production. However, co-elevation of [CO2] and Tair did not change litter production regardless of Wsoil regime for both species. Among litter chemistry, the lignin/N, which is a robust indicator of litter decomposability, of litter was changed in parallel with litter quantity (i.e., lignin/N ratio increased when litter quantity increased and vice versa) mainly due to dilution of N. Due to the opposite effect of warming and elevated [CO2] on litter quantity, lignin/N was not changed under co-elevated [CO2] and Tair at a given Wsoil regime for both species. Other litter chemistry including non-structural carbohydrates and minerals was also affected by [CO2], Tair, or Wsoil. However, changed litter chemistry did not change the CO2 emission from the soils amended with the litters; however, addition of litter with low lignin/N and high nutrients increased microbial biomass in the soil. This study enlarges our understanding of the effects of changed climatic variables on litter quantity, chemistry, and microbial decomposability and suggests that co-elevation of [CO2] and Tair may not cause a significant change in the litter parameters regardless of Wsoil. Study with mature trees at a natural forest should further improve our understanding.

1. Introduction Leaf litter (referred to as litter hereafter) plays important roles in the cycling of carbon (C) and nutrients such and nitrogen (N) and phosphorus (P) in forests (Wood et al., 2006). In addition, as forests store approximately 45% of total terrestrial C (Bonan, 2008) and 85% of the global biomass C (Saugier et al., 2001), litter also plays a critical role in global C cycling (Berg and McClaugherty, 2008; Prescott, 2010). Therefore, to predict C and nutrients cycling in the future, it is

necessary to understand how elevated atmospheric CO2 concentration ([CO2]), air temperature (Tair), and changed rainfall pattern affect quantity and quality of litter produced by trees (e.g., Liu et al., 2009; Norby et al., 2001). Among the climatic variables that might affect litter quantity and quality, the effects of elevated [CO2] have been well documented. A number of studies have shown that elevated [CO2] increase tree growth (e.g., Norby et al., 2005) and thus litter production (e.g., Zhang et al., 2017) due to so-called “CO2 fertilization effect” unless other resources

Abbreviations: Ccum, cumulative CO2-C; % CR, % C respired; lignin/N, ratios of lignin-to-N; MBC, soil microbial biomass C; NSC, non-structural carbohydrate; TGFCs, temperature-gradient field chambers; Tair, air temperature; Wsoil, soil water availability ⁎ Corresponding author. E-mail address: [email protected] (W.-J. Choi). 1 Joint first authorship. https://doi.org/10.1016/j.agrformet.2019.107795 Received 14 January 2019; Received in revised form 26 September 2019; Accepted 8 October 2019 0168-1923/ © 2019 Elsevier B.V. All rights reserved.

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2. Materials and methods

are limited. The elevated [CO2] further changes litter chemistry; i.e., the increased biomass often translates into reduced N concentration due to dilution effect and into increased lignin concentration, leading to increased ratios of lignin-to-N (lignin/N), which is commonly used as a robust surrogate of litter quality (e.g., Cha et al., 2017; Norby et al., 2001; Park et al., 2018). For example, in a meta-analysis, Norby et al. (2001) showed an overall 7.1% reduction in N concentration coupled with a 6.5% increase in lignin concentration by elevated [CO2]. Numerous studies showed that increased lignin/N retards litter decomposition as lignin is recalcitrant to microbial decomposition (Cha et al., 2017; Cotrufo and Ineson, 1996; Cotrufo et al., 1998). Elevated Tair is another climatic variable that might affect litter quantity and quality. Soil heating experiments (e.g., King et al., 1999) are available and direct effects of elevated Tair on litter decomposition in the soils are well documented (e.g., Rouifed et al., 2010); however, relevant studies on the effects of elevated Tair on litter quantity and quality is very limited probably due to difficulty in manipulating Tair compared to [CO2] (Lukac et al., 2010). Since the photosynthetic enzyme, ribulose bisphosphate carboxylase (Rubisco), quickly acclimates to temperature (Bernacchi et al., 2002) and photorespiration increases at temperatures above the optimum for Rubisco activity (e.g., around 25°C), elevated Tair may not directly increase tree growth and thus litter quantity (Lukac et al., 2010). However, elevated Tair may change litter chemistry through an enhanced allocation of nutrients to shoots and leaves (Domisch et al., 2002; Fotelli et al., 2005) and stimulation of soil N mineralization (Jarvis and Linder, 2000; Pendall et al., 2004). In addition, under climate change, soil water availability (Wsoil) might be another critical abiotic factor that affects tree growth (Cubasch et al., 2013). As Wsoil affects photosynthesis directly through regulation of stomatal conductance and indirectly through influencing nutrient availability (Kreuzwieser and Gessler, 2010), Wsoil might modify the effects of elevated [CO2] and Tair on the quantity and quality of litter (Lukac et al., 2010). Though elevated [CO2] and Tair and changes in Wsoil are expected to occur simultaneously in the future (Cubasch et al., 2013), our understanding on the changes in quantity and quality of litter produced by trees under different combinations of [CO2] × Tair × Wsoil is very limited (Wertin et al., 2010). In a previous study (Park et al., 2018), we have found that elevated [CO2] affect litter chemistry and microbial decomposability, but the effects of co-elevated [CO2] and Tair and changed soil water availability has not been explored yet. To fill the knowledge gap, we investigated changes in quantity, chemistry, and microbial decomposability of litters of two functionally different trees, Pinus densiflora (a coniferous evergreen species; pine) and Quercus variabilis (a broad-leaved deciduous species; oak), grown under different levels of [CO2] × Tair × Wsoil combinations. We hypothesized that 1) for litter quantity, elevated [CO2] would increase litter quantity due to the well-known “CO2 fertilization” effect, elevated Tair may not increase litter quantity as trees acclimate to changes in Tair, and high Wsoil would lead to increased litter quantity; and thus the combined effects of elevated [CO2] and Tair may increase litter quantity at a given Wsoil regime, and when high Wsoil is combined with co-elevation of [CO2] and Tair, litter quantity may further increase; 2) for litter chemistry, elevated [CO2] and high Wsoil would increase lignin/N due to N dilution with increased litter biomass, elevated Tair would decrease lignin/N through enhanced N supply to leaves, and thus, the direction and magnitude of changes in lignin/N may be determined by the relative effect of elevated [CO2] and Tair, and when high Wsoil is combined with co-elevation of [CO2] and Tair, lignin/N of litter may decrease; and 3) changed litter chemistry (e.g., lignin/N) by elevated [CO2] and Tair and changed Wsoil would affect decomposition of litter in the soils amended with the litter.

2.1. Experimental facility description This study was performed using temperature-gradient field chambers (TGFCs) with or without CO2 fumigation located at the experiment field of Chonnam National University (126° 53′ E, 35° 10′ N, alt. 33 m), Gwangju, South Korea. The details of the TGFCs are described in Park et al. (2018) and supplementary materials. Briefly, six independent chambers (2.4 m in width × 24.0 m in length × 2.0 m in height for each chamber) were used; three of which were for ambient [CO2] condition, and the rest were for elevated [CO2] condition. The [CO2] of the chambers assigned to the elevated [CO2] was controlled at 660 ppmv by fumigating CO2 from a pure CO2 cylinder, and in each chamber, a linear Tair gradient was created along the longitudinal axis of the chambers with diurnal fluctuations by solar radiation or supplying warm air. The Tair difference across the chambers was set at 3°C, and thus the TGFCs could simulate the A1B of IPCC Special Report Emission Scenarios which is close to Representative Concentration Pathways 6.0 (Cubasch et al., 2013). More details on the controlling and monitoring of [CO2] and Tair are described in the supplementary materials. Regarding precipitation in East Asia, annual precipitation in the period between 2081 and 2100 is expected to increase by 7% compared to the present with large annual variations (IPCC, 2014).

2.2. Experimental design and tree sapling growing experiment The present experiment was performed as a series of studies to investigate the single and multiple effects of elevated [CO2] and Tair and changed Wsoil on the growth and litter characteristics of the two functionally different tree species, pine and oak, and the effect of elevated [CO2] on litter chemistry has been reported in Park et al. (2018). The experimental design used in the present study was blocked split-plot with two levels of [CO2] as whole-plot treatments and with two levels of Tair, and two levels of Wsoil as progressive split-plot treatments (Table 1). Two-year old saplings of pine and oak were grown in pots (28 cm in diameter × 35 cm in height) packed with forest soil (40 kg on dry basis) that was collected from Mt. Naejang (35° 26′ N, 126° 45′ E) (Table 2) for two years. It is the best to conduct the experiments with mature trees in a forest; however, while recognizing the limitation of the present experiment, we believe that controlled experiments with saplings may provide a closer look at the ecophysiological responses to the changes in Table 1 CO2, temperature, and soil water availability treatments applied. Treatments CO2 concentrationa

Temperatureb

Water availabilityc

Code

Ambient (CA)

Ambient (TA)

Low (WL) High (WH) Low (WL) High (WH) Low (WL) High (WH) Low (WL) High (WH)

Elevated (TE) Elevated (CE)

Ambient (TA) Elevated (TE)

a

CATAWL CATAWH CATEWL CATEWH CETAWL CETAWH CETEWL CETEWH

Daily mean CO2 concentration was 335.0 ± 1.4 ppmv and 322.6 ± 1.3 ppmv for ambient and 638.6 ± 5.3 ppmv and 599.1 ± 3.8 ppmv for elevated regimes in the first and second seasons, respectively. b Daily mean temperature was 23.8 ± 0.3°C and 24.3 ± 0.3°C for ambient and 26.1 ± 0.3°C and 26.8 ± 0.3°C for elevated regimes in the first and second seasons, respectively. c Daily mean soil water content was 0.132 ± 0.003 cm3 H2O cm−3 soil and 0.086 ± 0.075 cm3 H2O cm−3 soil for low and 0.173 ± 0.002 cm3 H2O cm−3 soil and 0.154 ± 0.003 cm3 H2O cm−3 soil for high water availability regimes in the first and second seasons, respectively. 2

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The litter samples were hand-mixed thoroughly and a portion of the litter samples (5‒20 g depending on the litter quantity) was ground to fine powder with a ball mill (MM-200, Retsch GmbH 88 & Co., KG, Haan, Germany) and used for chemical analysis and the incubation experiment. In the present study, among several litter chemistry variables, we analyzed elemental compositions such as C, N, P, calcium (Ca), aluminum (Al), manganese (Mn), and organic compounds such as lignin and non-structural carbohydrate (NSC). Some elements (i.e. N, P, and Ca) are major nutrients for microbes (Prescott, 2010) and Mn is an essential element for lignolytic enzyme of saprotrophic white-rot fungi (Davey et al., 2007); whereas Al is toxic to microbes (Piña and Cervantes, 1996). Lignin is a typical recalcitrant compound; whereas NSC is readily decomposable compound (Prescott, 2010). The C isotope ratio (δ13C) and δ15N were also analyzed as δ13C is an indicator of photosynthetic gas exchange responses to environmental changes (Farquhar et al., 1989) and δ15N is related with N availability and loss in soils (Choi et al., 2017). The lignin contents were analyzed by a gravimetric method using hot sulfuric acid digestion (King and Heath, 1967). The determined lignin fraction may contain lignin-like materials as well as true lignin, this fraction was defined as lignin in this study (Osono and Takeda, 2004). The NSC contents were determined by a gravimetric method after gelatinization followed by enzyme (α-amylase and amyloglucosidase) reaction that solubilize the NSC (Ohnish and Horie, 1999). Total C and N concentrations were determined by a combustion method (Nelson and Sommers, 1996) using an elemental analyzer (FLASHEA1112, Thermo, USA). Mineral (P, Ca, Mn, and Al) concentrations were determined using an inductively coupled plasma (ICP) emission spectrophotometer (IRIS-AP, Thermo Jarrell Ash Corp., Fanklin, MA, USA) after digestion of 0.5 g of sample with a HNO3-HClO4-H2SO4 mixture (1:8:1). The C (δ13C) and N (δ15N) isotope ratios were determined with a continuous-flow stable isotope ratio mass spectrometer (IsoPrime-EA, Micromass, Manchester, UK). Carbon and N isotope compositions (δ) were calculated as

Table 2 Selected chemical properties of soils used for pot and incubation experiments. Variablea

Soils used for pot experiment

Soils used for incubation experiment

pH (1:5) Total C (g C kg−1) Total N (g N kg−1) NH4+ (mg N kg−1) NO3− (mg N kg−1) Available P (mg P2O5 kg−1)

5.10 (0.02) 7.2 (0.1) 0.9 (0.1) 9.4 (0.7) 0.2 (0.1) 8.5 (0.4)

5.93 (0.04) 7.4 (0.8) 0.8 (0.1) 14.1 (1.2) 1.1 (0.2) 7.4 (0.8)

Values are means with the standard errors in parentheses (n=3). a pH was measured at a 1-to-5 ratio of soil-to-water; total C and N concentration with a combustion method (Nelson and Sommers, 1996) using an elemental analyzer (FLAHEA-1112, Thermo, USA); NH4+ and NO3− with Kjeldhal distillation method after extracting with 2 M KCl at 1-to-5 ratio of soilto-extractant (Keeney and Nelson, 1982); available P with Bray #1 method (Kuo, 1996).

[CO2] and Tair during regeneration of trees (e.g., Mayoral et al., 2015; Wertin et al., 2010; Wertin et al., 2012). A total of 48 pots was prepared for two levels of the factors (two [CO2] × two Tair × two Wsoil × two tree species) in triplicates (three sets (block) of TGFCs). The pots received 6.7 g N m−2 (as NH4NO3), 7.6 g P2O5 m−2, and 5.2 g K2O5 m−2 (as KH2PO4) (10 mg N kg−1, 12 mg P2O5 kg−1, and 8 mg K2O kg−1) in May of each year. The N isotope ratio (δ15N) of the N fertilizer was –3.9 ± 0.1‰. The N rate was set by considering the annual atmospheric N (NH4+ + NO3−) deposition rate (about 6.2 – 7.2 mg N m−2) of the study area (Lee et al., 2012). To mimic forest soil conditions, the top 10 cm soil was mixed with 400 g of litter of either pine or oak collected from the forest. The lignin and N concentrations of the litters were 427.2 ± 5.7 g kg−1 and 11.2 ± 0.2 g kg−1 for pine and 382.1 ± 3.1 g kg−1 and 14.1 ± 0.1 g kg−1 for oak, respectively. In each TGFCs, two pots for each species were placed at 3 m (ambient Tair) and 18 m (elevated Tair) from the inlet to minimize the edgeeffect in the late April, and saplings were grown under the designated [CO2] and Tair conditions until the early October of each year. Water was supplied to the pots using a semi-automatic drip irrigation system equipped with soil moisture sensors (EC5, Decagon Devices, Inc., Pullman, WA, USA) to maintain soil moisture content between 0.1 and 0.2 cm3 H2O cm−3 soil during the growing seasons. For low and high Wsoil regimes, one and two drippers were inserted 10 cm deep into the pots, respectively. Weekly irrigation amount for each pot was 500 and 1000 mL for low and high Wsoil, respectively, in May, June, and September when evapotranspiration was relatively small, and irrigation was doubled in July and August when evapotranspiration was relatively great. The daily mean [CO2], Tair, and Wsoil of the treatments during the tree growing period of each year are depicted in the supplementary materials (Fig. S1), and the average values during the growing period are provided in the footnote of Table 1. It is worthy to note that the Wsoil under elevated Tair was lower than under ambient Tair by 39.9% for low Wsoil and by 21.6% for high Wsoil due to increased evapotranspiration by warming.

δ (‰) = [(R sample/R standard) − 1] × 1000 where R is the ratio of 13C/12C or 15N/14N, and the standards were the Vienna Pee Dee Belemnite standards for C and atmospheric N2 for N. Calibration for the analysis was performed using IAEA-C5 (wood, −25.5‰) and IAEA-C6 (sucrose, −10.8‰) for δ13C and IAEA-N1 and N2 (both ammonium sulfate, +0.4‰ and +20.3‰, respectively) for δ15N. The precision of the measurements was checked (n=10) in each run with an internal reference material, a litter sample (−26.1 ± 0.2‰ for δ13C and +1.3 ± 0.1‰ for δ15N) and was found to be better than 0.2‰. The C isotope discrimination factor (Δ13C) was calculated using the equation of Farquhar et al. (1989) and the Δ13C was corrected (Δ13Ccorr) using an equation that is based on a hyperbolic relationship between Δ13C and [CO2] to remove the contribution of elevated [CO2] to C isotope discrimination (Trahan and Schubert, 2015) (see details of the correction procedure in the supplementary materials). 2.4. Incubation experiment and CO2 measurement

2.3. Sampling and analysis of litter The amount of litter C respired was determined by measuring CO2 emission from soils amended with the litters in the laboratory incubation experiment. As we intended to investigate the effects of changed litter chemistry on litter decomposition, the incubation experiment was conducted with finely ground litter samples to minimize the potential effect of physical properties of litter including specific area (Cortez et al., 2007) and toughness of litter (Pérez-Harguindeguy et al., 2000) following some relevant studies (Cleveland et al., 2014; Park et al., 2018). However, it is also warned that grinding might also affect litter decomposition (Bremer et al., 1991; Handayanto et al., 1997; Rinkes et al., 2014).

In October of the second growing season when leaf and needle were still green, the saplings were covered with nylon nets to collect all the litterfall, and litters were collected in February of next year. Litter produced in the first year was not collected as litter chemistry of that litter might be affected by the growing conditions before the treatments were imposed. It is worthwhile to mention that for pine, there was not only senesced but also green litterfall probably due to disturbance of natural growing environmental conditions (Pérez-Suárez et al., 2009). The collected litter samples were washed with distilled water to remove dust and soil particles, dried at 60°C in an oven for 5 days, and weighed. 3

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negligible (<0.7% of total CO2 emission) in previous studies (Lee et al., 2011; Lim et al., 2012). The incubation experiment was stopped at 60 days as CO2 emission from the soils amended with litter decreased to the level of the soils without litter, and thus the soil respiration could be assumed to be stabilized. The rate of CO2 respiration was expressed as mg C kg soil−1 day−1, and the cumulative CO2-C (Ccum) evolved from both SOC and added litter over the incubation period was also calculated. The amount of CO2 derived from litter was calculated by subtracting Ccum of the control (soil only) from total Ccum of the samples (both soil and litter) by considering priming effect; i.e., litter-induced increase in the emission of CO2 from decomposition of indigenous soil C was also subtracted from total CO2 emission from the soils amended with litters (Kuzyakov et al., 2000) (details are provided in the supplementary materials). The % C respired (% CR) from the amended litter was calculated as percentage of the total litter-C added that was respired as CO2 (Ccum from litter C). At the end of incubation, soil microbial biomass C (MBC) was determined by chloroform fumigation and extraction method (Lee et al., 2016; Vance et al., 1987). No correction factor was applied for MBC calculation as the exact value was unknown.

For the incubation experiment, 3 g of litter collected from triplicated pots under the same [CO2], Tair, and Wsoil treatments were mixed homogenously and used as a composite sample. Around 3 kg of soils were collected from randomly selected 10 pots, mixed thoroughly, and used for the incubation. In the incubation experiment, to investigate the single effect of litter chemistry on litter decomposition by ruling out the effect of soil properties, the same soil was used in all litter treatment. Thirty g of the soil (<2 mm) were placed into a 100-mL beaker; a total of 48 beakers were prepared for the litters of pine and oak grown under the eight treatments (two [CO2] × two Tair × two Wsoil) in triplicates. Additional three beakers containing soils without litter addition were prepared for control, and three empty beakers were also included for blank titration. Incubation experiment procedure was described in detail by Park et al. (2018). The moisture content of the soils in the beakers was brought to 60% of water holding capacity by adding distilled water. The beakers containing the soils were placed into 1-L air-tight Mason jar and pre-incubated at 25 ± 1 °C in darkness for 5 days to restore and stabilize the microbial activity. The ground litter sample (1 g) was placed into the soil beakers and mixed thoroughly with a spatula. The amount of litter applied to soils was determined by considering the quantity of litterfall in the pots (Fig. 1). A 20-mL vial containing 10 mL of 0.5 N NaOH (CO2 trap) was placed into the Mason jar, and the jars were incubated at 25 ± 1 °C in the darkness for 60 days. The CO2 trap was collected from the jars and a new vial containing fresh NaOH was placed back in the jar at 1, 2, 3, 10, 25, 45, and 60 days of the incubation. The amount of CO2 trapped was determined by titration with 0.5 N HCl solution after the addition of 2 mL 1 N BaCl2 (Zibilske, 1994). During the incubation, the jars were aerated with hand fan for 1 min and the soil moisture content was adjusted by adding distilled water to the initial weight of the soil container at each CO2 measurements. When the CO2 measurement interval was longer than 5 days, aeration and soil watering were conducted every 5 days. Though CO2 may be lost during the aeration, we found that CO2 loss by aeration from the jars was

2.5. Statistical analysis Statistical analysis was performed using IBM SPSS Statistics 23 (IBM Crop., Armonk, New York, USA). Data were tested for normality of distribution with Kolmogorov-Smirnov test and homogeneity of variance with Levene's tests. Data on litter production and the concentrations of NSC, C, Mn, C/N, lignin/N, and Δ13Ccorr were skewed and thus log-transformed for further statistical analysis but original data were presented. Data on other litter chemistry such as Al, P and N, litter decomposition, and MBC were normally distributed and homogenous. For each species, the effects of [CO2], Tair, and Wsoil on litter quantity and chemistry and subsequent litter decomposition in the soils were assessed by analysis of variance (ANOVA) using the following Fig. 1. Litter production of pine and oak saplings grown under different CO2 concentration ([CO2]), air temperature (Tair), and soil water content (Wsoil) (A, left-side panel) and relative changes by each treatment against the corresponding counterpart (B, right-side panel). For litter production, values are the means of triplicates, and vertical bars indicate standard errors of the means (n=3). Details of the treatment codes (main factors and interaction) are provided in Table 1, and ANOVA is provided in Table 3. The same letter above the bars indicate that the values are not statistically different. For relative change, treatments that had significant effects were depicted, but some values that were not significant were also depicted for comparison. For pine, the effect of elevated [CO2] on litter production was significant regardless of Tair and Wsoil without any interaction with other treatments; the effect of elevated Tair was only significant with high Wsoil; and the effect of high Wsoil on litter production was significant, but its effect was greater under ambient Tair. For oak, elevated [CO2] and high Wsoil increased litter production independently without any interaction.

4

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3.2. Litter chemistry

linear mixed model:

All the litter chemistry variables were affected by one or more of [CO2], Tair, and Wsoil with or without interaction among the treatments for both species (Table 3 and Figs. 2–4). Lignin concentration of pine was increased (by 9.1%, P<0.001) but that of oak was decreased (by 6.8%, P=0.034) by elevated [CO2]. The NSC concentration of pine decreased (P<0.001) by elevated Tair, but the magnitude of decrement differs (P=0.029) with [CO2] and Wsoil. For oak, the NSC concentration increased (P=0.007) by high Wsoil without any effect of [CO2] and Tair. Carbon concentration was increased by elevated [CO2] for pine (P=0.013) and oak (P=0.003), and for oak, C concentration was also increased (P=0.038) by elevated Tair. For both pine and oak, N concentration was decreased (P=0.007 for pine and P=0.003 for oak) by elevated [CO2] but increased (both P<0.001) by elevated Tair, and for oak, N concentration was also decreased (P<0.001) by high Wsoil. The concentrations of other elements such as P, Ca, Al, and Mn as well as C/ N were all affected by either [CO2], Tair or Wsoil, and such effect of the individual treatment variable was affected by each other as indicated by the complicated interactions for both species (Table 3). The lignin/N of litter was affected by [CO2], Tair, and/or Wsoil for both species without interaction of the treatments (Table 3). For both species, lignin/N increased by elevated [CO2] (by 25.4% for pine and 13.8% for oak) but decreased (by 15.9% for pine and 19.2% for oak) by elevated Tair, and for oak, high Wsoil increased lignin/N (by 31.6%). Due to the opposite effects of elevated [CO2] and Tair on lignin/N, coelevation of [CO2] and Tair did not change lignin/N of litters for both species regardless of Wsoil level (Figs. 2 and 3). For both species, such changes in lignin/N were more strongly related to N concentration than to lignin concentration as indicated by the greater coefficient of determination for the relationship between N concentration and lignin/N than that for between lignin concentration and lignin/N (Fig. S2). Similarly, the changes in C/N was also driven by N concentration as supported by the correlation between N concentration and C/N (Fig. S2). The Δ13Ccorr decreased (P<0.001) by elevated [CO2] for both species. The δ15N decreased (P=0.018 for pine and P=0.013 for oak) by elevated [CO2] and increased (P=0.044 for pine and P=0.014 for oak) by elevated Tair. Comparing between species, on average across the treatments, pine

Zijkl = μ + Ci + Tj + Wk + (CT)ij + (CW)ik + (TW) jk + (CTW)ijk + εijkl (εijkl ∼ N(0,

σ 2))

where Zijkl is the response variable (such as litter quantity and chemistry) at ith (=1, 2) [CO2] (C), jth (=1, 2) Tair (T), and kth (=1, 2) soil water level (W) at lth (=1, 2, 3) replication within group. μ is the overall mean, and εijkl is the random variable errors within the experiment. At first, ANOVA was performed using the full model to test the effects of the three treatment variable ([CO2], Tair, and Wsoil). When a higher order-interaction was not significant, that terms were pooled to error term to obtain more degrees of freedom for the error term that allows a more powerful test of the main effects and interaction effects (Roy, 2001). When the treatment effects were significant (P < 0.05), the means were separated by Tukey's test. The level of significance for all statistical tests was set α= 0.05.

3. Results 3.1. Litter quantity Litter quantity was affected by [CO2], Tair, and Wsoil with or without interaction among the environmental variables (Table 3 and Fig. 1). On average, elevated [CO2] increased litter production for both pine (P=0.005) and oak (P=0.003), and such [CO2]-induced increases in litter production was affected neither by Tair nor by Wsoil. Elevated Tair decreased litter production of pine under high Wsoil but not under low Wsoil (P=0.004), and did not affect oak litter production regardless of [CO2] and Wsoil treatments. High Wsoil produced more (P<0.001) litter for both species compared to low Wsoil. The positive effect of high Wsoil on litter production was not interacted with [CO2] and Tair for oak; however, for pine, such effect of high Wsoil was more noticeable (P=0.004) under ambient Tair (increased by 82.4%) than that under elevated Tair (by 27.7%). Due to the suppressive effect of elevated Tair on litter production, co-elevation of [CO2] and Tair did not cause any change in litter production even under high Wsoil.

Table 3 Probability of analysis of variance for the effects of CO2 concentration (C), temperature (T), and soil water content (W) on litter quantity and chemistry of pine (Pinus densiflora) and oak (Quercus variabilis). Effectsa

Pine C T W C×T C×W T×W C×T×W Oak C T W C×T C×W T×W C×T×W

Quantity

Chemistryb Lignin

NSC

C

N

P

Ca

Al

Mn

C/N

Lignin/N

Δ13Ccorr

δ15N

0.005 0.002 <0.001 0.839 0.183 0.004 NS

<0.001 0.395 0.379 NS NS NS NS

0.189 <0.001 0.118 0.015 0.644 0.825 0.029

0.013 0.441 0.457 NS NS NS NS

0.007 <0.001 0.983 NS NS NS NS

0.039 <0.001 0.101 0.631 0.074 <0.001 NS

0.939 0.001 0.283 0.048 0.613 0.267 <0.001

0.145 0.746 0.028 0.001 0.983 <0.001 NS

<0.001 0.472 <0.001 0.910 0.566 0.911 <0.001

0.001 <0.001 0.183 0.013 0.300 0.026 NS

<0.001 0.002 0.661 NS NS NS NS

<0.001 0.686 0.389 NS NS NS NS

0.018 0.044 0.308 NS NS NS NS

0.003 0.952 <0.001 NS NS NS NS

0.034 0.102 0.717 NS NS NS NS

0.494 0.169 0.007 NS NS NS NS

0.003 0.038 0.162 NS NS NS NS

0.019 <0.001 <0.001 NS NS NS NS

<0.001 <0.001 <0.001 <0.001 0.076 0.003 NS

0.001 <0.001 <0.001 0.436 <0.001 0.071 0.013

<0.001 <0.001 <0.001 0.001 0.001 0.052 NS

<0.001 <0.001 <0.001 <0.001 <0.001 0.279 NS

<0.001 <0.001 <0.001 0.063 0.352 0.022 0.047

0.009 <0.001 <0.001 NS NS NS NS

<0.001 0.068 0.422 NS NS NS NS

0.013 0.014 0.515 NS NS NS NS

When a higher order-interaction was not significant (as indicated by NS), ANOVA was conducted for a lower order-interaction by pooling the terms to the error term. The bold indicates that the effects are significant at α=0.05. a Details of the treatments for the effects are provided in Table 1. b NSC, nonstructural carbohydrate; C, carbon; N, nitrogen; P, phosphorous; Ca, calcium; Al, aluminum; Mn, manganese; C/N, C-to-N ratio; Lignin/N, lignin-to-N ratio; Δ13Ccorr, corrected carbon isotope discrimination; δ15N, nitrogen isotope ratio. 5

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Fig. 2. Litter chemistry of pine saplings grown under different CO2 concentrations, air temperatures, and soil water contents. Values are the means of triplicates, and vertical bars indicate standard errors of the means (n=3). The same letter above the bars indicate that the values are not statistically different. Details of the treatment codes (main factors and interaction) are provided in Table 1, and ANOVA is provided in Table 3.

Wsoil (Fig. 6). Comparing between species, on average across, soils amended with oak litter had a greater MBC than those with pine litter by 72.3% (Fig. 5).

had a greater lignin concentration (by 31.9%) and lignin/N (by 23.6%) compared to oak; meanwhile oak had higher NSC (by 73.4%), Ca (by 2.8 fold), and Mn (by 4.4 fold) concentrations compared to pine (Figs. 2 and 3).

4. Discussion 3.3. Litter decomposition 4.1. Effects of [CO2], Tair, and Wsoil on litter production Litter addition significantly (P<0.001) increased CO2 emission from the soils compared to those without litter (Fig. S3). For pine litter, the Ccum from the soils amended with litter and % CR was not affected by any treatment variable including [CO2], Tair, and Wsoil, but those for oak litter produced under elevated [CO2] decreased compared with those produced under ambient [CO2] (Table 4 and Figs. 5 and 6). In spite of the effect of elevated [CO2] on decomposability of oak litter, warming with elevated [CO2] did not change litter decomposability of both species at a given Wsoil (Fig. 5). For pine, the concentration of MBC in the soils amended with litter was greater (P=0.010) for litter produced under elevated [CO2] than that under ambient [CO2] and such effect of [CO2] was interacted with Tair and Wsoil (Table 4 and Fig. 6). The interactive effect of Tair and Wsoil on MBC was also significant (Table 4 and Fig. 6); i.e., when litter produced under elevated Tair and high Wsoil was combined, MBC of the soils amended with the litter increased compared to those produced under elevated Tair or high Wsoil alone at a given [CO2] condition (Fig. 6). Due to such effect of elevated [CO2], elevated Tair and high Wsoil, MBC was greatest in the soils amended with litter produced under elevated [CO2]-elevated Tair-high Wsoil conditions (Fig. 5). For oak, MBC was affected by [CO2]-Tair-Wsoil in complicated manner as indicated by the significant interaction (P=0.024) among the three variables (Table 4), and the greatest MBC was observed for the soils amended with litter produced under ambient [CO2]-elevated Tair-low

Our results show that litter quantity increases by elevated [CO2], decreases by elevated Tair for pine but no change for oak, and increases under high Wsoil with interaction with each other, leading to production of greatest litter when elevated [CO2], ambient Tair, and high Wsoil were combined for both species (Fig. 2). Elevated [CO2] is known to stimulate tree growth as long as other factors such as nutrients and water availability are not limited (Idso and Idso, 1994; Kwak et al., 2016; Norby et al., 2005), leading to increased litter production (Zhang et al., 2017). The overall increment (24%) of litter production by elevated [CO2] found in the present study is similar to the increment (23 ± 2%) of net primary productivity by elevated [CO2] in four forest free-air CO2 enrichment experiment (Norby et al., 2005). The lowered Δ13Ccorr of litter grown under elevated [CO2] (Fig. 4) suggests that elevated [CO2] increased or up-regulated photosynthesis by increasing the carboxylation rate by Rubisco and competitively inhibiting the oxygenation of ribulose bisphosphate thereby reducing photorespiration while decreasing stomatal conductance (Long et al., 2004; Pinkard et al., 2010; Wang et al., 1996). Though it was hypothesized that elevated Tair might not affect litter production, this was true only for oak but not for pine (Table 3). In our study, warming-induced decreases in pine litter production was apparent under high Wsoil, which in turn implies that elevated Tair hampered tree growth which would have benefitted from high Wsoil as 6

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Fig. 3. Litter chemistry of oak saplings grown under different CO2 concentrations, air temperatures, and soil water contents. Values are the means of triplicates, and vertical bars indicate standard errors of the means (n=3). The same letter above the bars indicate that the values are not statistically different. Details of the treatment codes (main factors and interaction) are provided in Table 1, and ANOVA is provided in Table 3.

Fig. 4. Relative changes in litter chemistry against the corresponding counterpart treatments for pine (left panel) and oak (right panel) grown under different CO2 concentrations ([CO2]), air temperatures (Tair), and soil water contents (Wsoil): For each panel (1) lignin, (2) non-structural carbohydrate (NSC), (3) carbon, (4) nitrogen, (5) lignin/N, (6) corrected carbon isotope discrimination (Δ13Ccorr), and (7) nitrogen isotope ratio (δ15N). Details of the treatment codes (main factors and interaction) are provided in Table 1. The values of the chemistry were presented in Figs. 3 and 4, and ANOVA is provided in Table 3. For some chemistry variables (P, Ca, Al, Mn, and C/N), the relative changes as affected by [CO2], Tair, and Wsoil were not depicted as their interactions were too complicated.

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suggests that the effects of elevated Tair and changed Wsoil on litter production and associated tree physiology are inter-correlated (Thomas et al., 1999). In the present study, the lower Wsoil under elevated Tair than ambient Tair at a given irrigation regime (Table 1 and Fig. S1) indicates that elevated Tair might induce water stress and thus stomatal closure due to increased evapotranspiration demand (Oren et al., 1999), leading to decreased litter production of pine. Elevated Tair may also affect photosynthesis and photorespiration (Lukac et al., 2010). In the boreal forests where ambient Tair is mostly below the optimum, elevated Tair might increase photosynthesis as long as Tair does not increase over the optimum for Rubisco activity (e.g., around 25°C) (Wertin et al., 2012). In the temperate forest where the trees already experience Tair above the optimum, however, the opposite would be true (Lukac et al., 2010). It should be also noticed that O2 dissolves more efficiently than CO2 at high Tair which leads to increased photorespiration (Atkin et al., 2000; Weston and Bauerle, 2007). Though it is not straightforward to propose an optimum Tair for pine and oak saplings used in the present experiment, the decreased litter production of pine by elevated Tair (Fig. 1) suggests that elevated Tair (26.1 ± 0.3°C for 1st year and 26.8 ± 0.3°C for 2nd year) might induce photorespiration that reduces photosynthesis efficiency (Oishi et al., 2018). For oak, however, the negligible effect of elevated Tair on litter production suggests that oak species acclimate to warming-induced water stress by regulating stomatal conductance more efficiently compared to pine (Kwak et al., 2016; Renninger et al., 2015) probably due to thinner cross-section (Givnish, 2002) and less developed cutin layer (Wang and Feng, 2012) of oak species. Regarding Wsoil, as soil water availability is crucial for tree growth (Kreuzwieser and Gessler, 2010), the increase in litter production by high Wsoil for both species is obvious (Fig. 1). However, as discussed previously, elevated Tair should increase water loss through evapotranspiration (Lukac et al., 2010), and thus the benefit of high Wsoil would decrease by co-elevated Tair as compared to ambient Tair

Table 4 Probability of analysis of variance for the effects of sapling growing conditions such as CO2 concentration (C), air temperature (T), and soil water content (W) on the decomposition parameters of pine and oak of litters in the soils amended with the litters. Effectsa

Pine C T W C×T C×W T×W C×T×W Oak C T W C×T C×W T×W C×T×W

Cumulative CO2 emissionb

% Litter C respiredc

Microbial biomass carbond

0.590 0.730 0.396 NS NS NS NS

0.807 0.764 0.426 NS NS NS NS

0.010 0.073 0.524 0.013 0.020 <0.001 NS

0.018 0.376 0.637 NS NS NS NS

0.018 0.379 0.635 NS NS NS NS

0.366 0.122 0.078 0.016 0.956 0.398 0.024

When a higher order-interaction was not significant (as indicated by NS), ANOVA was conducted for a lower order-interaction by pooling the terms to the error term. The bold indicates that the effects are significant at α=0.05. a Details of the treatments for the effects are provided in Table 1. b Cumulative CO2 emission from litter (excluding soil) during 60-day incubation. c Calculated as % of litter C emitted as CO2 during 60-day incubation. d Measured at the end of 60-day incubation.

indicated by the lower magnitude of the increase in litter production when high Wsoil was combined with elevated Tair compared to with ambient Tair (Fig. 1). Such interaction between Tair and Wsoil further

Fig. 5. Litter-C respired during the 60-day incubation and microbial biomass C at the end of the 60-day incubation for the soils amended with litters of (A and B) pine and (C and D) oak that were grown under different CO2 concentrations, air temperatures, and soil water contents. Values are the means of triplicates, and vertical bars indicate standard errors of the means (n=3). The same letter above the bars indicate that the values are not statistically different. Details of the treatment codes are provided in Table 1, and ANOVA is provided in Table 4. Control is soil without litter addition, and thus litter C decomposition data are not applicable for A and C.

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Fig. 6. Relative changes in litter decomposition parameters: for pine, (A) microbial biomass C (MBC) in the soils amended with pine litter, and for oak, (B-1) cumulative CO2 emission from litter (Ccum), (B-2) % litter C respired (% CR), and (B-3) MBC in the soils amended with oak litter. Amended pine and oak litter were produced under different CO2 concentrations, air temperatures, and soil water contents. Details of the treatments are provided in Table 1, and relevant data are provided in Fig. 5, and ANOVA is provided in Table 4.

the higher δ15N of oak compared to pine litter (Figs. 2 and 3) implies that N cycling of oak soils is less tight due to faster N mineralization and nitrification rate as substrate quality of oak litter is better than pine litter (Son and Lee, 1997). The effects of Tair on lignin/N has rarely been reported. Our result shows that elevated Tair decreases lignin/N through increasing N concentration with little change in lignin concentration (Fig. 4). As litter production was decreased by elevated Tair (Fig. 1), such increases in N concentration by elevated Tair can be simply attributed to N enrichment resulting from decreased litter production. However, enhanced N mineralization under warmer conditions (Emmer and Tietema, 1990; MacDonald et al., 1995; Rustad et al., 2001) might have also contributed to the increased N concentration. In this context, increased δ15N of litter by elevated Tair at a given [CO2] (Fig. 4) indicates that tree assimilated N from enhanced mineralization of soil N that is likely to be enriched with 15N due to N loss as also reported by others (e.g., BassiriRad et al., 2003; Garten et al., 2011). The increased lignin/N under high Wsoil particularly for oak should also be attributed to decreased N concentration (Fig. 4) driven by increased litter production (Fig. 1) that causes N dilution. Comparing between species, the greater lignin/N of pine than oak is consistent with many other studies that reported broadleaf litter has a lower lignin/N than needle leaf litter (e.g., Lorenz et al., 2004; Pérez-Suárez et al., 2009). As NSC is mainly composed of sugars and starch, it may represent easily decomposable organic C fraction and thus is correlated with litter decomposition (Hättenschwiler and Jørgensen, 2010; Park et al., 2018). In the present study, the NSC concentration was not affected by [CO2] and literature suggests that the effects of elevated [CO2] on NSC concentration is not consistent; e.g., soluble carbohydrate concentration is not changed (Cotrufo et al., 1994), increases (Boerner and Rebbeck, 1995; King et al., 2001), or decreases (Lutze et al., 2000). However, NSC concentration was affected by Tair for pine and Wsoil for oak. For

condition particularly for pine. Taking the effects of the individual and multiple environmental factors on litter production into consideration together, our results suggest that the projected increases in [CO2] may increase litter production for both pine and oak particularly when water availability is not limited. However, concomitant warming may hamper the elevated [CO2]-enhanced litter production, resulting in insignificant changes in litter production regardless of Wsoil.

4.2. Effects of [CO2], Tair, and Wsoil on litter chemistry Increased lignin/N by elevated [CO2] found in the present study corroborates other studies that reported elevated [CO2] increases lignin/N through increased lignin concentration and decreased N concentration (Cha et al., 2017; Norby et al., 2001). In the present study, however, elevated [CO2] increased lignin concentration of pine litter but decreased that of oak litter (Fig. 4), suggesting that the effect of elevated [CO2] on secondary compound metabolism differs with species (Peñuelas et al., 1997). Therefore, the increased lignin/N for both species by elevated [CO2] should be ascribed primarily to decreased N concentration (Fig. 4) by N dilution due to increased litter biomass (Fig. 1) though trees are likely to uptake more N under elevated [CO2] to meet the increased N demand for biomass production (Norby et al., 2005; Zhang et al., 2017). Regarding tree uptake of N under elevated [CO2], Hofmockel et al. (2011) found that the δ15N of litter increased under elevated [CO2] due to enhanced mineralization of soil organic N and subsequent N loss that results in 15N enrichment of the remaining N. However, in the present study, the decreased δ15N of litter by elevated [CO2] (Fig. 4) suggests that trees supplemented N by assimilating N more efficiently under elevated [CO2] and thus N loss from the system was reduced probably due to increases in below-ground biomass that explores N (Norby et al., 2005; Zhang et al., 2017). Garten et al. (2011) also showed that δ15N of litter decreases by elevated [CO2], reflecting a tighter N cycle under N limiting conditions. In this context, 9

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litter addition, further suggested that substrate use efficiency, the proportion of assimilated substrates that is used for growth and enzyme production vs. being mineralized or respired (Cotrufo et al., 2013), is greater for oak litter than that for pine litter due to the higher NSC and lower lignin concentrations of oak litter (Fig. 3). Taken together, therefore, it is suggested that addition of litter grown under co-elevated [CO2] and Tair may not change CO2 emission in a short-term period. However, the changed MBC by addition of different litter highlights the necessity of further study to investigate the effect of changed litter chemistry on microbial C assimilation and associated changes in soil C dynamics.

pine, the decreased NSC by elevated Tair (Fig. 4) is coupled with decreased litter production (Fig. 1), suggesting that elevated Tair inhibited NSC accumulation probably due to warming-induced increases in photorespiration as previously discussed (Oishi et al., 2018). For oak, the increased NSC by high Wsoil suggests that oak allocated photosynthates to NSC more under better water conditions (Epron and Dreyer, 1996). The greater NSC concentration of oak than pine is in agreement with others; e.g., Li et al. (2016) reported that short-lived species (deciduous species) have a higher NSC concentration than longlived species (evergreen species). Though other litter chemistry variables such as P, Ca, Al, and Mn were also affected by either [CO2], Tair, Wsoil, or species, it was not straightforward to interpret the individual or combined effects of the treatments due to complicated interactions between the treatments (Table 3). Nevertheless, the consistently higher concentrations of Ca and Mn for oak than those for pine are in agreement with other studies that compared litter chemistry between evergreen coniferous and broad-leaved deciduous species (Berg and McClaugherty, 2008; Gholz et al., 2000). Combining the changed litter chemistry particularly lignin/N by [CO2], Tair, and Wsoil together, it was expected that elevated [CO2] may increase lignin/N, but co-elevation of Tair will negate such increase, leading to unchanged lignin/N under global warming with elevated [CO2] regardless of Wsoil.

5. Conclusion Our results suggest that either elevated [CO2] or elevated Tair alone may affect litter quantity, chemistry, and CO2 emission from the soils amended with the litters. However, co-elevation of [CO2] and Tair, which is the most probable expectation in the future, may not change the litter parameters for both pine and oak regardless of Wsoil due to the counterbalancing effect of elevated [CO2] and Tair on dry matter accumulation and on the concentration of carbohydrate compounds and elements. Though a high Wsoil produced more litter and changed litter chemistry, such effects were negated by elevated Tair. However, our results should be carefully implemented to the natural forests since this experiments were conducted with saplings (not with mature trees) and the litter samples were finely ground to minimize the effects of physical attributes of litter on decomposition. Nevertheless, with the given limitation, this study extends the current understanding of the effects of changing climatic variables on litter production, chemistry, and decomposability as most studies have considered single variable of elevated [CO2] or elevated Tair alone. Further studies with mature trees at a natural forest should further enlarge our understandings.

4.3. Effects of litter chemistry on soil respiration and MBC Among many litter chemistry variables, lignin/N is believed to be a robust predictor of litter quality and thus decomposability across various plant species (e.g., Prescott, 2010; Taylor et al., 1989; Zhang et al., 2008) though some studies (e.g., Park et al., 2018) reported that lignin/ N may not explain variations in litter decomposability within a species. Nevertheless, it is widely reported that high-quality litter with a low lignin/N decomposes faster than low-quality litter with a high lignin/N (Cotrufo et al., 2013; Manzoni et al., 2010; Rahman et al., 2013; Zhang et al., 2008). In the present study, however, though changes in [CO2], Tair, or Wsoil induced a wide range of litter chemistry particularly for lignin/N across the treatments, a significant change in the % CR from the amended litter was detected only for oak litter grown under elevated [CO2] vs. under ambient [CO2] (Fig. 6), which was associated with the increased lignin/N by elevated [CO2] (Fig. 4). Such marginal effect of litter chemistry (e.g., lignin/N) on litter decomposition suggests that changed lignin/N and other litter chemistry by environmental change may not always alter CO2 emission of soils amended with the litters, and thus lignin/N may not be a robust indicator of CO2 emission via litter decomposition (Norby et al., 2001; Park et al., 2018). However, it should be also cautioned that lignin is particularly important in the later stages of litter decomposition (e.g., Berg and McClaugherty, 2008), and thus the incubation period of our experiment may not be long enough to detect such role of lignin. Changes in MBC was more responsive to the addition of litters with different chemistry as compared to the respiration (Table 4 and Fig. 5). For both pine and oak, soils amended with relatively low lignin/N and C/N and high P and Ca concentration (e.g., litter produced under elevated [CO2]-elevated Tair-high Wsoil for pine) showed greater MBC compared to the others (Fig. 5). Therefore, it can be postulated that such changes in litter chemistry should favor for microbial assimilation of litter-derived C as microbes can easily access to substrate with low lignin/N, C/N, and Al but high nutrients such as P and Ca (Prescott, 2010). Comparing between species, the greater MBC of soils amended with oak litter than with pine litter is in agreement with many studies (e.g., Cheng et al., 2013; Iovieno et al., 2010; Ushio et al., 2008), which attribute the difference between species to the higher NSC, lower lignin/ N, and higher Ca, P, and Mn concentrations of oak than pine litter. In the present study, the greater MBC of soils with oak litter, together with insignificant difference in respiration of soils between pine and oak

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