Soil_microbial_biomass_activity_and_nitrogen_transformations_in_a_turfgrasschronosequence
Soil microbial biomass,activity and nitrogen transformations
in a turfgrass chronosequence
Wei Shi a,*,Huaiying Yao a,1,Daniel Bowman b
a
Department of Soil Science,North Carolina State University,Campus Box 9619,Raleigh,NC 27695-7619,USA
b
Department of Crop Science,North Carolina State University,Raleigh,NC 27695,USA
Received 16September 2004;received in revised form 13May 2005;accepted 19May 2005
Abstract
Understanding the chronological changes in soil microbial properties of turfgrass ecosystems is important from both the ecological and management perspectives.We examined soil microbial biomass,activity and N transformations in a chronosequence of turfgrass systems (i.e.1,6,23and 95yr golf courses)and assessed soil microbial properties in turfgrass systems against those in adjacent native pines.We observed age-associated changes in soil microbial biomass,CO 2respiration,net and gross N mineralization,and nitri?cation potential.Changes were more evident in soil samples collected from 0to 5cm than the 5to 15cm soil depth.While microbial biomass,activity and N transformations per unit soil weight were similar between the youngest turfgrass system and the adjacent native pines,microbial biomass C and N were approximately six times greater in the oldest turfgrass system compared to the adjacent native pines.Potential C and N mineralization also increased with turfgrass age and were three to four times greater in the oldest vs.the youngest turfgrass system.However,microbial biomass and potential mineralization per unit soil C or N decreased with turfgrass age.These reductions were accompanied by increases in microbial C and N use ef?ciency,as indicated by the signi?cant reduction in microbial C quotient (q CO 2)and N quotient (q N)in older turfgrass systems.Independent of turfgrass age,microbial biomass N turnover was rapid,averaging approximately 3weeks.Similarly,net N mineralization was w 12%of gross mineralization regardless of turfgrass age.Our results indicate that soil microbial properties are not negatively affected by long-term management practices in turfgrass systems.A tight coupling between N mineralization and immobilization could be sustained in mature turfgrass systems due to its increased microbial C and N use ef?ciency.q 2005Elsevier Ltd.All rights reserved.
Keywords:Microbial biomass;N mineralization;Nitri?cation;Microbial quotient;Bermudagrass;Turfgrass
1.Introduction
Turfgrasses,including golf courses,parks and home lawns,are essential components of the urban landscape,providing both recreational and environmental bene?ts (Beard and Green,1994).Over 20million ha,roughly 14%of the cropland area,is managed as turfgrasses in the USA (Qian and Follett,2002).There is widespread public concern that turfgrass systems are environmentally proble-matic due to intensive use of fertilizers,pesticides,and irrigation.Nitrate (NO K 3)pollution of water via leaching
and runoff has been a primary focus of environmental research efforts in turfgrass systems (Petrovic,1990;Geron et al.,1993;Miltner et al.,1996).
Denitri?cation has also recently received some attention (Horgan et al.,2002).Despite their fundamental role in governing soil N-cycle processes and therefore the environmental fate of soil and fertilizer N,soil microbes in turfgrass systems remain poorly https://www.sodocs.net/doc/e09880312.html,rmation on turfgrass soil microbiology is crucial to understanding the system’s ecology,and will facilitate the development and implementation of environmentally sound management programs,especially with respect to N fertilization.
Soil microbes affect the availability of soil N for uptake or loss mainly through the concurrent processes of mineralization and immobilization.A tight coupling between these processes could limit the pool size of soil mineral N and accordingly reduce the potential of N loss from soils.The balance between
mineralization
Soil Biology &Biochemistry 38(2006)311–319
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0038-0717/$-see front matter q 2005Elsevier Ltd.All rights reserved.doi:10.1016/j.soilbio.2005.05.008
*Corresponding author.Tel.:C 19195134641;fax:C 19195152167.
E-mail address:wei_shi@https://www.sodocs.net/doc/e09880312.html, (W.Shi).1
Present address:Environmental and Resource Sciences,Zhejiang Univeristy,Kaixuan Road,Hangzhou 310029,People’s Republic of China.
and immobilization is related to the quality of soil organic matter as well as the attributes of soil microbial community. As a general rule,net mineralization or net immobilization can be simply estimated with the growth ef?ciency of soil microbial community and the C-to-N ratios of the microbial community and its substrate(Chapin et al.,2002).In many undisturbed ecosystems,such as forests and native grass-lands,microbial N immobilization is often signi?cant and comparable to microbial N mineralization(Davidson et al., 1990;Stark and Hart,1997).In contrast,management practices imposed on agricultural and other managed systems often disturb soils.In these ecosystems,microbial N mineralization may become dominant and conceal the signi?cance of microbial N immobilization.For example,a recent study showed that microbial N immobilization was insigni?cant in an agricultural soil,even after amendment with compost(Shi and Norton,2000).However,?ndings to the contrary have been reported for agricultural soils. Sizeable microbial N immobilization occurred in cultivated soils that were subjected to long-term organic farming practices(Burger and Jackson,2003).The discrepancy may simply be due to differences in the quality of soil organic matter.However,the disparity in the results may also arise from the differences in microbial biomass,activity,and eco-physiology caused by management history.
Soil microbial biomass,activity and N transformations could be affected by a number of factors associated with the age of a turfgrass system.In newly created turfgrass systems,soil microbes are exposed to signi?cant soil disturbance and associated adjustments in soil physical and chemical properties due to construction and establish-ment.The prevailing disturbances may include partial replacement of surface soil with the subsoil or sand from an external source,soil compaction and an abrupt change in landscape cover and thus plant residues.As turfgrass systems age,soil microbes will be progressively challenged by changing environments associated with long-term management practices.As a major management component, N fertilization may have considerable impacts on soil and soil microbial community.Studies conducted in other managed ecosystems showed that N fertilization suppressed soil fungi and led to a bacteria-dominant community (Bardgett et al.,1996,1999;Yeates et al.,1997).N fertilization may also change the quality of soil organic matter(i.e.C-to-N ratio)due to biotic and abiotic stabilization of mineral N into soil organic matter(Sˇimek et al.,1999).Recent studies demonstrated that N fertiliza-tion altered soil enzyme activities(Andersson et al.,2004; Deforest et al.,2004).However,despite that turfgrass systems are generally managed at a high level,their soils are not tilled in the traditional sense.The grass canopy grows continuously,uninterrupted by harvest and crop removal. Leaf clippings are usually left on the turf and allowed to decompose.Consequently,turfgrasses represent a highly managed ecosystem in which soil organic C is likely to accumulate(Qian and Follett,2002;Bandaranayake et al., 2003).
A turfgrass chronosequence represents a practical system to evaluate temporal changes in soil microbial properties and N transformations that regulate soil N availability and thus the potential of N loss in turfgrass systems.Inclusion of adjacent natural lands from which turfgrass systems were constructed would facilitate a better assessment of ecological sustainability of the turfgrass system.We hypothesized that in spite of the possible impacts of soil disturbance during construction and subsequent long-term management practices,soil microbial biomass,activity and rates of N transformations would increase with soil organic C as turfgrass systems age.Our objectives were to(1) monitor changes in soil microbial biomass and activity,(2) evaluate the relationships of N transformations,and(3) assess soil microbial biomass C and N use ef?ciency as a function of turfgrass age.Soil microbial properties in turfgrass systems were then evaluated against those in adjacent natural ecosystems.
2.Materials and methods
2.1.Turf sites
Four golf courses were selected as study sites.Each was in or near the renowned Pinehurst Resort and Country Club, located in the Sandhills region of North Carolina,USA.The courses were established in1907,1979,1996,and2001and were95,23,6,and1years old,respectively,when soil samples were taken.They were in close proximity and had similar or identical soils(sand or loamy sand).Soil types are the Candor(Sandy,siliceous,thermic Arenic Paleudults)at three courses(95,23,and6years old)and Ailey(Loamy siliceous,thermic Arenic Kanhapludults)at the1-year-old course.All sites were planted to hybrid bermudagrass (Cynodon dactylon X transvaalensis),a warm-season perennial.The oldest site had been replanted with different grasses or varieties over the years,but a continuous canopy of turfgrass was maintained on all the courses.All sites received annual applications of N,usually in split applications(i.e.three or four times per year)averaging approximately150kg N ha K1yr K1.Although early records for the sites were not available,it is likely that the oldest course received lower amounts of N per year during the?rst half of the20th century,mainly from natural organic sources such as composted manure or feather meal. Inorganic and synthetic organic sources have been the most common N fertilizers during the past50years. Turfgrasses were also fertilized with phosphorus(P)and potassium(K),dolomitic lime(CaCO3C MgCO3)and treated with pesticides as needed.
All turf sites were constructed on undeveloped land.The ‘holes’of the golf courses were planted in de?ned areas cleared from pine forests.Native pines were left standing
W.Shi et al./Soil Biology&Biochemistry38(2006)311–319 312
between the holes,such that each hole is essentially an island of managed grassland surrounded by a non-managed buffer of native trees and a few understory plants. Considerable soil disturbance usually occurs during golf course construction,especially on more recent courses. Topsoil may be stockpiled,tree stumps are usually removed, and shaping surface contours mixes layers.Since the soils in the Sandhills region are almost uniformly sandy,the disturbance during construction probably had little affect on soil texture.We measured surface soil texture(i.e. 0–15cm depth)for samples collected from the1-yr-old turfgrass system and the adjacent native pines.Turfgrass soil contained91.3%sand,5.0%silt and3.7%clay,very similar to the pine soil which consisted of89.2%sand,8.0% silt and2.7%clay.A second difference between the turf and pines is that the pines are not fertilized.While they may not be considered a natural ecosystem,given their proximity to highly disturbed areas,these undisturbed zones represented a reasonable reference for the highly managed turfgrass systems and therefore were included in the current study to assess environmental and ecological sustainability of managed turfgrass systems.
2.2.Soil sampling
Soils were sampled from six individual fairways selected at random within each golf course in December2002when turfgrasses were dormant.Four cores(5cm diameter! 15cm length)were taken from each fairway/plot.The24 cores were assembled into four replications;each replica-tion consisted of one core each from the six fairways per golf course.Soil cores were obtained in an identical manner from the native pines(w2–3m from trees).Soils from these ‘buffers’were used to assess the variability between sites independent of the golf course development,and as a comparison for the highly managed turfgrass system.Intact soil cores were placed on ice and transported to the lab.The cores were then sectioned into0–5and5–15cm depths.Soil from each section was sieved(!4mm),and stored at48C for later analysis after visible roots and plant residues were removed with tweezers.
2.3.Soil chemical and microbiological analyses
The dry combustion method was used to determine total soil C and N using a Perkin–Elmer2400CHN analyzer.Soil NH C4-and(eNO K3C NO K2T-N were determined on a1M KCl extract using the colorimetric method with a Lachat?ow-injection autoanalyzer(Lachat Instruments, Mequon,WI).Soil pH was measured in water(soil(g)to H2O(ml)Z1:2.5).Selected soil properties are given in Table1.Soil C and N in the youngest turfgrass system were lower than those in native pines.This may be due to increased organic matter decomposition following soil disturbance,or more likely,the excavation and soil mixing and replacement associated with golf course construction.
Soil microbial biomass C and N were determined by the chloroform fumigation extraction method(Brookes et al., 1985;Vance et al.,1987).Organic C in fumigated and unfumigated extracts was measured with a total organic C analyzer(TOC-5000Shimadzu).Organic N in fumigated and unfumigated extracts was measured with the alkaline persulfate oxidation method(Cabrera and Beare,1993).We calculated soil microbial biomass C and N by dividing the difference of total extractable C(or N)between fumigated and unfumigated samples by the conversion factors0.45for biomass C and0.54for biomass N(Brookes et al.,1985; Vance et al.,1987).
https://www.sodocs.net/doc/e09880312.html, C and N mineralization
Net soil C mineralization in turfgrass and native pine soils was determined with a35-day incubation study.Brie?y,?ve 20ml scintillation vials,four containing w12g soil(dry wt equiv)and one containing5ml0.5M NaOH as an alkaline trap to absorb respired CO2–C,were placed in0.5l Mason
Table1
Selected soil properties at0–5and5–15cm soil depths of turfgrass systems and adjacent native pines
Soil C(mg C or N g K1soil)Soil N(mg C or N
g K1soil)
Soil C-to-N NH C
4
–N(m g N g K1
soil)
NO K3–N(m g N g K1
soil)
pH
0–5cm depth
Native pines26.2c0.9d28.9a 1.5a0.0d 4.7c
1-yr turf9.5d0.6d15.2b0.2a8.1c 6.4ab
6-yr turf30.4bc 2.3c13.4bc0.1a25.6b 6.4a
23-yr turf38.4b 3.1b12.6bc0.2a24.9b 6.4a
95-yr turf72.5a7.0a10.4c0.9a50.8a 6.1b
5–15cm depth
Native pines9.5b0.4bc26.7a0.5a0.2d 5.0d
1-yr turf 2.3c0.2d11.3bc0.2a 1.2cd 5.6c
6-yr turf 2.8c0.3cd9.2c0.0a 2.4c 6.3a
23-yr turf8.2b0.5b18.1b0.0a 4.6b 6.2a
95-yr turf13.3a 1.1a12.3bc0.0a 6.8a 5.9b
Different letters within each column of0–5cm or5–15cm soil depths indicate the signi?cant difference of mean values(P!0.05)by multiple comparisons of Bonferroni t-test.
W.Shi et al./Soil Biology&Biochemistry38(2006)311–319313
jars.Due to high soil organic C,only8g soil from the0–5cm soil depth of the oldest site was used.Distilled water was added to the jars to maintain high relative humidity and minimize soil water loss during the incubation.Three jars containing four empty scintillation vials and one alkaline trap were used as controls.All the soil samples were adjusted to a moisture content of45%water holding capacity and pre-incubated at room temperature(about218C)for1week before incubation.During the incubation,the alkaline traps were removed periodically(i.e.about every4and10days for the beginning and later periods of incubation,respectively) from the Mason jars,the jars were?ushed with fresh air for 30min and fresh alkaline traps were installed.To determine CO2–C production,alkaline trap solutions were titrated with 0.1M HCl(Zibilske,1994).Net C mineralization was calculated by summing all the CO2–C measurements during the incubation.
A set of incubation units was used to determine net soil N mineralization,potential nitri?cation and microbial biomass C and N during a35-day incubation.Each unit contained four scintillation vials with soil samples;one was used for the determination of soil inorganic N,one for potential nitri?cation,and the other two for microbial biomass C and N.Soil was removed for analysis of10and35days after the start of incubation.Soil inorganic N,microbial biomass C and N and potential nitri?cation on day0were determined on pre-incubated https://www.sodocs.net/doc/e09880312.html, soil N mineralized was calculated by subtracting day0inorganic N from that measured at the end of the incubation.Nitri?cation potential was assessed by the shaken soil slurry method(Hart et al.,1994b).
2.5.Gross N mineralization and microbial NH C4 consumption
We determined gross N mineralization and microbial NH C4consumption with the15N pool dilution technique (Hart et al.,1994a).The rates were measured5and21days after beginning the soil incubation.Two20ml scintillation vials containing w12g soil(dry wt equiv)were placed in 0.5l Mason jars(as before,8g soil from the0–5cm soil depth of the oldest site was used).Soil samples were labeled with15NH4Cl of w50%enrichment to determine rates of gross N mineralization and microbial NH C4consumption. The15NH4Cl solution was uniformly injected in the soil in 10aliquots with a needle and syringe,with the addition increasing the soil water content to w60%soil water holding capacity.The15NH4Cl was added at6m g N g K1 soil with the exception that10m g N g K1was used for the0–5cm samples from the oldest turfgrass system.This was due to the soil NH C4pool in the oldest system being insuf?cient for subsequent15N analysis
From each Mason jar,one soil sample was extracted with 100ml1M KCl1h after the15N injection and the other 25h later.A diffusion procedure was used to prepare samples for the analysis of15N in the NH C4pools(Stark and Hart,1996),and15N enrichments were analyzed by continuous-?ow direct combustion and mass spectrometry. The rates of gross N mineralization and microbial NH C4 consumption were calculated by the method of Hart et al. (1994a).
2.6.Microbial resource use ef?ciency
Microbial C quotient(q CO2,the CO2–C respiration per unit of soil microbial biomass)and microbial N quotient (q N,the mineralized N per unit of soil microbial biomass) were used to evaluate changes in soil microbial C and N use ef?ciency with the chronological development of turfgrass systems(Smith et al.,1994;Flie?bach et al.,2000).The q CO2was calculated by dividing the accumulated CO2–C in the35-day incubation by soil microbial biomass C and the q N was estimated by dividing the potentially mineralized N in the35-day incubation by soil microbial biomass N.
2.7.Data analysis
To determine the degree of similarity of soils from the four study sites,the soils under the native pines adjacent to the turfgrass systems were compared using one-way ANOVA.This analysis showed that these soils did not differ in chemical and microbiological properties.There-fore,the four pine buffers were considered as one treatment in the analysis of soil and microbiological data of turfgrass systems.ANOVA of a split-plot design with restricted randomization on sites was used to determine signi?cant differences among land uses,ages of turfgrass systems and soil depths;intact soil cores corresponding to individual sites(i.e.native pines,or1,6,23,and95-yr-old turfgrass systems)being the whole plot,soil depth being the split-plot,and four replications being nested within the individual sites.Separation of means was performed with Bonferroni multiple t-test(SAS Institute,Inc.,2001,Cary,NC,USA).
3.Results
3.1.Soil microbial biomass and activity
Soil microbial biomass C and N increased with age of the turfgrass systems(Fig.1).The increase was more pronounced in the0–5cm soil depth than in the5–15cm soil depth.Biomass C and N in the0–5cm soil depth from the oldest turfgrass system were about six times higher than those in the youngest turfgrass soil.Microbial biomass C-to-N ratio was lower in turfgrass systems than in the adjacent native pines(Fig.1),although statistical signi?cance only occurred in the0–5cm soil depth.
Microbial respiration(i.e.potentially mineralized C) increased with the age of turfgrass systems,again being more prominent in soils from0to5cm than in5to15cm (Fig.2).Soil in the youngest turfgrass system evolved slightly more CO2–C than the native pines,whereas the
W.Shi et al./Soil Biology&Biochemistry38(2006)311–319 314
oldest turfgrass system generated w 3times more CO 2–C than the native pine soil (Fig.2).3.2.Microbial N transformations
Potentially mineralized N increased signi?cantly with turfgrass age (w 4times increase from youngest to oldest site)in soils sampled from 0to 5cm (Fig.2).A rapid
increase in N mineralization potential occurred following turfgrass establishment,as indicated by the three-fold difference between the 1-yr-old turf site and the adjacent pines.Gross N mineralization,microbial NH C 4consumption and nitri?cation potential increased with turfgrass age and these changes were also more evident in the 0–5cm than in the 5–15cm soil depth (Fig.3).Rates of potential nitri?cation were consistently about twice the rates of gross N mineralization (Table 2),independent of turfgrass age.Similarly,rates of microbial NH C 4consumption were roughly twice the rates of gross N mineralization (Table 2).Despite the age factor and differences in soil environ-ment between turfgrass systems and native pines,the ratios of net-to-gross N mineralization and gross N mineraliz-ation-to-microbial biomass N did not change substantially (Table 2).For the 0–5cm soil depth,the average ratio of net-to-gross N mineralization was approximately 1–to–10,and the turnover time of microbial biomass N (i.e.microbial biomass-to-gross N mineralization ratios)was w 20days (Table 2).
3.3.Relationships of microbial biomass and mineralization to soil organic matter
Net C (or N)mineralization as a fraction of total soil C (or N)decreased with turfgrass system age (Table 3).This reduction was more signi?cant for soils sampled from the 0–5cm than the 5–15cm depth.In the youngest
turfgrass
Fig.1.Microbial biomass and its C-to-N ratio at 0–5and 5–15cm soil depth of turfgrass systems and adjacent native pines.Values are averages of soil samples from individual sites.Error bars represent the standard error of the
mean.
Fig.2.Potentially mineralized C and N for soils sampled from 0to 5and 5to 15cm soil depth of turfgrass systems and adjacent native pines.Values are averages of soil samples from individual sites.Error bars represent the standard error of the
mean.
Fig.3.Gross N mineralization,microbial NH C 4consumption and potential rates of nitri?cation for soils sampled from 0to 5and 5to 15cm soil depth of turfgrass systems and adjacent native pines.Values are averages of soil samples from individual sites.Error bars represent the standard error of the mean.
W.Shi et al./Soil Biology &Biochemistry 38(2006)311–319315
systems,approximately5%of soil C and2%of soil N mineralized during the incubation.By contrast,only1.6% of soil C and0.6%of soil N were mineralized in the oldest turfgrass system,equivalent to values from native pine soils (Table3).
Microbial biomass C(or N)as a fraction of total soil C (or N)also decreased with turfgrass age(Table3).This fraction was highest in the newly created turfgrass system, with the exception of microbial biomass N in the5–15cm soil depth.However,as the turfgrass system aged,the fraction of soil microbial biomass C and N declined, approaching to that in the native pine soil(Table3).3.4.Microbial resource use ef?ciency
Microbial C quotient(q CO2)and microbial N quotient (q N)changed with both the age of the turfgrass systems and the alterations in their soil environment from native pines(Table4).The values of q CO2decreased with turfgrass age in soil from0to5cm(Table4),but were not signi?cantly affected in soil from5to15cm. Similarly,q N values(0–5cm depth)were lower in old than in young turf soils.
4.Discussion
4.1.Soil microbial biomass and activity
It is generally accepted that soil microbial population size increases with the accumulation of soil organic matter (Jenkinson and Ladd,1981).While microbial biomass on a soil weight basis increased with age,it decreased on a soil C or N basis(Fig.1,Table3).This indicates that C and N available for microbial growth did not increase propor-tionate to the accumulation of soil organic C and N as turfgrasses aged.
In the short term,construction of turfgrass systems from native pines resulted in lower soil C(Table1),but microbial biomass and activity in the0–5cm soil depth remained unchanged(Figs.1and2).This suggests that in young, recently established turfgrass systems,soil microbes obtain their energy and C and N primarily from fresh organic materials.Turfgrasses contribute organic residues largely via clippings which sift into the canopy;depositing readily available soil C and N at the top of the soil pro?le.Root turnover adds organic C and N deeper in the soil pro?le,but the amounts are apparently limited compared to the accretion that occurs at the surface.Consequently,soil
Table2
The ratios of N transformations for soils sampled from0to5and5to15cm soil depth of turfgrass systems and adjacent native pines
Pot./Min.Con./https://www.sodocs.net/doc/e09880312.html, min/
Min MBN/Min., days
0–5cm depth
Native pines 1.59a0.72a0.08a23.13a
1-yr turf 3.16a 1.84b0.13a16.35a
6-yr turf 2.36a 2.43b0.17a25.77a
23-yr turf 1.94a 2.04b0.06a12.66a
95-yr turf 2.53a 1.62b0.12a21.49a
5–15cm depth
Native pines 6.09a 2.88a0.42b40.91b
1-yr turf14.45a 2.34a0.39b25.85ab
6-yr turf 2.69a 3.99a0.33b26.32a
23-yr turf 6.55a 4.75a0.54b34.90ab
95-yr turf 4.63a 2.16a0.07a21.81a Different letters within each column of0–5or5–15cm soil depth indicate signi?cant difference of mean values(P!0.05)by multiple comparisons of Bonferroni t-test.Min:gross N mineralization,Con:NH C4consumption, Pot:nitri?cation potential,Net min:net N mineralization,and MBN: microbial biomass N.
Table3
The percentage of total soil C and N that was mineralized or that was in microbial biomass for soils sampled from0to5and5to15cm soil depth of turfgrass systems and adjacent native pines
Mineralized C Mineralized
N
Biomass C Biomass N
as a fraction of total soil C or N(%)
0–5cm depth
Native pines 1.52d0.47c0.84c 3.44c
1-yr turf 4.82a 1.82a 1.91a 6.58a
6-yr turf 3.19b 1.02b 1.86ab 4.47b
23-yr turf 2.04c0.60c 1.77ab 3.77bc
95-yr turf 1.64cd0.59c 1.56b 3.17c
5–15cm depth
Native pines0.87c0.52bc0.73c 3.23a
1-yr turf 1.44b 1.27a 1.13a 2.41ab
6-yr turf 2.01a0.80ab 1.04ab 1.79b
23-yr turf 1.52b 1.11a0.65c 2.02b
95-yr turf0.63c0.20c0.83bc 2.03b Different letters within each column of0–5or5–15cm soil depths indicate the signi?cant difference of mean values(P!0.05)by multiple comparisons of Bonferroni t-test.Table4
Microbial C or N quotient(q CO2or q N)for soils sampled from0to5and5 to15cm soil depth of turfgrass systems and adjacent native pines
q CO2(m g CO2–C m g K1
MBC)
q N(m g Min.N m g K1
MBN)
0–5cm depth
Native pines 1.88b0.13b
1-yr turf 2.59a0.29a
6-yr turf 1.73b0.23a
23-yr turf 1.17c0.16b
95-yr turf 1.06c0.19b
5–15cm depth
Native pines 1.21bc0.17b
1-yr turf 1.32dc0.53a
6-yr turf 2.00ab0.47a
23-yr turf 2.35a0.55a
95-yr turf0.76d0.10b
Different letters within each column of0–5and5–15cm soil depth indicate signi?cant differences of mean values(P!0.05)by multiple comparisons of Bonferroni t-test.
W.Shi et al./Soil Biology&Biochemistry38(2006)311–319 316
microbial biomass and activity was reduced deeper in the pro?le following turf construction(Figs.1and2).
4.2.Soil N supplying capacity
The progressive increase in soil C and N associated with the chronological development of turfgrass systems improved soil N supplying capacity(i.e.potential N mineralization)(Fig.2).Soil N supplying capacity represents the quantity of soil organic N that is decom-posable and can provide N for plant uptake.It is an important but sometimes overlooked component of fertility programs and nutrient management in turfgrass systems. Experimentally,soil N supplying capacity is often estimated using a measure of potentially mineralized N(Shi et al., 1999).In the top5cm of turfgrass soils,potentially mineralized N increased immediately following the estab-lishment of turfgrass systems and also with turfgrass age (Fig.2).Changes in the5–15cm soil layer were less evident.Averaged for the entire0–15cm layer,which represents the majority of the turfgrass root zone,the soil N supplying capacity was w2.5times greater in the oldest compared to the youngest turfgrass system.
The soil C-to-N ratio is often considered a surrogate of soil organic C quality,and may thus be a determinant of potential N mineralization.Soil C-to-N ratios were similar among the turfgrass systems but differed signi?cantly between turfgrass systems and the native pines(Table1). Based on this,we predicted that potentially mineralized N, calculated as a percentage of soil N,would be independent of turfgrass age but would differ between turfgrass soils and those from the native pines.However,potentially miner-alized N per unit soil N decreased with the successional development of turfgrass systems(Table3).Thus,infer-ences regarding N mineralization between turfgrass systems and native pines cannot be made without considering the age of the turfgrass systems(Table3).A similar result was found for potentially mineralized C calculated per unit soil C(Table3).These data,together with the reduction in soil microbial biomass per unit soil C indicate that the stabilized soil C fraction increased relative to total soil C as turfgrass systems aged.
4.3.Microbial N transformations
Microbial N transformations increased in concert with soil microbial biomass and activity as a function of turfgrass age(Fig.3).Although we did not directly measure the rate of microbial N immobilization,the ratio of net-to-gross N mineralization was small(Table2),indicating that N immobilization was comparable to gross N mineralization. This implies that immobilization also increased with turfgrass age.Our results are consistent with those of Barrett and Burke(2000)who reported that microbial N transformation rates were positively correlated with soil organic C.
Nitri?cation governs soil NO K3concentration and there-fore the environmental fate of soil N.Heterotrophic microbes exert some control on nitri?cation by assimilating soil NH C4,thereby reducing NH C4available to soil nitri?ers. It is widely accepted that heterotrophs are stronger competitors than nitri?ers for soil NH C4.However,nitri?ers are stronger competitors than previously thought(Stark and Hart,1997;Shi and Norton,2000),possibly due to?ne-scale soil heterogeneity(Chen and Stark,2000).For example,some soil microsites may lack in adequate available C for heterotrophic microbes,yet sustain populations of nitrifers.It is within these microsites that nitri?ers would transform NH C4produced from N mineral-ization.While this may not be competition in the truest sense(the populations are spatially separate)the results,i.e. the production of NO K3,would be the same.Our data indicate that nitri?ers in turfgrass soils were competitive with heterotrophs,as evidenced by robust nitri?cation activity(Fig.3,Table2).
Microbial NO K3immobilization has received consider-able attention as a mechanism for stabilizing soil N and thus reducing N losses(Vitousek and Matson,1983;Stark and Hart,1997).Although we did not directly determine microbial NH C4vs.NO K3immobilization,we speculate that soil microbes in turfgrass systems assimilated substantial amount of NO K3for their growth.This is based on the presence of signi?cant nitri?cation potential yet relatively low concentrations of soil NO K3,and the fact that soil NO K3is the predominant N form available to heterotrophic microbes.
Differences in microbial biomass,activity and N transformations between turfgrass systems and native pines could be caused by combined effects of soil environmental factors,including but not limited to soil pH and the quantity and quality of soil organic C.Soil nitri?er activity is generally inhibited at acidic soil pH(Myrold, 1998).The lower potential rate of nitri?cation in native pines compared to turfgrass systems might be due to soil acidity(pH!5)in the native pine(Table1,Fig.3). However,there are contradictory reports regarding the impacts of soil pH and N fertilization on mineralization and immobilization(Neale et al.,1997;Fox,2004).Determining the relative impacts of soil environmental factors on N transformations was beyond the scope of this study.
4.4.Microbial eco-physiology and soil N processes
Soil N processes are the elaboration of microbial metabolism at the organismal level.Thus,altered microbial physiology can modify the rates of soil N processes.For example,enhanced microbial anabolism may increase microbial resource use ef?ciency and in turn the rate of microbial N immobilization.As a consequence,gross N immobilization may mirror gross N mineralization,result-ing in reduced net N mineralization.Despite the obvious importance in controlling soil N processes,microbial
W.Shi et al./Soil Biology&Biochemistry38(2006)311–319317
physiological functioning is often overlooked in assessing the soil N cycle(Smith et al.,1986;Blagodatsky et al., 1998).Instead,the quality of soil organic matter,often characterized as soil C-to-N ratio,is considered the primary determinant of N mineralization potential(i.e.the net result between gross N mineralization and immobilization).On one hand,we found that the soil C-to-N ratio(0–5cm depth) decreased with the age of the turfgrass system(Table1), leading us to predict that older turfgrass systems would produce more inorganic N.On the other hand,our data indicate that microbial communities might evolve towards higher C and N use ef?ciency(i.e.reduced q CO2and q N, Table4),indicative of tight coupling between gross N mineralization and immobilization in older turfgrass systems.It is possible that the increase in microbial C and N use ef?ciency counteracts the impact of soil organic C (i.e.C-to-N ratio).Accordingly,the interaction of microbial N mineralization and immobilization remained unchanged with the development of turfgrass systems(Table2). Bengtsson et al.(2003)provided evidence that gross N mineralization and immobilization and their interaction were more correlated to soil microbial physiology than to the soil C-to-N ratio.Our work supports the indispensable role that microbial physiology plays in determining soil N transformations and their interactions,and suggests that estimating soil N supply capacity based solely on soil organic C quality may lead to erroneous conclusions.
5.Conclusions
Changes in soil microbial properties and N transform-ations were observed with the chronological development of turfgrass systems.Although soil C and N in the oldest turfgrass system were8to10times greater than in the youngest turfgrass system,the potential C and N mineralization in the oldest was approximately three times greater than in the youngest turfgrass system.N mineralization potential increased with the accumulation of soil organic C and N in older turf ecosystems,but this increase was not in proportion to soil organic N.The change in soil organic C quality(i.e.C-to-N ratio)did not alter the interaction of microbial N transformations, possibly because its impact was offset by the change in microbial resource use ef?ciency.The increase in microbial resource ef?ciency indicates that old turfgrass systems had a greater capacity to conserve soil C and N compared to young turfgrass systems.Although gross N mineralization increased with the development of turfgrass systems and therefore with the increase in soil organic C,net N mineralization was less than12%of gross N mineralization.The tight coupling between microbial N mineralization and immobilization in old turfgrass systems was most likely due to the increase in microbial resource use ef?ciency.Acknowledgements
The center for Turfgrass Research and Education,North Carolina,USA?nancially supported the study.Dr Bir Thapa enthusiastically helped in taking soil samples.Howard Sanford and Mike Jennette kindly analyzed isotope labeled soil samples and soil organic matter.We appreciate the assistance of the Pinehurst Resort for the identi?cation of a chronosequence of turfgrass systems and for the permission of taking soil samples.We thank Dr Tom Rufty for his comments and discussion on this work.
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