Open Access

Effects of exotic species Larix kaempferi on diversity and activity of soil microorganisms in Dalaoling National Forest Park

Ecological Processes20154:10

DOI: 10.1186/s13717-015-0037-x

Received: 8 March 2015

Accepted: 14 June 2015

Published: 25 June 2015

Abstract

Introduction

Soil microbial community plays a crucial role in the ecological processes of soil ecosystem. Forest species introduction often changes profoundly soil ecological processes in the forest. Larix kaempferi (Lam.) was introduced to China from Japan as a timber tree species in the 1960s. The activity and functional diversity of soil microorganisms in the L. kaempferi forest in Dalaoling National Forest Park in Hubei Province, China, was studied to evaluate the effects of this exotic species on the local soil ecosystems.

Methods

Quadrates were set up randomly in the L. kaempferi forests cultivated in 1990 and 1996 and the surrounding Pinus armandii forest cultivated in 1990. Soil samples were collected using a soil corer at five locations along the diagonals in each quadrat. The activity and functional diversity of soil microorganisms were tested using the BIOLOG technique in laboratory.

Results

The diversity, activity, and carbon utilization pattern of soil microorganism community and soil physicochemical properties were all impacted by the introduced species. The average well color development (AWCD) and Shannon’s richness index (H) of the soil microorganism community in the L. kaempferi forest decreased with the increase in forest age and were significantly lower than those in the surrounding native P. armandii forest. The carbon source utilization pattern of soil microorganism community in a 23-year-old L. kaempferi forest differed significantly from a 17-year-old L. kaempferi forest and the P. armandii forest. The introduced species also resulted in the changes of soil physicochemical properties. The organic material content, total nitrogen, available nitrogen, and total phosphorus in the soil of L. kaempferi forest were significantly lower than those in the soil of P. armandii forest.

Conclusions

Introduction and long-time cultivation of L. kaempferi significantly altered the soil microbial functional diversity and activity and the soil physicochemical properties. The alteration increased with the increase of forest age.

Introduction

Soil microbial community is an essential component of the soil ecosystem. Soil microorganisms participate directly in the soil ecological processes including litter decomposition, humus formation, nutrient transformation and recycle, and waste degradation (De Deyn et al. 2004; Maila et al. 2005; Noah and Robert 2006). Soil microbial diversity and function are considered as important indicators for the assessment of soil quality as the microbial effects on soil ecological processes could further influence soil physicochemical properties, seedling regeneration, plant community development, and biodiversity (Onaindiaa et al. 2013; Owen et al. 2013; Sharma et al. 2011). The change of plant community in composition and structure often leads to the changes of soil microbial community in diversity and function. These changes would have certain impact on the ecological process of soil system that caused the change of plant community in turn (Mummey and Rillig 2006; Patrick 2006; Boudiaf et al. 2013). An introduction of forest species often changes obviously the composition, structure, species diversity, and productivity of plant community (Davies 2011; Omoro et al. 2010; Powell et al. 2013). As a result, the biomass, structure, and function of soil microorganism community are also influenced (Kourtev et al. 2002; Ravit et al. 2003; Chen et al. 2013). However, the effects of introduced forest species on soil microbial diversity and related ecological processes displayed inconsistent patterns as the effects were determined by many factors including plant growth characteristic, litter quality and quantity, roots and root secretions, phenology, climate condition, etc. (Ehrenfeld 2003; Chen et al. 2005; Steinlein 2013). Determining the effects of specific exotic plants in detail is critical to the sustainable forest management.

The global need for wood production has led to the increase of forest species introduction on the basis of their ability to adapt to local conditions and of their rapid growth. In 2010, planted forests accounted for 264 million hectares (7 % of the total forest area worldwide), an increase of 5 million hectares per year since 2005. A quarter of planted forests are composed of introduced species (Dodet and Collet 2012). A number of forest tree species, including Pinus elliottii, Acacia mangium, Thuja occidentalis, Abies firma, and Larix kaempferi, also have been introduced to China from abroad for forestry production in the last century. The introduction has promoted Chinese timber production in general and also caused a few ecological problems in some ecosystems, such as diversity loss and soil degradation (Yang et al. 2010). L. kaempferi, a cold-wet temperate tree species indigenous to Japan, was introduced to China in the 1960s and has become an important timber tree species distributed in Heilongjiang, Jilin, Liaoning, Hebei, Shandong, Henan, Jiangxi, and Hubei Province. L. kaempferi was introduced to Dalaoling National Forest Park (longitude 110° 43′ 42″–111° 22′ 2″, latitude 30° 58′ 50″–31° 07′ 23″), located in the southwestern Hubei Province in the late 1970s. Currently, there are over 700 hectares of L. kaempferi forests within the park as a result of its rapid growth and expansion. However, there is a report on biodiversity decline and seedling regeneration failure on local species (Xiao and Zeng 2005). The objectives of this study were to (1) determine the effect of the introduction and cultivation of L. kaempferi on the functional diversity and activity of the soil microbial community, (2) evaluate the changes in physicochemical proprieties of soil in the L. kaempferi forest, and (3) analyze the relationship between the functional diversity and activity of the soil microbial community and the physicochemical proprieties of soil in the L. kaempferi forest. The findings from this study may gain important scientific insights for forest management in the park.

Methods

Study sites and soil sampling

Experimental plots were established in field sites of three types of forest in the Dalaoling National Forest Park. The forests with close altitude, slope, and aspect included L. kaempferi forests cultivated in 1990 and 1996 and the surrounding P. armandii forest cultivated in 1990. P. armandii is a native species which has similar altitude adaptation with L. kaempferi in the Dalaoling National Forest Park. Soil samples were collected on 5 August 2013. Five quadrats (5 × 5 m2) were set up randomly at each of the four plot corners and in the center in a plot. Soil within the top 20-cm depth was collected using a soil corer at five locations along the diagonals in each quadrat and mixed thoroughly as a sample within each quadrat. Half an amount of each sample was placed directly into a sterile bag and sent to the laboratory, homogenized, sieved through a 2-mm filter, and stored in an icebox at 4 °C for microbial analysis. The other half of the sample was dried in air for physicochemical analysis.

BIOLOG analysis

A BIOLOG Microstation System (BIOLOG Inc., Hayward, CA, USA) was used to study the metabolic function of the soil microbial community. The BIOLOG technique proposes a simple and sensitive way to compare potential metabolic diversity of soil microbial communities and has been widely used in assessing microbial metabolic diversity in agricultural soils, forest soils, and under various vegetations as it represents certain metabolic functions in the microplates; the outcomes reflected the patterns of carbon source utilization (Grayston et al. 1998; Preston-Mafham et al. 2002; Zheng et al. 2005; Chen et al. 2013). We used ECO microplates to compare potential metabolic diversity of soil microbial communities among the three plantations. One ECO microplate contained three replicates of 31 different substrates to discriminate the heterotrophic microbial community. Five grams of fresh soil from each sample were suspended in 45 mL of sterile distilled water in a flask and sealed with silver paper. The flask containing the soil solution was shaken at 190 rpm for 20 min at 22 °C. Then, the soil suspension was allowed to settle for 10 min. Five milliliters of supernatant liquid was transferred to 45 mL of sterile distilled water in a flask. The procedure was repeated three times. Five milliliters of suspension was diluted 1000 times in a tenfold dilution series, from which 150 μL of the supernatant was inoculated to each well of the microplate. The microplates were incubated in the dark at 28 °C for 10 days, during which period color development in each well was measured at the wavelengths of 595 and 750 nm, respectively, every 24 h using an automated microplate reader (BIOLOG, Hayward, USA) (Classen et al. 2003; Chen et al. 2013).

The number of carbon substrates used by soil microorganisms (S), average well color development (AWCD), Shannon’s richness index (H), Simpson’s dominance index (D), and relative use efficiency of carbon resources (RUE) were evaluated and used as indicators to assess the soil microbial functional diversity and activity (Chen et al. 2013; Boudiaf et al. 2013). The average well color development reflecting the total ability of microorganisms to use carbon resource was determined using the method reported by Classen et al. (2003):
$$ \mathrm{AWCD}={\displaystyle \sum \left({C}_i - R\right)/n} $$

where C i represents the difference of optical density (OD) of a sample well recorded at the wavelengths of 590 and 750 nm. R is the optical density of the control well, and n is the total number of the sole carbon substrates (ECO plates n = 31). AWCD was treated as 0 when its value was below 0.06.

The number of carbon substrates used by soil microorganisms was derived by counting the wells with color development. Biodiversity was evaluated using Shannon’s richness index (H) and Simpson’s dominance index (D) (Wei et al. 2008; Chen et al. 2011):
$$ H = -{{\displaystyle \sum {P}_i \ln P}}_i, $$
$$ D = 1-{\displaystyle \sum {P_i}^2} $$

where P i is the proportional color development of the ith well over the total color development of all wells in a plate.

The RUE reflects the degree of microorganisms to use a carbon resource. RUE was derived from the ratio of the optical density of one kind of carbon substrate with the total optical density of all other carbon substrates among the seven major carbon substrates including monosaccharides and glycosides, amino acids, alcohols, amines, polymerization saccharides, lipids, and organic acids (Wei et al. 2008).

Determination of soil physicochemical properties

Soil water content (SWC) was determined gravimetrically by weighing the soil sample, drying it in an oven at 105 °C for 24 h, and then re-weighing the sample. Soil organic matter (OM) was measured using the potassium dichromate melting method, total nitrogen (TN) by the semi-micro Kjeldahl nitrogen determination apparatus, total phosphate (TP) by the NaOH alkali melting method, total potassium (TK) by the flame photometer method, available nitrogen (AN) by the diffusion method, and pH by the precision acidity meter, respectively (Bao 2000). Five replicates were tested for each forest type.

Data analysis

One-way analysis of variance (ANOVA) was performed to determine the effects of the introduction and cultivation of L. kaempferi on the soil microbial diversity and function. The parameters used in the analysis included forest type as an independent factor, the average well color development, Shannon’s richness index, Simpson’s dominance index, number of carbon substrates used by soil microorganisms, and indicators for measuring the physicochemical properties such as soil organic matter, total nitrogen, total phosphorus, total potassium, available nitrogen, and pH as dependent factors, respectively. All values were expressed as mean ± SE. The forest types included the 23-year-old and 17-year-old L. kaempferi forests and the P. armandii forest. The Duncan test method was conducted for multiple comparisons to assess the significance level of each parameter among treatments when the main effect was significant.

The structure of the bacterial community was characterized by classifying treatments according to their substrate utilization patterns using the principal component analysis (PCA) (Kourtev et al. 2003). The first and second principal component variances contained the information of carbon type and their contribution. The difference in principal component variances was used to represent the pattern of carbon utilization. The PCA results were presented as factor loading plots (Choi and Dobbs 1999). The relationship between microorganism diversity and function and soil physicochemical properties was determined by the correlation analysis of the average well color development, Shannon’s richness index, Simpson’s dominance index, number of carbon substrates used by soil microorganisms with soil organic matter, total nitrogen, total phosphorus, total potassium, available nitrogen, and pH, respectively. All above analyses were conducted using SPSS software (13.0).

Results

Functional diversity and activity of soil microorganism community

The introduction and long-time cultivation of L. kaempferi caused a significant change of microorganism community in diversity and activity (Table 1). The average well color development (AWCD) and richness index (H) used by microorganisms in soil microorganism community in the 23-year-old L. kaempferi forest decreased by 7.6 and 1.6 % in contrast with those in the 17-year-old L. kaempferi forest. Both of these indicators and the number of carbon substrates (S) in the 23-year-old L. kaempferi forest were significantly lower than those in the P. armandii forest (P < 0.05). However, the dominance index (D) did not differ significantly among forests (P > 0.05).
Table 1

Changes of function diversity and activity of the soil microbial community

Forest types

AWCD

H

D

S

23-year-old L. kaempferi forest

1.10 ± 0.02 a

3.23 ± 0.02 a

0.96 ± 0.00 a

26.76 ± 0.32 a

17-year-old L. kaempferi forest

1.19 ± 0.01 b

3.28 ± 0.01 b

0.96 ± 0.00 a

27.43 ± 0.29 ab

Pinus armandii forest

1.22 ± 0.02 b

3.29 ± 0.01 b

0.96 ± 0.00 a

27.79 ± 0.28 b

Note: Values are expressed as mean ± SE. Significance of the statistical test is reported at P < 0.05

AWCD average well color development, H Shannon’s richness index, D Simpson’s dominance index, S the number of carbon substrates used by soil microorganisms

Principal component analysis of carbon source utilization

The principal component analysis indicated that the introduction and cultivation of L. kaempferi also induced changes in the soil microorganism community and the pattern of carbon utilization (Fig. 1). The percent contribution from the first and second principal component variances were 83.94 and 8.82 %, respectively. The three plant communities differed significantly in the principal component 1 (PC1) and principal component 2 (PC2) (F = 95.998, P < 0.01; F = 195.998, P < 0.001), respectively. The 23-year-old L. kaempferi forest differed significantly from the 17-year-old L. kaempferi forest and the P. armandii forest in the carbon substrate utilization pattern; meanwhile, the difference was not significant between the 17-year-old L. kaempferi forest and the P. armandii forest.
Fig. 1

Principal component analysis of the utilization pattern of substrate carbon sources

Twelve of the 31 carbon sources in the BIOLOG ECO microplates contributed to the PC1. These carbon sources included 6 organic acid, 2 monosaccharides and glycosides, 2 amino acids, 1 lipid, and 1 polymeric carbohydrate (Table 2). Seven carbon sources mainly contributed to the PC2 and included 2 lipids, 2 monosaccharides and glycosides, 1 amino acid, 1 amine, and 1 alcohol. The important carbon sources contributing to both PC1 and PC2 were organic acid, monosaccharide, and glycoside, respectively (Table 2). The relative use efficiency of carbon source (RUE) changed with the type of carbon source and forest. A high relative use efficiency was found for organic acids and amino acids ranging from 22.78 to 25.41 %. By contrast, the relative use efficiency for other five carbon sources was relatively low ranging from 6.09 to 13.72 %. There was significant difference in the use efficiency for monosaccharides and glycosides, amines, and polymerization saccharides among the 23-year-old L. kaempferi forest, 17-year-old L. kaempferi forest, and the P. armandii forest (P < 0.05) (Fig. 2)
Table 2

The loading matrix of principal components

PC1

PC2

Carbon sources

Classification

r

Carbon sources

Classification

r

4-Hydroxybenzoic acid

Acids

1.00

d-Xylose

Monosaccharides and glycosides

0.97

d-Malic acid

Acids

1.00

l-Asparagine

Amino acids

0.97

Pyruvic acid methyl ester

Lipids

1.00

Tween 80

Lipids

0.95

β-Methyl-d-glucose

Monosaccharides and glycosides

0.98

Tween 40

Lipids

0.94

l-Serine

Amino acids

0.97

Phenylethylamine

Amines

0.86

d-Galactonic acid γ-lactone

Polymerization saccharides

0.96

d,l-α-Glycerol

Alcohols

0.79

α-Ketobutyric acid

Acids

0.93

Glucose-1-phosphate

Monosaccharides and glycosides

0.75

2-Hydroxybenzoic acid

Acids

0.87

   

α-d-Lactose

Monosaccharides and glycosides

0.86

   

l-Arginine

Amino acids

0.85

   

Itaconic acid

Acids

0.83

   

d-Glucosaminic acid

Acids

0.80

   

Note: r represents for the loading value of principal components

Fig. 2

Relative use efficiency of the seven carbon sources including monosaccharides and glycosides, amino acids, alcohols, amines, polymerization saccharides, lipids, and organic acids

Soil physicochemical properties

Soil physicochemical properties were also influenced significantly by the introduction of L. kaempferi (Table 3). The soil organic matter (OM), total nitrogen (TN), total phosphate (TP), available nitrogen (AN), and soil water content (SWC) in the P. armandii forest were all significantly higher than those in the L. kaempferi forest (P < 0.05). All physicochemical values of these indicators decreased with the increase of cultivation time. However, the difference of total potassium (TK) did not reach significant level among the three forests (P > 0.05).
Table 3

Changes in soil physicochemical properties under different forests

Forests

OM

TN

TP

TK

AN

pH

SWC

(g/kg)

(g/kg)

(g/kg)

(g/kg)

(mg/kg)

 

(%)

23-year-old L. kaempferi forest

67.32 ± 1.79 a

3.76 ± 0.07 a

0.74 ± 0.02 a

1.81 ± 0.07 a

0.30 ± 0.01 a

4.96 ± 0.06 a

66.06 ± 5.53 a

17-year-old L. kaempferi forest

72.38 ± 2.96 ab

3.95 ± 0.12 ab

0.64 ± 0.03 b

1.83 ± 0.11 a

0.32 ± 0.01 ab

5.39 ± 0.05 b

63.49 ± 4.64 a

Pinus armandii forest

76.22 ± 3.14 b

4.10 ± 0.12 b

0.97 ± 0.03 c

1.91 ± 0.12 a

0.36 ± 0.02 b

5.35 ± 0.08 b

85.03 ± 2.59 b

Note: Values are expressed as mean ± SE. Means followed by the same letter(s) within each column are not significant at P > 0.05

Relationship between activity and diversity of microorganism community and soil physicochemical properties

The average well color development (AWCD) had a very significant positive correlation with available nitrogen (AN) and pH (P < 0.05). However, there was no strong correlation among other physicochemical properties and microbial metabolic activity and function (P > 0.05) (Table 4).
Table 4

Pearson correlation analysis of chemical properties and microbial function

PCP

AWCD

H

S

OM

0.03 (0.84)

−0.02 (0.88)

−0.10 (0.54)

TN

0.06 (0.72)

0.16 (0.26)

0.21 (0.15)

TP

−0.03 (0.85)

0.07 (0.64)

0.06 (0.70)

TK

0.02 (0.89)

0.03 (0.82)

0.05 (0.75)

AN

0.09 (0.05)*

−0.01 (0.96)

−0.02 (0.93)

pH

0.50 (0.00)**

0.21 (0.13)

−0.03 (0.84)

SWC

0.03 (0.91)

−0.22 (0.37)

0.09 (0.73)

Note: Pearson correlation coefficients and P values in parentheses

* is significant at P<0.05

** is significant at P<0.001

Discussion

Diversity and activity of soil microorganism community

Introduction of exotic plant species not only influenced plant community structure but also led to the changes of soil microbial diversity and function and the soil physicochemical properties (Kourtev et al. 2003; Mummey and Rillig 2006). Previous reports showed that the introduction of exotic species displayed two patterns, either increased or decreased soil microbial activity and diversity (Saggar et al. 1999; Callaway et al. 2004). Duda et al. (2003) found that the soil bacterial diversity in the Halogeton glomeratus community, an invasive species in the western United States, was significantly higher than that in native community. However, many other studies supported the decreasing pattern (Lindsay and French 2004; Valéry et al. 2004; Li et al. 2006). Chen et al. (2011) reported that the introduction and cultivation of Pinus elliottii significantly reduced the soil microbial diversity and function compared to those in the native Pinus massoniana forest in the same region. Yang et al. (2008) found that the soil bacterial diversity in the L. kaempferi forest was significantly lower than that in the surrounding native Pinus tabulaeformis forest. In this study, we found that the activity and functional diversity of soil microbial communities in the 23-year-old L. kaempferi forest were significantly lower than the 17-year-old L. kaempferi forests and the surrounding P. armandii forest. Therefore, we concluded that the introduction and cultivation of L. kaempferi negatively influenced the local microbial activity and diversity. Under this circumstance, this type of impact increased as the forest stand aged.

Carbon source utilization and soil physicochemical properties

The cultivation of exotic species often affects soil ecological processes, especially the litter composition process (Lindsay and French 2004; Standish et al. 2004; Rodgers et al. 2008). The biochemical composition of exotic plant litter significantly differed from that of native species. The change of soil physicochemical properties resulting from the litter decomposition would affect the presence and activity of local microorganisms in the soil ecosystem, which in turn affected the soil ecological processes and soil physicochemical properties (Bilgo et al. 2012; Bragazza et al. 2007; Owen et al. 2013). Compared to the indigenous plants, the presence of exotic plants typically leads to the increase in net forest primary productivity or biomass (Ehrenfeld 2003). However, the influence pattern of exotic plant on soil ecological processes was not consistent as exotic plants affected the soil ecosystem processes through a variety of mechanisms (Hedge and Kriwoken 2000; Yeates and Williams 2001; Mack and D’Antonio 2003; van der Putten et al. 2007). The inhibition of exotic plant species on soil ecological processes depended on litter quantity, litter degradation, litter biochemical characteristics, and species ecological characteristics (Allison and Vitousek 2004; Valéry et al. 2004; Scott et al. 2001; Wolfe et al. 2008).

The introduction of L. kaempferi forest significantly changed the carbon source utilization pattern of the soil microorganism community in Dalaoling National Forest Park. The use efficiency of some carbon sources in the soil microorganism community in the L. kaempferi forest differed from those in the P. armandii forest and decreased with the increases in stand age. L. kaempferi also caused significant changes in soil physicochemical properties. Therefore, we concluded that the introduction and cultivation of L. kaempferi in the Dalaoling National Forest Park resulted in a decline in soil quality and soil fertility. The significant relationship between soil pH and AWCD suggested that L. kaempferi influenced soil activity by changing the soil pH. However, the detailed mechanism of introduction of L. kaempferi on soil microbial diversity and function is worthwhile for further research, such as how the litter affects specifically the composition of microbial community and soil physicochemical properties and the response of composition and structure of microbial community to the litter of exotic species.

Conclusions

Soil ecological process is an important part in the material cycle and energy flow of terrestrial ecosystem and is closely related with vegetation development and succession (Wardle et al. 2004; Noah and Robert 2006). Most artificial plantations alter soil ecological process and cause soil fertility decline and soil degradation, which is more prominent in exotic species forest because of their significant effect on soil microbial community diversity and physicochemical properties (Lorenzo et al. 2010; Patrick 2006). The long-term cultivation of L. kaempferi forest decreased the activity and functional diversity of soil microorganism community in Dalaoling National Forest Park. As a result, the soil physicochemical properties resulted in a decline in soil quality. The plant diversity and seedling regeneration in L. kaempferi forest was further impacted (Xiao and Zeng 2005). Modifying the negative effects of introduced forest species on soil ecological process is crucial to the sustainable forest management. Appropriate disturbance could reduce the effects of exotic plants on the local soil microorganism community (Xu et al. 2008; Carvalho et al. 2010). Zhang (2001) reported that thinning plantation stands increased soil microbe quantities, strengthened soil enzyme activities, decreased bulk density, and enhanced soil total porosity degree and available nutrients. Our primary field investigation showed that thinning the L. kaempferi forest stands increased the diversity of soil microorganism communities and improved soil texture (Song et al. 2013). The mechanism that thinning improves soil fertility is that the increased understory biodiversity after thinning enhances the increase of quantity and diversity of soil microbe and, therefore, strengthens bioactivity of soil and accelerates nutrient cycling of soil (Zhang 2001). The appropriate thinning approach and frequency and the response of L. kaempferi forest to thinning are going to be tested in our future research to provide more information for the sustainable management of the forest.

Declarations

Acknowledgements

This work was supported by the National Natural Science Foundation of China (51379105). We appreciate Professor Yinghua Huang and Binhe Gu for their helpful comments on this manuscript and Wei Song and Jiacheng Xiang with the field experiments.

Authors’ Affiliations

(1)
International Center for Ecological Protection and Management in the Three Gorges Area, Hubei Province, The China Three Gorges University
(2)
Engineering Research Center of the Ministry of Education for the Three Gorges Reservoir Region’s Eco-Environment, The China Three Gorges University

References

  1. Allison SD, Vitousek PM (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawaii. Oecologia 141:612–619View ArticleGoogle Scholar
  2. Bao S (2000) Soil and agricultural chemistry analysis, 3rd edn. China Agriculture Press, Beijing (in Chinese)Google Scholar
  3. Bilgo A, Sangare SK, Thioulouse J, Prin Y, Hien V, Galiana A, Baudoin E, Hafidi M, Bâ AM, Duponnois R (2012) Response of native soil microbial functions to the controlled mycorrhization of an exotic tree legume, Acacia holosericea in a Sahelian ecosystem. Mycorrhiza 22:175–187View ArticleGoogle Scholar
  4. Boudiaf I, Baudoin E, Sanguin H, Beddiar A, Thioulouse J, Galiana A, Prin Y, Le Roux C, Lebrun M, Duponnois R (2013) The exotic legume tree species, Acacia mearnsii, alters microbial soil functionalities and the early development of a native tree species, Quercus suber, in North Africa. Soil Biol Biochem 65:172–179View ArticleGoogle Scholar
  5. Bragazza L, Siffi C, Iacumin P, Gerdol R (2007) Mass loss and nutrient release during litter decay in peatland: the role of microbial adaptability to litter chemistry. Soil Biol Biochem 39:257–267View ArticleGoogle Scholar
  6. Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427:731–733View ArticleGoogle Scholar
  7. Carvalho LM, Antunes PM, Martins-Loucao MA, Klironomos JN (2010) Disturbance influences the outcome of plant–soil biota interactions in the invasive Acacia longifolia and in native species. Oikos 119:1172–1180View ArticleGoogle Scholar
  8. Chen FL, Zheng H, Yang BS, Ouyang ZY, Zhang K, Tu NM (2011) Effects of exotic species slash pine (Pinus elliottii) litter on the structure and function of the soil microbial community. Acta Ecol Sin 31:3543–3550 (in Chinese with English abstract)Google Scholar
  9. Chen FL, Zheng H, Zhang K, Ouyang ZY, Lan J, Li HL, Shi Q (2013) Changes in soil microbial community structure and metabolic activity following conversion from native Pinus massoniana plantations to exotic Eucalyptus plantations. Forest Ecol Manag 291:65–72View ArticleGoogle Scholar
  10. Chen HL, Li YJ, Li B, Chen JK, Wu JH (2005) Impacts of exotic plant invasions on soil biodiversity and ecosystem processes. Biodivers Sci 13:555–565 (in Chinese with English abstract)View ArticleGoogle Scholar
  11. Choi KH, Dobbs FC (1999) Comparison of two kinds of BIOLOG microplates (GN and ECO) in their ability to distinguish among aquatic microbial communities. J Microbiol Meth 36:203–213View ArticleGoogle Scholar
  12. Classen AT, Boyle SI, Haskins KE, Overby ST, Hart SC (2003) Community level physiological profiles of bacteria and fungi: plate type and incubation temperature influences on contrasting soils. FEMS Microbiol Ecol 44:319–328View ArticleGoogle Scholar
  13. Davies KW (2011) Plant community diversity and native plant abundance decline with increasing abundance of an exotic annual grass. Oecologia 167:481–491View ArticleGoogle Scholar
  14. De Deyn GB, Raaijmakers CE, van Der Putten WH (2004) Plant community development is affected by nutrients and soil biota. J Ecol 92:824–834View ArticleGoogle Scholar
  15. Dodet M, Collet C (2012) When should exotic forest plantation tree species be considered as an invasive threat and how should we treat them? Biol Invasions 14:1765–1778View ArticleGoogle Scholar
  16. Duda JJ, Freeman DC, Emlen JM, Belnap J, Kitchen SG, Zak JC, Sobek E, Tracy M, Montante J (2003) Differences in native soil ecology associated with invasion of the exotic annual chenopod, Halogeton glomeratus. Biol Fert Soils 38:72–77View ArticleGoogle Scholar
  17. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523View ArticleGoogle Scholar
  18. Grayston SJ, Wang SQ, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378View ArticleGoogle Scholar
  19. Hedge P, Kriwoken LK (2000) Evidence for effects of Spartina anglica invasion on benthic macrofauna in Little Swanport estuary, Tasmania. Austral Ecol 25:150–159View ArticleGoogle Scholar
  20. Kourtev PS, Ehrenfeld JG, Haggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83:3152–3166View ArticleGoogle Scholar
  21. Kourtev PS, Ehrenfeld JG, Haggblom M (2003) Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol Biochem 35:895–905View ArticleGoogle Scholar
  22. Li WH, Zhang CB, Jiang HB, Xin GR, Yang ZY (2006) Changes in soil microbial community associated with invasion of the exotic weed, Mikania micrantha H.B.K. Plant Soil 281:309–324View ArticleGoogle Scholar
  23. Lindsay EA, French K (2004) Chrysanthemoides monilifera ssp. rotundata invasion alters decomposition rates in coastal areas of south-eastern Australia. Forest Ecol Manag 198:387–399View ArticleGoogle Scholar
  24. Lorenzo P, Rodriguez-Echeverrıa S, Gonzalez L, Freitas H (2010) Effect of invasive Acacia dealbata Link on soil microorganisms as determined by PCR-DGGE. Appl Soil Ecol 44:245–251View ArticleGoogle Scholar
  25. Mack MC, D’Antonio CM (2003) Exotic grasses alter controls over soil nitrogen dynamics in a Hawaiian woodland. Ecol Appl 13:154–166View ArticleGoogle Scholar
  26. Maila MP, Randima P, Surridge K, Drønen K, Cloete TE (2005) Evaluation of microbial diversity of different soil layers at a contaminated diesel site. Int Biodeter Biodegr 55:39–44View ArticleGoogle Scholar
  27. Mummey DL, Rillig MC (2006) The invasive plant species Centaurea maculosa alters arbuscular mycorrhizal fungal communities in the field. Plant Soil 288:81–90View ArticleGoogle Scholar
  28. Noah F, Robert BJ (2006) The diversity and biogeography of soil bacterial communities. PNAS 103:626–631View ArticleGoogle Scholar
  29. Omoro LMA, Pellikka PKE, Rogers PC (2010) Tree species diversity, richness, and similarity between exotic and indigenous forests in the cloud forests of Eastern Arc Mountains, Taita Hills, Kenya. J Forest Res 21:255–264View ArticleGoogle Scholar
  30. Onaindiaa M, Ametzaga-Arregi I, Sebastián MS, Mitxelena A, Rodríguez-Loinaz G, Peña L, Alday JG (2013) Can understory native woodland plant species regenerate under exotic pine plantations using natural succession? Forest Ecol Manag 308:136–144View ArticleGoogle Scholar
  31. Owen SM, Sieg CH, Johnson NC, Gehring CA (2013) Exotic cheat grass and loss of soil biota decrease the performance of a native grass. Biol Invasions 15:2503–2517View ArticleGoogle Scholar
  32. Patrick JB (2006) Biological invasion: linking the aboveground and belowground consequences. Appl Soil Ecol 32:1–5View ArticleGoogle Scholar
  33. Powell KI, Chase JM, Knight TM (2013) Invasive plants have scale-dependent effects on diversity by altering species-area relationships. Science 339:316–318View ArticleGoogle Scholar
  34. Preston-Mafham J, Boddy L, Randerson PF (2002) Analysis of microbial community functional diversity using sole-carbon-source utilisation profiles—a critique. FEMS Microbil Ecol 42:1–14Google Scholar
  35. Ravit B, Ehrenfeld JG, Haggblom M (2003) A comparison of sediment microbial communities associated with Phragmites australis and Spartina alterniflora in two brackish wetlands of New Jersey. Estua Coast 26:465–474View ArticleGoogle Scholar
  36. Rodgers VL, Wolfe BE, Werden LK, Finzi AC (2008) The invasive species Alliaria petiolata (garlic mustard) increases soil nutrient availability in northern hardwood-conifer forests. Oecologia 157:459–471View ArticleGoogle Scholar
  37. Saggar S, McIntosh PD, Hedley CB, Knicker H (1999) Changes in soil microbial biomass, metabolic quotient, and organic matter turnover under Hieracium (H. pilosella L.). Biol Fert Soils 30:232–238View ArticleGoogle Scholar
  38. Scott NA, Saggar S, McIntosh PD (2001) Biogeochemical impact of Hieracium invasion in New Zealand’s grazed tussock grasslands: sustainability implications. Ecol Appl 11:1311–1322View ArticleGoogle Scholar
  39. Sharma SK, Ramesh A, Sharma MP, Joshi OP, Govaerts B, Steenwerth KL, Karlen DL (2011) Microbial community structure and diversity as indicators for evaluating soil quality. Sustain Agr Rev 5:317–358View ArticleGoogle Scholar
  40. Song NN, Bai L, Chen FQ (2013) The effects of disturbance on soil microbial diversity and function of Larix kaempferi forest, International Conference on Frontiers of Environment, Energy and Bioscience (ICFEEB)., pp 101–106Google Scholar
  41. Standish RJ, Williams PA, Robertson AW, Scott NA, Hedderley DI (2004) Invasion by a perennial herb increases decomposition rate and alters nutrient availability in warm temperate lowland forest remnants. Biol Invasions 6:71–81View ArticleGoogle Scholar
  42. Steinlein T (2013) Invasive alien plants and their effects on native microbial soil communities. Prog Bot 74:293–319View ArticleGoogle Scholar
  43. Valéry L, Bouchard V, Lefeuvre JC (2004) Impact of the invasive native species Elymus athericus on carbon pools in a salt marsh. Wetlands 24:268–276View ArticleGoogle Scholar
  44. Van Der Putten WH, Klironomos JN, Wardle DA (2007) Microbial ecology of biological invasions. ISME J 1:28–37View ArticleGoogle Scholar
  45. Wardle DA, Bardgett RD, Klironomos JN (2004) Ecological linkages between aboveground and belowground biota. Science 304:692–1633View ArticleGoogle Scholar
  46. Wei D, Yang Q, Zhang JZ, Wang S, Chen XL, Zhang XL, Li WQ (2008) Bacterial community structure and diversity in a black soil as affected by long-term fertilization. Pedophere 18:582–592View ArticleGoogle Scholar
  47. Wolfe BE, Rodgers VL, Stinson KA, Pringle A (2008) The invasive plant Alliaria petiolata (garlic mustard) inhibits ectomycorrhizal fungi in its introduced range. J Ecol 96:777–783View ArticleGoogle Scholar
  48. Xiao QH, Zeng SQ (2005) Effect on regeneration pattern of secondary forest in Dalaoling forest farm to stand composition and fertility of forestry land. Hubei Forest Sci Technol 131:18–22 (in Chinese with English abstract)Google Scholar
  49. Xu QF, Jiang PK, Xu ZH (2008) Soil microbial functional diversity under intensively managed bamboo plantations in southern China. J Soils Sediment 8:177–183View ArticleGoogle Scholar
  50. Yang B, ZhuoY PXY, Xu HG, Li B (2010) Alien terrestrial herbs in China: diversity and ecological insights. Biodivers Sci 8:660–666 (in Chinese with English abstract)Google Scholar
  51. Yang X, Cao J, Dong MX, Ma XJ (2008) Effects of exotic Larix kaempferi on forest soil quality and bacterial diversity. Chin J Appl Ecol 19:2109–2116 (in Chinese with English abstract)Google Scholar
  52. Yeates GW, Williams PA (2001) Influence of three invasive weeds and site factors on soil microfauna in New Zealand. Pedobiologia 45:367–383View ArticleGoogle Scholar
  53. Zhang DH (2001) Influence of thinning on soil fertility in artificial forests. Chin J Appl Ecol 12:672–676 (in Chinese with English abstract)Google Scholar
  54. Zheng H, Ouyang ZY, Wang XK, Fang ZG, Zhao TQ, Miao H (2005) Effects of regenerating forest cover on soil microbial communities: a case study in hilly red soil region, southern China. Forest Ecol Manage 217:244–254View ArticleGoogle Scholar

Copyright

© Chen et al. 2015

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited.