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Parent materials have stronger effects than land use types on microbial biomass, activity and diversity in red soil in subtropical China
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Pedobiologia - Journal of Soil Ecology journal homepage: www.elsevier.de/pedobi
Parent materials have stronger effects than land use types on microbial biomass, activity and diversity in red soil in subtropical China Huan Deng a,b , Yong-Jie Yu a,b , Jin-E. Sun a,b , Jin-Bo Zhang a,b , Zu-Cong Cai a,b , Guang-Xia Guo c , Wen-Hui Zhong a,b,∗ a Jiangsu Provincial Key Laboratory of Materials Cycling and Pollution Control, School of Geography Science, Nanjing Normal University, Nanjing 210023, China b Jiangsu Center for Collaborative Innovation in Geographical Information Resource Development and Application, Nanjing 210023, China c Key Laboratory of Alpine Ecology and Biodiversity, Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing 100085, China
a r t i c l e
i n f o
Article history: Received 27 August 2014 Received in revised form 5 February 2015 Accepted 5 February 2015 Keywords: CLPP PLFA Redundancy analysis Soil texture
a b s t r a c t To examine the effect of parent materials and land use types on micro-organisms of red soil, we sampled soils from the combination of three land use types including coniferous forest, shrub and farmland, and three parent materials including granite, tertiary red sandstone and quaternary red earth. Soil microbial biomass and diversity was estimated using phospholipid fatty acids (PLFA) while microbial activity and functional diversity were determined using community level physiological profiles (CLPP) with Biolog® Eco-plates. In addition, a series of soil physicochemical properties were established. Results showed that parent materials explained a larger part of total variance of microbial biomass, activity and diversity than land use types, though both parent materials and land use types had a significant effect. The PLFA amount and microbial activity was highest in granite but lowest in quaternary red earth. Redundant analysis (RDA) showed that sand and clay content, which were determined by parent materials, significantly influenced both PLFAs and CLPP. Our study suggests that soil parent material may be a more important driver of soil microbial communities than land use type in the red soils of the region sampled here. Therefore, researchers should explicitly account for soil origin in studies seeking to understand the effects of land use on microbial community structure and function. © 2015 Elsevier GmbH. All rights reserved.
Introduction Red soil (Ultisols and Oxisols in US Soil Taxonomy), one of the typical subtropical soils, is widely distributed in southern China. The red soil region covers about two million km2 or 21% of China’s land area, and supports 40% of the nation’s population (Huang et al. 2012). However, mainly due to the wet climate and hilly landscape, red soils are heavily weathered and leached soils, and are characterized by low pH and deficiencies in available nutrients, particularly N and P (Zhong and Cai 2007). The nutrient limitation and acidic stress not only restrict the production of plants and crops, but also lead to relatively low microbial biomass, activity and diversity (Yin et al. 2014). The degradation of red soil has largely been due to
∗ Corresponding author at: School of Geography Science, Nanjing Normal University, Nanjing 210023, China. +86 25 85891352. E-mail address: [email protected] (W.-H. Zhong).
inappropriate practices such as deforestation (Zhang et al. 2010). As a result, it is urgent to find sustainable means to reduce red soil degradation and improve soil quality (Ma et al. 2014). Land use types have significant influence on red soil quality. Since soil micro-organisms play a crucial role in nutrient cycling and are sensitive to environmental change, microbial properties including microbial biomass, activity and diversity have been widely used as diagnostic indicators to evaluate the effect of land use types on soil quality (Bending et al. 2004). Deng et al. (2010) studied the effect of vegetative restoration on microbial biomass and diversity of degraded red soil. Ying et al. (2013) compared the effect of restoration, degradation (logging), cropland, and pine plantation on soil microbial community by using DNA- and PLFAbased methods. Yin et al. (2014) evaluated soil microbial functional diversity of degraded red soil restored with different vegetation types. In these studies, the effect of land use type was attributed to soil physicochemical properties, which however, were not solely determined by land use types.
http://dx.doi.org/10.1016/j.pedobi.2015.02.001 0031-4056/© 2015 Elsevier GmbH. All rights reserved.
Please cite this article in press as: Deng, H., et al., Parent materials have stronger effects than land use types on microbial biomass, activity and diversity in red soil in subtropical China. Pedobiologia - J. Soil Ecol. (2015), http://dx.doi.org/10.1016/j.pedobi.2015.02.001
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Parent materials largely affect the soil formation process and soil physicochemical properties (Miller and Donahue 1990) and have a dramatic influence on soil micro-organisms (Steven et al. 2013). In subtropical region of China, red soil is typically derived from quaternary red earth, tertiary red sandstone or granite (Zhao et al. 1988). Only a few studies have addressed the effect of parent materials on specific characteristics of red soil. Lou et al. (2004) studied CO2 emission from soil, which was derived from granite, tertiary red sandstone and quaternary red clay. Results exhibited an emission order of granite > tertiary red sandstone > quaternary red clay. Xu and Cai (2007) showed that red soil denitrification capacity was significantly affected by parent materials and land use types. However, denitrification is a specific function and carried out by only a small group of micro-organisms. Thus, our knowledge about the effect of parent materials on soil microbial community and their functions in red soil is still limited. The severe degradation and relatively low microbial activity in the red soil region have been attributed to the rainy climate, hilly landscape and inappropriate land use, yet the significance of parent materials is seldom studied and little understood. Comparisons between the effect of parent materials and other factors, e.g. land use types, would help understand its significance. Phospholipid fatty acids (PLFA) analysis has been widely accepted as a reliable method to evaluate the microbial community diversity and biomass (Deng et al. 2009). In addition, the relative amount of specific groups of micro-organisms can be addressed by their ‘signature’ PLFAs. Soil micro-organisms and their functions can be linked by community level physiological profile (CLPP), which was intensively employed to study soil microbial activity and functional diversity (Liu et al. 2010). Combining PLFA and CLPP methods was adequate to make an integrated evaluation of micro´ bial community (Chodak and Niklinska 2010). In this study, soil samples were collected from three land use types including coniferous forest, shrub and farmland derived from three parent materials including granite, tertiary red sandstone and quaternary red earth. To minimize the effect of climate and landscape on the study, the sampling sites were selected in a plain with similar annual average temperature and precipitation. Because there is one sampling area for each parent material, researchers may argue that this type of experiment has pseudoreplication. However, the nature of landscape-scale studies precludes replications in the way they are constructed in lab experimentation. Concerns about pseudoreplication in ecological studies may cause ‘unwarranted stigmatization of a reasonable way to test predictions referring to large-scale systems’ (Oksanen 2001). Therefore, some studies on large-scale ecosystem have been carried out with pseudoreplication when true replication is not available under natural condition (Chauvat et al. 2007). Consequently, our experimental strategy allowed us to distinguish between the effect of parent materials and land use types, though we are aware of the possible bias caused by pseudoreplication. We hypothesize that parent materials may have a more profound effect than land use types on microbial biomass, activity and diversity of red soil through soil physicochemical properties. By using CLPP and PLFA methods, we aimed to determine the effects of parent materials and land use types on integrated microbial properties including microbial biomass, activity, community diversity and functional diversity. Materials and methods Site description and soil sampling Sampling sites were located in Yingtan City (27◦ 52 –28◦ 17 N, 116◦ 56 –117◦ 30 E), Jiangxi Province, and a typical subtropical region of southern China (Fig. 1). The average annual temperature and precipitation of the city is 18.4 ◦ C and 1785 mm, respectively.
Granite, quaternary red earth and tertiary red sandstone derived soil were mainly located at N 28◦ 18 , E 117◦ 12 ; N 28◦ 13 , E 116◦ 49 and N 28◦ 4 , E 116◦ 48 , respectively. In sampling sites, the major land use types include natural secondary coniferous Pinus massoniana forest, shrub with diverse species dominated by Lespedaza bicolor and peanut (Arachis hypogaea) farmland that had been converted from bush forest that was clear-cut for at least thirty years. Soil sampling Three sites where soil was derived from granite (Gran), quaternary red earth (Earth) or tertiary red sandstone (Sand) were selected for soil sampling in May 2009. Each site covers an area of more than 12 km2 . The climate and landscape over the three sampling sites is nearly the same since the distance between sites is less than 51 km and the sites are located in a plain. The average annual temperature and precipitation between the three sites varied within 0.4 ◦ C and 100 mm. In each site, soil was sampled from three land use types including a natural secondary coniferous forest (Conif), a shrub and a peanut farmland (Farm). As a result, there are nine soil groups combining three parent materials and three land use types, namely, Gran-Conif, Gran-Shrub, Gran-Farm, Earth-Conif, Earth-Shrub, Earth-Farm, Sand-Conif, Sand-Shrub and Sand-Farm. In each site, three plots with slopes less than 10◦ and a distance of more than 200 m between plots were selected to represent a soil group. In each plot, surface soil samples (0–20 cm) at three randomly selected points (0.5 m × 0.5 m) were collected and mixed to represent the plot. Therefore, a total of 27 soil samples were collected. Soil samples were sieved through a 2 mm diameter mesh, and subsequently either stored at 4 ◦ C for less than two weeks before PLFA and CLPP measurements or air dried for physicochemical analysis. Prior to PLFA and CLPP analyses, the soil was adjusted to 50% of the maximum water holding capacity (WHC), which was determined using the gravimetric method (Allen 1989) and pre-incubated at room temperature for seven days. Soil physicochemical analysis Soil chemical properties were analyzed according to Lu (2000). Briefly, soil pH was established using a pH glass electrode at a soil water ratio of 1:2.5 (w/v). Soil organic C was determined by dichromate oxidation and total N by Kjeldahl digestion; hydrolysable N by alkali-hydrolyzed diffusing method; total P by alkali-meltingmolybdenum-blue method; available K by ammonium acetate extraction and atomic absorption spectrometry; soil total Al by atomic absorption spectrometry; cation exchange capacity (CEC) by saturation with ammonium acetate; soil texture by the sieve and pipette method. Community-level physiological profiles (CLPP) CLPPs of soil microbial communities were assessed by using BIOLOG Eco-plates (Biolog Inc., Hayward, CA) according to Garland (1997). Ten grams of fresh soil samples was suspended in 100 ml of sterile phosphate buffer (0.05 M, pH 7.0) and shaken for 30 min. One milliliter of the soil suspension was then diluted tenfold in sterile phosphate buffer (0.05 M, pH 7.0). Subsequently, 150 l of this dilution was added to each well of an Eco-plate. Plates were incubated at 25 ◦ C and measured at 590 nm using an Emax precision micro plate reader (Biolog Inc., Hayward, CA) every 12 h for one week. Phospholipid fatty acid (PLFA) analysis Soil microbial PLFA was determined with a modified BlighDyer method (Bligh and Dyer 1959; Deng et al. 2009).
Please cite this article in press as: Deng, H., et al., Parent materials have stronger effects than land use types on microbial biomass, activity and diversity in red soil in subtropical China. Pedobiologia - J. Soil Ecol. (2015), http://dx.doi.org/10.1016/j.pedobi.2015.02.001
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Fig. 1. Geographic location and land use situation of the study sites. (A–C) represent typical parent materials of quaternary red earth, tertiary red sandstone, and granite, respectively. Three main land use types of coniferous forest, shrub and peanut farmland were selected in sites A, B and C.
Briefly, each soil sample (2 g of dry weight) was extracted using 15 ml Bligh & Dyer extracting solution (0.1 M citric acid buffer:chloroform:methanol = 0.8:1:2). The extract was separated with chloroform, acetone and methanol on a silica solid phase extraction column. Phospholipids were dried with nitrogen gas, then hydrolyzed and saponified with alkaline methanol to generate phospholipid fatty acid methyl esters, which were measured with the MIDI Sherlock Microbial Identification System (MIDI Inc., Newark, DE). Concentrations of individual PLFAs was calculated based on the internal standard 19:0 FAME. A total of 58 PLFA biomarkers were classified into bacteria and fungi. Bacteria were further classified into gram-positive bacteria (G+ ) and gramnegative bacteria (G− ). The fatty acids 18:36c and 18:19c were used as biomarkers of fungi. The straight and branched chain fatty acids were used as biomarkers of G+ specific fatty acids, e.g. i14:0, a15:0. Cyclopropane, saturated and mono-unsaturated fatty acids were used as biomarkers of G− specific fatty acids, e.g. 10:0, 16:1 2OH, cy17:0 (Zelles et al. 1995).
2012). A two-way ANOVA followed with Tukey’s post hoc tests at a significance level of P < 0.05 to determine significant effects of parent materials and land use types as well as interactions of these factors. The ANOVA also evaluated the percentage of total variance explained by land use types and parent materials by calculating the proportion of mean square of a factor in the sum of mean square. All statistical analysis except for RDA was conducted using the SPSS 16.0 (SPSS Inc., Chicago, IL). RDA was conducted using CANOCO 5.0 (Microcomputer Power, Ithaca, NY) to determine the effect of soil physicochemical properties on PLFA and CLPP. In RDA, significant environmental variables (P < 0.05) were selected using a forward selection followed by a Monte Carlo permutation test based on 999 random permutations. Variables displaying an inflation factor greater than 20 were excluded from RDA analyses (Sapp et al. 2007). A total of 38 PLFAs and 31 carbon sources were included in the RDA, but for clarity only the PLFAs or carbon sources with high component scores (>0.6) for the first two ordination axes were displayed.
Statistics
Results
The BIOLOG data after 72 h incubation with 0.6 average well color development (AWCD) were analyzed as the follows (Garland and Mills 1991; Zak et al. 1994): (1) average well color development (AWCD); (2) Shannon index (H ); and (3) redundancy analysis (RDA). PLFA data were also subject to H and RDA (Wang and Tam
Soil physicochemical properties Two-way ANOVA showed that the factor of soil parent material had a significant effect on soil physicochemical properties except for available K, total Al, silt and CEC (Table 1). Quaternary red earth
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Table 1 Two-way ANOVA of soil physicochemical properties including organic carbon (OC), total nitrogen (TN), total phosphorus (TP), hydrolysable nitrogen (HN), available potassium (AK), total aluminum (Al), clay, silt and sand content and cation exchange capacity (CEC). Variables
DF
OC (g kg−1 )
TN (g kg−1 )
TP (g kg−1 )
HN (g kg−1 )
AK (g kg−1 )
Al (g kg−1 )
pH
Clay (%)
Silt (%)
Sand (%)
CEC (mol kg−1 )
Post hoc tests Granite Quaternary red earth Tertiary red sandstone
– – –
48.13a 20.43b 46.64a
1.78a 0.97b 1.59a
0.52a 0.33b 0.51a
0.18a 0.10b 0.16a
0.12a 0.08a 0.10a
1.72a 1.88a 1.58a
4.70a 4.64a 4.38b
10.39b 20.71a 14.16b
23.96b 65.64a 31.67a 47.62b 28.89ab 56.94ab
9.67a 11.68a 9.15a
Coniferous forest Shrub Peanut farmland
– – –
47.36a 50.51a 17.33b
1.61a 1.82a 0.91b
0.52a 0.37a 0.47a
0.15a 0.19a 0.09b
0.08a 0.10a 0.12a
2.19a 1.80ab 1.19b
4.44b 4.51b 4.77a
16.33a 15.92a 13.01a
29.06a 28.33a 27.14a
54.61a 55.75a 59.86a
10.10a 10.30a 10.09a
F value Parent material (P) Land use type (L) P×L
2 2 4
28.7*** 39.6*** 5.4**
17.3*** 21.7*** 4.2*
6.3** 2.9 20.0
6.4** 11.3** 2.4
1.7 2.4 6.6**
0.5 5.2* 0.7
10.5** 11.0** 7.2**
15.5*** 1.9 0.9
4.0* 0.2 1.0
8.8** 0.8 0.9
1.4 0.01 1.0
33% 45% 12% 10%
30% 39% 15% 16%
11% 1% 72% 16%
21% 36% 14% 29%
23% 24% 33% 20%
55% 7% 6% 32%
% of total variance P L P×L Error
2 2 4 18
11% 11% 44% 34%
3% 32% 8% 56%
26% 2% 13% 59%
43% 4% 9% 44%
11% – 17% 72%
In post hoc tests, means (n = 3) followed by same letter indicate no significant difference between three parental materials or between three land use types. * P < 0.05. ** P < 0.01. *** P < 0.001.
had more clay but lower carbon, nitrogen and phosphorus content than the other two parent materials, regardless of the land use types. The factor of land use type was only significant for chemical properties including organic C, total N, hydrolysable N, total Al and pH. Farmland had lower carbon, nitrogen and Al content than coniferous forest and shrub. There were strong interactions between parent materials and land use types for organic C, total N, available K and pH. Parent material explained a much larger part of the total variance of clay, silt and sand content and CEC than land use type. Soil microbial properties Two-way ANOVA showed that the factor of parent material had a significant effect on all the microbial properties (Table 2). Granite was the most while quaternary red earth the least abundant in AWCD, total PLFA, bacterial and fungal PLFA, G+ and G− PLFA, and H of PLFA and CLPP. The factor of land use type was significant for microbial properties except for fungi to bacteria ratio, G+ to G− ratio and H of PLFA. Parent material explained a much larger part of the total variance of microbial biomass, activity and diversity than land use type. RDA of PLFA and CLPP data RDA was applied to reveal the correlations between soil physicochemical properties and PLFA and CLPP data (Figs. 2 and 3). For PLFA data, the first two components of the RDA explained 24.1% and 20.6% of the total variance, respectively. Significant factors (P < 0.05) were organic C, hydrolysable N, pH, clay, sand and available K. Together, they explained 60.1% of the variation of PLFA profile (Fig. 2a). Soil pH and clay content dominated the first and second component of RDA, respectively. Separation along the first component was mainly related to land use types while that along the second component was mainly related to parental materials. Soil pH was the highest in farmland soil but lowest in coniferous soil. Clay content prevailed under quaternary red earth. PLFAs (Fig. 2b) were highly correlated with clay (i16:0, i17:0, 16:1 2OH), pH (a15:0, 17:0 2OH, 14:0 3OH, i15:1 G, 10:0, i14:0, i17:0 3OH), available K (16:15c), organic C and hydrolysable N (15:0 3OH, 18:15c, i15:0, 18:1 2OH, 16:0 2OH).
For CLPP data, the first two components of the RDA explained 23.2% and 6.2% of the total variance, respectively. Significant factors (P < 0.05) were total P, sand, silt, pH, clay and available K, and they, together, explained 55.3% of the total variation (Fig. 3a). All of the significant factors dominated the first component of RDA. Separation along the first component was mainly related to soil group, i.e. between Gran-Conif, Gran-Shrub and GranFarm, and also between parent materials within coniferous forest and shrub. Carbon sources that highly correlated with clay were l-asparagine (amino acids) and d,l-␣-glycerolphosphate (carbohydrates), with silt it was l-serine (amino acids), with available K-glucose-1-phosphate (carbohydrates), with sand-d-xylose (carbohydrates), with pH the carbon sources were ␣-cyclodextrin (polymers), glycogen (polymers), d-cellobiose (carbohydrates), ␣d-lactose (carbohydrates), -methyl-d-glucoside (carbohydrates), and with total P they were l-arginine (amino acids) and d-mannitol (carbohydrates) (Fig. 3b). Discussion Soil physicochemical properties Parent material, which had a decisive effect on soil texture (Nosrati et al. 2011) explained a much larger percentage of the variance in clay, silt and sand content than land use type in the present study. For organic C, total N and hydrolysable N content, land use type explained more variance than parent material, indicating that these soil chemical properties were mainly affected by land use type. The strong interactions between land use type and parent material suggest that the trend of soil chemical properties between parent materials varied with land use types. Organic C and total N of coniferous forest and shrub were lower in quaternary red earth than the other parent materials. In this study, granite and tertiary red sandstone lead to coarse-textured soil while quaternary red earth resulted in fine-textured soil, which is similar to previous studies (Hu et al. 2003). Coarse-textured soil may be favorable for plant growth and accumulation of organic matter due to its good drainage and aeration. Within each parent material, organic C, total N and hydrolysable N were generally lower while total P and available K were higher in farmland than coniferous forest and shrub. The difference between land use types could be attributed to the carbon accumulation in coniferous forest and shrub, and carbon
Please cite this article in press as: Deng, H., et al., Parent materials have stronger effects than land use types on microbial biomass, activity and diversity in red soil in subtropical China. Pedobiologia - J. Soil Ecol. (2015), http://dx.doi.org/10.1016/j.pedobi.2015.02.001
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a
clay (9.0%) TP (11.0%)
AXIS-2 20.6%
AXIS-2 6.2%
sand (9.7%) pH (9.2%)
AK (7.4%) clay (8.4%)
-0.6
pH (11.2%) AK (7.2%) sand (8.0%)
silt (9.6%)
-1.0
1.0
AXIS-1 23.2%
-1.0
1.0
AXIS-1 24.1%
0.6
-1.0
HN (11.2%) OC (13.5%)
b sand
TP c3
0.8
c20
c13
c16 16:1 2OH
b
i17:0
c24
pH c28
18:0
clay
c5
c1
18:1ω9c 16:0 N alcohol
i16:0
AK 16:0
c25
c7
c29
clay c15
14:0 i18:0 17:0 2OH i14:0 3OH 15:0 3OH
-0.8
18:1ω5c 18:1 2OH 16:0 2OH
-0.8
OC
c8 a15:0 i15:1G
HN
16:1ω5c
AK
i14:0 10:0 pH i17:0 3OH
sand
i15:0
-0.8
0.8
Fig. 2. Redundancy analysis of the soil physicochemical properties with PLFA data. (a) Correlation between samples and soil physicochemical properties. Each sample combines a land use type: coniferous forest (tri-angle), shrub (square) or peanut farmland (circle), and a parent material: granite (gray), tertiary red sandstone (hollow) or quaternary red earth (dark). (b) Correlation between soil physicochemical properties and PLFAs that have high absolute scores (>0.6) on each of the first two axes.
removal in farmland, the presence of L. bicolor which is an N-fixing plant in shrub, and the application of P and K fertilizer in farmland. The lower soil Al content in farmland may be due to plant uptake and harvest. Soil microbial properties The present study was a general assessment of the effect of land use types and parent materials on a series of microbial properties, including soil microbial biomass, activity, microbial diversity and functional diversity. The results clearly showed that the parent material factor explained most of the total variance in microbial biomass, activity and diversity, suggesting that this factor may have a more profound effect on soil micro-organisms than land use type. Granite had greater microbial biomass, activity and diversity than the other parent materials. The significant differences between land use types mainly existed within granite and tertiary
c14
silt
-0.8
10-me 17:0
0.8
3 Fig. 3. Redundancy analysis of the soil physicochemical properties with CLPP data after 72 h incubation. (a) Correlation between samples and soil physicochemical properties. Each sample combines a land use type: coniferous forest (tri-angle), shrub (square) or peanut farmland (circle), and a parent material: granite (gray), tertiary red sandstone (hollow) or quaternary red earth (dark). (b) Correlation between soil physicochemical properties and carbon sources that have high absolute scores (>0.6) on each of the first two axes. c1: -methyl-d-glucoside; c3: l-arginine; c5: d-xylose; c7: l-asparagine; c8: Tween; c13: d-mannitol; c14: 4-hydroxybenzoic acid; c15: l-serine; c16: ␣-cyclodextrin; c20: glycogen; c24: d-cellobiose; c28: ␣d-lactose.
red sandstone, where the microbial properties of farmland were significantly lower than those of shrub. However, considering there was only one sampling site, although with replicates, for each parent material in the study site, we should be cautious about interpreting the effect of parent materials since there may be other soil properties that vary in the different locations that drive at least part of these responses but were not measured. In most studies, microbial biomass, activity, diversity and functional diversity were higher in forest than farmland since agricultural practices such as tillage, removal of litters and the application of fertilizers exert stress on micro-organisms (Zhao et al. 2012). The soils under shrub and coniferous forest also differed because of the variable quality and quantity of carbon input (Deng et al. 2010). In quaternary red earth there was no significant difference between land use types for PLFA data, indicating that the effect of land use type on soil micro-organisms varied between parent materials. This was also confirmed by the significant interaction between parent materials and land use types. Previous studies showed variation of specific PLFAs between land use types, especially the proportion of G− bacteria and the
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Table 2 Two-way ANOVA of soil microbial properties including average well color development (AWCD), total, bacterial and fungal PLFA, the ratio of fungal to bacterial PLFA (Fungi/Bacteria), gram positive (G+ ) and gram negative (G− ) PLFA, the ratio of G+ to G− PLFA (G+ /G− ), Shannon index (H ) of PLFA and CLPP data. G+ /G−
H of PLFA
H of CLPP
0.72a 0.39c
30.43a 11.68c
22.15a 8.35c
3.96a 1.99c
0.18b 0.24a
8.76a 3.13c
13.39a 5.22c
0.64b 0.61b
2.71a 2.46b
3.17a 2.80c
–
0.54b
19.47b
13.48b
2.75b
0.21b
5.56b
7.92b
0.72a
2.60a
3.03b
Coniferous forest Shrub Peanut farmland
– – –
0.42b 0.65a 0.59a
21.48a 25.52a 14.57b
15.51a 18.02a 10.44b
3.10a 3.45a 2.14b
0.21a 0.21a 0.21a
6.10a 7.26a 4.09b
9.42a 10.76a 6.36b
0.65a 0.66a 0.66a
2.59a 2.61a 2.58a
2.85b 3.12a 3.04a
F value Parent material (P) Land use type (L) P×L
2 2 4
40.9*** 20.1*** 6.3**
38.2*** 13.2*** 5.7**
39.1*** 12.0*** 6.6**
25.6*** 11.9** 6.1**
10.8** 0.3 0.26
47.0*** 15.3*** 9.9***
33.0*** 9.7** 5.0*
7.9** 0.1 4.2*
10.90** 0.19 0.53
41.53*** 21.50*** 6.29**
49% 25% 16% 10%
53% 18% 16% 13%
53% 16% 18% 13%
44% 20% 21% 15%
53% 3% 3% 41%
52% 17% 22% 10%
54% 16% 16% 14%
52% 2% 5% 41%
49% 26% 15% 10%
Post hoc tests Granite Quaternary red earth Tertiary red sandstone
% of total variance P L P×L Error
AWCD
– –
2 2 4 18
Fungi/bacteria
G− PLFA (g g−1 )
Bacterial PLFA (g g−1 )
DF
Fungal PLFA (g g−1 )
G+ PLFA (g g−1 )
Total PLFA (g g−1 )
Variables
28% 1% 39% 32%
In post hoc tests, means (n = 3) followed by same letter indicate no significant difference between three parental materials or between three land use types. * P < 0.05. ** P < 0.01. *** P < 0.001.
fungi/bacteria ratio, which were considered indicators of land use change. However, the G− /G+ ratio was also found unchanged between land use types (McKinley et al. 2005). In our study, no change in this ratio was observed among land use types. The RDA of the PLFA profiles of the land use types clearly showed that the profiles were closely related to the variation in organic C and nitrogen content. Along with OC and HN, both G+ (i15:0, 15:0 3OH, 16:0 2OH, 10-me 17:0) and G− (18:15c, 18:1 2OH) bacteria shifted rather than G-bacteria alone. Moreover, only G+ bacteria changed in the opposite direction of OC and HN (14:0, 16:0, 18:0, 16:0 N alcohol). The G+ bacteria could survive better in resource-limited environment (Gartzia-Bengoetxea et al. 2009) and they may also indicate land use change. The fungi to bacteria ratio varied among parent materials rather than land use type. It has been suggested that land use change does not inevitably alter fungi to bacteria ratio (Lauber et al. 2008). In our study, the reason could be that the difference among land use types was masked by parent materials. The RDA exhibited that organic C and nitrogen content and soil texture have strong association with PLFA profiles. Moreover, it was not surprising that soil organic carbon and nutrient content changed with land use type (Vaccari et al. 2012). Soil texture, however, was determined by parent material (Nosrati et al. 2011) and had a decisive effect on DNA-based bacterial community composition (Johnson et al. 2003). In our study, it is worth noting that although significant physicochemical properties varied between the plot of PLFA profiles and that of CLPP, soil texture was significant for both plots. Our results indicate that soil texture is a major driver of micro-organisms and their functions.
Conclusion The study clearly showed that both land use type and parent material have significant effect on soil microbial biomass, activity and diversity, though parent material explained a larger part of the variance than land use type, thus predominating. In general, granite and shrub had greater soil microbial biomass, activity and diversity than quaternary red earth and farmland, respectively. Nevertheless, we cannot exclude that the results are partly biased by pseudoreplication of parental materials and thus, the data should be interpreted
with caution. We suggest that it is the interaction between parent material and land use type that contributes to red soil degradation rather than only inappropriate land use type. Our result provides some input for land use planning in the red soil region. To preserve soil quality, a reasonable collocation of parent materials and land use type should be considered.
Acknowledgments This work was supported by grants from National Natural Science Foundation of China (41271255), Major Program of Natural Science Research of Jiangsu Higher Education Institutions (12KJA170001), and the Priority Academic Program Development of Jiangsu Higher Education Institutions.
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Pedobiologia - Journal of Soil Ecology journal homepage: www.elsevier.de/pedobi
Parent materials have stronger effects than land use types on microbial biomass, activity and diversity in red soil in subtropical China Huan Deng a,b , Yong-Jie Yu a,b , Jin-E. Sun a,b , Jin-Bo Zhang a,b , Zu-Cong Cai a,b , Guang-Xia Guo c , Wen-Hui Zhong a,b,∗ a Jiangsu Provincial Key Laboratory of Materials Cycling and Pollution Control, School of Geography Science, Nanjing Normal University, Nanjing 210023, China b Jiangsu Center for Collaborative Innovation in Geographical Information Resource Development and Application, Nanjing 210023, China c Key Laboratory of Alpine Ecology and Biodiversity, Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing 100085, China
a r t i c l e
i n f o
Article history: Received 27 August 2014 Received in revised form 5 February 2015 Accepted 5 February 2015 Keywords: CLPP PLFA Redundancy analysis Soil texture
a b s t r a c t To examine the effect of parent materials and land use types on micro-organisms of red soil, we sampled soils from the combination of three land use types including coniferous forest, shrub and farmland, and three parent materials including granite, tertiary red sandstone and quaternary red earth. Soil microbial biomass and diversity was estimated using phospholipid fatty acids (PLFA) while microbial activity and functional diversity were determined using community level physiological profiles (CLPP) with Biolog® Eco-plates. In addition, a series of soil physicochemical properties were established. Results showed that parent materials explained a larger part of total variance of microbial biomass, activity and diversity than land use types, though both parent materials and land use types had a significant effect. The PLFA amount and microbial activity was highest in granite but lowest in quaternary red earth. Redundant analysis (RDA) showed that sand and clay content, which were determined by parent materials, significantly influenced both PLFAs and CLPP. Our study suggests that soil parent material may be a more important driver of soil microbial communities than land use type in the red soils of the region sampled here. Therefore, researchers should explicitly account for soil origin in studies seeking to understand the effects of land use on microbial community structure and function. © 2015 Elsevier GmbH. All rights reserved.
Introduction Red soil (Ultisols and Oxisols in US Soil Taxonomy), one of the typical subtropical soils, is widely distributed in southern China. The red soil region covers about two million km2 or 21% of China’s land area, and supports 40% of the nation’s population (Huang et al. 2012). However, mainly due to the wet climate and hilly landscape, red soils are heavily weathered and leached soils, and are characterized by low pH and deficiencies in available nutrients, particularly N and P (Zhong and Cai 2007). The nutrient limitation and acidic stress not only restrict the production of plants and crops, but also lead to relatively low microbial biomass, activity and diversity (Yin et al. 2014). The degradation of red soil has largely been due to
∗ Corresponding author at: School of Geography Science, Nanjing Normal University, Nanjing 210023, China. +86 25 85891352. E-mail address: [email protected] (W.-H. Zhong).
inappropriate practices such as deforestation (Zhang et al. 2010). As a result, it is urgent to find sustainable means to reduce red soil degradation and improve soil quality (Ma et al. 2014). Land use types have significant influence on red soil quality. Since soil micro-organisms play a crucial role in nutrient cycling and are sensitive to environmental change, microbial properties including microbial biomass, activity and diversity have been widely used as diagnostic indicators to evaluate the effect of land use types on soil quality (Bending et al. 2004). Deng et al. (2010) studied the effect of vegetative restoration on microbial biomass and diversity of degraded red soil. Ying et al. (2013) compared the effect of restoration, degradation (logging), cropland, and pine plantation on soil microbial community by using DNA- and PLFAbased methods. Yin et al. (2014) evaluated soil microbial functional diversity of degraded red soil restored with different vegetation types. In these studies, the effect of land use type was attributed to soil physicochemical properties, which however, were not solely determined by land use types.
http://dx.doi.org/10.1016/j.pedobi.2015.02.001 0031-4056/© 2015 Elsevier GmbH. All rights reserved.
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Parent materials largely affect the soil formation process and soil physicochemical properties (Miller and Donahue 1990) and have a dramatic influence on soil micro-organisms (Steven et al. 2013). In subtropical region of China, red soil is typically derived from quaternary red earth, tertiary red sandstone or granite (Zhao et al. 1988). Only a few studies have addressed the effect of parent materials on specific characteristics of red soil. Lou et al. (2004) studied CO2 emission from soil, which was derived from granite, tertiary red sandstone and quaternary red clay. Results exhibited an emission order of granite > tertiary red sandstone > quaternary red clay. Xu and Cai (2007) showed that red soil denitrification capacity was significantly affected by parent materials and land use types. However, denitrification is a specific function and carried out by only a small group of micro-organisms. Thus, our knowledge about the effect of parent materials on soil microbial community and their functions in red soil is still limited. The severe degradation and relatively low microbial activity in the red soil region have been attributed to the rainy climate, hilly landscape and inappropriate land use, yet the significance of parent materials is seldom studied and little understood. Comparisons between the effect of parent materials and other factors, e.g. land use types, would help understand its significance. Phospholipid fatty acids (PLFA) analysis has been widely accepted as a reliable method to evaluate the microbial community diversity and biomass (Deng et al. 2009). In addition, the relative amount of specific groups of micro-organisms can be addressed by their ‘signature’ PLFAs. Soil micro-organisms and their functions can be linked by community level physiological profile (CLPP), which was intensively employed to study soil microbial activity and functional diversity (Liu et al. 2010). Combining PLFA and CLPP methods was adequate to make an integrated evaluation of micro´ bial community (Chodak and Niklinska 2010). In this study, soil samples were collected from three land use types including coniferous forest, shrub and farmland derived from three parent materials including granite, tertiary red sandstone and quaternary red earth. To minimize the effect of climate and landscape on the study, the sampling sites were selected in a plain with similar annual average temperature and precipitation. Because there is one sampling area for each parent material, researchers may argue that this type of experiment has pseudoreplication. However, the nature of landscape-scale studies precludes replications in the way they are constructed in lab experimentation. Concerns about pseudoreplication in ecological studies may cause ‘unwarranted stigmatization of a reasonable way to test predictions referring to large-scale systems’ (Oksanen 2001). Therefore, some studies on large-scale ecosystem have been carried out with pseudoreplication when true replication is not available under natural condition (Chauvat et al. 2007). Consequently, our experimental strategy allowed us to distinguish between the effect of parent materials and land use types, though we are aware of the possible bias caused by pseudoreplication. We hypothesize that parent materials may have a more profound effect than land use types on microbial biomass, activity and diversity of red soil through soil physicochemical properties. By using CLPP and PLFA methods, we aimed to determine the effects of parent materials and land use types on integrated microbial properties including microbial biomass, activity, community diversity and functional diversity. Materials and methods Site description and soil sampling Sampling sites were located in Yingtan City (27◦ 52 –28◦ 17 N, 116◦ 56 –117◦ 30 E), Jiangxi Province, and a typical subtropical region of southern China (Fig. 1). The average annual temperature and precipitation of the city is 18.4 ◦ C and 1785 mm, respectively.
Granite, quaternary red earth and tertiary red sandstone derived soil were mainly located at N 28◦ 18 , E 117◦ 12 ; N 28◦ 13 , E 116◦ 49 and N 28◦ 4 , E 116◦ 48 , respectively. In sampling sites, the major land use types include natural secondary coniferous Pinus massoniana forest, shrub with diverse species dominated by Lespedaza bicolor and peanut (Arachis hypogaea) farmland that had been converted from bush forest that was clear-cut for at least thirty years. Soil sampling Three sites where soil was derived from granite (Gran), quaternary red earth (Earth) or tertiary red sandstone (Sand) were selected for soil sampling in May 2009. Each site covers an area of more than 12 km2 . The climate and landscape over the three sampling sites is nearly the same since the distance between sites is less than 51 km and the sites are located in a plain. The average annual temperature and precipitation between the three sites varied within 0.4 ◦ C and 100 mm. In each site, soil was sampled from three land use types including a natural secondary coniferous forest (Conif), a shrub and a peanut farmland (Farm). As a result, there are nine soil groups combining three parent materials and three land use types, namely, Gran-Conif, Gran-Shrub, Gran-Farm, Earth-Conif, Earth-Shrub, Earth-Farm, Sand-Conif, Sand-Shrub and Sand-Farm. In each site, three plots with slopes less than 10◦ and a distance of more than 200 m between plots were selected to represent a soil group. In each plot, surface soil samples (0–20 cm) at three randomly selected points (0.5 m × 0.5 m) were collected and mixed to represent the plot. Therefore, a total of 27 soil samples were collected. Soil samples were sieved through a 2 mm diameter mesh, and subsequently either stored at 4 ◦ C for less than two weeks before PLFA and CLPP measurements or air dried for physicochemical analysis. Prior to PLFA and CLPP analyses, the soil was adjusted to 50% of the maximum water holding capacity (WHC), which was determined using the gravimetric method (Allen 1989) and pre-incubated at room temperature for seven days. Soil physicochemical analysis Soil chemical properties were analyzed according to Lu (2000). Briefly, soil pH was established using a pH glass electrode at a soil water ratio of 1:2.5 (w/v). Soil organic C was determined by dichromate oxidation and total N by Kjeldahl digestion; hydrolysable N by alkali-hydrolyzed diffusing method; total P by alkali-meltingmolybdenum-blue method; available K by ammonium acetate extraction and atomic absorption spectrometry; soil total Al by atomic absorption spectrometry; cation exchange capacity (CEC) by saturation with ammonium acetate; soil texture by the sieve and pipette method. Community-level physiological profiles (CLPP) CLPPs of soil microbial communities were assessed by using BIOLOG Eco-plates (Biolog Inc., Hayward, CA) according to Garland (1997). Ten grams of fresh soil samples was suspended in 100 ml of sterile phosphate buffer (0.05 M, pH 7.0) and shaken for 30 min. One milliliter of the soil suspension was then diluted tenfold in sterile phosphate buffer (0.05 M, pH 7.0). Subsequently, 150 l of this dilution was added to each well of an Eco-plate. Plates were incubated at 25 ◦ C and measured at 590 nm using an Emax precision micro plate reader (Biolog Inc., Hayward, CA) every 12 h for one week. Phospholipid fatty acid (PLFA) analysis Soil microbial PLFA was determined with a modified BlighDyer method (Bligh and Dyer 1959; Deng et al. 2009).
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Fig. 1. Geographic location and land use situation of the study sites. (A–C) represent typical parent materials of quaternary red earth, tertiary red sandstone, and granite, respectively. Three main land use types of coniferous forest, shrub and peanut farmland were selected in sites A, B and C.
Briefly, each soil sample (2 g of dry weight) was extracted using 15 ml Bligh & Dyer extracting solution (0.1 M citric acid buffer:chloroform:methanol = 0.8:1:2). The extract was separated with chloroform, acetone and methanol on a silica solid phase extraction column. Phospholipids were dried with nitrogen gas, then hydrolyzed and saponified with alkaline methanol to generate phospholipid fatty acid methyl esters, which were measured with the MIDI Sherlock Microbial Identification System (MIDI Inc., Newark, DE). Concentrations of individual PLFAs was calculated based on the internal standard 19:0 FAME. A total of 58 PLFA biomarkers were classified into bacteria and fungi. Bacteria were further classified into gram-positive bacteria (G+ ) and gramnegative bacteria (G− ). The fatty acids 18:36c and 18:19c were used as biomarkers of fungi. The straight and branched chain fatty acids were used as biomarkers of G+ specific fatty acids, e.g. i14:0, a15:0. Cyclopropane, saturated and mono-unsaturated fatty acids were used as biomarkers of G− specific fatty acids, e.g. 10:0, 16:1 2OH, cy17:0 (Zelles et al. 1995).
2012). A two-way ANOVA followed with Tukey’s post hoc tests at a significance level of P < 0.05 to determine significant effects of parent materials and land use types as well as interactions of these factors. The ANOVA also evaluated the percentage of total variance explained by land use types and parent materials by calculating the proportion of mean square of a factor in the sum of mean square. All statistical analysis except for RDA was conducted using the SPSS 16.0 (SPSS Inc., Chicago, IL). RDA was conducted using CANOCO 5.0 (Microcomputer Power, Ithaca, NY) to determine the effect of soil physicochemical properties on PLFA and CLPP. In RDA, significant environmental variables (P < 0.05) were selected using a forward selection followed by a Monte Carlo permutation test based on 999 random permutations. Variables displaying an inflation factor greater than 20 were excluded from RDA analyses (Sapp et al. 2007). A total of 38 PLFAs and 31 carbon sources were included in the RDA, but for clarity only the PLFAs or carbon sources with high component scores (>0.6) for the first two ordination axes were displayed.
Statistics
Results
The BIOLOG data after 72 h incubation with 0.6 average well color development (AWCD) were analyzed as the follows (Garland and Mills 1991; Zak et al. 1994): (1) average well color development (AWCD); (2) Shannon index (H ); and (3) redundancy analysis (RDA). PLFA data were also subject to H and RDA (Wang and Tam
Soil physicochemical properties Two-way ANOVA showed that the factor of soil parent material had a significant effect on soil physicochemical properties except for available K, total Al, silt and CEC (Table 1). Quaternary red earth
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Table 1 Two-way ANOVA of soil physicochemical properties including organic carbon (OC), total nitrogen (TN), total phosphorus (TP), hydrolysable nitrogen (HN), available potassium (AK), total aluminum (Al), clay, silt and sand content and cation exchange capacity (CEC). Variables
DF
OC (g kg−1 )
TN (g kg−1 )
TP (g kg−1 )
HN (g kg−1 )
AK (g kg−1 )
Al (g kg−1 )
pH
Clay (%)
Silt (%)
Sand (%)
CEC (mol kg−1 )
Post hoc tests Granite Quaternary red earth Tertiary red sandstone
– – –
48.13a 20.43b 46.64a
1.78a 0.97b 1.59a
0.52a 0.33b 0.51a
0.18a 0.10b 0.16a
0.12a 0.08a 0.10a
1.72a 1.88a 1.58a
4.70a 4.64a 4.38b
10.39b 20.71a 14.16b
23.96b 65.64a 31.67a 47.62b 28.89ab 56.94ab
9.67a 11.68a 9.15a
Coniferous forest Shrub Peanut farmland
– – –
47.36a 50.51a 17.33b
1.61a 1.82a 0.91b
0.52a 0.37a 0.47a
0.15a 0.19a 0.09b
0.08a 0.10a 0.12a
2.19a 1.80ab 1.19b
4.44b 4.51b 4.77a
16.33a 15.92a 13.01a
29.06a 28.33a 27.14a
54.61a 55.75a 59.86a
10.10a 10.30a 10.09a
F value Parent material (P) Land use type (L) P×L
2 2 4
28.7*** 39.6*** 5.4**
17.3*** 21.7*** 4.2*
6.3** 2.9 20.0
6.4** 11.3** 2.4
1.7 2.4 6.6**
0.5 5.2* 0.7
10.5** 11.0** 7.2**
15.5*** 1.9 0.9
4.0* 0.2 1.0
8.8** 0.8 0.9
1.4 0.01 1.0
33% 45% 12% 10%
30% 39% 15% 16%
11% 1% 72% 16%
21% 36% 14% 29%
23% 24% 33% 20%
55% 7% 6% 32%
% of total variance P L P×L Error
2 2 4 18
11% 11% 44% 34%
3% 32% 8% 56%
26% 2% 13% 59%
43% 4% 9% 44%
11% – 17% 72%
In post hoc tests, means (n = 3) followed by same letter indicate no significant difference between three parental materials or between three land use types. * P < 0.05. ** P < 0.01. *** P < 0.001.
had more clay but lower carbon, nitrogen and phosphorus content than the other two parent materials, regardless of the land use types. The factor of land use type was only significant for chemical properties including organic C, total N, hydrolysable N, total Al and pH. Farmland had lower carbon, nitrogen and Al content than coniferous forest and shrub. There were strong interactions between parent materials and land use types for organic C, total N, available K and pH. Parent material explained a much larger part of the total variance of clay, silt and sand content and CEC than land use type. Soil microbial properties Two-way ANOVA showed that the factor of parent material had a significant effect on all the microbial properties (Table 2). Granite was the most while quaternary red earth the least abundant in AWCD, total PLFA, bacterial and fungal PLFA, G+ and G− PLFA, and H of PLFA and CLPP. The factor of land use type was significant for microbial properties except for fungi to bacteria ratio, G+ to G− ratio and H of PLFA. Parent material explained a much larger part of the total variance of microbial biomass, activity and diversity than land use type. RDA of PLFA and CLPP data RDA was applied to reveal the correlations between soil physicochemical properties and PLFA and CLPP data (Figs. 2 and 3). For PLFA data, the first two components of the RDA explained 24.1% and 20.6% of the total variance, respectively. Significant factors (P < 0.05) were organic C, hydrolysable N, pH, clay, sand and available K. Together, they explained 60.1% of the variation of PLFA profile (Fig. 2a). Soil pH and clay content dominated the first and second component of RDA, respectively. Separation along the first component was mainly related to land use types while that along the second component was mainly related to parental materials. Soil pH was the highest in farmland soil but lowest in coniferous soil. Clay content prevailed under quaternary red earth. PLFAs (Fig. 2b) were highly correlated with clay (i16:0, i17:0, 16:1 2OH), pH (a15:0, 17:0 2OH, 14:0 3OH, i15:1 G, 10:0, i14:0, i17:0 3OH), available K (16:15c), organic C and hydrolysable N (15:0 3OH, 18:15c, i15:0, 18:1 2OH, 16:0 2OH).
For CLPP data, the first two components of the RDA explained 23.2% and 6.2% of the total variance, respectively. Significant factors (P < 0.05) were total P, sand, silt, pH, clay and available K, and they, together, explained 55.3% of the total variation (Fig. 3a). All of the significant factors dominated the first component of RDA. Separation along the first component was mainly related to soil group, i.e. between Gran-Conif, Gran-Shrub and GranFarm, and also between parent materials within coniferous forest and shrub. Carbon sources that highly correlated with clay were l-asparagine (amino acids) and d,l-␣-glycerolphosphate (carbohydrates), with silt it was l-serine (amino acids), with available K-glucose-1-phosphate (carbohydrates), with sand-d-xylose (carbohydrates), with pH the carbon sources were ␣-cyclodextrin (polymers), glycogen (polymers), d-cellobiose (carbohydrates), ␣d-lactose (carbohydrates), -methyl-d-glucoside (carbohydrates), and with total P they were l-arginine (amino acids) and d-mannitol (carbohydrates) (Fig. 3b). Discussion Soil physicochemical properties Parent material, which had a decisive effect on soil texture (Nosrati et al. 2011) explained a much larger percentage of the variance in clay, silt and sand content than land use type in the present study. For organic C, total N and hydrolysable N content, land use type explained more variance than parent material, indicating that these soil chemical properties were mainly affected by land use type. The strong interactions between land use type and parent material suggest that the trend of soil chemical properties between parent materials varied with land use types. Organic C and total N of coniferous forest and shrub were lower in quaternary red earth than the other parent materials. In this study, granite and tertiary red sandstone lead to coarse-textured soil while quaternary red earth resulted in fine-textured soil, which is similar to previous studies (Hu et al. 2003). Coarse-textured soil may be favorable for plant growth and accumulation of organic matter due to its good drainage and aeration. Within each parent material, organic C, total N and hydrolysable N were generally lower while total P and available K were higher in farmland than coniferous forest and shrub. The difference between land use types could be attributed to the carbon accumulation in coniferous forest and shrub, and carbon
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a
clay (9.0%) TP (11.0%)
AXIS-2 20.6%
AXIS-2 6.2%
sand (9.7%) pH (9.2%)
AK (7.4%) clay (8.4%)
-0.6
pH (11.2%) AK (7.2%) sand (8.0%)
silt (9.6%)
-1.0
1.0
AXIS-1 23.2%
-1.0
1.0
AXIS-1 24.1%
0.6
-1.0
HN (11.2%) OC (13.5%)
b sand
TP c3
0.8
c20
c13
c16 16:1 2OH
b
i17:0
c24
pH c28
18:0
clay
c5
c1
18:1ω9c 16:0 N alcohol
i16:0
AK 16:0
c25
c7
c29
clay c15
14:0 i18:0 17:0 2OH i14:0 3OH 15:0 3OH
-0.8
18:1ω5c 18:1 2OH 16:0 2OH
-0.8
OC
c8 a15:0 i15:1G
HN
16:1ω5c
AK
i14:0 10:0 pH i17:0 3OH
sand
i15:0
-0.8
0.8
Fig. 2. Redundancy analysis of the soil physicochemical properties with PLFA data. (a) Correlation between samples and soil physicochemical properties. Each sample combines a land use type: coniferous forest (tri-angle), shrub (square) or peanut farmland (circle), and a parent material: granite (gray), tertiary red sandstone (hollow) or quaternary red earth (dark). (b) Correlation between soil physicochemical properties and PLFAs that have high absolute scores (>0.6) on each of the first two axes.
removal in farmland, the presence of L. bicolor which is an N-fixing plant in shrub, and the application of P and K fertilizer in farmland. The lower soil Al content in farmland may be due to plant uptake and harvest. Soil microbial properties The present study was a general assessment of the effect of land use types and parent materials on a series of microbial properties, including soil microbial biomass, activity, microbial diversity and functional diversity. The results clearly showed that the parent material factor explained most of the total variance in microbial biomass, activity and diversity, suggesting that this factor may have a more profound effect on soil micro-organisms than land use type. Granite had greater microbial biomass, activity and diversity than the other parent materials. The significant differences between land use types mainly existed within granite and tertiary
c14
silt
-0.8
10-me 17:0
0.8
3 Fig. 3. Redundancy analysis of the soil physicochemical properties with CLPP data after 72 h incubation. (a) Correlation between samples and soil physicochemical properties. Each sample combines a land use type: coniferous forest (tri-angle), shrub (square) or peanut farmland (circle), and a parent material: granite (gray), tertiary red sandstone (hollow) or quaternary red earth (dark). (b) Correlation between soil physicochemical properties and carbon sources that have high absolute scores (>0.6) on each of the first two axes. c1: -methyl-d-glucoside; c3: l-arginine; c5: d-xylose; c7: l-asparagine; c8: Tween; c13: d-mannitol; c14: 4-hydroxybenzoic acid; c15: l-serine; c16: ␣-cyclodextrin; c20: glycogen; c24: d-cellobiose; c28: ␣d-lactose.
red sandstone, where the microbial properties of farmland were significantly lower than those of shrub. However, considering there was only one sampling site, although with replicates, for each parent material in the study site, we should be cautious about interpreting the effect of parent materials since there may be other soil properties that vary in the different locations that drive at least part of these responses but were not measured. In most studies, microbial biomass, activity, diversity and functional diversity were higher in forest than farmland since agricultural practices such as tillage, removal of litters and the application of fertilizers exert stress on micro-organisms (Zhao et al. 2012). The soils under shrub and coniferous forest also differed because of the variable quality and quantity of carbon input (Deng et al. 2010). In quaternary red earth there was no significant difference between land use types for PLFA data, indicating that the effect of land use type on soil micro-organisms varied between parent materials. This was also confirmed by the significant interaction between parent materials and land use types. Previous studies showed variation of specific PLFAs between land use types, especially the proportion of G− bacteria and the
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Table 2 Two-way ANOVA of soil microbial properties including average well color development (AWCD), total, bacterial and fungal PLFA, the ratio of fungal to bacterial PLFA (Fungi/Bacteria), gram positive (G+ ) and gram negative (G− ) PLFA, the ratio of G+ to G− PLFA (G+ /G− ), Shannon index (H ) of PLFA and CLPP data. G+ /G−
H of PLFA
H of CLPP
0.72a 0.39c
30.43a 11.68c
22.15a 8.35c
3.96a 1.99c
0.18b 0.24a
8.76a 3.13c
13.39a 5.22c
0.64b 0.61b
2.71a 2.46b
3.17a 2.80c
–
0.54b
19.47b
13.48b
2.75b
0.21b
5.56b
7.92b
0.72a
2.60a
3.03b
Coniferous forest Shrub Peanut farmland
– – –
0.42b 0.65a 0.59a
21.48a 25.52a 14.57b
15.51a 18.02a 10.44b
3.10a 3.45a 2.14b
0.21a 0.21a 0.21a
6.10a 7.26a 4.09b
9.42a 10.76a 6.36b
0.65a 0.66a 0.66a
2.59a 2.61a 2.58a
2.85b 3.12a 3.04a
F value Parent material (P) Land use type (L) P×L
2 2 4
40.9*** 20.1*** 6.3**
38.2*** 13.2*** 5.7**
39.1*** 12.0*** 6.6**
25.6*** 11.9** 6.1**
10.8** 0.3 0.26
47.0*** 15.3*** 9.9***
33.0*** 9.7** 5.0*
7.9** 0.1 4.2*
10.90** 0.19 0.53
41.53*** 21.50*** 6.29**
49% 25% 16% 10%
53% 18% 16% 13%
53% 16% 18% 13%
44% 20% 21% 15%
53% 3% 3% 41%
52% 17% 22% 10%
54% 16% 16% 14%
52% 2% 5% 41%
49% 26% 15% 10%
Post hoc tests Granite Quaternary red earth Tertiary red sandstone
% of total variance P L P×L Error
AWCD
– –
2 2 4 18
Fungi/bacteria
G− PLFA (g g−1 )
Bacterial PLFA (g g−1 )
DF
Fungal PLFA (g g−1 )
G+ PLFA (g g−1 )
Total PLFA (g g−1 )
Variables
28% 1% 39% 32%
In post hoc tests, means (n = 3) followed by same letter indicate no significant difference between three parental materials or between three land use types. * P < 0.05. ** P < 0.01. *** P < 0.001.
fungi/bacteria ratio, which were considered indicators of land use change. However, the G− /G+ ratio was also found unchanged between land use types (McKinley et al. 2005). In our study, no change in this ratio was observed among land use types. The RDA of the PLFA profiles of the land use types clearly showed that the profiles were closely related to the variation in organic C and nitrogen content. Along with OC and HN, both G+ (i15:0, 15:0 3OH, 16:0 2OH, 10-me 17:0) and G− (18:15c, 18:1 2OH) bacteria shifted rather than G-bacteria alone. Moreover, only G+ bacteria changed in the opposite direction of OC and HN (14:0, 16:0, 18:0, 16:0 N alcohol). The G+ bacteria could survive better in resource-limited environment (Gartzia-Bengoetxea et al. 2009) and they may also indicate land use change. The fungi to bacteria ratio varied among parent materials rather than land use type. It has been suggested that land use change does not inevitably alter fungi to bacteria ratio (Lauber et al. 2008). In our study, the reason could be that the difference among land use types was masked by parent materials. The RDA exhibited that organic C and nitrogen content and soil texture have strong association with PLFA profiles. Moreover, it was not surprising that soil organic carbon and nutrient content changed with land use type (Vaccari et al. 2012). Soil texture, however, was determined by parent material (Nosrati et al. 2011) and had a decisive effect on DNA-based bacterial community composition (Johnson et al. 2003). In our study, it is worth noting that although significant physicochemical properties varied between the plot of PLFA profiles and that of CLPP, soil texture was significant for both plots. Our results indicate that soil texture is a major driver of micro-organisms and their functions.
Conclusion The study clearly showed that both land use type and parent material have significant effect on soil microbial biomass, activity and diversity, though parent material explained a larger part of the variance than land use type, thus predominating. In general, granite and shrub had greater soil microbial biomass, activity and diversity than quaternary red earth and farmland, respectively. Nevertheless, we cannot exclude that the results are partly biased by pseudoreplication of parental materials and thus, the data should be interpreted
with caution. We suggest that it is the interaction between parent material and land use type that contributes to red soil degradation rather than only inappropriate land use type. Our result provides some input for land use planning in the red soil region. To preserve soil quality, a reasonable collocation of parent materials and land use type should be considered.
Acknowledgments This work was supported by grants from National Natural Science Foundation of China (41271255), Major Program of Natural Science Research of Jiangsu Higher Education Institutions (12KJA170001), and the Priority Academic Program Development of Jiangsu Higher Education Institutions.
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