Sei sulla pagina 1di 8

Journal of

Plant Ecology Soil microbial biomass carbon and

PAGES 175–182 nitrogen in forest ecosystems of

doi: 10.1093/jpe/rtq022 Northeast China: a comparison

between natural secondary forest
Advanced Access published
on 4 August 2010

available online at
and larch plantation
Kai Yang1, Jiaojun Zhu1,*, Min Zhang1,2, Qiaoling Yan1 and

Downloaded from by Osbert Sun on August 19, 2010

Osbert Jianxin Sun3
Qingyuan Experimental Station of Forest Ecology, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang
110016, China
Graduate School, Chinese Academy of Sciences, Beijing 100039, China
MOE Key Laboratory for Silviculture and Conservation, Beijing Forestry University, Beijing 100083, China
*Correspondence address. Institute of Applied Ecology, Chinese Academy of Sciences, 72 Wenhua Road,
Shenyang 110016, China. Tel: 86-24-83970342; Fax: 86-24-83970342. E-mail:


Aims increasing soil depth in the two types of stands. The ratios of MBC to
Natural secondary forest (NSF) and larch plantation are two of the SOC (MBC/SOC) and MBN to TN (MBN/TN) were also significantly
predominant forest types in Northeast China. However, how the lower in the LOP than in the NSF. Moreover, the values of MBC,
two types of forests compare in sustaining soil quality is not well un- MBC/SOC, and MBN/TN significantly varied with time and followed
derstood. This study was conducted to determine how natural sec- a similar pattern during the growing season, all with an apparent
ondary forest and larch plantation would differ in soil microbial peak in summer. Our results indicate that NSF is better in sustaining
biomass and soil organic matter quality. soil microbial biomass and nutrients than larch plantation in the tem-
perate Northeast China. This calls for cautions in large-scale conver-
sions of the native forests to coniferous plantations as a forest
Microbial biomass carbon (MBC), microbial biomass nitrogen (MBN),
management practice on concerns of sustaining soil productivity.
soil organic carbon (SOC) and total nitrogen (TN) in the 0- to 15-cm
and 15- to 30-cm soil layers were investigated by making chemical
Keywords: microbial biomass carbon d microbial biomass
and biological measurements in the montane region of eastern Liaon-
nitrogen d soil quality d temperate forests
ing Province, Northeast China, during the growing season of 2008 in
stands of NSF and Larix olgensis plantation (LOP). Received: 24 March 2010 Revised: 21 June 2010 Accepted: 9 July
Important Findings
We found that soil MBC and MBN were significantly lower in the
LOP than in the NSF. Both MBC and MBN declined significantly with

China, NSFs account for as much as 70% of the regional forests

INTRODUCTION (Hao et al. 2000), of which large areas have been turned into
Natural secondary forests (NSFs) widely occur in temperate larch plantations for fast timber production since the 1950s
regions around the world (Wang and Yang 2007). They are (Wang et al. 2006). However, concerns for biological
formed through natural regeneration following stand-replacing conservation of forest resources and mitigation of climate
disturbances of primary forests by anthropogenic activities or change in the context of global change have created large inter-
by extreme natural events (Zhu and Liu 2007). In Northeast ests in assessing the changes of soil quality and carbon

Ó The Author 2010. Published by Oxford University Press on behalf of the Institute of Botany, Chinese Academy of Sciences and the Botanical Society of China.
All rights reserved. For permissions, please email:
176 Journal of Plant Ecology

sequestration capacity with conversion of natural forests to are studies demonstrating that the maximum values of micro-
plantations and/or other land uses (Chen and Li 2003; Shi bial biomass may occur in summer (Gallardo and Schlesinger
et al. 2009; Wang and Yang 2007; Yang et al. 2007). 1994; Zhong and Makeschin 2006) or spring (Diaz-Raviña et al.
There is a widespread perception that plantations are 1995; Zhu and Carreiro 2004) or show no significant seasonal
generally inferior to naturally regenerated forest stands in nu- variations (Bauhus and Barthel 1995). The variable results
trient cycling and soil quality (Burton et al. 2007; Liu et al. suggest that seasonal variations in soil microbial biomass
1998); while this view is supported by a large body of literature probably depend on the specific forest ecosystems and climatic
(Behera and Sahani 2003; Kasel and Bennett 2007; Yan et al. factors.
2008; Zhang et al. 2009), there also exist contradictory exper- In this study, the concentrations of microbial biomass C and
imental results. For example, the study of Li et al. (2005) shows N, soil organic C, total N and the relationships between soil or-
that there is no significant difference in total soil organic car- ganic matter and microbial biomass in the 0- to 15-cm and 15-
bon (SOC) between a pine plantation (5.59 6 0.09 kg m 2) to 30-cm soil layers were compared between the stands of NSF
and a secondary mixed forest (5.68 6 0.16 kg m 2) in Puerto and LOP in the montane region of eastern Liaoning Province,
Rico. Our previous study also indicates that NSF and Northeast China. The specific objectives of this study were to
Larix olgensis plantation (LOP) differ in chemical composi- determine: (1) how NSFs and larch plantations would differ

Downloaded from by Osbert Sun on August 19, 2010

tion of soil P but not in overall P availability in eastern in soil microbial biomass and soil organic matter quality and
Liaoning Province of Northeast China (Yang et al. 2010), where (2) how soil microbial biomass would vary seasonally for the
L. olgensis is an introduced species and known to have a slow two forest types of forests under temperate climatic conditions.
rate of litter decomposition than the tree species in the natural We hypothesize that the stands of LOP would have markedly
forests (Liu et al. 1998). A conversion from natural forest to lower soil microbial biomass and activity, hence slower nutrient
coniferous plantation is generally found to reduce SOC stock cycling than the NSFs because of the slower rate of litter decom-
(Guo and Gifford 2002) and result in a decline in soil organic position in L. olgensis than in the tree species in the NSFs.
matter quality (Behera and Sahani 2003; He et al. 2006).
Soil microbial biomass, which can be either a source or sink
of available nutrients, plays a critical role in nutrient transfor-
mation in terrestrial ecosystems (Singh et al. 1989). Any
change in the microbial biomass may affect soil organic matter Site description and experimental design
turnover. Thus, the soil microbial activity has a direct influ- The study was conducted at Qingyuan Experimental Station of
ence on ecosystem stability and fertility (Smith et al. 1993). Forest Ecology of Institute of Applied Ecology, Chinese Acad-
In general, microbial biomass can be used for assessing soil emy of Sciences. The station is located in a mountainous region
quality of different types of vegetation (Groffman et al. in the eastern Liaoning Province, Northeast China (lati-
2001; Zeng et al. 2009) as well as for evaluating soil perturba- tude 41°51’N, longitude 124°54’E, elevation 500–1100 m
tion and restoration (Ross et al. 1982; Smith and Paul 1990). above sea level). The climate of the region is a continental
Forest types influence soil microbial biomass and activities monsoon type with a humid and rainy summer and a cold
by determining the quantity and quality of organic matter and snowy winter. Mean annual air temperature varies be-
inputs (Hackl et al. 2004; Xu et al. 2008). Shifts in plant com- tween 3.9 and 5.4°C with the minimum of 37.6°C in January
munity composition may affect SOC dynamics as a result of and the maximum of 36.5°C in July. The mean annual
changes in the amount and chemical composition of plant res- precipitation ranges between 700 and 850 mm, of which
idues returned to the soil (Jin et al. 2010), which in turn influ- 80% rain falls in June, July and August. The frost-free period
ences the pool size and activity of the soil microbial biomass lasts for 130 days on average, with an early frost in October and
(Kasel and Bennett 2007). late frost in April (Zhu et al. 2007). The mean monthly temper-
Besides forest types, seasonal variations of temperature, ature and precipitation during the growing season of 2008 are
rainfall, plant development, and organic matter accumulation shown in Fig. 1. The soil type is a typical brown forest soil with
from litterfall also have great influences on soil microbial bio- a thickness of 60–80 cm. The brown forest soil belongs to
mass (Chen et al. 2005; Devi and Yadava 2006; Maithani et al. Udalfs according to the second edition of US Soil Taxonomy
1996; Tonon et al. 2005). Fluctuations in the size of soil micro- (1999).
bial biomass during the growing season are considered an im- The study site was originally occupied by primary mixed
portant factor in controlling the turnover of soil carbon and broadleaved-Korean pine (Pinus koraiensis Sieb. et Zucc.) for-
nitrogen. Therefore, information on seasonal variations in soil ests until 1930s and subsequently subjected to decades of un-
microbial biomass is needed to improve our understanding on regulated timber removal. A large fire in the early 1950s
soil nutrient transformation and availability. In temperate for- cleared off the entire forests and the site was gradually replaced
ests, however, several studies on the seasonal dynamics of soil by a mixture of naturally regenerating broadleaved native tree
microbial biomass in recent decades have reported inconsis- species. Since 1960s, patches of the secondary natural forests
tent findings (e.g. Bauhus and Barthel 1995; Gallardo and were cleared and replaced by larch (L. olgensis or Larix keampferi
Schlesinger 1994; Zhu and Carreiro 2004). For instance, there [Lamb.] Carr.) plantations (Wang and Yang 2007).
Yang et al. | Soil microbial C and N in temperate forests 177

Precipitation Temperature GmbH, Hanau, Germany). Soil MBC and MBN were deter-
25 300
Mean air temperature ( )
mined by fumigation–extraction method (Brookes et al.

Precipitation (mm) 1
20 250 1985; Vance et al. 1987a). For each plot, three out of six sub-
200 samples (each 10.0 g fresh soil) were fumigated with ethanol-
150 free chloroform for 24 h at 25°C in an evacuated extractor. The
100 remaining samples were treated as control. Fumigated and
5 50 non-fumigated soils were extracted with 40 ml 0.5 mol l 1
K2SO4 (soil:extractant = 1:4) and shaken for 1 h on a reciprocal
0 0
Apr May Jun Jul Aug Sep Oct shaker. The extracts were filtered using Whatman No.42 filter
paper with diameter 7 cm and frozen stored at 15°C prior to
Figure 1: mean monthly air temperature and precipitation in the analysis. The total organic carbon and nitrogen in the extracts
study area in 2008 in eastern Liaoning Province, Northeast China.
were measured using a Multi N/C 3000 analyzer (Elementar
Analysensysteme GmbH). Soil pH was estimated on a 1:2.5
Our sample plots were set up on three stands of NSF and soil–water mixture. Gravimetric soil water content was calcu-
three stands of LOP of the age 16–44 years. The six stands lated from mass loss after drying for 12 h at 105°C sepa-

Downloaded from by Osbert Sun on August 19, 2010

have a similar topographical feature and the underlying soils rately for the 0- to 15 and 15- to 30-cm soil layers. The
are developed from the same parental materials. In each of forest floor litter was determined using six mesh traps (each
the stands, three 20 3 20-m plots were laid out in September an area of 1.0 m2) installed 0.5 m above the soil surface.
2006. The NSF plots consisted of the tree layer, the under- The fine root (<2mm in diameter) biomass was estimated from
story component and the herbage component. The tree layer eight soil cores (each an area of 28.3 cm2) in each plot. (Table 2)
includes Juglans mandshurica Maxim., Quercus mongolica All data are expressed on oven-dry (105°C) soil weight basis.
Fischer ex Ledebour, Acer mono Maxim., Fraxinus rhyncho- MBC was calculated as:
phylla Hance and Ulmus macrocarpa Hance; the understory
MBC = EC =kEC ;
component includes Acer triflorun Kom., Acer tegmentosum
Maxim, Asarum hetelotopoides var. mandshricum Maxim. and where EC = (organic C extracted from fumigated soils)
Syringa amurensis Rupr; and the herbage component includes (organic C extracted from non-fumigated soils) and
Cardamine leucantha (Tausch) OE Schulz, Allium monanthum kEC = 0.45 (Wu et al. 1990).
Maxim., Arisaema amurense Maxim., and Polygonatum involu- MBN was calculated as:
cratum Maxim. The LOP plots contain the shrub layer and the MBN = EN =kEN ;
herbage layer. The shrub layer includes A. tegmentosum, Acer
pseudo-sieboldianum (Pax.) Kom., Schisandra chinensis (Turcz.) where EN = (total N extracted from fumigated soils) (total N
Bail., Syringa wolfi Schneid. and Acanthopanax senticosus (Rupr. extracted from non-fumigated soils) and kEN = 0.54 (Brookes
et Maxim.) Harms., and the herbage layer includes et al. 1985).
C. leucantha, Rubia sylvatica Nakai and Spuriopimpinella brachy-
Statistical analysis
carpa (Kom.) Kitag.
The statistical analyses were conducted with SPSS 11.5.
Soil sampling and chemical analysis A three-way analysis of variance (ANOVA) was used to test
In spring, summer and autumn, mineral soil samples at 0- to the effects of forest type, sampling season, and soil depth on
15-cm and 15- to 30-cm depths were collected on 25 April, 18 soil microbial biomass and soil chemical properties. Pearson’s
July and 19 September 2008, respectively. The experimental correlation analysis was used to determine whether there were
design did not include winter season because of the snow cover significant interrelationships among the measured properties
and frozen soils, which made the winter sampling impractical. of the soils.
Litter layer was removed before mineral soil sampling. Nine
soil samples were randomly collected on each plot using
a stainless cylinder with 5 cm diameter. The samples collected
from each stand were mixed and homogenized by compositing The SOC and TN concentrations
soils at the same depth from three plots. The composited soils Concentration of SOC and C/N ratio differed significantly be-
were divided into two parts: one was sieved to pass through tween NSF stands and LOP stands (P < 0.05). Moreover, the
a 2-mm mesh immediately and stored at 4°C until analysis concentration of SOC in the 0- to 15-cm layer of the NSF stands
for the estimation of microbial biomass carbon (MBC) and mi- was significantly higher than that in the LOP stands (Table 1).
crobial biomass nitrogen (MBN), the other air-dried and However, there was no significant difference in TN concentra-
passed through a 0.25-mm sieve for SOC and total nitrogen tion between the NSF and LOP stands (Table 1). Concentra-
(TN). tions of SOC and TN decreased with depth and did not
The SOC and TN were analyzed by dry combustion on differ among the seasons (Table 1). The C/N ratios of two soil
a Vario EL III elemental analyzer (Elementar Analysensysteme layers (0–15 cm and 15- to 30-cm depth for the two forests)
178 Journal of Plant Ecology

Table 1: three-way ANOVA on SOC, TN, C/N and soil water contents in the 0- to 15 and 15- to 30-cm soil layers in the NSF and the LOP in
eastern Liaoning Province, Northeast China

Soil depth (cm) Season Forest type SOC (g kg 1) TN (g kg 1) C/N Soil water content (%) pH

0–15 Spring NSF 50.5 6 4.2 4.2 6 0.4 12.3 6 0.3 30.4 6 1.2 5.82 6 0.03
LOP 34.7 6 1.8 3.2 6 0.2 10.9 6 0.2 27.5 6 0.6 5.55 6 0.05
Summer NSF 49.8 6 3.9 3.9 6 0.4 13.1 6 0.3 34.8 6 1.1 nd
LOP 37.0 6 2.4 3.3 6 0.3 11.4 6 0.2 30.9 6 0.8 nd
Autumn NSF 46.7 6 4.6 3.7 6 0.5 12.9 6 0.2 26.7 6 0.9 nd
LOP 36.8 6 2.0 3.2 6 0.2 11.4 6 0.1 21.7 6 1.3 nd
15-30 Spring NSF 23.4 6 2.8 2.2 6 0.3 11.1 6 0.2 24.0 6 0.5 5.91 6 0.05
LOP 24.0 6 1.9 2.4 6 0.1 10.0 6 0.2 22.9 6 1.2 5.71 6 0.04
Summer NSF 22.5 6 2.0 2.0 6 0.2 11.6 6 0.2 25.2 6 1.9 nd
LOP 23.4 6 1.9 2.2 6 0.1 10.6 6 0.1 25.0 6 0.7 nd
Autumn NSF 25.8 6 3.2 2.2 6 0.3 11.7 6 0.2 19.6 6 0.8 nd

Downloaded from by Osbert Sun on August 19, 2010

LOP 25.5 6 0.9 2.4 6 0.1 10.4 6 0.1 18.5 6 1.2 nd
Three-way ANOVA results
Forest type * ns ** ** /
Sampling season ns ns ** ** /
Depth ** ** ** ** /
Forest 3 season ns ns ns ns /
Forest 3 depth * ns ns ** /
Season 3 depth ns ns ns ns /
Forest 3 season 3 depth ns ns ns ns /

ns denotes not significant; nd denotes not determined. Values shown in Table 1 are means 6 standard error (n = 3).
P < 0.05, **P < 0.01.

Table 2: forest litterfall (t hm 2 y 1) and fine root biomass (g m 2) 0-15 cm 15-30 cm

to 30-cm soil depth for the NSF and the LOP in eastern Liaoning
Province, Northeast China 800 LOP
MBC concentration
(mg kg-1)

Forest type Forest litterfall Fine root biomass 600

NSF 2.99 295.3 400

LOP 1.15 114.4 200

spring summer autumn spring summer autumn

ranged from 10.0 to 13.1 and were significantly (P < 0.01)

affected by sampling seasons.
MBN concentration

60 *
Soil MBC, MBN, MBC/SOC and MBN/TN ratios
(mg kg-1)

Results from three-way ANOVA indicated that both forest 40 *

types and sampling seasons had significant effects on MBC
concentration; the soil MBN was significantly affected by forest
types, but not the sampling season. The MBC and MBN con- 0
centrations were also significantly influenced by soil layers spring summer autumn spring summer autumn
(P < 0.01). In general, concentrations of MBC and MBN
showed higher values in the NSF stands than in the LOP stands
Figure 2: MBC and MBN in the soils of NSF and LOP in different sea-
across seasons (Fig. 2, P < 0.01). The values of soil MBC and sons in eastern Liaoning Province, Northeast China. Vertical bars in-
MBN were 30–38% and 18–34% lower in the 0- to 15-cm dicate standard errors of three stands.
layer and 27–37% and 7–28% lower in the 15- to 30-cm layer,
respectively, in the LOP stands than in the NSF stands across concentration was higher in summer than in spring and au-
the three seasons (Fig. 2). There was significant seasonal var- tumn at both soil depths. Soil MBN did not display apparent
iation in soil MBC for both forest types (P < 0.05); soil MBC seasonal patterns (Fig. 2).
Yang et al. | Soil microbial C and N in temperate forests 179

There were significant effects of forest types and seasons on in the NSF in each season. This may suggest that the NSF
the ratios of MBC/SOC and MBN/TN. In addition, the interac- stands would be of advantage to sustain soil fertility.
tion between forest type and soil layer significantly influenced Many factors have been suggested to explain the effects of
the MBC/SOC ratio. The MBC/SOC ratio was ;0.0130 in the vegetation type on microbial biomass in soils (Hackl et al.
NSF stands and 0.0115 in the LOP stands in the 0- to 15-cm 2004). For example, differences in the quantity and quality
layer and 0.0143 in the NSF stands and 0.0085 in the LOP of substrate inputs via varying litter and root types and asso-
stands in the 15- to 30-cm layer, across seasons. The MBN ciated nutrient specificity can be crucial drivers to influence
to TN ratio, MBN/TN, was 0.0142 in the NSF stands and the soil microbial biomass (Feng et al. 2009; Jin et al. 2010).
0.0110 in the LOP stands for the 0- to 15-cm layer, and It is well known that soil microbial biomass greatly depends
0.0137 in the NSF stands and 0.0098 in the LOP stands for on soil organic matter as substrate; a decrease in SOC causes
the 15- to 30-cm layer, respectively, across seasons (Fig. 3). reduction in soil microbial biomass (Chen et al. 2005). Thus,
The ratios of MBC/SOC and MBN/TN varied significantly the higher MBC and MBN in the NSF stands than that in
across sampling seasons both in NSF and LOP stands, which LOP stands are mainly attributable to the greater availability
were higher in summer than in spring and autumn. of organic matter in NSF stands. This is evident from the

Downloaded from by Osbert Sun on August 19, 2010

Relationships between soil organic matter and
microbial biomass y = 11.658x - 6.453

MBC (mg kg )
R = 0.777**
There was a strong positive correlation of SOC and MBC 1000
(R2 = 0.78, n = 36, Fig. 4) or MBN (R2 = 0.83, n = 36,
Fig. 4) and of TN and MBC (R2 = 0.66, n = 36, Fig. 5) or
MBN (R2 = 0.77, n = 36, Fig. 5) based on a combined data 0
0.0 20.0 40.0 60.0 80.0
set for both forest types. The two forest types did not differ sig-
nificantly in the relationships of SOC with MBC or MBN and of SOC (g kg )
TN with MBC or MBN.
MBN (mg kg ) 80.0 y = 0.874x + 4.453

60.0 R = 0.834**
Results in this study indicate that the two stand types differ 20.0
markedly in soil microbial biomass. The concentrations of 0.0
MBC and MBN were significantly lower in the LOP stands than 0.0 20.0 40.0 60.0 80.0
SOC (g kg )

Figure 4: relationship between SOC and MBC or MBN for the NSF
0-15 cm 15-30 cm
2.5 and the LOP in eastern Liaoning Province, Northeast China (n = 36,
NSF i.e. three stands 3 two soil depths 3 three seasons 3 two stand types).
2.0 LOP

1.5 * NSF LOP


1500 y = 128.92x + 6.7935

MBC (mg kg )

1.0 2

R = 0.665**
spring summer autumn spring summer autumn 0
0.0 2.0 4.0 6.0 8.0
2.5 TN (g kg )

2.0 * *
80.0 y = 10.006x + 4.4454
MBN (mg kg )

1.5 *

* 60.0 R = 0.766**

1.0 40.0

0.5 20.0
0.0 0.0 2.0 4.0 6.0 8.0
spring summer autumn spring summer autumn
Season TN (g kg )

Figure 3: the ratios of MBC to SOC and MBN to TN in the soils of NSF Figure 5: relationship between soil TN and MBC or MBN for the NSF
and LOP in different seasons in eastern Liaoning Province, Northeast and the LOP in eastern Liaoning Province, Northeast China (n = 36, i.e.
China. Vertical bars indicate standard errors of three stands. three stands 3 two soil depths 3 three seasons 3 two stand types).
180 Journal of Plant Ecology

significant positive correlations between soil microbial biomass alterations of soil conditions (Sparling 1992). This value is also
and soil organic matter, in agreement with the finding by used as for comparison of soil quality parameter across soils
Wang and Wang (2007). A decline of soil organic matter in with different organic matter contents (Joergensen and Scheu
the LOP stands as compared with the NSF stands may be 1999). The MBC/SOC ratio can reflect the relationship and
explained by: (1) loss of soil organic matter due to removal interactions between the MBC and mineral SOC (Insam and
of slash and plant residues during site preparation and (2) poor Domsch 1988). In other words, the MBC/SOC ratio is inter-
litter quantity and quality, such as pine litter in larch planta- preted as substrate available and the portion of total soil carbon
tion containing a large amount of recalcitrant compounds, lead immobilized in microbial cells. In this, the ratios of MBC/SOC
to a lower rate of decomposition and consequently slower and MBN/TN were lower in the LOP stands than in the NSF
transformation of particulate organic matter into mineral soil stands in both 0- to 15-cm and 15- to 30-cm soil layers. Similar
component (Leckie et al. 2004). results have been previously founds by Liu et al. (1998) and
The concentrations of MBC in this study (192–776 mg kg-1) Wang and Wang (2007). Relatively lower MBC/SOC ratio
fall well within the range observed in temperate forest soils in the LOP stands may be ascribed to the inhibition of microbial
(Vance et al. 1987b; Zhong and Makeschin 2006), whereas immobilization, whereas a relatively higher MBC/SOC ratio in
the concentrations of MBN (22–58 mg kg 1) are lower than the NSF stands may be explainable by more diversified organic

Downloaded from by Osbert Sun on August 19, 2010

those in the temperate humid forest soils (Diaz-Raviña et al. substrate production as a result of mixed species.
1995; Gómez-Luna et al. 2009). The low MBN from our study In this study, the ratios of MBC/SOC and MBN/TN varied with
site may be due to the rapid rate of N mineralization and N season, attaining higher values in summer and lower in spring or
leaching in the temperate secondary forest soils (Li et al. 2001). autumn. The seasonal average of the MBC/SOC ratio is 1.18%
The two stand types in this study exhibited a significant sea- lower than the values reported for other temperate forests (1.8–
sonal variation in soil MBC, but soil MBN was less variable. 2.9%; Vance et al. 1987b). Furthermore, the seasonal average
Seasonal variations of soil microbial biomass reflect the degree of MBN/TN ratio (1.22%) is also lower than that of temperate
of immobilization–mineralization of soil carbon and nitrogen. forest soils (1.6–3.0%; Zhong and Makeschin 2006), resulting
A decrease in soil microbial biomass can result in mineraliza- possibly from low soil organic matter (Jones et al. 2008).
tion of nutrients, whereas an increase in microbial biomass In conclusion, our results suggest that the NSF is better in
may lead to immobilization of nutrients (McGill et al. 1986). sustaining the microbial biomass and soil organic matter qual-
In both NSF and LOP stands, MBC concentration was higher ity than larch plantation in Northeast China. This calls for cau-
in summer than in spring and autumn. This finding is consis- tions in large-scale conversions of the native forests to
tent with some of the previous studies in temperate forest coniferous plantations as a forest management practice on
regions (Bohlen et al. 2001). However, the patterns of seasonal concerns of sustainable soil productivity.
variations in MBC in our study differ from that reported for
subtropical humid forest, in which the highest values of micro-
bial biomass are observed during the winter and the lowest FUNDING
during the rainy season (Maithani et al. 1996). It has been sug-
gested that soil moisture is important in determining MBC of The Academy of Sciences / State Administration of Foreign
temperate forest soils and is a major factor controlling the mi- Experts Affairs (CAS/SAFEA) International Partnership Pro-
crobial biomass (Diaz-Raviña et al. 1995). In this study, the sea- gram for Creative Research Teams (KZCX2-YW-445); National
sonal dynamics of soil water content coincided with the Forestry Scientific Support Program (2006BAD03A0903
seasonal variations in rainfall of the study area, which was and 2006BAD03A0401); Non-commercial Forest Project
higher in summer and lower in spring and autumn. The sea- (200804027-05).
sonal variations in soil moisture may be responsible for the var-
iation in MBC in both types of stands, as soil water content was
significantly related to MBC concentrations (R2 = 0.74 and P < REFERENCES
0.01 in the NSF stands; R2 = 0.58 and P < 0.01 in the LOP
Bauhus J, Barthel R (1995) Mechanisms for carbon and nutrient re-
stands). Chen et al. (2003) also found similar relationships be- lease and retention in beech forest gaps. II. The role of soil microbial
tween soil water content and MBC in pine plantations in the biomass. Plant Soil 168–169:585–92.
subtropical zone. In addition, the mean monthly temperature Behera N, Sahani U (2003) Soil microbial biomass and activity in re-
was 21°C in summer and 10°C in spring or autumn in our sponse to Eucalyptus plantation and natural regeneration on tropical
study area. Thus, the higher MBC in summer may well be re- soil. For Ecol Manage 174:1–11.
lated to the high temperature in July. A combination of in- Bohlen PJ, Groffman PM, Driscoll CT, et al. (2001) Plant-soil-microbial
creased soil moisture, temperature and plant root activity in interactions in a northern hardwood forest. Ecology 82:965–78.
summer all favor soil microbial biomass activities and higher Brookes PC, Landman A, Pruden G, et al. (1985) Chloroform
microbial biomass in the temperate forest ecosystem. fumigation and release of soil N: a rapid direct extraction method
Soil MBC/SOC ratio, or microbial quotient, has been widely to measure microbial biomass N in soil. Soil Biol Biochem
used as an indicator of future changes in organic matter due to 17:837–42.
Yang et al. | Soil microbial C and N in temperate forests 181

Burton J, Chen CR, Xu ZH, et al. (2007) Gross nitrogen transformations Kasel S, Bennett LT (2007) Land-use history, forest conversion, and
in adjacent native and plantation forests of subtropical Australia. soil organic carbon in pine plantations and native forests of south
Soil Biol Biochem 39:426–33. eastern Australia. Geoderma 137:401–13.
Chen CR, Xu ZH, Blumfield TJ, et al. (2003) Soil microbial biomass Leckie SE, Prescott CE, Grayston SJ (2004) Forest floor microbial
during the early establishment of hoop pine plantation: seasonal community response to tree species and fertilization of regenerating
variation and impacts of site preparation. For Ecol Manage coniferous forests. Can J Forest Res 34:1426–35.
186:213–25. Li GC, Han XG, Huang JH, et al. (2001) A review of affecting factors of
Chen TH, Chiu CY, Tian GL (2005) Seasonal dynamics of soil microbial soil nitrogen mineralization in forest ecosystems. Acta Ecol Sin
biomass in coastal sand dune forest. Pedobiologia 49:645–53. 21:1187–95 (in Chinese with English abstract).
Chen XW, Li BL (2003) Change in soil carbon and nutrient Li YQ, Xu M, Zou XM, et al. (2005) Comparing soil organic carbon dy-
storage after human disturbance of a primary Korean pine forest namics in plantation and secondary forest in wet tropics in Puerto
in Northeast China. For Ecol Manage 186:197–206. Rico. Global Change Biol 11:239–48.
Devi NB, Yadava PS (2006) Seasonal dynamics in soil microbial Liu SR, Li XM, Niu LM (1998) The degradation of soil fertility in
biomass C, N and P in a mixed-oak forest ecosystems of Manipur, pure larch plantations in the northeastern of China. Ecol Eng
North-east India. Appl Soil Ecol 31:220–7. 10:75–86.
Diaz-Raviña M, Acea MJ, Carballas T (1995) Seasonal changes in mi- Maithani K, Tripathi RS, Arunachalam A, et al. (1996) Seasonal dynam-

Downloaded from by Osbert Sun on August 19, 2010

crobial biomass and nutrient flush in forest soils. Biol Fertil Soils ics of microbial biomass C, N and P during regrowth of a disturbed
19:220–6. subtropical humid forest in north-east India. Appl Soil Ecol 4:31–7.
Feng WT, Zou XM, Schaefer D (2009) Above- and belowground carbon McGill MB, Gannon KR, Robertson JA, et al. (1986) Dynamics of soil
inputs affect seasonal variations of soil microbial biomass in a sub- microbial biomass and water soluble organic C in Breton L after 50
tropical monsoon forest of southwest China. Soil Biol Biochem years of cropping to two rotation. Can J Soil Sci 66:1–19.
41:978–83. Ross DJ, Speir TW, Tate KR, et al. (1982) Restoration of pasture after
Gallardo A, Schlesinger WH (1994) Factors limiting microbial topsoil removal: effect of soil carbon and nitrogen mineralization, mi-
biomass in the mineral soil and forest floor of a warm-temperate crobial biomass and enzyme activities. Soil Biol Biochem 14:575–81.
forest. Soil Biol Biochem 26:1409–15. Shi Z, Li YQ, Wang SJ, et al. (2009) Accelerated soil CO2 efflux after
Gómez-Luna BE, Rivera-Mosqueda MC, Dendooven L, et al. (2009) conversion from secondary oak forest to pine plantation in south-
Charcoal production at kiln sites affects C and N dynamics and eastern China. Ecol Res 24:1257–65.
associated soil microorganisms in Quercus spp. temperate forests Singh JS, Raghubanshi AS, Singh RS, et al. (1989) Microbial biomass
of central Mexico. Appl Soil Ecol 41:50–8. acts as a source of plant nutrients in dry tropical forest and savanna.
Groffman PM, McDowell WH, Myers JC, et al. (2001) Soil microbial Nature 338:499–500.
biomass and activity in tropical riparian forests. Soil Biol Biochem Smith JL, Papendick RI, Bezdicek DF, et al. (1993) Soil organic matter
33:1339–48. dynamics and crop residue management. In Metting FB Jr (ed).
Guo LB, Gifford RM (2002) Soil carbon stocks and land use change: Soil Microbial Ecology. New York: Marcel Dekker Inc, 65–94.
a meta analysis. Global Change Biol 8:345–60. Smith JL, Paul EA (1990) The significance of soil microbial biomass
Hackl E, Bachmann G, Zechmeister-Boltenstern S (2004) Microbial estimations. In Bollag JM, Stotzky G (eds). Soil Biochemistry.
nitrogen turnover in soils under different types of natural forest. New York: Marcel Dekker Inc., 357–96.
For Ecol Manage 188:101–12. Sparling GP (1992) Ratio of microbial biomass carbon to soil organic
Hao ZQ, Wang QL, Dai LM (2000) The importance of the national pro- carbon as a sensitive indicator of changes in soil organic matter. Aust
gramme for natural forests conservation on biodiversity conserva- J Soil Res 30:195–207.
tion in northeast state owned forest areas of China. In Xu ZH (ed). Tonon G, Boldreghini P, Gioacchini P (2005) Seasonal changes in mi-
Go Forward the 21st Century’s Chinese Biodiversity Conservation. crobial nitrogen in an old broadleaf forest and in a neighbouring
Beijing, China: China Forestry Publishing House, 21–6. young plantation. Biol Fertil Soils 41:101–8.
He YJ, Wang QK, Wang SL, et al. (2006) Characteristics of soil microbial Vance ED, Brookes PC, Jenkinson DS (1987a) An extraction method
biomass carbon and nitrogen and their relationships with soil for measuring soil microbial biomass C. Soil Biol Biochem 19:703–7.
nutrients in Cunninghamia lanceolata plantations. Chin J Appl Ecol Vance ED, Brookes PC, Jenkinson DS (1987b) Microbial biomass meas-
17:2292–6 (in Chinese with English abstract). urements in forest soil: the use of the chloroform fumigation-incu-
Insam H, Domsch KH (1988) Relationship between soil organic carbon bation method in strongly acid soils. Soil Biol Biochem 19:697–702.
and microbial biomass on chronosequences of reclamation sites. Wang CK, Yang JY (2007) Rhizospheric and heterotrophic compo-
Microbiol Ecol 15:177–88. nents of soil respiration in six Chinese temperate forests. Global
Jin H, Sun OJ, Liu J (2010) Changes in soil microbial biomass and com- Change Biol 13:123–31.
munity structure with addition of contrasting types of plant litter in Wang CM, Oy H, Shao B, et al. (2006) Soil carbon changes following
a semiarid grassland ecosystem. J Plant Ecol. In press. afforestation with Olga Bay Larch (Larix olgensis Henry) in North-
Joergensen RG, Scheu S (1999) Depth gradients of microbial eastern China. J Integr Plant Biol 48:503–12.
and chemical properties in moder soils under beech and spruce. Wang QK, Wang SL (2007) Soil organic matter under different forest
Pedobiologia 43:134–44. types in Southern China. Geoderma 142:349–56.
Jones DL, Hughes LT, Murphy DV, et al. (2008) Dissolved organic Wu J, Joergensen RG, Pommerening B, et al. (1990) Measurement of
carbon and nitrogen dynamics in temperate coniferous forest plan- soil microbial biomass C by fumigation-extraction—an automated
tations. Eur J Soil Sci 59:1038–48. procedure. Soil Biol Biochem 22:1167–9.
182 Journal of Plant Ecology

Xu ZH, Ward S, Chen CR, et al. (2008) Soil carbon and nutrient pools, pine (Pinus sylvestris var. mongolica) in sandy lands in Keerqin, north-
microbial properties and gross nitrogen transformations in adjacent eastern China. Plant Soil 317:121–33.
natural forest and hoop pine plantations of subtropical Australia. Zhang J, Wang SL, Feng ZW, et al. (2009) Stability of soil organic car-
J Soil Sediment 8:99–105. bon changes in successive rotations of Chinese fir (Cunninghamia
Yan ER, Wang XH, Huang JJ, et al. (2008) Decline of soil nitrogen min- lanceolata (Lamb.) Hook) plantations. J Environ Sci 21:352–9.
eralization and nitrification during forest conversion of evergreen Zhong ZK, Makeschin F (2006) Differences of soil microbial biomass
broad-leaved forest to plantations in the subtropical area of Eastern and nitrogen transformation under two forest types in central
China. Biogeochemistry 89:239–51. Germany. Plant Soil 283:287–97.
Yang K, Zhu JJ, Yan QL, et al. (2010) Changes of soil P chemistry as Zhu JJ, Liu SR (2007) Conception of secondary forest and its relation
affected by conversion of natural secondary forests to larch planta- to ecological disturbance degree. Chin J Ecol 26:1085–93 (in Chinese).
tions. For Ecol Manage 260:422–8. Zhu JJ, Mao ZH, Hu LL, et al. (2007) Plant diversity of secondary forests
Yang YS, Chen GS, Guo JF, et al. (2007) Soil respiration and carbon in response to anthropogenic disturbance levels in montane regions
balance in a subtropical native forest and two managed plantations. of northeastern China. J For Res 12:403–16.
Plant Ecol 193:71–84. Zhu WX, Carreiro MM (2004) Variations of soluble organic nitrogen
Zeng DH, Hu YL, Chang SX, et al. (2009) Land cover change effects on and microbial nitrogen in deciduous forest soils along an urban-

Downloaded from by Osbert Sun on August 19, 2010

soil chemical and biological properties after planting Mongolian rural gradient. Soil Biol Biochem 36:279–88.