African Journal of Microbiology Research Vol. 6(31), pp. 6091-6098, 16 August, 2012 Available online at http://www.academicjournals.org/AJMR DOI: 10.5897/AJMR12.688 ISSN 1996-0808 ©2012 Academic Journals

Full Length Research Paper

Soil carbon, nitrogen and microbial biomass dynamics of subalpine Abies fabri forest in Gongga Mountain, Southwest China

Feipeng Xiao1,2* and Weijun Huang2

1College of Civil Engineering and Architecture, Guangxi University, Nanning 530004, China. 2Guangxi Hydraulic and Electric Polytechnic, Nanning 530023, China.

Accepted 28 May, 2012

+ - Soil organic carbon (SOC), soil microbial biomass C, soil total nitrogen (N), NH4 -N and NO3 -N dynamics were measured in subalpine Abies fabri forest at different growth phases which include the mature forest (MF, 3100 m a.s.l.), the middle age forest (MAF, 2998 m a.s.l.) and the succession forest of mixed Abies fabri and Populus purdomii Rehd (SF, 2947 m a.s.l.) of Gongga Mountain, Southwest China. SOC concentrations decreased significantly with increasing depth and at a given depth (0-10 cm, 10-20 cm, 20-40 cm, 40-60 cm and 60-100 cm), SOC was greater in MF than that in MAF and SF. The average SOC concentration in MF (50.99 g kg-1) was almost six times than that in MAF (7.97 g kg-1) and SF (6.25 g kg-1). Soil microbial biomass C fluctuated in time and was higher in August than that in June + - + - and October under all A. fabri forests. Soil NH4 -N, NO3 -N and soil available N (NH4 -N + NO3 -N) were higher in MF than those in MAF and in SF. The average soil available N concentrations were 21.61, 12.57 and 10.91 mg kg-1 under MF, MAF and SF, respectively.

Key words: Soil organic carbon, soil nitrogen, Abies fabri forest, Gongga Mountain.

INTRODUCTION

Soil carbon (C) pool containing about 1500-2000 Pg C, Soil organic carbon (SOC) is well known to maintain has been considered as the largest pool of C in terrestrial several functions. Being the major component of soil ecosystems and plays an important role in the global organic matter (SOM), it is a determinant of soil physical carbon cycle (Li et al., 2005; Rasmussen et al., 2006). and chemical properties, an important proxy for soil Forests are the most extensively distributed vegetation- biological activity and a measure of soil productivity type ecosystems in the world and cover approximately (Batjes and Sombroek, 1997; Rossi et al., 2009). SOC one-third of the earth land surface (Li et al., 2000). plays an important role in climate change processes by Approximately 40% of the global soil C inventory resides acting either as source or sink of atmospheric CO2 in forest ecosystems and a relatively small change in (Jiménez et al., 2008). Microorganisms have a funda- forest soil C inventories could have important implications mental role in the biogeochemical cycles of the elements for the global C budget (Carten et al., 1999; Diochon et and in the formation of soil structure, it is widely accepted al., 2009). Therefore, the study of soil carbon dynamics is that a high level of microbial size and activity is critically important to our ability to understand the carbon necessary for the maintenance of an adequate quality of balance in forest ecosystems and their responses to soil (Bastida et al., 2007; Anderson et al., 2008; Feng et future global climate change (Davidson et al., 2000). al., 2009). Microbial C, especially the microbial C-to-SOC ratio, can reveal the status of microorganisms in the C availability of forest soils and is considered to be a quantitative indicator for carbon dynamics in soils (Xu et *Corresponding author. E-mail: [email protected]. al., 2006, 2007). Nitrogen (N) is generally considered the 6092 Afr. J. Microbiol. Res.

single element most likely to be limiting to forest pro- Neotectonic movement leads to the prominent vertical zonation of duction (Knoepp and Swank, 2002; Schimel and Bennett, vegetation with forest types ranging from valley subtropical 2004), and affects biogeochemical cycles of other vegetation to alpine cold vegetation gradient (Wang et al., 2004; Lu et al., 2008). Rich species resources with strong primary ecological elements mainly through the process of litter decom- environment and well preserved original conditions provides ideal position (Wang et al., 2007). Therefore N is important in sites for scientific research of background regimes of forest regulating ecosystem process (Vitousek et al., 1997). Soil ecosystem C, N pools and cycles and their comparative studies is the primary and most immediate N pool for plants and under different anthropogenic disturbances. The Gongga Mountain microbes in forested ecosystems (Wang et al., 2007). Region is located in the transitional region from the subtropical monsoon climate zone to frigid climate zone of the Qinghai-Tibet Although there are typically large quantities of N in soil Plateau. This region to be characterized by high precipitation, ecosystems, most is bond in organic forms unavailable to cloudy days, cold winters and cool summers due to the impacts of plants. Only small quantities of N are in accessible east-southern monsoon from the Pacific (Dong et al., 2003; Shan et + mineral forms, such as ammonium (NH4 ) and nitrate al., 2004). - + - The subalpine A. fabri forest in this study was at 2900-3100 m (NO3 ) (Bonito et al., 2003). NH4 -N and NO3 -N are the main forms which microorganisms and plants uptake N altitude in the Hailuogou valley which located on the east slope of Gongga Mountain. Alpine ecosystem observation and experiment from soil. The mechanism and rate of soil organic N station of Gongga Mountain (3000 m observation plot) which mineralization which the amount of N released through belongs to the Chinese Ecosystem Research Network (CERN) is the decomposition of organic matter during a certain located in this area. Based on meteorological data collected by the period of time has important influence on the availability station, the annual mean air temperature is 3.8°C, the lowest mean + - air temperature occurred in January (–4.5°C), and the highest mean of NH4 and NO3 to microorganisms and plants in forests (Diekmann and Falkengren-Grerup, 1998; Vestgarden air temperature occurred in July (12.7°C). The average annual + precipitation is 1949 mm, 70% of which occurs from June to and Kjønaas, 2003). NH4 derived from organic matter - October, and annual potential evaporation averages 264 mm mineralization is being transformed into NO3 through the (Cheng and Luo, 2003; Shan et al., 2004; Lu et al., 2008; He and + nitrification process (Gallardo et al., 2006). NH4 -N and Tang, 2008). The virgin forest succession gradient is very good - NO3 N content variations with different season because of here, having the A. fabri forest, the main body of the frigid- temperature, moisture and other ecological factors have temperate-zone subalpine dark coniferous forest of the east slope of Gongga Mountain, including the mature forest of the climax been found in many forests (Pinay et al., 1995; Smith et succession phase (MF), the middle age forest of the middle al., 1998; Laverman et al., 2000; Pérez et al., 2004; succession phase (MAF) and the succession forest of mixed A. García-Oliva et al., 2006). fabri and Populus purdomii Rehd (SF). The soil is the typical As one of the most important species of subalpine dark mountain dark brown soil in A. fabri forest, which has a high sand coniferous forest, Abies fabri grows in the southwestern content (> 65%) and strong permeability. mountains of China, especially in the Gongga Mountains at elevations between 2800–3400 m. There are a few Soil samples studies of soil C, N cycles in subalpine dark coniferous forest of Gongga Mountain (Cheng and Luo, 2003; Dong Soil samples were collected from three types A. fabri, including the et al., 2003; Wang et al., 2004, 2005; Lu and Cheng, mature forest (MF, 3100 m a.s.l.), the middle age forest (MAF, 2998 2009) that provides an understanding of how natural and m a.s.l.) and the succession forest of mixed A. fabri and Populus human-related disturbances may affect the size and rate purdomii Rehd (SF, 2947 m a.s.l.). Six plots were established in each forest stand, provides six replications. Soil sampling was of change in soil C, N pools, and consequences for the conducted by depth with separation into five soil horizons (0-10 cm, structure, composition and functioning of the forest soil. 10-20 cm, 20-40 cm, 40-60 cm and 60-100 cm) to analyzed soil But there are no reports of soil C, N dynamics related to physical and chemical property differences in September 2005. Soil different A. fabri forest types. The aim of this study was to samples for microbial biomass C in each forest stands were collected three times in June, August and October 2005 with the determine the SOC, soil microbial biomass C, soil total N, + - NH +-N and NO -N dynamics of the subalpine A. fabri depth of 0-20 cm. And soil samples for soil NH4 -N and NO3 -N 4 3 were collected four times in April, June, August and October 2005 forest located in the Gongga Mountain, which will with the same depth (0-20 cm). Samples were randomly taken at 6- improve our understanding about the dynamics of forest 8 points of each plot and later pooled to one sample per plot. Soil soil C, N so as to provide a scientific basis for the samples were kept in cool boxes to the laboratory and analyzed research of the response mechanism of the soils to the immediately. climate change.

Laboratory analyses

MATERIALS AND METHODS Soil physical and chemical properties were determined as per the regular analysis methods (Liu, 1996). Soil bulk densities (g cm-3) Study area calculations were based on volume of bulked soil cores and oven dried mass determinations. Soil particle-size fractions were Gongga Mountain is situated on the Quaternary sections of the determined by the pipette method following H2O2 treatment to eastern Tibetan Plateau with the longitude 29° 20′~30° 20′ and the destroy organic matter and subsequent dispersion of soil latitude 101° 30′~102° 15′, and is the highest mountain in Sichuan suspensions by Na-hexametaphosphate. SOC was determined province with the summit of 7556 m above sea level. The great using wet oxidation with K2Cr2O7. Total nitrogen analysis followed height difference (1100 - 7556 m) derived from the Quaternary the micro-Kjeldahl digestion method. The determination of total P Xiao and Huang 6093

Table 1. Soil physical and chemical properties of Abies fabri forest in Gongga Mountain.

Depth (cm) BD1 (g·cm-3) Sand (%) Silt (%) Clay (%) N total (g·kg-1) P total (g·kg-1) K total (g·kg-1) The mature Abies fabri forest (MF) 0-10 65.61b 27.50a 6.89a 4.71a 1.08a 18.67a 0.632b 10-20 69.36b 25.41ab 5.23ab 3.32b 1.15a 18.96a 20-40 0.83ab 78.31a 17.83bc 3.86bc 2.23c 1.30a 19.30a 40-60 0.95ab 81.22a 15.50c 3.28bc 1.81cd 1.19a 21.21a 60-100 1.00a 82.10a 15.50c 2.40c 1.32d 1.15a 21.43a

The middle age Abies fabri forest (MAF) 0-10 76.56b 20.47a 2.97a 0.89a 0.96b 32.20b 1.362b 10-20 77.81ab 19.45ab 2.74a 0.35b 1.04a 32.91b 20-40 1.53a 78.47ab 18.56ab 2.97a 0.22b 1.08a 33.95ab 40-60 1.55a 79.16ab 18.21ab 2.63ab 0.19b 1.08a 34.82ab 60-100 1.53a 81.92a 15.92b 2.16b 0.17b 1.10a 36.19a

The succession forest of mixed Abies fabri and Populus purdomii Rehd (SF) 0-10 79.59a 17.47a 2.94a 0.92a 1.02a 27.42a 1.282b 10-20 79.87a 17.52a 2.61a 0.31b 1.02a 28.59a 20-40 1.49a 81.01a 16.77a 2.22a 0.20bc 1.06a 29.21a 40-60 1.50a 78.70a 18.28a 3.02a 0.18bc 1.04a 29.39a 60-100 1.60a 77.83a 19.34a 2.83a 0.15c 1.04a 30.83a

1 BD: Bulk Density; 2 BD of soil layer 0-20 cm, mean values followed by different letters are different from each other at P < 0.05.

as carried out using the NaOH digestion method and the density, soil texture, total N, total P and total K determination of total K as carried out using the HF-HClO4 digestion concentrations (Table 1). At a given depth soil bulk method. density was greater in MF than that in MAF and SF, and Microbial biomass C was determined according to the CHCl3 fumigation–extraction method in field-moist samples (Vance et al., soil bulk density increased significantly with increasing 1987). Fumigated and nonfumigated samples were incubated depth. The soils under MF had lower sand contents during 24 h at 25°C at constant moisture content. Microbial C was (75.32%) than soils under MAF (79.40%) and SF extracted from both fumigated and nonfumigated samples with 0.5 (78.79%), but higher clay contents (4.33%) than under M K2SO4. C was measured using the automated CO2 analyzer. MAF (2.73%) and SF (2.69%). There were significant Microbial biomass C was calculated by subtracting the extracted C in unfumigated samples from that measured in fumigated samples differences for sand, silt and clay contents among the and dividing it by a Kc value of 0.45 (Joergensen, 1996). Inorganic different depths in MF and MAF (Table 1). The sand + - N as NH4 and NO3 was extracted from a 5 g fresh soil sample by content of soils under MF and MAF increased shaking for 30 min with 50 ml of 2 M KCl. The extracts were filtered significantly with increasing depth and the silt and clay and nitrate and ammonium were determined calorimetrically by the content of soils decreased significantly with increasing phenol-hypochlorite method. depth, but the soil texture of soils under SF did not

significantly differ among different depths (Table 1). Soil Statistical analysis total N concentrations ranged from 4.71 to 1.32 g kg-1 in MF, from 0.89 to 0.17 g kg-1 in MAF and from 0.91 to 0.15 Statistical analyses were carried out by using the statistical g kg-1 in SF with the depth of soils from 0-10 cm to 60- package SPSS 11.5. Analysis of Variance (ANOVA) was used to test the statistical significance of trends in SOC data. Significantly 100 cm and total N concentrations significantly different averages were separated with standard error of means to decreased with depth under all the forests. Soil total P evaluate least significant difference (LSD). All test were evaluated concentrations were not significant difference among + at p<0.05. Additionally, soil microbial biomass C, soil NH4 -N and different forests and different depths. At a given depth - NO3 -N were analyzed using generalized linear mixed models soil total K concentrations were lower in MF than that in (GLMM). MAF and SF (Table 1).

RESULTS SOC and microbial biomass C Soil physical and chemical properties SOC of Surface soil (0-10 cm) concentrations were 80.92 There were clear effects of A. fabri forest type on soil bulk g kg-1 under MF, 15.56 g kg-1 under MAF and 15.67 g kg-1 6094 Afr. J. Microbiol. Res.

1 2 3

Figure 1. SOC at 0-100 cm depth of Abies fabri forest in Gongga Mountain: (1) MF, (2) MAF, (3) SF.

under SF and SOC concentrations decreased signifi- August and October under MAF and SF than those in + - cantly with increasing depth (Figure 1). SOC con- April and June. Under MF soil NH4 -N / NO3 -N ratio centrations declined to 27.49, 5.25 and 5.34 g kg-1 in the appeared in April (Table 2). 60-100 cm layer under MF, MAF and SF respectively. At a given depth SOC was greater in MF than that in MAF and SF and the average SOC concentration in MF (50.99 DISCUSSION g kg-1) was almost six times than that in MAF (7.97 g kg-1) and SF (6.25 g kg-1). Soil microbial biomass C was much Soil C, N dynamics higher under MF than that under MAF and SF. For example, soil microbial biomass C in MF was about 3 Soil samples for the present study were taken from times in comparison with that in MAF and about 2 times different type subalpine A. fabri forests located in the in comparison with that in SF (Figure 2). Microbial Gongga Mountain. The results showed that SOC concen- biomass C fluctuated in time, with a considerable trations decreased significantly with increasing depth in variation in concentrations among different months (Table all A. fabri forests (Figure 1). The SOC decreased with 2). Soil microbial biomass C was higher in August than increasing depth reported by many studies, such as that in June and October under all A. fabri forests. forests along an elevation gradient in the southern Appalachian Mountains (Carten et al., 1999), old-growth montane coniferous forest in Isla Chiloé (Zarin et al., + - Soil NH4 -N and NO3 -N 1998), six common European tree specie forest at six sites in Denmark (Vesterdal et al., 2008) and so on. Soil + - Soil NH4 -N and NO3 -N concentrations in the different microbial biomass constitutes a transformation matrix for A. fabri forest types in time are presented in Figure 3. In all the natural organic materials in the soil and acts as a + - + general, soil NH4 -N, NO3 -N and soil available N (NH4 - labile reservoir for plant-available nutrients, especially N, - N + NO3 -N) were higher in MF than those in MAF and in P and S (Srivastava and Singh, 1989). Because micro- + SF. Soil NH4 -N concentrations in three forest types organisms affect soil fertility and hence the functioning of were higher in April and June and were lower in August ecosystems, measurement of soil microbial biomass has - and in October. Soil NO3 -N concentrations kept the attracted considerable attention in recent years + same variation trends as the soil NH4 -N concentrations. (Hopmans et al., 2005; Goberna et al., 2006; Bastida et Soil available N concentration was defined as the sum of al., 2007). Zhong and Makeschin (2006) reported that in + - soil NH4 -N concentration and soil NO3 -N concentration. central Germany under beech stand soil microbial The average soil available N concentrations were 21.61, biomass C was 2 to 5 times higher in November samples 12.57 and 10.91 mg kg-1 under MF, MAF and SF than in August and April. In this study, the result shows respectively. Soil available N also showed higher that soil microbial biomass C was higher in August than concentrations in April and in June and lower in August that in June and October under all A. fabri forests. The + and October. The highest ratio (2.83) of soil NH4 -N to size and activity of the soil microbial biomass is regulated - NO3 -N appeared in October under MAF and the lowest mainly by the availability of organic C, climatic conditions, + - value (0.69) of soil NH4 -N / NO3 -N ratio appeared in and other factors such as soil nutrient status. + - + - June under MF. Soil NH4 -N / NO3 -N ratio was higher in NH4 -N and NO3 -N are the accessible mineral forms Xiao and Huang 6095

1 0.9 ) MF -1 0.8 MAF 0.7 SF 0.6 0.5 0.4 0.3 0.2 Microbial biomass carbon (g kg (g carbon biomass Microbial 0.1 0 June August October Month

Figure 2. Microbial biomass C dynamics of Abies fabri forest in Gongga Mountain.

+ - Table 2. Summary GLMM statistics for seasonal patterns in soil microbial biomass C, soil NH4 -N and NO3 -N at three contrasting Abies fabri forests.

Type Date Type × Date Index d.f. F P d.f. F P d.f. F P - NO3 -N 2 37.94 <0.001 3 55.44 <0.001 6 2.12 0.064 + NH4 -N 2 46.29 <0.001 3 61.39 <0.001 6 27.96 <0.001 + - NH4 -N + NO3 -N 2 61.25 <0.001 3 85.46 <0.001 6 13.16 <0.001 + - NH4 -N / NO3 -N 2 7.38 0.001 3 8.64 <0.001 6 5.53 <0.001 Microbial biomass carbon 2 18.60 <0.001 2 3.30 0.046 4 1.22 0.317

Data given are degree of freedom (d.f.) and F and P-values for main and interactive effects. Significant levels in boldfaces.

+ - which microorganisms and plants uptake N from soil. The and October. Soil NH4 -N / NO3 -N ratio was higher in + - availability of NH4 -N and NO3 -N is believed to limit forest August and October under MAF and SF than those in + - production because many forests show growth response April and June and under MF soil higher NH4 -N / NO3 - to improve mineral N fertilizers (Pastor et al., 1984; N ratio appeared in April. During the growing season + - Bonito et al., 2003). Soil NH4 -N and NO3 N showed plant growth is stimulated by rising soil temperature and clearly seasonal variations in many forests. For example, increasing fluxes of photosynthetically active radiation; in two typical riparian forests along the River Garonne, this increases the demand for inorganic N. The period of + southwest France soil NH4 -N concentration increased maximum plant uptake was preceded by peaks in the similarly after the flood events and in late summer in both rates of soil microbial production of inorganic N, and - sites and soil NO3 -N increased sharply in summer (Pinay variations in seasonal patterns of N transformation et al., 1995). In southern Chilean forest ecosystems soil matched the variation in plant growth. + - available N (NH4 -N + NO3 -N) showed marked seasonality in these lowland rainforests, with a higher internal N flux during the winter months, and found that Comparisons among different type Abies fabri soil available N in upper and deep soil horizons positively forests correlated with monthly precipitation (Pérez et al., 2004). In subalpine A. fabri forests of Gongga Mountain soil The A. fabri forest in the eastern slope of Gongga + - NH4 -N and NO3 -N concentrations in three forest types Mountain is one type of subalpine dark coniferous forests were higher in April and June and were lower in August of southwestern China. According to field investigation 6096 Afr. J. Microbiol. Res.

25 18

20 MF 16 MF

) MAF 14 -1

) MAF 15 SF -1 12 SF

10

-N (mg kg -N(mg +

4 10

-N (mg kg -N(mg 8

- 3 NH 6 5 NO 4 2 0 April June August October 0 a Month April June August October b Month

45 3 40 2.5 MF ) MF -1 35 MAF

MAF -N 30 - 2 SF SF 3

-N (mg kg -N(mg 25 -

3 1.5

20 NO -N/

+ 4 1

-N+NO 15

NH

+ 4 10 NH 0.5 5 0 0 April June August October April June August October c d Month Month

Figure 3. Soil NH4+ -N and NO3- -N dynamics of Abies fabri forest in Gongga Mountain: (a) NH4+ -N, (b) NO3- -N, c . NH4+ -N + NO3- -N, d. NH4+ -N / NO3- -N.

the oldest age of mature natural A. fabri forest is about appear as MF> SF>MAF, and the CH4 consumption flux 160 years, the average age of middle aged A. fabri forest as MF>MAF>SF. The existence of the above relations is and mixed A. fabri and Populus purdomii Rehd forests related to soil physiochemical properties and differences are 80 and 40 years respectively (Gao and Gao, 2007). of community compositions of various sites. Cheng and The MF community is dominated by A. fabri, its Luo (2003) found that for MF site the soil had complete composition is very complex and its stratification obvious. structure and higher organic content and soil C pool for The species composition of SF is much more the whole layer is 143.1 t ha-1, contributing 82.5% in the complicated than that of the MF and the species upper layer and 27.5% in the lower layer; and for MAF composition of MAF lies between that of the MF and the site the soil C pool was only 30.7 t ha-1. In the present SF. The proportions of A. fabri found in the MF, MAF and study the result shows that SOC and soil microbial SF are 80, 79 and 51%, which shows an decreasing biomass C were greater in MF than those in MAF and trend and this phenomenon agrees with the SF. For example, soil microbial biomass C in MF was characteristics of A. fabri at different evolving phase (Gao about 3 times in comparison with that in MAF and about 2 and Gao, 2007). Dong et al (2003) reported that the flux times in comparison with that in SF. Soil N concentrations + - in relations to soil N2O emission of all the three sites kept the same trends. Soil NH4 -N, NO3 -N and soil Xiao and Huang 6097

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