Soil-nitrogen net mineralization increased after nearly six years of continuous nitrogen additions in a subtropical bamboo ecosystem

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ORIGINAL PAPER

Soil-nitrogen net mineralization increased after nearly six years of continuous nitrogen additions in a subtropical bamboo ecosystem

Yin-long Xiao1•Li-hua Tu1•Gang Chen1•Yong Peng1•Hong-ling Hu1•Ting-xing Hu1•Li Liu2

©Northeast Forestry University and Springer-Verlag Berlin Heidelberg 2015

In order to understand the effects of increasing atmospheric nitrogen(N)deposition on the subtropical bamboo ecosystem,a nearly six-year f i eld experiment was conducted in aPleioblastus amarusplantation in the rainy region of SW China,near the western edge of Sichuan Basin.Four N treatment levels—control(no N added),low-N(50 kg N ha-1a-1),medium-N(150 kg N ha-1a-1), and high-N(300 kg N ha-1a-1)—were applied monthly in theP.amarusplantation starting in November 2007.In June 2012,we collected intact soil cores in the bamboo plantation and conducted a 30-day laboratory incubation experiment.The results showed that the soil N net mineralization rate was 0.96±0.10 mg N kg-1day-1,under control treatment.N additions stimulated the soil N net mineralization,and the high-N treatment signif i cantly increased the soil N net mineralization rate compared with the control.Moreover,the soil N net mineralization rate was signif i cantly and positively correlated with the f i ne root biomass,the soil microbial biomass nitrogen content and the soil initial inorganic N content,respectively, whereas it was negatively correlated with the soil pH value. There were no signif i cant relationships between the soil N net mineralization rate and the soil total nitrogen(TN) content and the soil total organic carbon content and the soil C/N ratio and the soil microbial biomass carbon content,respectively.These results suggest that N additions would improve the mineral N availability in the topsoil of theP.amarusplantation through the effects of N additions on soil chemical and physical characteristics and f i ne-root biomass.

Nitrogen addition⋅Soil nitrogen net mineralization⋅Soil chemical and physical characteristics⋅Fine root biomass⋅Pleioblastus amarusplantation

Introduction

Since the 1960s,human activities have greatly promoted the release of reactive nitrogen(N)to the environment (Galloway et al.2003).Increasing reactive N has largely increased the amount of atmospheric N deposition added to terrestrial ecosystems around the world(Vitousek et al. 1997;Galloway et al.2004).The increasing N deposition has generated signif i cant effects on terrestrial ecosystems. For example,it may signif i cantly inf l uence the productivity of forest ecosystems(Thomas et al.2010),and it also may negatively impact the biodiversity of terrestrial ecosystems (Standish et al.2012;Porter et al.2012).As a common limiting element for plant growth in many terrestrial ecosystems(Vitousek et al.1982;Aber et al.1989),the cycling and availability of N can not only affect the process of succession and primary productivity in terrestrial ecosystems(Sparrius et al.2012;Morris and Standford 2011;Huang et al.2011;Hutchison and Henry 2010;Bundy et al.2011),but also further exert great inf l uence on climate change(Erisman et al.2011;Niu et al.2010).

Soil N mineralization largely determines its availability in soils and the rate of N cycling in forest ecosystems (Lovett and Rueth 1999).This is the biological process whereby organic N is converted to inorganic forms available for plant utilization.Given the importance of soil N mineralization,much research has been done but with inconsistent results in terms of the effects of N deposition on soil N mineralization.For example,there were studies fi nding that N deposition increased soil mineralization rates (Biudes and Vourlitis 2012;Sparrius and Kooijman 2013), whereas results that N deposition did not exert signif i cant effects on soil N mineralization rates were also reported (Turner and Henry 2010;Emmett et al.1995).This discrepancy largely depend on the comprehensive effects of N deposition on soil chemo-physical characteristics and f i neroot biomass in soils,both of which can inf l uence soil mineralization rates by affecting microbial activity in soils directly or indirectly(Rao et al.2009;Vourlitis et al.2007; Sparrius and Kooijman 2013;Fornara and Tilman 2012).

Notably,most of the studies have been conducted in semiarid shrub lands and coniferous and broad-leafed forests. However,studies about the responses of the bamboo forest soil N mineralization to N deposition have not been seen. Bamboo forestsare one ofthe mostimportantforesttypesand are distributed throughout the world,covering approximately 3678 k ha in total.About 2.5 billion people depend economically around bamboo in the world(Lobovikov et al. 2007).In China,bamboo plantations account for 3%of the forestarea(Chen etal.2009),and are mainly distributed in the southern provinces,where the level of atmospheric N deposition is among the highest in the world(Fang et al.2011,Tu et al.2011a).Therefore,it is critical to explore the effects of increasing N deposition on the soil N mineralization in the bamboo plantations in this region.In the present study,we determined the effects of nitrogen additions on soil-nitrogen net mineralization in aPleioblastus amarusplantation in the rainy region ofsouthwestChina,which located in the Sichuan basin,in western China(Zhuang and Gao 2002).Our objectives were(1)to detect how soil N mineralization in the bamboo plantation would change under N addition treatments,and(2)to explore the relationships between the soil chemo-physical characteristics,f i ne-root biomass and soil N mineralization in the bamboo plantation.

Materials and methods

Site description

The N addition experiment began in November 2007,in an 8-year oldPleioblastus amarus(10 ha)stand in Liujiang, SW,China(29°95′N,103°38′E,altitude 600 m a.s.l.).The region has a mid-subtropical humid mountainous climate (Zhuang and Gao 2002).The annual mean relative humidity is 86%and the monthly mean temperature is 6.6°C in January and 25.7°C in July.The mean annual precipitation from 1980 to 2000 was 1490 mm.The background wet N deposition measured in 2008 and 2009 was 82 and 113 kg N ha-1a-1,respectively(Tu et al. 2011a).The site was covered from cropland toP.amarusplantation since 2000,as part of the National Project of Converting Farmland to Forests(NPCFF).P.amarusis one of the bamboo species with a large forestation area in this region.At the time of our study,the plant density was 52,000 trees ha-1,and the mean diameter at breast height (DBH)was 2.3 cm.The aboveground dry biomass was 25.4 kg m-2in November 2007(Tu et al.2011b).The soil at the site is Dystric Purpli-Orthic Primosols,which is derived from purple sandstone and shale(Zhu and Li 1989).There was very little shrubbery or herbs in the understory at the time of experiment.

Experiment design

Twelve plotswere established,each measuring 3×3 m with about 5 m intervals.Four treatments were applied to 12 plots (3 plots per treatment):namely control(without N added); low-N(50 kg N ha-1a-1);medium-N(150 kg N ha-1-a-1);and high-N(300 kg N ha-1a-1).Three replicate plots were established for each treatment,and the plots were randomly selected to receive treatments.Fertilizer(NH4NO3) applications occurred monthly in 12 equal applications beginning in November 2007.In each application,the fertilizer was weighed,dissolved in 1 l of water,and applied to each plot using a portable sprayer.The control plot received 1 l water without any fertilizer.

Sampling method

In each plot,we randomly selected 3 sampling sites as replicates.After removing vegetation and litter,two polyvinylchloride(PVC)pipes(internal diameter 5 cm, length 12 cm and wall thickness 2 mm)were inserted into the top 10 cm of the mineral soil(the distance between the 2 pipes＜15 cm)in June 2012.One of the two pipes obtained in each sampling site was used to analyze the soil chemo-physical characteristics and the f i ne-root biomass, and the other one was used to incubate.All PVC pipes were sealed by Paraf i lm membranes and then gauzes were used to cover the Paraf i lm membranes and held by rubber rings to prevent the loss of soil samples.Subsequently,all of the pipes obtained were immediately transported to the laboratory for future analysis and incubation.

Soil analysis

For each plot,composite soil samples coming from one pipe of soil obtained at each sampling site were gently mixed;visible roots were picked out by tweezers;soil samples were homogenized and sieved through 2-mm mesh to remove rocks and other large pieces of organic matter; and then used for testing the following soil chemical and physical characteristics.Soil pH was measured with a glass electrode in a 1:2 mixture(by mass)of soil and water. Gravimetric soil moisture content was measured by drying soil subsamples at 105°C for 24 h.Soil microbial biomass carbon(MBC)and microbial biomass nitrogen(MBN) were determined by the chloroform fumigation extraction method with extraction coeff i cients of 0.45 and 0.54 for biomass C and N,respectively(Brooks et al.1985;Vance et al.1987).Soil organic C(TOC)and total N(TN)contents were determined using dichromate digestion and Kjeldahl distillation method(Nelson and Sommers 1982; Bremner 1965).Concentration of nitrate in soils was calculated from the difference of UV absorption at 210 nm (Kandeler 1995),whereas concentration of ammonium was measured using the indophenol-blue absorption(635 nm) method(Hidaka 1999).The concentrations of the NO3--N and ammonium,determined before incubation,were taken as the initial values.The f i ne roots taken out the soils in pipes were washed in running water and then dried at 65°C for 48 h and then weighed to calculate the f i ne root biomass.

Soil incubation

We removed the gauze covered on the other pipe obtained from each sampling site and replaced the spoiled Paraf i lm membranes with new ones.The pipes then were incubated in a constant-temperature room at 25°C in the dark for 30 days.The mineralization of the soil organic N was determined after a 30-day laboratory incubation period. Because there were no signif i cant differences between the gravimetric soil moisture contents under the four treatments(Table 1)and the Paraf i lm membranes could prevent water penetration and allow gas exchange effectively,we did not adjust the water content of soil cores during the incubation.The soil inorganic N(nitrate+ammonium) after incubation was measured as described above.

Data analysis

Rates of the soil net N mineralization during the incubation period were calculated from the differences of inorganic N concentrations between the initial and after incubation samples.Rates of nitrif i cation,ammonization and mineralization were calculated using the following equations:

wheretiandti+1were the initial and conclusion times, respectively,andtin this present study meant 30 days; [ammonium]iand[ammonium]i+1were the mean concentrations of ammonium of the soil cores of each treatment before and after incubation,respectively.The mean concentrations—[nitrate]iand[nitrate]i+1—of nitrate in the soil cores of each treatment were measured before and after incubation.Aammonium,Anitrate,andAmineralizationwere the accumulation of ammonium,nitrate and total inorganic N (ammonium+nitrate)during the incubation,respectively.Rammonium,RnitrateandRmineralizationrepresented soil net ammonization rate,nitrif i cation rate and N mineralization rate,respectively.

Statistical analyses

All statistical procedures were performed with statistical software package SPSS 16.0 for Windows(SPSS Inc., USA).One-way ANOVA with Fisher’s least signif i cant differences(LSD)test was used to test the differences of soil net ammonization,nitrif i cation,and N mineralization among N addition treatments,and to examine the impacts of N additions on soil chemo-physical characteristics and fi ne-root biomass.Pearson’s correlation was conducted to analyze the relationships between soil net N mineralization rates and soil chemo-physical characteristics and f i ne root biomass.

For all the data,LSD tests were used to separate means at the 0.05 probability level.Mean values in the text are given±1SE.

Results

Soil chemical and physical characteristics and f i ne root biomass

Nitrogen additions decreased the soil pH values,which ranged from 4.46±0.15 under the control treatment to 4.12±0.18 under the high-N treatment and there was a signif i cant difference between high-N and control (P＜0.05,Table 1).

Table 1 The soil chemo-physical characters and f i ne root biomass under N addition treatments before incubation

Soil inorganic N(the total amount of ammonium and nitrate)increased with N additions,which were 10.32± 1.56,10.28±0.86,12.15±0.49,and 14.36±1.54 mg kg-1under the control,low-N,medium-N and high-N treatment,respectively(Table 1)and the difference between the high-N treatment and the control was signif i cant (P＜0.05).The mean soil MBN content of the control plots was 0.023±0.0009 mg g-1(Table 1).N additions significantly increased the soil MBN content(P＜0.05).As for the soil TN content,it was 0.83±0.07 mg g-1under the control treatment(Table 1),and only high-N signif i cantly increased it by 13.2%compared with control(P＜0.05).

As to the soil MBC content,there was no signif i cant difference between control and low-N and medium-N (P＞0.05),while high-N signif i cantly increased it by 14.10%compared with control(P＜0.05).In the control plot,the soil TOC content was 9.75±0.36 mg g-1,while the average soil TOC contents were 10.01±0.22, 9.82±0.19,and 10.14±0.17 mg g-1in the low-N, medium-N and high-N plots,respectively(Table 1). Compared with control,low-N and high-N signif i cantly increased the soil TOC content(P＜0.05,Table 1).

Nitrogen additions did not pose a signif i cant impacton the mean soilC/Nratio,which were11.77±1.38,11.82±0.38, 11.47±0.48,and 10.77±0.43 in the control,low-N,medium-N,and high-N plots,respectively(P＞0.05,Table 1).

The f i ne-root biomass was 616.42±72.85 g m-2under the control treatment.Although the biomass increased with additions,the signif i cant difference in the f i ne-root biomass could only be found between high-N and control (P＜0.05,Table 1).

Soil N net mineralization and nitrif i cation

In the control plots,the mean of the soil N net mineralization rate was 0.96±0.10 mg N kg-1day-1(Table 2). The mean soil N net mineralization rates were 0.98±0.11, 1.06±0.11 and 1.35±0.13 mg kg-1day-1in the low-N,medium-N,and high-N treatment plots,respectively (Table 2).N additions increased soil N net mineralization rates by 2.08–40.63%,but the only signif i cant increase for soil N net mineralization between high-N and control (P＜0.05).The mean soil net nitrif i cation rate of the control plot was 0.064±0.032 mg kg-1day-1(Table 2), which only contributed to 6.67%of the soil net N mineralization rate.

The soil net nitrif i cation rates increased with the higher addition of N,which ranged from 0.069±0.007 mg kg-1day-1under low-N treatment to 0.145±0.005 mg kg-1day-1under high-N treatment.Although the high-N treatment signif i cantly increased the soil net nitrif i cation rate(P＜0.05),it still merely contributed to 10.74%of the soil net N mineralization rate,which indicates that ammonization was the main process for soil N net mineralization in thisP.amarusplantation.

Table 2 The effects of N addition on soil N net mineralization rate in the P.amarus plantation

Relationships between soil N net mineralization and soil chemo-physical characteristics and f i ne-root biomass

The soil N net mineralization rate for all four treatments was positively correlated with the f i ne-root biomass,soil MBN content,and soil inorganic N atP＜0.0001,P＜0.0001,andP=0.018,respectively,while it was negatively correlated with the soil pH value atP＜0.0001 (Fig.1).There were no signif i cant relationships between the soil net N mineralization rate and the soil TN content (P=0.09,R2=0.26),soil TOC content(P=0.09,R2=0.26),C/N ratio(P=0.38,R2=0.08),and the soil MBC content(P=0.10,R2=0.25),respectively(Fig.1).

Fig.1 The relationships for each treatment between soil net N mineralization rate and soil chemo-physical characteristics and f i ne root biomass in the P.amarus plantation

Discussion

The high-N signif i cantly increased the soil nitrif i cation, which still merely accounted for less than 11%of soil N mineralization in each treatment plot in theP.amarusplantation.The soil net ammonization rates and ammonium content in all of the treatments were greater than their corresponding soil N net nitrif i cation rates and nitrate content.This f i nding indicates that ammonization is dominant in the N transformation process and implies that the ammonium is the major form thatP.amaruslikes to utilize. Ammonization is helpful in preventing N leaching loss in the form of nitrate effectively in theP.amarusplantation.

Soil N mineralization in theP.amarusplantation was stimulated by N additions,consistent with the results of many other studies(Sparrius and Kooijman 2013;Vourlitis et al.2007;Gundersen et al.1998;Vitousek et al.1982). Considering that the soil pipes of the four treatments underwent the same temperature and similar gravimetric soil moisture content,we extrapolate that the different soil chemo-physical characteristics and f i ne-root biomass resulting from the different treatments may largely contribute to this stimulation.The linear model relationships found in this study between the soil N net mineralization rates and the soil chemo-physical characteristics and the fi ne-root biomass supports this conclusion.

To be specif i c,N additions signif i cantly increased the soil inorganic N,which was consistent with other resports (Song et al.2013;Liu et al.2011).We found that soil N net mineralization rate was signif i cantly and positively correlated with soil inorganic N for all treatment plots.This may be caused by the mechanism that increases of soil inorganic N was benef i cial for easing the competitions of N between mineralization of ammonif i ers and nitrif i ers,and plant uptake and immobilization of heterotrophic microorganisms so as to increase soil N mineralization(Matson et al. 1999;Aber et al.1998,1989).

Meanwhile,N additions signif i cantly increased soil MBN content in theP.amarusplantation.As a major N sink during N immobilization and a source during N mineralization,the increase in soil MBN content is helpful to reduce the immobilization of N,thus increasing soil N mineralization(Bardgett et al.2007;Singh et al.1989; Wardle et al.2004).That is probably why a signif i cant and positive relationship exists between soil N net mineralization rate and soil MBN content in theP.amarusplantation, which was also consistent with many other related studies (Dong et al.2012;Smaill et al.2010).

As one of the most important soil chemical characteristics,soil pH can strongly affect the rates of soil N transformation(Tietema et al.1992;Bertrand et al.2007). Soil pH can be regarded both as a factor affecting soil N mineralization and as a result of this process(Uri et al. 2003).In the present study,N addition signif i cantly decreased soil pH values in theP.amarusplantation.Many other studies also revealed that soil pH values were negatively correlated with soil N net mineralization rate(Lovett and Rueth 1999;Zhao et al.2010).However,the results in terms of the relationships between soil pH and soil N net mineralization were inconsistent.For example,Cookson et al.(2007)conducted a laboratory incubation of forest soils and reported that soil pH was positively correlated with soil N net mineralization;Tietema et al.(1992)found there was no signif i cant relationship between soil pH and soil N net mineralization.The major reason behind the different relationships may be due to the different impact extent of pH values on gross N mineralization and immobilization rates(Cheng et al.2013).Specif i cally,either gross N immobilization rates increased slower or decreased faster than gross N mineralization rates with soil pH decreasing with N additions.This could result in an increasing tendency in soil N net mineralization rates with decreasing soil pH in theP.amarusplantation.

Fine-root biomass is the largest component of belowground production and plays a substantial role in the biogeochemical cycles of terrestrial ecosystems(Yuan and Chen 2012;McCormack et al.2013).In our study,we found N addition stimulated the increase of f i ne-root biomass,which coincides with other studies(Fornara and Tilman 2012;Yuan and Chen 2012).Moreover,a positive linear relationship was found between f i ne-root biomass and soil net N mineralization rate.It was reported that the increase in f i ne-root biomass can lead to the increase of root-derived C(Xu and Juma 1994;Darwent 2003).Normally,root-derived C is positively correlated with the microbial release of extracellular enzymes involving in the breakdown of organic N,which is coupled with stimulating microbial activity and accelerating N transformation in the soils(Yin et al.2013).Thus,the increase of f i ne-root biomass may contribute to the phenomenon of the increase of soil N net mineralization under N additions.

A large body of studies conducted during a growing season identify soil C/N ratio as an important predictor of soil N mineralization and nitrif i cation rates(Lovett et al. 2002;Christenson et al.2009).In the present study,the failure to detect a signif i cant relationship between soil C/N ratio and N mineralization parameters is somewhat surprising.However,this may imply a shift in controls on soil N transformation processes under N additions.

On the whole,our results suggest that N additions would improve mineral N availability in the topsoil of theP. amarusplantation through the effects of N additions on soil chemical and physical characteristics and f i ne-root biomass.However,the response of soil N transformationprocesses in this ecosystem to N deposition in the long run is uncertainty,for the continuous increases of N deposition in this area.

AcknowledgmentsThis study was funded by the National Science Foundation of China(No.31300522)and Specialized Research Fund for the Doctoral Program of Higher Education of China(No. 20125103120018).

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15 March 2014/Accepted:3 May 2014/Published online:21 July 2015

Project funding:This research was supported by the National Natural Science Foundation of China(No.31300522)and Specialized

Research Fund for the Doctoral Program of Higher Education of China(No.20125103120018).

The online version is available at http://www.springerlink.com

Corresponding editor:Chai Ruihai

✉Li-hua Tu iamtlh@163.com

1College of Forestry,Sichuan Agricultural University, Chengdu 611130,Sichuan,China

2Personnel Department,Sichuan Agricultural University, Ya’an 625014,Sichuan,China