Warming and forest management interactively affect the decomposition of subalpine forests on the eastern Tibetan Plateau: A four-year experiment

Geoderma 239–240 (2015) 223–228

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Warming and forest management interactively affect the decomposition of subalpine forests on the eastern Tibetan Plateau: A four-year experiment Zhenfeng Xu a,b,⁎, Chunzhang Zhao b, Huajun Yin b, Qing Liu b,⁎ a b

Institute of Forest Ecology, Sichuan Agricultural University, Chengdu, 611130, China Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, 610041, China

a r t i c l e

i n f o

Article history: Received 22 July 2014 Received in revised form 21 October 2014 Accepted 24 October 2014 Available online 8 November 2014 Keywords: Litter decomposition Experimental warming Reforestation Plantation Natural forest Tibetan Plateau

a b s t r a c t Increased rates of litter decomposition due to climatic warming have great potential to modify the carbon balance in forest soils, with consequent feedbacks to climate change. Reforestation could affect responses of litter decomposition to warming by altering litter type and soil conditions. However, less is known about the interactive impacts of forest management and climate change on litter decomposition. Here, we conducted a 4-year field experiment to investigate the effects of experimental warming on the decomposition of dragon spruce (Picea asperata Mast.) and red birch (Betula albo-sinensis Burk.) foliar litter in two contrasting sites (a dragon spruce plantation and a natural forest) using litter-bag method on the eastern Tibetan Plateau of China. During the four years of decomposition in the field, a clear pattern of faster mass loss was observed in red birch litter compared to dragon spruce needle. Additionally, regardless of warming regimes and litter types, mass loss rates were higher in the natural forest site than in the plantation site. Warming did not affect mass loss of dragon spruce litter during the early decomposition stage, but increased it over the later decomposition stage. In contrast, warming had enhanced mass loss of red birch litter on most sampling days. Red birch litter was more sensitive to warming compared with dragon spruce needle. Our results clearly indicated that reforestation can alter litter quality and soil conditions, and further affect the litter decomposition of subalpine forest ecosystem to projected climatic warming. This calls for incorporating forest management practice in climate–carbon models to better understand carbon dynamics of forest ecosystems under climate change. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Global warming is predicted to impact most regions of the northern hemisphere and will be particularly pronounced at high latitudes and altitudes (IPCC, 2007). Temperature is one of the most important factors controlling plant litter decomposition (Ruark, 1993) and litter decomposition is a major component of the global carbon budget (Aerts, 1997, 2006). Thus, warming-induced increases in rates of litter decomposition might greatly affect the carbon balance in forest soils, with consequent feedbacks to climate change (Rustad and Fernandez, 1998). Litter decomposition is hierarchically controlled by the triad: environmental conditions N “litter quality” (chemical and physical composition of the litter) N soil organisms (Aerts, 1997). A review has shown that effects of warming on litter decay varied among litter types, biomes, warming techniques and sites (Aerts, 2006). For a given ecosystem, the rate of litter decay is mostly influenced by litter quality. High quality litters are often characterized by higher N concentrations and lower C:N ⁎ Corresponding authors at: Institute of Forest Ecology, Sichuan Agricultural University, Chengdu 611830, China. E-mail addresses: [email protected] (Z. Xu), [email protected] (Q. Liu).

http://dx.doi.org/10.1016/j.geoderma.2014.10.018 0016-7061/© 2014 Elsevier B.V. All rights reserved.

and lignin:N ratios, and can decompose faster compared to low quality litters (Sanchez, 2001). The effect of warming on litter decomposition may be dependent on the initial chemical properties of plant litter, such as nutrient concentration, carbon components and stoichiometry (Fierer et al., 2005). Moreover, the decomposition rate of plant litter is also substantially influenced by soil nutrients and/or organisms. Therefore, land use change may cause significant changes in litter quality and soil conditions of ecosystem, and further impact the responses of litter decay to climate change. The subalpine/alpine forests on the Tibetan Plateau are considered to be very vulnerable and sensitive to global warming since warming is expected to increase by 2.6–5.2 °C by 2100 on the Tibetan Plateau (Chen et al., 2013). Picea asperata Mast. and Betula albo-sinensis Burk. are two key tree species in this region and reforestation is the main forest management practice (Xu et al., 2010). Over the last decades, natural coniferous forests on the eastern Tibetan Plateau were deforested and reforested with dragon spruce. Reforestation may therefore induce great changes in decomposition dynamics through altering litter quality and soil conditions. To gain mechanistic insights into the complex interplay of these factors of landscape change, it is very important to disentangle the relative role of warming, litter quality and soil condition on

Z. Xu et al. / Geoderma 239–240 (2015) 223–228

litter decay in this region. Therefore, we conducted a four-year experiment in two contrasting soils to investigate the effects of experimental warming on the decomposition of two different litter types (dragon spruce needle and red birch leaves) which are dominant litter types for reforested and natural sites respectively. The aim of the experiment was to assess if changes in decomposition dynamics are due to changes in litter type or/and changes in the site conditions and how this relationship is affected by warming. Specifically, the objectives were to determine: 1) how experimental warming affects litter decomposition of the two litter types; and 2) whether there are differences in mass loss between litter types and sites under the warming conditions. 2. Materials and methods 2.1. Site description The study was conducted on two sites that were within approx. 300 m distance of each other. One site was in a dragon spruce plantation and the other is in a spruce-fir-dominated natural forest. Both experimental sites are located at the Miyaluo Experimental Forest of Lixian County on the eastern Tibetan Plateau (31°35′ N; 102°35′ E; 3150 m a.s.l). Soils at two sites are classified as belonging to the mountain brown soil series (Chinese taxonomy). The basic soil properties are as follows: organic C 44.82 ± 3.25 g kg− 1, total N 2.95 ± 0.34 g kg− 1, total P 0.65 ± 0.03 g kg− 1, total K 14.16 ± 0.39 g kg− 1 and pH 6.19 ± 0.47 for the plantation; organic C 145.02 ± 14.87 g kg−1, total N 9.56 ± 1.19 g kg−1, total P 0.67 ± 0.07 g kg−1, total K 11.31 ± 0.51 g kg− 1 and pH 5.85 ± 0.65 for the natural forest (Xu et al., 2010). In late September 2008, six open top chambers (OTC) were set up in two contrasting forests with similar canopy, respectively. Further details of the experimental design are described in our previous paper (Xu et al., 2010). 2.2. Litterbag construction and chemical analyses Naturally fallen leaves of dragon spruce and red birch were collected with litter collectors in September 2009. Litter samples were air dried to a constant mass. Litter decomposition was determined using the litterbag method under field conditions. Each litterbag (15 × 20 cm, dimension), made of a 1 × 1 mm polyethylene mesh, contained a total 10.00 g of air-dried leaves/needles. For each litter type, duplicate sets of litter bags (10 per plot) were deployed on the soil surface in the respective treatment section in late October 2009. In order to avoid the edge effects of OTC, litter bags were put in the center of OTC at the two sites. We sampled one litterbag from each OTC or control plot on six occasions: early spring 2010 (April), late autumn 2010 (October), early spring 2011, late autumn 2011, later autumn 2012, and early spring 2013. In the laboratory, extraneous matter such as other plant materials, rocks and soil animals were handpicked from the decomposed litters, and the clean samples were then oven-dried at 85 °C to a constant mass. Mass loss was calculated as the difference between the initial dry mass and the actual dry mass of leaves at each sampling date. Total carbon was analyzed with a total C/N analyzer (Multi N/C 2100, Analytik Jena AG, Germany) and total nitrogen was determined using a UDK152 apparatus (Velp Scientifica, Ulpiate, Milan, Italy). The powdered samples were digested with a concentrated acid mixture of HNO3–HClO4 (3:1, v/v) and heated at 160 °C for 5 h. Then, total phosphorus was determined by inductively coupled plasma spectroscopy (ICP-MS, IRIS Advantage 1000, Thermo Elemental, Waltham, MA, USA). Lignin and cellulose were measured using the Acid Detergent Lignin method.

respectively. Near surface temperature at 30 cm height was measured by the sensors (DS1921G-F5, Maxim Integrated Products, Dallas Semiconductor Inc., Sunnyvale, California) connected to a dataloger (Campbell AR5, Avalon, USA). OTC manipulations increased near surface temperature (30 cm) by approximately 1.2 °C and 1.3 °C, respectively, in 2009 and 2010. Temperature data in 2011 and 2012 were not monitored successfully due to instrument failure. Soil volumetric moisture 10 cm soil depth was measured with a hand-held probe (IMKO, Germany). Soil moisture within the OTCs on average was decreased by 3.5% (absolute difference) and 4.4% over the experimental period in the natural forest and plantation, respectively (Fig. 1). 2.4. Soil sampling and analysis Soil samples were collected from the topsoil (0–15 cm) in late autumn (October) 2010, 2011 and 2012. Five cores were randomly taken at each plot. The five soil cores from each plot were mixed to get one composite sample and delivered immediately to the laboratory for routine biological analysis. Extractable inorganic N (ammonium and nitrate) was extracted with a 2 M KCl extracting water solution. Ammonium and nitrate in extract were measured by colorimetry. Soil microbial biomass C was determined using the fumigation–extraction method (Vance et al., 1987). Soil extractable organic C in the K2SO4 extracts before and after the fumigation was quantified using a total C/N analyzer (Multi N/C 2100, Analytik Jena AG, Germany). The released C was converted to MBC using Kec−0.45 (Vance et al., 1987). 2.5. Data analyses Repeated-measures analysis of variance (ANOVA) was used to examine the effects of OTC treatment, litter type and time. Two-way ANOVA was used to test the effects of OTC treatment and litter type on decay constant (k value) in each site. Two-way ANOVA was also used to test the effects of forest type and OTC treatment on soil extractable N and microbial biomass C. After the verification of the general ANOVA hypothesis, detailed comparisons between the values were performed with Tukey's HSD post-hoc tests. The difference in initial chemical properties between litter types was determined using a paired t-test. All statistical tests were performed using the Software Statistical Package for the Social Sciences (SPSS) version 17.0. Decomposition rates were calculated from dry mass remaining using a single negative exponential decay model y = e−kt, where y is the fraction of mass remaining at time t, t is the time elapsed in years and k is the annual decay constant (Olson, 1963). We used the nonlinear regression to estimate k value based on untransformed data. 60 Natural forest-control

Natural forest-OTC

Plantation-control

Plantation-OTC

OTC : P <0.05; date : P <0.001 Soil moisture(%)

224

40

a a ab b

To quantify the environmental factors affected by the OTC, two automatic recording systems were set up in both experimental sites,

b

a ab

b

a a

a a b

b

c

a b

20

0 2010/April

2.3. Microclimate monitoring

a

b b

a b

a

a

2010/October

2011/April

2011/October 2012/October

2013/April

Fig. 1. Soil moisture in the OTCs and control plots during the experimental period. Values are means ± SD. Significant effects from repeated-measures ANOVA are shown in italicized text. Values on the same collection date with different letters are significantly different at P b 0.05. n = 4.

Z. Xu et al. / Geoderma 239–240 (2015) 223–228

225

3. Results 3.1. Initial litter chemistry

3.3. Mass remaining The dragon spruce needles had a loss of 38.7–46.9% of their initial mass during the experimental period (Fig. 3). By the end of decomposition, red birch had lost 47.9–58.2% of their initial mass (Fig. 3). Irrespective of the treatments, red birch, on average, decayed 8.8% (absolute difference) more rapidly than dragon spruce during the experimental period (Fig. 3). Regardless of warming regimes, both red birch and dragon spruce decomposition rates incubated in the natural forest site were 4.0% and 2.5% greater than those buried in the plantation site, respectively (Fig. 3). Both litter types showed differential responses to the experimental warming (Fig. 3). Dragon spruce litter decomposed at the similar rate in the OTC and control plots on the first 3 sampling dates (Fig. 3). After this period, dragon spruce needle decay rates were increased by OTC manipulations in both sites (Fig. 3). In contrast, positive effects of warming on litter decay rates of red birch occurred at the earlier period of the experiment. In addition, OTC warming, on average, increased the decay rates of red birch by 2.6% and 3.8% in the plantation and natural forest sites over the experimental period, respectively (Fig. 3). The patterns of litter decomposition over the experimental duration were well described by the exponential model, xt/x0 = e−kt. Statistical analysis showed that warming (F = 11.492; P b 0.01) and litter type (F = 111.496; P b 0.001) alone had significant effect on the values of decay constant (k) (Fig. 4). The values of decay constant, k, of red birch were significantly higher than those of dragon spruce in any treatment. Irrespective of litter types, the k values in the natural forest site was greater than those of the plantation site (F = 22.325; P = 0.089, Fig. 4).

Table 1 Initial leaf litter chemistry of dragon spruce and red birch from the subalpine forests of eastern Tibetan Plateau, China.

(g/kg)

Plantation-OTC

N

P

(g/kg)

(g/kg)

C/N

C/P

8.1 ± 0.9a 1.3 ± 0.1a 60.3 ± 3.2a 375.6 ± 18.2a 488.3 ± 5.4a 472.4 ± 3.8b 14.2 ± 1.1b 2.2 ± 0.2b 33.3 ± 1.8b 214.7 ± 16.5b

Values are means ± SD; n = 3; values within the same column with different letters are significantly different at P b 0.05.

-1

Extractable inorganic N (mg kg )

(a)

OTC : P <0.01; date : P <0.05 site : P <0.001; OTC ×site : P <0.01

60

a

a

a

40 b

b

b

20

c c

d

c

c

b

0 2010/October

2011/October

2012/October

900

(b)

site : P <0.01; date : P <0.05

-1

Warming increased extractable inorganic N (nitrate plus ammonium) in both sites and warming effect was stronger in the natural forest as compared to plantation (F = 46.657; P b 0.001; Fig. 2 a). Regardless of warming regimes, extractable inorganic N was significantly higher in the natural forest than in the plantation (F = 104.185; P b 0.001; Fig. 2a). Conversely, soil microbial biomass C often was not sensitive to warming (F = 5.737; P N 0.05; Fig. 2b). However, in the control plots, microbial biomass C was higher in the natural forest than in the plantation (F = 24.779; P b 0.001; Fig. 2b).

Microbial biomass C(mg kg )

3.2. Soil inorganic N and microbial biomass C

Spruce Birch

Natural forest-OTC

Plantation-control 80

Total C contents in the initial litters were significantly higher in the dragon spruce litter than the red birch letter (P b 0.05; t-test; Table 1). Initial N and P concentrations were lower in the dragon spruce needle relative to those of the red birch litter (all P b 0.01; t-test; Table 1). Conversely, C/N and C/P ratios were significantly higher in the dragon spruce litter versus the red birch litter (all P b 0.01; t-test; Table 1).

Litter type C

Natural forest-control

600

a a a

b b b

c c

a a

ab b

300

0 2010/October

2011/October

2012/October

Fig. 2. Extractable inorganic N and microbial biomass C in the OTCs and control plots during the experimental period. Values are means ± SD. Significant effects from repeatedmeasures ANOVA are shown in italicized text. Values on the same collection date with different letters are significantly different at P b 0.05. n = 4.

4. Discussion For a given ecosystem, litter quality is considered as the most important factor influencing decomposition rate (Aerts and De Caluwe, 1997). Recently, a review has revealed that even at the global scale, litter quality is the most important direct regulator of litter decomposition (Zhang et al., 2008). High quality litters are often characterized by higher N concentrations and lower C:N and lignin:N ratios, and can decompose faster in comparison with low quality litters (Sanchez, 2001). In the present case, dragon spruce (coniferous and evergreen) and red birch (broadleaf and deciduous), two dominant plant species with contrasting life forms and tissue chemistry, were chosen in this experiment. In line with our expectations, the leaf litters of red birch had higher N concentration and lower C:N, C:P and lignin:N ratios relative to dragon spruce needle. As a consequence, red birch leaf litter decayed faster than dragon spruce litter. Regardless of warming regimes and sites, the values of decay constant, k, of red birch were significantly higher than those of dragon spruce. These tendencies are similar to those observed in previous studies of the decomposability of plants in this region (Deng et al., 2009; Xu et al., 2012). The significant differences in the rate of litter decomposition between litter types can, therefore, mainly attribute to differences in litter quality. Additionally, red birch has a more fragile structure, while dragon spruce is more fibrous. The physically resistant cuticular boundary of the needles may be more difficult for microbes to break down. A recent study has found that red birch litter is more palatable to soil fauna compared to needle litter in this region (Liu et al., 2013). Lastly, specific leaf area of red birch is much greater than that of dragon spruce (Yin et al., 2008a, 2008b). Obviously, red birch was

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Z. Xu et al. / Geoderma 239–240 (2015) 223–228

Mass remaining(%)

100

OTC-Spruce OTC-Birch

(a)

Plantation site a a ab b

80

OTC : P <0.01 litter type : P <0.001 date : P <0.001 a OTC×litter type: P <0.05

a a b

a b

b 60

a

c

b

a

c c

b b

a b c c

c

Control-Spruce

OTC-Spruce

Control-Birch

OTC-Birch

100

Mass remaining(%)

Control-Spruce Control-Birch

40

(b)

Natural foerst site a a ab b

80

a a a a

b b

OTC : P <0.01 litter type : P <0.001 date : P <0.001 OTC×litter type: P <0.05

a

b

60

c

b

a

c

b

d

c c

a a b b

40 0

12

24

36

48

0

12

Months

24

36

48

Months

Fig. 3. Effects of OTC warming on litter decomposition of dragon spruce and red birch in two contrasting forest soils of the eastern Tibetan Plateau. Values are means ± SD. Significant effects from repeated-measures ANOVA are shown in italicized text. Values on the same collection date with different letters are significantly different at P b 0.05. n = 6.

more accessible to microbes and soil fauna compared to dragon spruce. Similarly, leaching of soluble compounds from red birch litter may be more probable during the early mass loss relative to dragon spruce needle. Soil condition is one of the most important factors regulating the litter composition. Reforestation induced significant changes on soil physical and biochemical properties in this region (Liu et al., 2002). In the present study, regardless of warming regimes, both red birch and dragon spruce decomposition rates incubated in the natural forest site were significantly greater than those buried in plantation site, respectively. This is different from the results observed in the two contrasting forests (plantation and secondary) in wet tropics in Puerto Rico (Li et al., 2005). Microbes play critical roles in litter decomposition in forest ecosystems. Slight changes in the microbial biomass or community structure may affect the carbon degradation (Saffigna et al., 1989). Therefore, the differences in soil microbial properties could partly be responsible for litter mass loss differences in two forest sites. During the experimental

period, the comparatively low microbial biomass C was observed in the plantation, which reflected poor microbial growth. In addition, soil nutrients, especially nitrogen availabilities, generally have profound impacts on litter decomposition (Melillo et al., 1982). Higher soil inorganic nitrogen content is favorable for litter decomposition (Liu et al., 2006). Our study has indicated that soil extractable inorganic N was higher in the natural forest than in the plantation over the experimental stage. Thus, mass loss differences in both sites may be partly attributed to the differences in soil nitrogen availabilities. Litter decomposition is a complex ecological process that is strongly influenced by environmental factors (Aerts, 1997, 2006; Zhang et al., 2008). Temperature is a key factor that governs litter decomposition (Ruark, 1993; Aerts, 1997). Several techniques (e.g., open-top chambers, heating cables and infrared heaters) have already been used to manipulate temperature experimentally (Aerts, 2006; Luo et al., 2009; Su et al., 2010). At present, warming effects on litter decomposition have widely been reported in various terrestrial ecosystems (Aerts,

(b) 0.4

(a) 0.4

0.2

Natural forest site a

b

c

d

0.3 -1

OTC : p <0.05 litter type : p <0.001

k value (y )

0.3

-1

k value (y )

Plantation site

0.2 0.1

0.0

0.0 OTC

Spruce

control

OTC

Birch

OTC : p <0.01 b litter type : p <0.001

c

0.1

control

a

d

control

OTC

Spruce

control

OTC

Birch

Fig. 4. Decay constant (K, y−1, r2 range 0.86–0.95, P b 0.05) for litters of red birch and dragon spruce as affected by experimental warming in the plantation and natural forest sites on the eastern Tibetan Plateau, China. Values are means ± SD. Significant effects from ANOVA are shown in italicized text. Values with different letters are significantly different at P b 0.05. n = 6.

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2006). However, no consistent patterns have been observed. For example, artificial warming increased litter mass loss in arctic dwarf shrub, subalpine meadow and boreal forest (Robinson et al., 1995; Rustad and Fernandez, 1998; Verburg et al., 1999; Luo et al., 2009) but did not affect the decomposition rates of plant litters in a forest-tundra ecotone (Sjögersten and Wookey, 2004). On the other hand, Aerts (2006) found that warming effects on litter mass loss were dependent strongly on the method used. OTC often declined mass losses (Sjögersten and Wookey, 2004), whereas heating cables generally increased mass loss (e.g., Robinson et al., 1995; Verburg et al., 1999). OTC-caused soil drying could, to some extent, explain this decline in decay rates. However, in the present case, OTC warming increased mass loss rates of the two litter types in both sites. Our previous study has also found that OTC's manipulation reduced soil moisture in both sites on the all sampling dates. However, the warming-caused decline in soil moisture might be less important in influencing soil microbial activities and nutrient availabilities because soil moisture in the OTCs still remained at a relatively high level due to frequent rainfall. Additionally, litter bags were deployed in the center of the OTCs, which may minimize the edge effects (e.g., precipitation). Therefore, OTC-induced soil drying mechanisms are not considered to be relevant at our experimental site. Litter quality may, to some degree, determine the sensitivity of litter decomposition to global warming (Aerts, 2006). Thus, responses of litter decay could depend strongly on the initial conditions of litters. In this study, the two litter types represented differential responses to the OTC manipulations over time. In this study, warming did not affect the early decomposition of dragon spruce, but increased it over the later stage. In contrast, warming stimulated the decay rates of red birch litter on the most of sampling dates. The initial quality could partly explain this response differences. Conifer needles generally have more recalcitrant C components as compared to broadleaf leaves (Shirato and Yokozawa, 2006). Warming-increased microbial activity may easily result in greater decomposition in red birch litter. Moreover, physically resistant cuticular boundary of the needles may need more time for microbes to break down (Rustad and Fernandez, 1998). On the other hand, irrespective of litter types, warming appeared to result in greater mass loss in the natural forest site versus in the plantation site. This was possibly because warming had greater positive effects on soil nitrogen availabilities and microbial biomass. Red birch and dragon spruce forests are two dominant forest types. In the current case, warming can stimulate the litter decomposition of dragon spruce and red birch during the long-term period. Litter decomposition rates may change owing to direct effects of climate change on microbial activity and/or to indirect effects on microbial activity through changing litter quality (Cornelissen et al., 2007). Our study clearly suggested that inter-specific differences in litter quality and decomposability (red birch and dragon spruce) were substantially larger than warming induced responses. Additionally, litter mass loss and the warming response of red birch were larger relative to those of dragon spruce litter. Obviously, reforestation (from birch to dragon spruce or from mixed forest (birch + spruce and/or fir) to spruce) dramatically altered the litter quality of local forest ecosystems, and further affected the responses of litter decomposition to projected global warming. On the other hand, warming increased soil respiration in both sites and the response was stronger in the natural forest compared to the plantation (Xu et al., 2010). Litter composition is one of the important components of soil respiration. Therefore, similar response in soil respiration partly supports the results in litter response in both sites. If this is true, reforestation would decrease the amount of C released to the atmosphere from forest ecosystems in this area. Acknowledgments We thank the staff in the Forestry Bureau of Western Sichuan for their kind help in field investigations. This study was supported by the

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National Natural Science Foundation of China (31200474, 31100446, 31100446), the National Key Technologies R & D in China (2011BAC09B05), the Postdoctoral Science Foundation of China (2013M540714, 2014T70880), and the Scientific Research Fund of Sichuan Provincial Education Department (12ZA105).

References Aerts, R., 1997. Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79, 439–449. Aerts, R., De Caluwe, H., 1997. Nutritional and plant-mediated controls on leaf litter decomposition of Carex species. Ecol. 78, 244–260. Aerts, R., 2006. The freezer defrosting: global warming and litter decomposition rates in cold biomes. J. Ecol. 94, 713–724. Chen, H., Zhu, Q., Peng, C., Wu, N., Wang, Y., Fang, X., Gao, Y., Zhu, D., Yang, G., Tian, J., Kang, X., Piao, S., Yang, H., Xiang, W., Luo, Z., Jiang, H., Song, X., Zhang, Y., Yu, G., Zhao, X., Gong, P., Yao, T., Wu, J., 2013. The impacts of climate change and human activities on biogeochemical cycles on the Qinghai-Tibetan Plateau. Global Change Biol. 19, 2940–2955. Cornelissen, J.H.C., Van Bodegom, P.M., Aerts, R., Callaghan, T.V., Van Logtestijn, R.S.P., Alatalo, J., Chapin, F.S., Gerdol, R., Gudmundsson, J., Gwynnjones, D., Hartley, A.E., Hik, D.S., Hofgaard, A., Jónsdóttir, J.S., Karlsson, S., Klein, J.A., Laundra, J., Magnusson, B., Michelsen, A., Molau, U., Onipchenko, V.G., Quested, H.M., Sandvik, S.M., Schmidt, I.K., Shaver, G.R., Solheim, B., Soudzilovskaia, N.A., Stenström, A., Tolvanen, A., Totland, Ø., Wada, N., Welker, J.M., Zhao, X.Q., Team, M.O.L., 2007. Global negative vegetation feedback to climate warming responses of litter decomposition rates in cold biomes. Ecol. Lett. 10, 619–627. Deng, R., Yang, W., Feng, R., Hu, J., Qin, J., Xiong, X., 2009. Mass loss and element release of litter in the subalpine forest over one freeze–thaw season. Acta Ecol. Sin. 29, 5730–5735. Fierer, N., Craine, J.M., McLauchlan, K., Schimel, J.P., 2005. Litter quality and the temperature sensitivity of decomposition. Ecology 86, 320–326. IPCC, 2007. Climate Change 2007: The Physical Science Basis. Contribution of Working group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK/New York, NY, USA. Li, Y.Q., Xu, M., Zou, X.M., Shi, P.J., Zhang, Y.Q., 2005. Comparing soil organic carbon dynamics in plantation and secondary forest in wet tropics in Puerto Rico. Global Change Biol. 11, 239–248. Liu, Q., Wu, Y., Chen, Q., 2002. Ecological Research on Subalpine Coniferous Forest in China. Sichuan University Press, Sichuan. Liu, P., Huang, J.H., Han, X.G., Sun, O., Zhou, Z.Y., 2006. Differential responses of litter decomposition to increased soil nutrients and water between two contrasting grassland plant species of Inner Mongolia, China. Appl. Soil Ecol. 34, 266–275. Liu, R., Li, W., Yang, W., Tan, B., Wang, W., Xu, Z., Wu, F., 2013. Contributions of soil fauna to litter decomposition in alpine/subalpine forests. Chin. J. Appl. Ecol. 24, 3354–3360. Luo, C., Xu, G., Chao, Z., Wang, S., Lin, X., Hu, Y., Zhang, Z., Duan, J., Chang, X., Su, A., Li, Y., Zhao, X., Du, M., Tang, Y., Kimball, B., 2009. Effect of warming and grazing on litter mass loss and temperature sensitivity of litter and dung mass loss on the Tibetan Plateau. Global Change Biol. 6, 1–12. Melillo, J.M., Aber, J.D., Muratore, J.F., 1982. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63, 621–626. Olson, J.S., 1963. Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44, 322–332. Robinson, C.H., Wookey, P.A., Parsons, A.N., Potter, J.A., Lee, J.A., Callaghan, T.V., 1995. Responses of plant litter decomposition and nitrogen mineralization to simulated environmental change in a high arctic polar semi-desert and a subarctic dwarf shrub heath. Oikos 74, 503–512. Ruark, G.A., 1993. Modeling soil temperature effects on in situ decomposition rates for fine roots of loblolly pine. For. Sci. 9, 118–129. Rustad, L.E., Fernandez, I.J., 1998. Soil warming: consequences for foliar litter decay in a spruce-fir forest in Maine, USA. Soil Sci. Soc. Am. J. 62, 1072–1080. Saffigna, P.G., Powlson, D.S., Brookes, P.C., Thomas, G.A., 1989. Influence of sorghum residues and tillage on soil organic matter and soil microbial biomass in an Australian Vertisol. Soil Biol. Biochem. 21, 759–765. Sanchez, F.G., 2001. Loblolly pine needle decomposition and nutrient dynamics as affected by irrigation, fertilization, and substrate quality. For. Ecol. Manag. 152, 85–96. Shirato, Y., Yokozawa, M., 2006. Acid hydrolysis to partition plant material into decomposable and resistant fractions for use in the Rothamsted carbon model. Soil Biol. Biochem. 38, 812–816. Sjögersten, S., Wookey, P.A., 2004. Decomposition of mountain birch leaf litter at the forest-tundra ecotone in the Fennoscandian Mountains in relation to climate and soil conditions. Plant Soil 262, 215–227. Su, A., Lin, Q., Li, Y., Du, M., 2010. Effects of litter quality and climate change along an elevation gradient on litter mass loss in an alpine meadow ecosystem on the Tibetan Plateau. Plant Ecol. 209, 257–268. Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19, 703–707. Verburg, P.S.J., Van Loon, W.K.P., L¨ukewille, A., 1999. The CLIMEX soil-heating experiment: soil response after 2 years of treatment. Biol. Fertil. Soils 28, 271–276. Xu, Z., Wan, C., Xiong, P., Tang, Z., Hu, R., Cao, G., Liu, Q., 2010. Initial responses of soil CO2 efflux and C, N pools to experimental warming in two contrasting forest ecosystems, Eastern Tibetan Plateau, China. Plant Soil 336, 183–195. Xu, Z., Pu, X., Yin, H., Zhao, C., Liu, Q., 2012. Warming effects on the early decomposition of three litter types, Eastern Tibetan Plateau, China. Eur. J. Soil Sci. 63, 360–367.

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Z. Xu et al. / Geoderma 239–240 (2015) 223–228

Yin, H., Liu, Q., Lai, T., 2008a. Warming effects on growth and physiology in the seedlings of the two conifers Picea asperata and Abies faxoniana under two contrasting light conditions. Ecol. Res. 23, 459–469. Yin, H., Lai, T., Cheng, X., Jiang, X., Liu, Q., 2008b. Warming effects on growth and physiology of seedlings of Betula albo-sinensis and Abies faxoniana under two contrasting

light conditions in subalpine coniferous forest of western Sichuan, China. J. Plant Ecol. 32, 1072–1083. Zhang, D.Q., Hui, D.F., Luo, Y.Q., Zhou, G.Y., 2008. Rates of litter decomposition in terrestrial ecosystems: global patterns and controlling factors. J. Plant Ecol. 6, 85–93.