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Changes in soil P chemistry as affected by conversion of natural secondary forests to larch plantations
Forest Ecology and Management 260 (2010) 422–428
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Changes in soil P chemistry as affected by conversion of natural secondary forests to larch plantations Kai Yang a,b , Jiao-Jun Zhu a,∗ , Qiao-Ling Yan a , Osbert Jianxin Sun c a b c
Qingyuan Experimental Station of Forest Ecology, Institute of Applied Ecology, Chinese Academy of Sciences, 72 Wenhua Road, Shenyang 110016, China Graduate University of Chinese Academy of Sciences, Beijing 100039, China MOE Key Laboratory for Silviculture and Conservation, Institute of Forestry and Climate Change Research, Beijing Forestry University, Beijing 100083, China
a r t i c l e
i n f o
Article history: Received 21 January 2010 Received in revised form 28 April 2010 Accepted 29 April 2010 Keywords: Acid phosphatase activity Larch plantation Microbial biomass Natural secondary forest Northeast China Soil P chemistry
a b s t r a c t To assess the impact of conversion of native forests to monocultural larch plantations on soil chemical properties, we compared the total and various fractions of soil phosphorus (P) and acid phosphatase activity (APA) between natural secondary forests (NSF) and Larix olgensis plantations (LOP) on a montane forest site in eastern Liaoning Province, Northeast China. We found that the concentrations of total P (TP), inorganic P, and iron-bound P (Fe-P) were significantly higher, and the concentrations of microbial biomass P (MBP), sodium bicarbonate-extractable organic P (NaHCO3 -Po), and APA were significantly lower, in the LOP stands than in the NSF stands; whilst organic P, sodium bicarbonate-extractable inorganic P (NaHCO3 -Pi), aluminum-bound P (Al-P) and calcium-bound P (Ca-P) were comparable between the two forest types. Our study also showed that the ratios of MBP/TP, NaHCO3 -Pi/TP, NaHCO3 -Po/TP, and APA significantly varied with time during the growing season. Moreover, the concentrations of NaHCO3 Pi, NaHCO3 -Po, and MBP had significant (P < 0.01) and positive linear relationships with APA. Overall, results from this study suggest that conversion of native forests to larch plantations in the region is more likely to cause compositional change in soil P than to result in reduction in overall P availability. Crown Copyright © 2010 Published by Elsevier B.V. All rights reserved.
1. Introduction Mixed broadleaved-Korean pine (Pinus koraiensis Sieb. Et Zucc) forest is one of the most important regional climax forest types in Northeast China, of which more than 70% have become natural secondary forests after a century of timber exploitation and historical natural disturbances (Zhu et al., 2007). To meet the growing demands for timber, extensive areas of these secondary forests have been replaced by plantations predominantly of larch species (Zhu et al., 2008). In the eastern Liaoning Province of Northeast China, for example, there are about 200,000 ha of Larix olgensis Henry plantations in the montane regions (Liu et al., 2007); these plantations intersperse with the remnant natural forests to form mosaic of plantation/natural secondary forest landscapes. Given the extensive coverage and economic value, larch plantations have in recent years attracted much attention in their role for contributing to ecosystem functioning as well as timber production. Impacts of larch plantations on soil properties and nutrient cycling have been a particular research interest for concerns on sustainable forest productivity.
∗ Corresponding author. Tel.: +86 24 83970342; fax: +86 24 83970300. E-mail address: [email protected] (J.-J. Zhu).
Many studies have demonstrated that changes in land cover can influence soil biological properties and nutrient cycling (Yeates et al., 1997; Oberson et al., 2001; Sharma et al., 2004). However, the directions of the influences can vary depending on the type of land cover change. For example, it is reported that land cover change from grassland to conifers results in a reduction in soil microbial biomass, rate of soil respiration, and phosphatase activity (Chen et al., 2000). Similarly, changes from native forests to larch plantations have been found to result in significant decline in soil C and N concentrations (Chen and Li, 2003). In contrast, a conversion from native savanna to rice–pasture rotations causes improvement in biological properties (Gijsman et al., 1997). In general, conversion of natural forests to plantations has been found to result in reduction in soil nutrient availability and deterioration in microbiological properties (Wang and Wang, 2007; Yan et al., 2008). Compared with other major nutrients, P is known to be the least mobile element and to have low availability to plants under most soil conditions. The availability of P for plant growth depends on complex geochemical and biochemical processes (Walker and Syers, 1976). Land cover change may affect P inputs and outputs, resulting in an altered P balance and changes in P forms (Ross et al., 1999), and alter soil P transformation by modifying soil physical, chemical and biological properties, especially soil microbial processes (Chen et al., 2008). Soil microorganisms play a key role in facilitating P transformations through mineralization of P from
0378-1127/$ – see front matter. Crown Copyright © 2010 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2010.04.038
K. Yang et al. / Forest Ecology and Management 260 (2010) 422–428
organic sources, synthesis and release of organic P, and solubilization of barely soluble P forms (Oberson et al., 2001). Microbes also have the ability to rapidly immobilize considerable amounts of P when labile C is readily available (Bünemann et al., 2004). Most P utilized by plants is in inorganic forms (Marschner, 1995). Organic P accounts for about 15–80% of total P (Condron and Tiessen, 2005); the organically bound P needs to be mineralized to become available for plant uptake and utilization. Phosphatase activity has been considered to be an important driver in this mineralization process and to reflect organic P mineralization potential of soils (Chen, 2003; Criquet et al., 2004). However, the studies of Dilly and Nannipieri (2001) and Olander and Vitousek (2000) show that increased P availability depresses phosphatase activity in forest soils. Therefore the relationship between phosphatase activity and soil P availability still remains a controversial issue. Knowledge of the seasonal variation in soil P fractions is important for understanding the dynamics of P availability and mineralization in soils (Magid and Nielsen, 1992). Seasonal changes in soil P fractions may reflect P uptake by plants and mineralization–immobilization processes. The fluctuation in P fractions during the growing season, particularly soil P transformation process, is considered an important factor in controlling P availability and ultimately in influencing plant nutrition (Eviner et al., 2006). Several studies on temperate ecosystems have shown a considerable seasonal variation of P fractions (Chen et al., 2003; Styles and Coxon, 2007; Zhao et al., 2009). However, there also appear inconsistent findings (e.g. Tate et al., 1991; Magid and Nielsen, 1992; Fabre et al., 1996). For instance, the maximum values of soil bicarbonate-extractable inorganic P and bicarbonate-extractable organic P have been found to occur in summer (Zhao et al., 2009) or winter (Fabre et al., 1996), or there lacks significant seasonal variation in soil resin-extractable inorganic P (Tate et al., 1991). The variable results suggest that seasonal variation in soil P fractions might be dependent of ecosystem types and climatic conditions. In this study, we compared various forms of soil P between natural secondary forests and larch plantations in the montane region of eastern Liaoning Province of Northeast China, with aims to understand how the two contrasting forest types may differ in soil P properties. Detailed measurements were made on soil total P (TP), various fractions of soil P (i.e. organic P, inorganic P, sodium bicarbonate-extractable organic P, sodium bicarbonate-extractable inorganic P, aluminum-bound P, iron-bound P, and calcium-bound P), and the factors affecting P cycling and transformation (i.e. microbial biomass P and acid phosphatase activity). The objectives of this study were to determine: (1) how natural secondary forests and larch plantations would differ in the quantity and compositional structure of soil P; and (2) how seasonally variable the various P fractions would be in forests of the temperate climate. Our study was to test the hypothesis that forest conversion from native forests to larch plantations would reduce P availability and result in substantive compositional changes of soil P.
2. Materials and methods 2.1. Site description and experimental design The study was conducted at the Qingyuan Experimental Station of Forest Ecology of Institute of Applied Ecology, Chinese Academy of Sciences. The station is located in a mountainous region in the eastern Liaoning Province, Northeast China (latitude 41◦ 51 N, longitude 124◦ 54 E, elevation 500–1100 m above sea level). The climate of the region is a continental monsoon type with a humid and rainy summer, and a cold and dry winter. Mean annual air temperature varies between 3.9 and 5.4 ◦ C, and the maximum and minimum temperatures are 36.5 and −37.6 ◦ C. Annual precipitation fluctu-
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ates between 700 and 850 mm, with more than 80% falling during June–August. The growing season is from early April to late October (Zhu et al., 2007). The brown forest soil belongs to Udalfs according to the second edition of U.S. Soil Taxonomy (1999). The soil is a clay loamy soil (sand: 25.6%, silt: 51.2%, clay: 23.2%). The study site was originally occupied by primary mixed broadleaved-Korean pine forests until 1930s and subsequently subjected to decades of unregulated timber removal. A large fire that occurred in the early 1950s completely cleared off the original forests and the site was replaced by a mixture of naturally regenerating broadleaved native tree species. Since 1960s, patches of the secondary natural forests were cleared for larch plantations. Our sample plots were set up on three stands of natural secondary forests and three stands of larch plantations of the age 16–44 years. The six stands were selected from separate small watersheds over an area of 100 ha, with experimental plots set up on sites of slightly variable altitudes (from 568 to 730 m above sea level) and on gentle slopes of variable aspects as strict controls of altitude and slope aspect proven highly difficult because of the fragmented landscape in the region. Larch plantations often occur in small patches among the natural secondary forest stands in our study area. Where possible, we set up the larch plantation plots close to, but not necessarily adjacent with, the natural secondary forest sites to avoid complication by variation in topographical features. Overall, the six stands have the same topographical features and are on soils developed from the same parental material, i.e. granite gneiss. Soil depth of the study site varied from 60 to 80 cm and was comparable between LOP and NSF stands. However, the two types of stands differed in the thickness of the litter layer and A-horizon soil layer; the litter layer depth was 4.4–6.0 cm in the LOP stands and 2.7–5.6 cm in the NSF stands, whilst the A-horizon soil layer depth was 6.5–8.5 cm in the LOP stands and 8–10 cm in the NSF stands; the AB-horizon soil layer depth was about 10 cm; and the B-horizon soil depth varied between 30 and 40 cm. In each of the stands, three 20 m × 20 m plots were laid out in September 2006. The plots of natural secondary forests consisted of Juglans mandshurica, Quercus mongolica, Acer mono, Fraxinus rhynchophylla and Ulmus macrocarpa in the tree layer, A. triflorun, A. tegmentosum, A. mandshricum and Syringa amurensis in the understory component, and Cardamine leucantha, Allium monanthum, Arisaema amurense, and Polygonatum involucratum in the herbage component. The plots of larch plantations contain Acer tegmentosum, A. pseudo-sieboldianum, Schisandra chinensis, Syringa wolfi and Acanthopanax senticosus in the shrub layer and Cardamine leucantha, Rubia sylvatica, Spuriopimpinella brachycarpa in the herbage layer. 2.2. Soil sampling Soil samples were collected during the growing season in spring (April), summer (July) and autumn (September) of 2008. Soil cores of 5 cm in diameter were taken at nine random locations on each plot after removing litters, and each soil core was separated into 0–15 and 15–30 cm layers. The nine samples of the same layer on each plot were mixed as a composite sample, which was further divided into three sets of sub-samples. One set of the sub-samples was processed to pass through a 2 mm sieve, and stored at 4 ◦ C for measurements of microbial biomass P (MBP) and acid phosphatase activity (APA); one was air-dried and passed through a 1 mm sieve for analysis of soil pH, sodium bicarbonate-extractable inorganic P (NaHCO3 -Pi) and sodium bicarbonate-extractable organic P (NaHCO3 -Po); the remaining sub-sample was air-dried, and homogenized and passed through a 0.25 mm sieve for analyses of soil organic C (SOC), total N (TN), TP, organic P and fractions of inorganic P. The basic soil physical and chemical properties, seasonal variations in soil water content (%, v/v) in the natural secondary
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Table 1 Soil physiochemical characteristics in the natural secondary forest (NSF) and the Larix olgensis plantation (LOP). Forest type
SOC (g kg−1 )
0–15
NSF LOP
15–30
NSF LOP
Soil depth (cm)
TN (g kg−1 )
C/N
50.45 ± 4.25 34.70 ± 1.86
4.21 ± 0.52 3.20 ± 0.17
23.42 ± 2.63 23.97 ± 1.90
2.18 ± 0.32 2.38 ± 0.16
a
Soil bulk density (g cm−3 )
pH
12.3 ± 0.2 10.9 ± 0.1
a
5.82 ± 0.03 5.55 ± 0.05
1.32 ± 0.03 1.31 ± 0.01
11.1 ± 0.3a 10.0 ± 0.1
5.91 ± 0.05a 5.71 ± 0.04
1.45 ± 0.03 1.49 ± 0.02
a
SOC: soil organic C; TN: soil total N. Values shown in tables are means ± standard errors (n = 3). a Indicate significant differences between the natural secondary forest and the Larix olgensis plantation of the corresponding depth at P = 0.05 levels.
forest stands and larch plantations are listed in Tables 1 and 2, respectively. 2.3. Soil analyses Soil pH was estimated on a 1:2.5 soil–water mixture. Soil bulk density samples were measured at each soil depth using a known volume metal container. Bulk density measurements were performed by drying the soil at 105 ◦ C for 12 h and then reweighing the samples. Gravimetric soil water content was calculated from mass loss after drying for 12 h at 105 ◦ C in 0–15 and 15–30 cm of soil layers, respectively. The SOC and TN were analyzed by dry combustion on a Vario EL III elemental analyzer (Germany). The TP was determined following H2 SO4 –HClO4 digestion (Olsen and Sommers, 1982). Organic P was determined by ignition method of Saunders and Williams (1955), and inorganic P was computed as the difference between the TP and organic P. Soil MBP was determined by the chloroform fumigation extraction (soil: extractant [0.5 mol L−1 NaHCO3 ] ratio 1:20) method. The MBP was estimated from the relationship EP /KEP , where EP is the difference between inorganic P extracted from fumigated and unfumigated soils and KEP = 0.40 (Brookes et al., 1982). The correction for chloroform released P that was absorbed by soil colloids during extraction was made by adding 25 mg P kg−1 soil during extraction and then corrected for its recovery (Brookes et al., 1982). Soil APA was assayed by the method of Tabatabai (1994) at pH 6.5. Soil acid phosphatase activity was assayed at pH 6.5 rather than at the soil pH because of: (1) that the difference in soil pH between the NSF stands and the LOP stands is about 0.2–0.3 units apart; and (2) that the soil pH value of 6.5 is optimum for acid phosphatase activity. The NaHCO3 -Pi and NaHCO3 -Po were determined by Bowman and Cole (1978) method. The fractionation of inorganic P in soils was determined by a modified Chang and Jackson procedure (as described by Petersen and Corey, 1966). Soil samples were sequentially extracted with 0.5 mol L−1 NH4 F for aluminum-bound P (Al-P) determination, 0.1 mol L−1 NaOH for iron-bound P (Fe-P), and 0.5 mol L−1 H2 SO4 for calcium-bound P (Ca-P). All phosphate ions were determined by the ascorbic acid molybdenum antimony spectrophotometric method.
Table 2 Seasonal variations in soil water content (%, v/v) in the natural secondary forest (NSF) and the Larix olgensis plantation (LOP).
Fig. 1. Soil total P (TP), organic P (Po), and inorganic P (Pi) in the natural secondary forest (NSF) and the Larix olgensis plantation (LOP) at different seasons (standard errors from 3 samples shown by vertical bars).
2.4. Statistical analyses All reported values are expressed on air-dry soil weight basis. Statistical analyses were performed by using the SPSS 11.5 for Windows. One-way ANOVA was performed by soil layer, and LSD’s (least significant difference) test was applied post hoc to distinguish the differences of soil physiochemical properties between the NSF and the LOP. Repeated measures analysis of variance (ANOVA) was used to test the effects of forest types on various P variables of the same soil layer across the growing season. When there were significant interactions between the forest type and sampling season, one-way ANOVA was used to test the effects of vegetation type on soil P variables by sampling season and the effects of sampling season on soil P variables by forest types. Data were tested for normality and homogeneity of error variances to determine whether transformations were needed. Pearson linear correlations were used to assess the relationships between acid phosphatase activities and active soil P fractions (including MBP, NaHCO3 -Po and NaHCO3 -Pi).
Soil depth (cm)
Sampling season
Forest type NSF
LOP
3. Results
0–15
Spring Summer Autumn
30.4 ± 1.2a 34.8 ± 1.1a 26.7 ± 0.9a
27.5 ± 0.6 30.9 ± 0.8 21.7 ± 1.3
3.1. Total P, organic P, and inorganic P fractions
15–30
Spring Summer Autumn
24.0 ± 0.5 25.2 ± 1.9 19.6 ± 0.8
22.9 ± 1.2 25.0 ± 0.7 18.5 ± 1.2
Values shown in tables are means ± standard errors (n = 3). a Indicate significant differences between the natural secondary forest and the Larix olgensis plantation in same season of the corresponding depth at P = 0.05 levels.
Concentrations of total P and inorganic P were significantly higher in the LOP stands than in the NSF stands in both 0–15 and 15–30 cm soil layers (Fig. 1, P < 0.05), whilst the organic P concentration did not vary between the NSF and LOP stands each sampling season (Fig. 1). Sampling season had no significant effect on soil total P, inorganic P and organic P. Across the three seasons, soil
K. Yang et al. / Forest Ecology and Management 260 (2010) 422–428
Fig. 2. Soil Al-P, Fe-P and Ca-P in natural secondary forest (NSF) and Larix olgensis plantation (LOP) at different seasons (standard errors from 3 samples shown by vertical bars).
organic P accounted for 53–64% of total P in both types of stands, with the NSF stands having higher ratios of organic P to total P than LOP stands (Table 3). For inorganic P fractions, the NSF stands had significantly lower Fe-P concentration than the LOP stands. Specifically, the average concentrations of soil Fe-P in the NSF stands were 51.3 mg kg−1 lower in the 0–15 cm soil layer and 35.2 mg kg−1 lower in the 15–30 cm soil layer, respectively, than in the LOP stands across seasons (Table 3 and Fig. 2). There were no significant difference between NSF and LOP for Al-P and Ca-P concentrations in spring and autumn. Effects of forest type on Al-P and Ca-P concentrations were significant in summer in the 0–15 cm soil layer (P < 0.05). The NSF stands had significantly higher Al-P concentration and lower Ca-P concentration than the LOP stands. All the inorganic P fractions were lower in the 15–30 cm soil layer than in the 0–15 cm soil layer for both forest types (Fig. 2). The seasonal average concentrations of the inorganic P fractions followed a descending order of: FeP > Ca-P > Al-P. There was no significant effect of sampling season on concentrations of Al-P, Fe-P and Ca-P (Fig. 2). 3.2. Soil MBP, NaHCO3 -Po, and NaHCO3 -Pi MBP and NaHCO3 -Po concentrations were higher in the NSF stands than in the LOP stands in the 0–15 cm soil layer in spring and summer, and decreased with soil depth (Fig. 3). In the 0–15 cm soil layer, the concentrations of MBP and NaHCO3 -Po averaged across seasons were 14.2 and 4.2 mg kg−1 higher in the NSF stands than in the LOP stands, respectively (Table 3). The NaHCO3 -Pi concentration did not differ between the NSF and LOP stands across
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Fig. 3. Soil microbial biomass P (MBP), sodium bicarbonate-extractable organic P (NaHCO3 -Po) and sodium bicarbonate-extractable inorganic P (NaHCO3 -Pi) in the natural secondary forest (NSF) and the Larix olgensis plantation (LOP) at different seasons (standard errors from 3 samples shown by vertical bars).
seasons in both 0–15 and 15–30 cm soil layers. There was a significant effect of sampling season on MBP in both soil layers in the LOP stands, but not in the NSF stands. In the LOP stands, MBP concentration was higher in summer than in spring and autumn, with the maximum difference being 11.1 mg kg−1 in the 0–15 cm soil layer and 5.2 mg kg−1 in the 15–30 cm soil layer, respectively (Fig. 3). There was also a significant seasonal variation in soil NaHCO3 Po in the both types of stands in the two soil layers; significantly higher NaHCO3 -Po concentrations were also observed in summer than in spring and autumn (Fig. 3) (P < 0.05). In the NSF stands, the maximum seasonal difference in NaHCO3 -Po concentration was 13.9 mg kg−1 in the 0–15 cm soil layer and 10.7 mg kg−1 in the 15–30 cm soil layer, respectively; whilst in the LOP stands, the maximum seasonal difference in NaHCO3 -Po concentration was 3.0 mg kg−1 in the 0–15 cm soil layer and 3.6 mg kg−1 in the 15–30 cm soil layer, respectively. The NaHCO3 -Pi concentrations were relatively stable across seasons in both NSF and LOP stands. Effects of forest type on MBP/TP and NaHCO3 -Po/TP ratios were significant across seasons in both soil layers (Fig. 4): in the 0–15 cm soil layer, the MBP/TP was 5.5% in the NSF stands and 2.6% in the LOP stands; where as in the 15–30 cm soil layer, the MBP/TP was 1.8% in the NSF stands and 1.4% in the LOP stands. The NaHCO3 -Po/TP was 2.8% in the NSF stands and 1.6% in the LOP stands in the 0–15 cm layer, and 1.7% in the NSF stands and 1.0% in the LOP stands in the 15–30 cm layer, respectively, across seasons (Fig. 4). The difference in NaHCO3 -Pi/TP between the NSF and LOP stands was dependent on the sampling season. The NaHCO3 -Pi/TP was generally higher in the NSF stands than in the LOP stands. The MBP/TP and NaHCO3 Po/TP showed the similar seasonal patterns as MBP and NaHCO3 -Po
Table 3 The average (n = 9) of soil P fractions (mg kg−1 ) and acid phosphatase activities (mg kg−1 h−1 ) in the natural secondary forest (NSF) and the Larix olgensis plantation (LOP) across seasons. Soil depth (cm)
Forest type
Po
Pi
Al-P
Fe-P
Ca-P
MBP
NaHCO3 -Po
NaHCO3 -Pi
APA
0–15
NSF LOP
741 1025
TP
475 543
272 481
17.8 15.2
84.9 136.2
70.0 78.3
40.3 26.1
19.8 15.6
10.2 10.1
818 673
15–30
NSF LOP
627 897
376 495
251 402
13.9 11.6
68.0 103.2
53.5 53.4
12.5 11.8
10.1 8.3
4.5 5.2
448 277
TP: total P; Po: organic P; Pi: inorganic P; MBP: microbial biomass P; NaHCO3 -Po: sodium bicarbonate-extractable organic P; NaHCO3 -Pi: sodium bicarbonate-extractable inorganic P; APA: acid phosphatase activity.
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Fig. 4. Percent (%) of various active P fractions of soils in the natural secondary forest (NSF) and the Larix olgensis plantation (LOP) at different seasons (standard errors from 3 samples shown by vertical bars).
Fig. 5. Seasonal variation in acid phosphatase activity (APA) of soils in the natural secondary forest (NSF) and the Larix olgensis plantation (LOP) (standard errors from 3 samples shown by vertical bars).
in the two types of stands. There was a significant effect of sampling season on NaHCO3 -Pi/TP in both soil layers in the NSF stands (P < 0.05), but not in the LOP stands.
Fig. 6. Relationship between acid phosphatase activity and microbial biomass P (A), sodium bicarbonate-extractable organic P (NaHCO3 -Po) (B) and sodium bicarbonate-extractable inorganic P (NaHCO3 -Pi) (C) for the natural secondary forest and the Larix olgensis plantation in three seasons (n = 36, i.e. three plots × two soil depths × three seasons × two forest types). *, ** Significant at P < 0.05 and P < 0.01 respectively.
4. Discussion 3.3. Soil APA The value of APA was significantly greater in the NSF stands than in the LOP regardless of soil depth and sampling season (with an exception of the APA in the 0–15 cm soil layer in autumn), and was higher in the 0–15 cm soil layer than in the 15–30 cm soil layer (Fig. 5). The average value of soil APA in the NSF stands was 145 mg kg−1 h−1 greater in the 0–15 cm soil layer, and 171 mg kg−1 h−1 greater in the 15–30 cm soil layer, respectively, than in the LOP stands across seasons (Table 3). There was a significant effect of sampling season on APA in the 15–30 cm soil layer, with the maximum APA found in autumn, and the minimum in summer for both forest types. The maximum seasonal differences in APA were 189 mg kg−1 h−1 in the NSF stands and 124 mg kg−1 h−1 in the LOP stands, respectively. 3.4. Relationships between active soil P fractions and APA APA was positively correlated with MBP based on a combined dataset for both forest types (r = 0.822, P < 0.01, n = 36). Significant and positive correlations were also found for APA-NaHCO3 -Po and APA-NaHCO3 -Pi (Fig. 6). The two forest types did not differ in the relationships of APA with MBP, NaHCO3 -Po, and NaHCO3 -Pi.
This study has shown that the two forest types differed markedly in soil P chemistry. We found that the concentrations of total P, inorganic P, and Fe-P were significantly higher, and the concentrations of MBP, NaHCO3 -Po, and APA were significantly lower, in the LOP stands than in the NSF stands; whilst concentrations of organic P, NaHCO3 -Pi, Al-P, and Ca-P were comparable between the two forest types. The finding of generally greater amount of soil P in larch plantation than in natural secondary stand was contrary to our initial expectation of a reduced soil P availability with land cover change from native forests to coniferous plantations. Many factors may attribute to differences between different forest types in soil P. For example, differences in the quantity of plant litter inputs and chemical composition of the litter may be crucial ˜ et al., 2008; Redel drivers to alter the soil P concentration (Ordónez et al., 2008). In addition, plant species composition and root type can also influence soil P status in the ecosystem scale (Grierson and Adams, 2000). In this study, the difference in total P between the two forest types may be explained firstly by more abundant understory shrubs in the LOP (personal observation) and secondly by greater organic matter input as decaying roots and slash when original forest trees were cleared for planting L. olgensis. It has been shown by Liu et al. (1998) that the role of the shrub species and
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understory vegetation is very important in sustaining soil fertility in larch plantations. The organic matter inputs from leave decompositions can also affect P cycling in the soil (Wood et al., 2009). The results of this study also revealed seasonal patterns of total P, organic P and inorganic P for both two forest types, i.e. the concentrations of total P, organic P and inorganic P were relatively stable over time in both NSF and LOP stands. This result was consistent with previous studies in temperate forest ecosystems by Fabre et al. (1996). Since P as orthophosphate is largely the preferred source for plant P uptake, knowledge of the inorganic P fractions within soils is essential to understanding P bioavailability (McDowell and Stewart, 2006). It should be noted that the low pH values of the soils (5.55–5.91) might also influence the behavior of P due to P binding by Al and Fe in acid soils (Richter et al., 2006). The high proportion of Fe-P in the two forest types in our study was consistent with previous research in Chinese fir forest soils (Chen, 2003). The relative distribution of inorganic P fractions for the two forest types in decreasing order was Fe-P, Ca-P and Al-P in our study, which differed with the finding of Barroso and Nahas (2005) that the percentages of the P fractions decreased in the order of Fe-P, Al-P and Ca-P in Brazilian soils. Al-P content in the two forest types was lower than that in Brazilian soils because the former is a less weathered soil. In the current study, the concentrations of inorganic P fractions were significantly affected by forest types, especially the Fe-P fraction. Different phosphate-solubilizing microorganisms between the NSF and LOP stands may be responsible for Fe-P concentrations (Barroso and Nahas, 2005). Furthermore, the Fe oxide concentration could dominate the mechanisms governing values of Fe-P in temperate forest ecosystems (Darke and Walbridge, 2000). The results support the viewpoint that the soil inorganic P content varies with different forest ecosystems (Redel et al., 2008). Generally, Al-P increases with declining soil pH (Chen, 2003). But, in our study, Al-P concentration was not significant difference between the NSF and LOP stands, albeit significantly lower soil pH in the LOP stands than that in the NSF stands. The difference in soil pH between the NSF and LOP stands (0.2–0.3) could be too small to impose significant effects. Soil microbial biomass is an important component in most terrestrial ecosystems. A small change in microbial biomass could have a major impact on plant nutrient availability, at least in the shortterm. Furthermore, the P held in soil microbial biomass is a readily available P source for plants. In this study, soil MBP in the LOP was lower than in the NSF stands, supporting the finding of Wang and Wang (2007) that soil microbial biomass in pure coniferous plantations was lower than in natural broadleaved forests. Differences in the quantity and quality of organic matter returned to soil between the NSF and LOP stands, especially labile organic matter (including microbial biomass C), could be responsible for changes in soil MBP. On the other hand, changes in MBP between the NSF and the LOP stands observed in this study could also be influenced by microclimatic modifications, such as decreases in soil water content due to increased evaporation or hydraulic redistribution in the LOP stands. The results of a greater NaHCO3 -Po concentration in the NSF stands could be explained by faster microbial decomposition of plant litters in this forest type. Differences in the active soil P fractions (including MBP and NaHCO3 -Po) between the NSF and LOP stands implicate that soil organic P status might deteriorate following conversion of natural secondary forests to larch plantations. We found that the ratios of MBP/TP, NaHCO3 -Po/TP and NaHCO3 -Pi/TP were generally higher in soils of the NSF stands than of the LOP stands across seasons, and that MBP/TP and NaHCO3 -Po/TP were significantly higher in summer than in spring or autumn, which suggest that it is important to take temporal variations into consideration in the sampling
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strategy. The value of soil bioavailable P depends on the factors such as mineralization–immobilization of organic P, and adsorption–desorption and precipitation–dissolution of inorganic P (Frossard et al., 2000). Recently, Styles and Coxon (2007) shows that labile inorganic P concentration follows a distinct seasonal trend of winter maximum and summer minimum in western Ireland. However, we found that the NaHCO3 -Po/TP ratio was higher in summer and lower in spring or autumn in our study, contrary to the findings of Chen et al. (2003) and Styles and Coxon (2007). This may be because the NaHCO3 -Po fraction was affected by microbial biomass P and plant uptake (Fabre et al., 1996). Additionally, climatic factors such as soil and air temperatures, soil water content can also influence the seasonal dynamics of MBP and NaHCO3 -Po fraction (Magid and Nielsen, 1992). Phosphatase activity plays an important role in P bioavailability. It has been suggested as an indicator of P availability in soils and soil quality (Chen, 2003). Soil acid phosphatase activities in this study falls well within the range of the values reported in other forest ecosystems (Chen et al., 2000). Low soil APA activity observed in LOP stands than those in NSF stands were related to decrease soil organic matter and microbial biomass. We found that seasonal variations in acid phosphatase activities were small for both forest types and the maximum acid phosphatase activities in NSF and LOP occurred in autumn. Criquet et al. (2004) also reported a seasonal increase in the acid phosphatase activities during the cold period in an evergreen oak litter of the French Mediterranean area. In this study, acid phosphatase activities were significantly correˇ lated with MBP, consistent with the finding of Snajdr et al. (2008) that soil acid phosphatase positively correlated with total microbial biomass in Quercus petraea forest soil. In our study, APA was also positively correlated with NaHCO3 -Po and NaHCO3 -Pi, which is consistent with the previous finding by Grierson and Adams (2000), but differed with findings of Dilly and Nannipieri (2001) and Olander and Vitousek (2000). These contradicting findings may attribute to differences in the concentration of NaHCO3 -Pi because the concentrations of NaHCO3 -Pi in the range of 3.4–11.8 mg kg−1 in this study were much lower than in other studies (e.g. Dick, 1994). In summary, results from this study showed that the contents of soil MBP and NaHCO3 -Po were significantly higher in the native forest stands than in the larch plantation, whilst there was no significant difference in NaHCO3 -Pi between the two forest types, indicating that the native forests are better in maintaining soil organic P fertility than larch plantations. Our results also suggest that conversion of native forests to larch plantations in the region is more likely to cause compositional change in soil P than to result in reduction in overall P availability. Acknowledgements This research was supported by the 11th-Five-Year National Science and Technology Research Projects (2006BAD03A0401, 2006BAD03A0903) and the CAS/SAFEA International Partnership Program for Creative Research Teams (KZCX2-YW-445) and National Non-commercial Forests Project (200804027-05). References Barroso, C.B., Nahas, E., 2005. The status of soil phosphate fractions and the ability of fungi to dissolve hardly soluble phosphates. Appl. Soil Ecol. 29, 73–83. Bowman, R.A., Cole, C.V., 1978. An exploratory method for fractionation of organic phosphorus from grassland soils. Soil Sci. 125, 95–101. Brookes, P.C., Powlson, D.S., Jenkinson, D.S., 1982. Measurement of microbial biomass phosphorus in soil. Soil Biol. Biochem. 14, 319–329. Bünemann, E.K., Bossio, D.A., Smithson, P.C., Frossard, E., Oberson, A., 2004. Microbial community composition and substrate use in a highly weathered soil as affected by crop rotation and P fertilization. Soil Biol. Biochem. 36, 889–901.
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Changes in soil P chemistry as affected by conversion of natural secondary forests to larch plantations Kai Yang a,b , Jiao-Jun Zhu a,∗ , Qiao-Ling Yan a , Osbert Jianxin Sun c a b c
Qingyuan Experimental Station of Forest Ecology, Institute of Applied Ecology, Chinese Academy of Sciences, 72 Wenhua Road, Shenyang 110016, China Graduate University of Chinese Academy of Sciences, Beijing 100039, China MOE Key Laboratory for Silviculture and Conservation, Institute of Forestry and Climate Change Research, Beijing Forestry University, Beijing 100083, China
a r t i c l e
i n f o
Article history: Received 21 January 2010 Received in revised form 28 April 2010 Accepted 29 April 2010 Keywords: Acid phosphatase activity Larch plantation Microbial biomass Natural secondary forest Northeast China Soil P chemistry
a b s t r a c t To assess the impact of conversion of native forests to monocultural larch plantations on soil chemical properties, we compared the total and various fractions of soil phosphorus (P) and acid phosphatase activity (APA) between natural secondary forests (NSF) and Larix olgensis plantations (LOP) on a montane forest site in eastern Liaoning Province, Northeast China. We found that the concentrations of total P (TP), inorganic P, and iron-bound P (Fe-P) were significantly higher, and the concentrations of microbial biomass P (MBP), sodium bicarbonate-extractable organic P (NaHCO3 -Po), and APA were significantly lower, in the LOP stands than in the NSF stands; whilst organic P, sodium bicarbonate-extractable inorganic P (NaHCO3 -Pi), aluminum-bound P (Al-P) and calcium-bound P (Ca-P) were comparable between the two forest types. Our study also showed that the ratios of MBP/TP, NaHCO3 -Pi/TP, NaHCO3 -Po/TP, and APA significantly varied with time during the growing season. Moreover, the concentrations of NaHCO3 Pi, NaHCO3 -Po, and MBP had significant (P < 0.01) and positive linear relationships with APA. Overall, results from this study suggest that conversion of native forests to larch plantations in the region is more likely to cause compositional change in soil P than to result in reduction in overall P availability. Crown Copyright © 2010 Published by Elsevier B.V. All rights reserved.
1. Introduction Mixed broadleaved-Korean pine (Pinus koraiensis Sieb. Et Zucc) forest is one of the most important regional climax forest types in Northeast China, of which more than 70% have become natural secondary forests after a century of timber exploitation and historical natural disturbances (Zhu et al., 2007). To meet the growing demands for timber, extensive areas of these secondary forests have been replaced by plantations predominantly of larch species (Zhu et al., 2008). In the eastern Liaoning Province of Northeast China, for example, there are about 200,000 ha of Larix olgensis Henry plantations in the montane regions (Liu et al., 2007); these plantations intersperse with the remnant natural forests to form mosaic of plantation/natural secondary forest landscapes. Given the extensive coverage and economic value, larch plantations have in recent years attracted much attention in their role for contributing to ecosystem functioning as well as timber production. Impacts of larch plantations on soil properties and nutrient cycling have been a particular research interest for concerns on sustainable forest productivity.
∗ Corresponding author. Tel.: +86 24 83970342; fax: +86 24 83970300. E-mail address: [email protected] (J.-J. Zhu).
Many studies have demonstrated that changes in land cover can influence soil biological properties and nutrient cycling (Yeates et al., 1997; Oberson et al., 2001; Sharma et al., 2004). However, the directions of the influences can vary depending on the type of land cover change. For example, it is reported that land cover change from grassland to conifers results in a reduction in soil microbial biomass, rate of soil respiration, and phosphatase activity (Chen et al., 2000). Similarly, changes from native forests to larch plantations have been found to result in significant decline in soil C and N concentrations (Chen and Li, 2003). In contrast, a conversion from native savanna to rice–pasture rotations causes improvement in biological properties (Gijsman et al., 1997). In general, conversion of natural forests to plantations has been found to result in reduction in soil nutrient availability and deterioration in microbiological properties (Wang and Wang, 2007; Yan et al., 2008). Compared with other major nutrients, P is known to be the least mobile element and to have low availability to plants under most soil conditions. The availability of P for plant growth depends on complex geochemical and biochemical processes (Walker and Syers, 1976). Land cover change may affect P inputs and outputs, resulting in an altered P balance and changes in P forms (Ross et al., 1999), and alter soil P transformation by modifying soil physical, chemical and biological properties, especially soil microbial processes (Chen et al., 2008). Soil microorganisms play a key role in facilitating P transformations through mineralization of P from
0378-1127/$ – see front matter. Crown Copyright © 2010 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2010.04.038
K. Yang et al. / Forest Ecology and Management 260 (2010) 422–428
organic sources, synthesis and release of organic P, and solubilization of barely soluble P forms (Oberson et al., 2001). Microbes also have the ability to rapidly immobilize considerable amounts of P when labile C is readily available (Bünemann et al., 2004). Most P utilized by plants is in inorganic forms (Marschner, 1995). Organic P accounts for about 15–80% of total P (Condron and Tiessen, 2005); the organically bound P needs to be mineralized to become available for plant uptake and utilization. Phosphatase activity has been considered to be an important driver in this mineralization process and to reflect organic P mineralization potential of soils (Chen, 2003; Criquet et al., 2004). However, the studies of Dilly and Nannipieri (2001) and Olander and Vitousek (2000) show that increased P availability depresses phosphatase activity in forest soils. Therefore the relationship between phosphatase activity and soil P availability still remains a controversial issue. Knowledge of the seasonal variation in soil P fractions is important for understanding the dynamics of P availability and mineralization in soils (Magid and Nielsen, 1992). Seasonal changes in soil P fractions may reflect P uptake by plants and mineralization–immobilization processes. The fluctuation in P fractions during the growing season, particularly soil P transformation process, is considered an important factor in controlling P availability and ultimately in influencing plant nutrition (Eviner et al., 2006). Several studies on temperate ecosystems have shown a considerable seasonal variation of P fractions (Chen et al., 2003; Styles and Coxon, 2007; Zhao et al., 2009). However, there also appear inconsistent findings (e.g. Tate et al., 1991; Magid and Nielsen, 1992; Fabre et al., 1996). For instance, the maximum values of soil bicarbonate-extractable inorganic P and bicarbonate-extractable organic P have been found to occur in summer (Zhao et al., 2009) or winter (Fabre et al., 1996), or there lacks significant seasonal variation in soil resin-extractable inorganic P (Tate et al., 1991). The variable results suggest that seasonal variation in soil P fractions might be dependent of ecosystem types and climatic conditions. In this study, we compared various forms of soil P between natural secondary forests and larch plantations in the montane region of eastern Liaoning Province of Northeast China, with aims to understand how the two contrasting forest types may differ in soil P properties. Detailed measurements were made on soil total P (TP), various fractions of soil P (i.e. organic P, inorganic P, sodium bicarbonate-extractable organic P, sodium bicarbonate-extractable inorganic P, aluminum-bound P, iron-bound P, and calcium-bound P), and the factors affecting P cycling and transformation (i.e. microbial biomass P and acid phosphatase activity). The objectives of this study were to determine: (1) how natural secondary forests and larch plantations would differ in the quantity and compositional structure of soil P; and (2) how seasonally variable the various P fractions would be in forests of the temperate climate. Our study was to test the hypothesis that forest conversion from native forests to larch plantations would reduce P availability and result in substantive compositional changes of soil P.
2. Materials and methods 2.1. Site description and experimental design The study was conducted at the Qingyuan Experimental Station of Forest Ecology of Institute of Applied Ecology, Chinese Academy of Sciences. The station is located in a mountainous region in the eastern Liaoning Province, Northeast China (latitude 41◦ 51 N, longitude 124◦ 54 E, elevation 500–1100 m above sea level). The climate of the region is a continental monsoon type with a humid and rainy summer, and a cold and dry winter. Mean annual air temperature varies between 3.9 and 5.4 ◦ C, and the maximum and minimum temperatures are 36.5 and −37.6 ◦ C. Annual precipitation fluctu-
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ates between 700 and 850 mm, with more than 80% falling during June–August. The growing season is from early April to late October (Zhu et al., 2007). The brown forest soil belongs to Udalfs according to the second edition of U.S. Soil Taxonomy (1999). The soil is a clay loamy soil (sand: 25.6%, silt: 51.2%, clay: 23.2%). The study site was originally occupied by primary mixed broadleaved-Korean pine forests until 1930s and subsequently subjected to decades of unregulated timber removal. A large fire that occurred in the early 1950s completely cleared off the original forests and the site was replaced by a mixture of naturally regenerating broadleaved native tree species. Since 1960s, patches of the secondary natural forests were cleared for larch plantations. Our sample plots were set up on three stands of natural secondary forests and three stands of larch plantations of the age 16–44 years. The six stands were selected from separate small watersheds over an area of 100 ha, with experimental plots set up on sites of slightly variable altitudes (from 568 to 730 m above sea level) and on gentle slopes of variable aspects as strict controls of altitude and slope aspect proven highly difficult because of the fragmented landscape in the region. Larch plantations often occur in small patches among the natural secondary forest stands in our study area. Where possible, we set up the larch plantation plots close to, but not necessarily adjacent with, the natural secondary forest sites to avoid complication by variation in topographical features. Overall, the six stands have the same topographical features and are on soils developed from the same parental material, i.e. granite gneiss. Soil depth of the study site varied from 60 to 80 cm and was comparable between LOP and NSF stands. However, the two types of stands differed in the thickness of the litter layer and A-horizon soil layer; the litter layer depth was 4.4–6.0 cm in the LOP stands and 2.7–5.6 cm in the NSF stands, whilst the A-horizon soil layer depth was 6.5–8.5 cm in the LOP stands and 8–10 cm in the NSF stands; the AB-horizon soil layer depth was about 10 cm; and the B-horizon soil depth varied between 30 and 40 cm. In each of the stands, three 20 m × 20 m plots were laid out in September 2006. The plots of natural secondary forests consisted of Juglans mandshurica, Quercus mongolica, Acer mono, Fraxinus rhynchophylla and Ulmus macrocarpa in the tree layer, A. triflorun, A. tegmentosum, A. mandshricum and Syringa amurensis in the understory component, and Cardamine leucantha, Allium monanthum, Arisaema amurense, and Polygonatum involucratum in the herbage component. The plots of larch plantations contain Acer tegmentosum, A. pseudo-sieboldianum, Schisandra chinensis, Syringa wolfi and Acanthopanax senticosus in the shrub layer and Cardamine leucantha, Rubia sylvatica, Spuriopimpinella brachycarpa in the herbage layer. 2.2. Soil sampling Soil samples were collected during the growing season in spring (April), summer (July) and autumn (September) of 2008. Soil cores of 5 cm in diameter were taken at nine random locations on each plot after removing litters, and each soil core was separated into 0–15 and 15–30 cm layers. The nine samples of the same layer on each plot were mixed as a composite sample, which was further divided into three sets of sub-samples. One set of the sub-samples was processed to pass through a 2 mm sieve, and stored at 4 ◦ C for measurements of microbial biomass P (MBP) and acid phosphatase activity (APA); one was air-dried and passed through a 1 mm sieve for analysis of soil pH, sodium bicarbonate-extractable inorganic P (NaHCO3 -Pi) and sodium bicarbonate-extractable organic P (NaHCO3 -Po); the remaining sub-sample was air-dried, and homogenized and passed through a 0.25 mm sieve for analyses of soil organic C (SOC), total N (TN), TP, organic P and fractions of inorganic P. The basic soil physical and chemical properties, seasonal variations in soil water content (%, v/v) in the natural secondary
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Table 1 Soil physiochemical characteristics in the natural secondary forest (NSF) and the Larix olgensis plantation (LOP). Forest type
SOC (g kg−1 )
0–15
NSF LOP
15–30
NSF LOP
Soil depth (cm)
TN (g kg−1 )
C/N
50.45 ± 4.25 34.70 ± 1.86
4.21 ± 0.52 3.20 ± 0.17
23.42 ± 2.63 23.97 ± 1.90
2.18 ± 0.32 2.38 ± 0.16
a
Soil bulk density (g cm−3 )
pH
12.3 ± 0.2 10.9 ± 0.1
a
5.82 ± 0.03 5.55 ± 0.05
1.32 ± 0.03 1.31 ± 0.01
11.1 ± 0.3a 10.0 ± 0.1
5.91 ± 0.05a 5.71 ± 0.04
1.45 ± 0.03 1.49 ± 0.02
a
SOC: soil organic C; TN: soil total N. Values shown in tables are means ± standard errors (n = 3). a Indicate significant differences between the natural secondary forest and the Larix olgensis plantation of the corresponding depth at P = 0.05 levels.
forest stands and larch plantations are listed in Tables 1 and 2, respectively. 2.3. Soil analyses Soil pH was estimated on a 1:2.5 soil–water mixture. Soil bulk density samples were measured at each soil depth using a known volume metal container. Bulk density measurements were performed by drying the soil at 105 ◦ C for 12 h and then reweighing the samples. Gravimetric soil water content was calculated from mass loss after drying for 12 h at 105 ◦ C in 0–15 and 15–30 cm of soil layers, respectively. The SOC and TN were analyzed by dry combustion on a Vario EL III elemental analyzer (Germany). The TP was determined following H2 SO4 –HClO4 digestion (Olsen and Sommers, 1982). Organic P was determined by ignition method of Saunders and Williams (1955), and inorganic P was computed as the difference between the TP and organic P. Soil MBP was determined by the chloroform fumigation extraction (soil: extractant [0.5 mol L−1 NaHCO3 ] ratio 1:20) method. The MBP was estimated from the relationship EP /KEP , where EP is the difference between inorganic P extracted from fumigated and unfumigated soils and KEP = 0.40 (Brookes et al., 1982). The correction for chloroform released P that was absorbed by soil colloids during extraction was made by adding 25 mg P kg−1 soil during extraction and then corrected for its recovery (Brookes et al., 1982). Soil APA was assayed by the method of Tabatabai (1994) at pH 6.5. Soil acid phosphatase activity was assayed at pH 6.5 rather than at the soil pH because of: (1) that the difference in soil pH between the NSF stands and the LOP stands is about 0.2–0.3 units apart; and (2) that the soil pH value of 6.5 is optimum for acid phosphatase activity. The NaHCO3 -Pi and NaHCO3 -Po were determined by Bowman and Cole (1978) method. The fractionation of inorganic P in soils was determined by a modified Chang and Jackson procedure (as described by Petersen and Corey, 1966). Soil samples were sequentially extracted with 0.5 mol L−1 NH4 F for aluminum-bound P (Al-P) determination, 0.1 mol L−1 NaOH for iron-bound P (Fe-P), and 0.5 mol L−1 H2 SO4 for calcium-bound P (Ca-P). All phosphate ions were determined by the ascorbic acid molybdenum antimony spectrophotometric method.
Table 2 Seasonal variations in soil water content (%, v/v) in the natural secondary forest (NSF) and the Larix olgensis plantation (LOP).
Fig. 1. Soil total P (TP), organic P (Po), and inorganic P (Pi) in the natural secondary forest (NSF) and the Larix olgensis plantation (LOP) at different seasons (standard errors from 3 samples shown by vertical bars).
2.4. Statistical analyses All reported values are expressed on air-dry soil weight basis. Statistical analyses were performed by using the SPSS 11.5 for Windows. One-way ANOVA was performed by soil layer, and LSD’s (least significant difference) test was applied post hoc to distinguish the differences of soil physiochemical properties between the NSF and the LOP. Repeated measures analysis of variance (ANOVA) was used to test the effects of forest types on various P variables of the same soil layer across the growing season. When there were significant interactions between the forest type and sampling season, one-way ANOVA was used to test the effects of vegetation type on soil P variables by sampling season and the effects of sampling season on soil P variables by forest types. Data were tested for normality and homogeneity of error variances to determine whether transformations were needed. Pearson linear correlations were used to assess the relationships between acid phosphatase activities and active soil P fractions (including MBP, NaHCO3 -Po and NaHCO3 -Pi).
Soil depth (cm)
Sampling season
Forest type NSF
LOP
3. Results
0–15
Spring Summer Autumn
30.4 ± 1.2a 34.8 ± 1.1a 26.7 ± 0.9a
27.5 ± 0.6 30.9 ± 0.8 21.7 ± 1.3
3.1. Total P, organic P, and inorganic P fractions
15–30
Spring Summer Autumn
24.0 ± 0.5 25.2 ± 1.9 19.6 ± 0.8
22.9 ± 1.2 25.0 ± 0.7 18.5 ± 1.2
Values shown in tables are means ± standard errors (n = 3). a Indicate significant differences between the natural secondary forest and the Larix olgensis plantation in same season of the corresponding depth at P = 0.05 levels.
Concentrations of total P and inorganic P were significantly higher in the LOP stands than in the NSF stands in both 0–15 and 15–30 cm soil layers (Fig. 1, P < 0.05), whilst the organic P concentration did not vary between the NSF and LOP stands each sampling season (Fig. 1). Sampling season had no significant effect on soil total P, inorganic P and organic P. Across the three seasons, soil
K. Yang et al. / Forest Ecology and Management 260 (2010) 422–428
Fig. 2. Soil Al-P, Fe-P and Ca-P in natural secondary forest (NSF) and Larix olgensis plantation (LOP) at different seasons (standard errors from 3 samples shown by vertical bars).
organic P accounted for 53–64% of total P in both types of stands, with the NSF stands having higher ratios of organic P to total P than LOP stands (Table 3). For inorganic P fractions, the NSF stands had significantly lower Fe-P concentration than the LOP stands. Specifically, the average concentrations of soil Fe-P in the NSF stands were 51.3 mg kg−1 lower in the 0–15 cm soil layer and 35.2 mg kg−1 lower in the 15–30 cm soil layer, respectively, than in the LOP stands across seasons (Table 3 and Fig. 2). There were no significant difference between NSF and LOP for Al-P and Ca-P concentrations in spring and autumn. Effects of forest type on Al-P and Ca-P concentrations were significant in summer in the 0–15 cm soil layer (P < 0.05). The NSF stands had significantly higher Al-P concentration and lower Ca-P concentration than the LOP stands. All the inorganic P fractions were lower in the 15–30 cm soil layer than in the 0–15 cm soil layer for both forest types (Fig. 2). The seasonal average concentrations of the inorganic P fractions followed a descending order of: FeP > Ca-P > Al-P. There was no significant effect of sampling season on concentrations of Al-P, Fe-P and Ca-P (Fig. 2). 3.2. Soil MBP, NaHCO3 -Po, and NaHCO3 -Pi MBP and NaHCO3 -Po concentrations were higher in the NSF stands than in the LOP stands in the 0–15 cm soil layer in spring and summer, and decreased with soil depth (Fig. 3). In the 0–15 cm soil layer, the concentrations of MBP and NaHCO3 -Po averaged across seasons were 14.2 and 4.2 mg kg−1 higher in the NSF stands than in the LOP stands, respectively (Table 3). The NaHCO3 -Pi concentration did not differ between the NSF and LOP stands across
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Fig. 3. Soil microbial biomass P (MBP), sodium bicarbonate-extractable organic P (NaHCO3 -Po) and sodium bicarbonate-extractable inorganic P (NaHCO3 -Pi) in the natural secondary forest (NSF) and the Larix olgensis plantation (LOP) at different seasons (standard errors from 3 samples shown by vertical bars).
seasons in both 0–15 and 15–30 cm soil layers. There was a significant effect of sampling season on MBP in both soil layers in the LOP stands, but not in the NSF stands. In the LOP stands, MBP concentration was higher in summer than in spring and autumn, with the maximum difference being 11.1 mg kg−1 in the 0–15 cm soil layer and 5.2 mg kg−1 in the 15–30 cm soil layer, respectively (Fig. 3). There was also a significant seasonal variation in soil NaHCO3 Po in the both types of stands in the two soil layers; significantly higher NaHCO3 -Po concentrations were also observed in summer than in spring and autumn (Fig. 3) (P < 0.05). In the NSF stands, the maximum seasonal difference in NaHCO3 -Po concentration was 13.9 mg kg−1 in the 0–15 cm soil layer and 10.7 mg kg−1 in the 15–30 cm soil layer, respectively; whilst in the LOP stands, the maximum seasonal difference in NaHCO3 -Po concentration was 3.0 mg kg−1 in the 0–15 cm soil layer and 3.6 mg kg−1 in the 15–30 cm soil layer, respectively. The NaHCO3 -Pi concentrations were relatively stable across seasons in both NSF and LOP stands. Effects of forest type on MBP/TP and NaHCO3 -Po/TP ratios were significant across seasons in both soil layers (Fig. 4): in the 0–15 cm soil layer, the MBP/TP was 5.5% in the NSF stands and 2.6% in the LOP stands; where as in the 15–30 cm soil layer, the MBP/TP was 1.8% in the NSF stands and 1.4% in the LOP stands. The NaHCO3 -Po/TP was 2.8% in the NSF stands and 1.6% in the LOP stands in the 0–15 cm layer, and 1.7% in the NSF stands and 1.0% in the LOP stands in the 15–30 cm layer, respectively, across seasons (Fig. 4). The difference in NaHCO3 -Pi/TP between the NSF and LOP stands was dependent on the sampling season. The NaHCO3 -Pi/TP was generally higher in the NSF stands than in the LOP stands. The MBP/TP and NaHCO3 Po/TP showed the similar seasonal patterns as MBP and NaHCO3 -Po
Table 3 The average (n = 9) of soil P fractions (mg kg−1 ) and acid phosphatase activities (mg kg−1 h−1 ) in the natural secondary forest (NSF) and the Larix olgensis plantation (LOP) across seasons. Soil depth (cm)
Forest type
Po
Pi
Al-P
Fe-P
Ca-P
MBP
NaHCO3 -Po
NaHCO3 -Pi
APA
0–15
NSF LOP
741 1025
TP
475 543
272 481
17.8 15.2
84.9 136.2
70.0 78.3
40.3 26.1
19.8 15.6
10.2 10.1
818 673
15–30
NSF LOP
627 897
376 495
251 402
13.9 11.6
68.0 103.2
53.5 53.4
12.5 11.8
10.1 8.3
4.5 5.2
448 277
TP: total P; Po: organic P; Pi: inorganic P; MBP: microbial biomass P; NaHCO3 -Po: sodium bicarbonate-extractable organic P; NaHCO3 -Pi: sodium bicarbonate-extractable inorganic P; APA: acid phosphatase activity.
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Fig. 4. Percent (%) of various active P fractions of soils in the natural secondary forest (NSF) and the Larix olgensis plantation (LOP) at different seasons (standard errors from 3 samples shown by vertical bars).
Fig. 5. Seasonal variation in acid phosphatase activity (APA) of soils in the natural secondary forest (NSF) and the Larix olgensis plantation (LOP) (standard errors from 3 samples shown by vertical bars).
in the two types of stands. There was a significant effect of sampling season on NaHCO3 -Pi/TP in both soil layers in the NSF stands (P < 0.05), but not in the LOP stands.
Fig. 6. Relationship between acid phosphatase activity and microbial biomass P (A), sodium bicarbonate-extractable organic P (NaHCO3 -Po) (B) and sodium bicarbonate-extractable inorganic P (NaHCO3 -Pi) (C) for the natural secondary forest and the Larix olgensis plantation in three seasons (n = 36, i.e. three plots × two soil depths × three seasons × two forest types). *, ** Significant at P < 0.05 and P < 0.01 respectively.
4. Discussion 3.3. Soil APA The value of APA was significantly greater in the NSF stands than in the LOP regardless of soil depth and sampling season (with an exception of the APA in the 0–15 cm soil layer in autumn), and was higher in the 0–15 cm soil layer than in the 15–30 cm soil layer (Fig. 5). The average value of soil APA in the NSF stands was 145 mg kg−1 h−1 greater in the 0–15 cm soil layer, and 171 mg kg−1 h−1 greater in the 15–30 cm soil layer, respectively, than in the LOP stands across seasons (Table 3). There was a significant effect of sampling season on APA in the 15–30 cm soil layer, with the maximum APA found in autumn, and the minimum in summer for both forest types. The maximum seasonal differences in APA were 189 mg kg−1 h−1 in the NSF stands and 124 mg kg−1 h−1 in the LOP stands, respectively. 3.4. Relationships between active soil P fractions and APA APA was positively correlated with MBP based on a combined dataset for both forest types (r = 0.822, P < 0.01, n = 36). Significant and positive correlations were also found for APA-NaHCO3 -Po and APA-NaHCO3 -Pi (Fig. 6). The two forest types did not differ in the relationships of APA with MBP, NaHCO3 -Po, and NaHCO3 -Pi.
This study has shown that the two forest types differed markedly in soil P chemistry. We found that the concentrations of total P, inorganic P, and Fe-P were significantly higher, and the concentrations of MBP, NaHCO3 -Po, and APA were significantly lower, in the LOP stands than in the NSF stands; whilst concentrations of organic P, NaHCO3 -Pi, Al-P, and Ca-P were comparable between the two forest types. The finding of generally greater amount of soil P in larch plantation than in natural secondary stand was contrary to our initial expectation of a reduced soil P availability with land cover change from native forests to coniferous plantations. Many factors may attribute to differences between different forest types in soil P. For example, differences in the quantity of plant litter inputs and chemical composition of the litter may be crucial ˜ et al., 2008; Redel drivers to alter the soil P concentration (Ordónez et al., 2008). In addition, plant species composition and root type can also influence soil P status in the ecosystem scale (Grierson and Adams, 2000). In this study, the difference in total P between the two forest types may be explained firstly by more abundant understory shrubs in the LOP (personal observation) and secondly by greater organic matter input as decaying roots and slash when original forest trees were cleared for planting L. olgensis. It has been shown by Liu et al. (1998) that the role of the shrub species and
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understory vegetation is very important in sustaining soil fertility in larch plantations. The organic matter inputs from leave decompositions can also affect P cycling in the soil (Wood et al., 2009). The results of this study also revealed seasonal patterns of total P, organic P and inorganic P for both two forest types, i.e. the concentrations of total P, organic P and inorganic P were relatively stable over time in both NSF and LOP stands. This result was consistent with previous studies in temperate forest ecosystems by Fabre et al. (1996). Since P as orthophosphate is largely the preferred source for plant P uptake, knowledge of the inorganic P fractions within soils is essential to understanding P bioavailability (McDowell and Stewart, 2006). It should be noted that the low pH values of the soils (5.55–5.91) might also influence the behavior of P due to P binding by Al and Fe in acid soils (Richter et al., 2006). The high proportion of Fe-P in the two forest types in our study was consistent with previous research in Chinese fir forest soils (Chen, 2003). The relative distribution of inorganic P fractions for the two forest types in decreasing order was Fe-P, Ca-P and Al-P in our study, which differed with the finding of Barroso and Nahas (2005) that the percentages of the P fractions decreased in the order of Fe-P, Al-P and Ca-P in Brazilian soils. Al-P content in the two forest types was lower than that in Brazilian soils because the former is a less weathered soil. In the current study, the concentrations of inorganic P fractions were significantly affected by forest types, especially the Fe-P fraction. Different phosphate-solubilizing microorganisms between the NSF and LOP stands may be responsible for Fe-P concentrations (Barroso and Nahas, 2005). Furthermore, the Fe oxide concentration could dominate the mechanisms governing values of Fe-P in temperate forest ecosystems (Darke and Walbridge, 2000). The results support the viewpoint that the soil inorganic P content varies with different forest ecosystems (Redel et al., 2008). Generally, Al-P increases with declining soil pH (Chen, 2003). But, in our study, Al-P concentration was not significant difference between the NSF and LOP stands, albeit significantly lower soil pH in the LOP stands than that in the NSF stands. The difference in soil pH between the NSF and LOP stands (0.2–0.3) could be too small to impose significant effects. Soil microbial biomass is an important component in most terrestrial ecosystems. A small change in microbial biomass could have a major impact on plant nutrient availability, at least in the shortterm. Furthermore, the P held in soil microbial biomass is a readily available P source for plants. In this study, soil MBP in the LOP was lower than in the NSF stands, supporting the finding of Wang and Wang (2007) that soil microbial biomass in pure coniferous plantations was lower than in natural broadleaved forests. Differences in the quantity and quality of organic matter returned to soil between the NSF and LOP stands, especially labile organic matter (including microbial biomass C), could be responsible for changes in soil MBP. On the other hand, changes in MBP between the NSF and the LOP stands observed in this study could also be influenced by microclimatic modifications, such as decreases in soil water content due to increased evaporation or hydraulic redistribution in the LOP stands. The results of a greater NaHCO3 -Po concentration in the NSF stands could be explained by faster microbial decomposition of plant litters in this forest type. Differences in the active soil P fractions (including MBP and NaHCO3 -Po) between the NSF and LOP stands implicate that soil organic P status might deteriorate following conversion of natural secondary forests to larch plantations. We found that the ratios of MBP/TP, NaHCO3 -Po/TP and NaHCO3 -Pi/TP were generally higher in soils of the NSF stands than of the LOP stands across seasons, and that MBP/TP and NaHCO3 -Po/TP were significantly higher in summer than in spring or autumn, which suggest that it is important to take temporal variations into consideration in the sampling
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strategy. The value of soil bioavailable P depends on the factors such as mineralization–immobilization of organic P, and adsorption–desorption and precipitation–dissolution of inorganic P (Frossard et al., 2000). Recently, Styles and Coxon (2007) shows that labile inorganic P concentration follows a distinct seasonal trend of winter maximum and summer minimum in western Ireland. However, we found that the NaHCO3 -Po/TP ratio was higher in summer and lower in spring or autumn in our study, contrary to the findings of Chen et al. (2003) and Styles and Coxon (2007). This may be because the NaHCO3 -Po fraction was affected by microbial biomass P and plant uptake (Fabre et al., 1996). Additionally, climatic factors such as soil and air temperatures, soil water content can also influence the seasonal dynamics of MBP and NaHCO3 -Po fraction (Magid and Nielsen, 1992). Phosphatase activity plays an important role in P bioavailability. It has been suggested as an indicator of P availability in soils and soil quality (Chen, 2003). Soil acid phosphatase activities in this study falls well within the range of the values reported in other forest ecosystems (Chen et al., 2000). Low soil APA activity observed in LOP stands than those in NSF stands were related to decrease soil organic matter and microbial biomass. We found that seasonal variations in acid phosphatase activities were small for both forest types and the maximum acid phosphatase activities in NSF and LOP occurred in autumn. Criquet et al. (2004) also reported a seasonal increase in the acid phosphatase activities during the cold period in an evergreen oak litter of the French Mediterranean area. In this study, acid phosphatase activities were significantly correˇ lated with MBP, consistent with the finding of Snajdr et al. (2008) that soil acid phosphatase positively correlated with total microbial biomass in Quercus petraea forest soil. In our study, APA was also positively correlated with NaHCO3 -Po and NaHCO3 -Pi, which is consistent with the previous finding by Grierson and Adams (2000), but differed with findings of Dilly and Nannipieri (2001) and Olander and Vitousek (2000). These contradicting findings may attribute to differences in the concentration of NaHCO3 -Pi because the concentrations of NaHCO3 -Pi in the range of 3.4–11.8 mg kg−1 in this study were much lower than in other studies (e.g. Dick, 1994). In summary, results from this study showed that the contents of soil MBP and NaHCO3 -Po were significantly higher in the native forest stands than in the larch plantation, whilst there was no significant difference in NaHCO3 -Pi between the two forest types, indicating that the native forests are better in maintaining soil organic P fertility than larch plantations. Our results also suggest that conversion of native forests to larch plantations in the region is more likely to cause compositional change in soil P than to result in reduction in overall P availability. Acknowledgements This research was supported by the 11th-Five-Year National Science and Technology Research Projects (2006BAD03A0401, 2006BAD03A0903) and the CAS/SAFEA International Partnership Program for Creative Research Teams (KZCX2-YW-445) and National Non-commercial Forests Project (200804027-05). References Barroso, C.B., Nahas, E., 2005. The status of soil phosphate fractions and the ability of fungi to dissolve hardly soluble phosphates. Appl. Soil Ecol. 29, 73–83. Bowman, R.A., Cole, C.V., 1978. An exploratory method for fractionation of organic phosphorus from grassland soils. Soil Sci. 125, 95–101. Brookes, P.C., Powlson, D.S., Jenkinson, D.S., 1982. Measurement of microbial biomass phosphorus in soil. Soil Biol. Biochem. 14, 319–329. Bünemann, E.K., Bossio, D.A., Smithson, P.C., Frossard, E., Oberson, A., 2004. Microbial community composition and substrate use in a highly weathered soil as affected by crop rotation and P fertilization. Soil Biol. Biochem. 36, 889–901.
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