Decomposition kinetics of soil carbon of different age from a forest exposed to 8 years of elevated atmospheric CO2 concentration

Soil Biology & Biochemistry 40 (2008) 2670–2677

Contents lists available at ScienceDirect

Soil Biology & Biochemistry journal homepage: www.elsevier.com/locate/soilbio

Decomposition kinetics of soil carbon of different age from a forest exposed to 8 years of elevated atmospheric CO2 concentration Lina Taneva*, Miquel A. Gonzalez-Meler Department of Biological Sciences, University of Illinois at Chicago, 845 W. Taylor Street M/C 066, Chicago, IL 60607, USA

a r t i c l e i n f o

a b s t r a c t

Article history: Received 10 March 2008 Received in revised form 30 May 2008 Accepted 14 July 2008 Available online 12 August 2008

Ecosystem exposure to elevated atmospheric CO2 concentration can often leads to increased ecosystem carbon (C) fluxes, as well as greater net primary production. Changes in the soil C pool with elevated [CO2] are more difficult to measure and therefore remain poorly understood. In this study, we carried out a series of laboratory soil incubations, in order to determine whether 8 years of ecosystem exposure to elevated [CO2] altered decomposition dynamics of two age classes of soil C in a temperate coniferous forest. Our objectives were to determine whether there were differences in the decomposition kinetics of soil C up to 8 years old (Cpost-tr) and soil C older than 8 years (Cpre-tr), in the absence of concurrent plant activity. We collected soil from the Duke Forest Free Air CO2 Enrichment site in North Carolina and incubated whole and crushed (all macroaggregates dispersed) soil from two depth increments (0–5 cm and 5–15 cm) for 102–127 days. We found that mineral soil from the treatment plots had higher respiration rates in the absence of concurrent plant activity than mineral soil from plots under ambient CO2 conditions. These differences in respiration rate were only significant in 0–5 cm soil and could be largely explained by higher initial respiration rates of soil collected from the CO2-treated plots. Disruption of soil macroaggregates did not result in a difference in efflux rate in soil from this forest under ambient or elevated CO2 conditions at either depth. The specific respiration rate of Cpost-tr was higher than that of Cpre-tr in the top 5 cm of soil, while the opposite was true for 5–15 cm of soil. Even though Cpost-tr was assimilated by the ecosystem more recently than Cpre-tr, their decay constants were similar at both depths. These results suggest that, in the absence of plant activity, the mineralization of soil C of different ages in this forest may be under similar biological and/or biochemical control. Therefore, if the higher initial rates of decomposition of Cpost-tr seen in these experiments are sustained in the field, greater labile pool size of recently added C, and potentially faster cycling of this pool, may in part explain higher soil respiration rates and limited soil C accumulation under elevated [CO2] in this forest. Ó 2008 Elsevier Ltd. All rights reserved.

Keywords: Soil carbon Carbon sequestration Elevated CO2 Stable carbon isotopes Soil organic matter Carbon cycle FACE Soil incubation Physical protection

1. Introduction Rising atmospheric CO2 concentration ([CO2]) and its potential to alter global climate have amplified research attention to the carbon (C) storage capacity of the terrestrial biosphere, in both plant biomass and soil pools. Increasing atmospheric [CO2] can alter the cycling of C in terrestrial ecosystems by increasing the magnitude of ecosystem C fluxes (King et al., 2004; Bernhardt et al., 2006; Ainsworth and Rogers, 2007), as well as the pool size of above- and belowground plant biomass (DeLucia et al., 1999; Matamala and Schlesinger, 2000; Norby et al., 2005; Moore et al.,

* Corresponding author: Environment and Natural Resources Institute, University of Alaska Anchorage, 707 A Street, Anchorage, AK 99503, USA. Tel.: þ1 907 786 4785; fax: þ1 907 257 2707. E-mail address: [email protected] (L. Taneva). 0038-0717/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2008.07.013

2006). Even though greater plant biomass production under elevated [CO2] may result in increased soil C inputs, most ecosystem-scale CO2 enrichment experiments report no significant increases in soil C content (Leavitt et al., 2001; Schlesinger and Lichter, 2001; Van Groenigen et al., 2003; Hoosbeek et al., 2004; Lichter et al., 2005; but see Jastrow et al., 2005). The large spatial heterogeneity of SOM may prevent the detection of small increases in soil C content with elevated [CO2] (Hungate et al., 1996; Jastrow et al., 2005). Another potential explanation for this inconsistency is that enhanced C inputs under elevated [CO2] may be allocated to labile C pools that turn over rapidly and are not incorporated into stable SOM pools with long residence times (Lichter et al., 2005; Taneva et al., 2006), but may lead to observed increases in soil respiration rates (King et al., 2004). The mechanisms involved in the storage, transformation, and turnover of the additional C entering soils when ecosystems are exposed to elevated atmospheric [CO2] are not well understood, but are of critical

L. Taneva, M.A. Gonzalez-Meler / Soil Biology & Biochemistry 40 (2008) 2670–2677

importance to the accurate evaluation of the long-term storage capacity of soils for anthropogenic C. Soil C balance is a function of plant C inputs and C outputs through heterotrophic respiration. Increased C inputs to soils with elevated [CO2] have been hypothesized to lead to both soil C and nutrient accumulation (Diaz et al., 1993) and, in contrast, to greater soil C and N cycling rates and increased decomposition (Zak et al., 1993). Furthermore, there is increasing evidence that enhanced plant activity and belowground C inputs under elevated [CO2] can, directly or indirectly, lead to increases in SOM decomposition dynamics (Hoosbeek et al., 2004; Subke et al., 2004; Trueman and Gonzalez-Meler, 2005; Allard et al., 2006). Ecosystem exposure to elevated [CO2] may therefore indirectly lead to interactions between labile and more recalcitrant soil C pools, but it remains unclear whether such changes in soil C cycling are mainly brought about by the presence of plant activity or are the result of further and lasting changes in soil C pool dynamics. Recently, the importance of the relationship between soil physical protection and SOM dynamics has been highlighted (Jastrow et al., 1996; Six et al., 2000) and SOM sequestration in afforested soils and restored grasslands has been shown to occur mainly within soil aggregates (Jastrow et al., 1996; DeGryze et al., 2004). Labile organic C can become physically protected within soil aggregates, which can render it unavailable to microorganisms, and thus relatively new C can accumulate in soil pools with long residence times (Oades, 1984; Elliott and Coleman, 1988; Jastrow et al., 1996). Soil physical protection mechanisms depend in part on the quantity and quality of belowground C inputs (Six et al., 2001), as well as on soil microbial activity (Six et al., 1999), which have been shown to be affected by elevated atmospheric [CO2] in some ecosystems (Matamala and Schlesinger, 2000; Montealegre et al., 2002). Anthropogenic changes in environmental conditions that may alter mechanisms of soil C protection or aggregate turnover can therefore potentially accelerate the loss of soil C by exposing protected C to microbial degradation. In this study, we conducted a series of laboratory incubation experiments to evaluate the dynamics of soil C oxidation as a function of C age and macroaggregate protection in soils collected from the Free Air CO2 Enrichment (FACE) experiment in the Duke Forest (Chapel Hill, NC, USA). Our objectives were: (1) to determine whether differences in soil C decomposition dynamics between soil from the elevated CO2-treated and control plots exist in the absence of concurrent plant activity; (2) to determine the extent to which soil macroaggregate protection affects soil C mineralization; and (3) to evaluate the mineralization kinetics of soil C of two different age groups: C assimilated by the ecosystem before fumigation began 8 years previously and soil C assimilated over the previous 8 years in both soil with and without intact macroaggregates.

2671

exceeds 5 m/s. Starting 16 December 2002, fumigation was reduced to daytime only. The loblolly pine plantation was established in 1983, with 3year-old seedlings planted at 2  2.4 m spacing. Through natural regeneration, a number of hardwood species have become established in the understory, the most abundant of which are Acer rubrum, Liquidambar styraciflua, Liriodendron tulipifera, Ulmus alata, and Cercis canadensis. Soils at the site are clay-rich, low fertility Ultic Alfisols, derived from igneous rock, with a pH of w5. Fine roots are found mostly in the upper 20 cm of the soil profile (Matamala and Schlesinger, 2000). Mean annual temperature is 15.5  C and mean annual precipitation is 1140 mm. 2.2. Ecosystem

13

C tracer

The CO2 used for fumigation at FACTS-1 is strongly depleted in 13C vs. PDB (d13C z43.1  0.6& SE, where d13C ¼ [(Rsample  Rreference)/ Rreference]  1000 and R ¼ 13C/12C). By increasing atmospheric [CO2] by 200 ml/l in the treatment plots, the d13C of atmospheric CO2 is changed from about 8 to 20  0.4&. Consequently, new needles and fine roots produced under FACE have a d13C of 41.8  0.3 & and 39.2  0.8& compared to d13C of 29.9  0.2& and 27.6  0.2& at ambient conditions, respectively (Matamala et al., 2003). The fumigated forest plots have been exposed to a continuous ecosystem 13C label since the beginning of the CO2 treatment in 1996 and, through its incorporation into plant biomass, the 13C label has been incorporated into soil organic matter and can be detected in soil-respired CO2 (Andrews et al., 1999; Taneva et al., 2006). 2.3. Soil sampling and preparation Soils were sampled to a depth of 30 cm in March 2005 at four randomly chosen locations within each plot at FACTS-1, using a 5.4 cm diameter slide hammer soil corer. The soil was frozen to 20  C and transported on dry ice to the laboratory. Soil cores were divided into 0–5 cm, 5–15 cm, and 15–30 cm depth increments prior to processing; the 15–30 cm increment was not part of the experiments described in this study. Roots, plant fragments, debris and rocks were removed by hand from moist soil. Root-free soil was sieved to pass a 2-mm screen and then dried at 65  C for 5–7 days. In order to disperse all physical protection of SOM by soil aggregates, a subsample of soil was ground manually with a mortar and pestle to pass through a 180 mm sieve. Thus, there were two soil treatments for the soil incubation experimentsdwhole soil (WS), with all micro- and macro-aggregates intact, and crushed soil (CS), with all soil macroaggregates disrupted. The d13C values of the soil were determined with a Finnegan Delta Plus XL isotope ratio mass spectrometer (Bremen, Germany).

2. Materials and methods

2.4. Laboratory soil incubations

2.1. Site description

Mineralizable soil C and the degree of protection from decomposition provided by soil macroaggregates were evaluated during extended laboratory incubations of root-free moist samples of either whole soil (WS) or crushed soil (CS) at the 0–5 cm and 5– 15 cm depth increments. Moisture content of the dried soil samples was adjusted to and maintained at 80% field capacity with deionized water. Duplicate, 30 g subsamples from each FACE plot (ambient and elevated [CO2]), each depth (0–5 cm and 5–15 cm), and each soil treatment (WS and CS) were placed into a 0.9 l Mason jar and incubated in the dark at 25  C. A layer of glass wool was placed on the bottom of the jar to facilitate aeration and to prevent drying of the soil sample. The soil samples were mixed with 30 g of sterilized sand to avoid changes in soil aggregation during the incubation period. Jars were capped with a perforated lid to avoid anoxic conditions. Two control jars contained no soil. Soil samples

The Forest Atmosphere Carbon Transfer and Storage 1 (FACTS-1) research site is located in the Blackwood Division of the Duke Forest, near Chapel Hill, NC, USA (35 580 N 79 050 W). The Free Air CO2 Enrichment (FACE) experiment at FACTS-1 is composed of six 30-m diameter plots in an intact loblolly pine (Pinus taeda) plantation. Three of the experimental plots are fumigated with CO2 to maintain an atmospheric [CO2] that is approximately 200 ml/l above ambient, or about 567  4 ml/l (averaged from 1996 to 2004; K. Lewin and R. Nettles, personal communication); the three control plots are fumigated with ambient air only (Hendrey et al., 1999). Continuous fumigation of all plots began on 27 August 1996, when the trees were 15 years old. Fumigation is switched off when temperatures are below 5  C and when sustained wind speed

2672

L. Taneva, M.A. Gonzalez-Meler / Soil Biology & Biochemistry 40 (2008) 2670–2677

from the 0–5 cm depth were incubated for 127 days for WS and 103 days for CS. Soils from the 5–15 cm depth were incubated for 125 days for WS and 102 days for CS. The incubation system consisted of a pump, a soda lime column placed in line before the Mason jar, a desiccant column placed between the jar and the glass flask, where the respired CO2 was eventually collected, and an IRGA (LiCor 6252, Lincoln, NE, USA; see Hymus et al., 2005). All components of the incubation system were connected to each other with Bev-A-LineÒ tubing (0.5 cm inner diameter). Before sample incubation, the jar, the 150-ml glass flask, and the line were flushed with CO2-free air by pumping ambient air through the soda lime column. When CO2 in the system declined and stabilized at a concentration reflecting only sample respiration (w2–5 ml/l), the jar was closed with three-way valves (Swagelok, Solon, OH, USA) for the incubation period, allowing for respired CO2 to accumulate. Prior to collecting the respired CO2 from each sample, the incubation system was once again flushed with CO2-free air, this time bypassing the closed incubation jar, to ensure the lines and flask were free of CO2. The flow of CO2-free air was then passed through the jar and the respired CO2 was carried through the desiccant column and into the glass flask. As respired CO2 was transferred out of the chamber, the CO2 concentration increased steadily, reaching a maximum value between 400 and 3000 ml/l. When the maximum [CO2] was reached, the flask was closed before the [CO2] started to decline. The CO2 in the collected gas samples was purified from water vapor, N2, and other atmospheric gases by cryogenic distillation extraction and pure CO2 samples were analyzed for their stable C isotope composition with a Finnegan Delta Plus XL (Bremen, Germany) isotope ratio mass spectrometer, operated in Gas Bench mode.

2.5. Soil CO2 efflux The change in [CO2] over the incubation period was converted from ml/l jar headspace to mg CO2-C/l by applying the Ideal Gas Law, according to the following equation (Robertson et al., 1999):

each consecutive day from days 0–130. Cumulative efflux was calculated using these daily rates. 2.6. Mixing models and end-member determination The CO2 evolved during each incubation period was partitioned into C that was photosynthetically fixed since the beginning of CO2 fumigation in 1996 (referred to as ‘post-treatment’ C) and C assimilated under ambient [CO2] before fumigation started (referred to as ‘pre-treatment’ C), according to the following two end-member mixing equation:

d13 CCO2 ¼ f d13 Cpre-tr þ ð1  f Þd13 Cpost-tr

where d13CCO2 is the measured d13C of soil-respired CO2 at time t, d13Cpost-tr is the end-member for post-treatment C, d13Cpre-tr is the end-member for pre-treatment C at incubation time t and f represents the fraction of pre-treatment C in soil CO2 at incubation time t (Taneva et al., 2006). The d13Cpre-tr is determined by directly measuring d13CCO2 from the jars containing soil from the control plots at FACTS-1 at time t. This measured value incorporates respiration from both recalcitrant and labile soil C pools under ambient CO2 conditions. Because the d13C of recalcitrant soil C pools has little or no seasonal variation (Balesdent and Mariotti, 1996), any potential variability in d13C of soil-respired CO2 in the control plots during the incubation period will be due to differences in the signature of labile soil C pools. Because the d13C of the atmosphere in the enriched plots was changed by a constant value (E) at the beginning of the experiment and because photosynthetic discrimination against 13C is the same under ambient and elevated [CO2] (due to lack of photosynthetic acclimation and conserved Ci/Ca between ambient and elevated [CO2] plots (Ellsworth, 1999)), the difference in d13C of new photosynthate in the control and treatment plots also equals E. Therefore, the end-member for the d13C of soil-respired CO2 in the enriched plots (d13Cpost-tr) can be derived by subtracting E from the measured d13Cpre-tr and Eq. (4) can be rearranged as follows:

f ¼ Cm ¼ ðCv  M  PÞ=ðR  TÞ

(1)

where Cm is the mg CO2-C/l headspace, Cv is ml/lv CO2 per l headspace, M is the molecular weight of CO2-C (12 mg/mol), P is the barometric pressure in atm, R is the universal gas constant, and T is the incubation temperature in Kelvin, where (R T) is 24.45 mol air/l air at a pressure of 1 atm and a temperature of 25  C. The flux of CO2-C during the incubation period was calculated according to the following equation (Robertson et al., 1999):

F ¼ Crate  V=W

(2)

where F is the C mineralization rate, expressed as mg CO2-C/g soil per day, Crate is the change in [CO2] over the incubation period, expressed as mg CO2-C/l headspace per day, V is the headspace volume of jar (l), calculated as total jar volume less soil, sterilized sand, glass wool and water volume, and W is the dry mass of soil in the incubation jar (g). Cumulative efflux was calculated by gap-filling each data set, in order to obtain daily efflux rates for days 0–130. A second order exponential decay function was fitted to the data set of measured daily rates for each soil treatment and each depth, according to the following equation:

f ðxÞ ¼ y0 þ a expð  ktÞ

(3)

where y0 is the asymptote of the generated decay curve, a is the initial CO2 efflux rate, and k is the decay constant. Using the parameters of each function, the daily efflux rate was calculated for

(4)



d13 CRs CO2  d13 Cpost-tr

. E

(5)

where E was measured to be 12.0  0.1& (Taneva et al., 2006). 2.7. Data analysis The effects of CO2 treatment (ambient and elevated), soil treatment (WS and CS), and depth (0–5 cm and 5–15 cm) on soil CO2 efflux were tested with an analysis of covariance (ANCOVA; Statistica v. 6, Tulsa, OK). The effects of soil treatment (WS and CS), and depth (0–5 cm and 5–15 cm) on the specific mineralization rates of pre-treatment and post-treatment C in the fumigated plots at FACTS-1 were also compared with an ANCOVA. The parameters generated by the second order exponential decay functions describing the mineralization of pre-treatment and post-treatment C for each soil treatment and depth were compared with two-tailed t-tests. 3. Results 3.1. Soil CO2 efflux Respiration rates were higher in 0–5 cm whole or crushed soil than in 5–15 cm soil from both treatment and control plots (P < 0.0001; Fig. 1). Additionally, soil collected from the treatment plots had higher respiration rates than control soil at 0–5 cm depth (P < 0.001), while rates were similar at the 5–15 cm depth (Fig. 1). There were no significant differences in efflux between crushed

L. Taneva, M.A. Gonzalez-Meler / Soil Biology & Biochemistry 40 (2008) 2670–2677

160

CS 0-5 cm

WS 0-5 cm

140

2673

Elevated [CO2] Ambient [CO2]

120 100 80

µg C g soil-1 day-1

60 40 20 0 30

WS 5-15 cm

CS 5-15 cm

25 20 15 10 5 0 0

20

40

60

80

100

120

140 0

20

40

60

80

100

120

140

Incubation period (days) Fig. 1. . Daily CO2 efflux rate during the incubation period for whole soil (WS) and crushed soil (CS) collected from the fumigated (closed circles) and control (open circles) plots at FACTS-1. Values represent means  standard error (n ¼ 3).

and whole soil (P > 0.2; Fig. 1). Crushed soil from the treatment plots had higher respiration rate than crushed soil from the control plots, but the difference was only marginally significant (P ¼ 0.07; Fig. 1). Cumulative efflux from soil from CO2 treatment plots was higher than that from control plots in the 0–5 cm depth, both from WS and 3000

CS (Fig. 2). At the 5–15 cm depth, cumulative efflux was similar between ambient and elevated [CO2]-treated WS or CS (Fig. 2). Based on modeled (gap-filled) cumulative efflux values, total C respired during an incubation period of 130 days was 32% higher in elevated [CO2]-treated WS and 47% higher in elevated [CO2]-treated CS at the 0–5 cm depth (Table 1). At 5–15 cm soil depth, the amount

CS 0-5 cm

WS 0-5 cm 2500 2000 1500 1000

µg CO2-C

500 Elevated [CO2] Ambient [CO2]

0 700

WS 5-15 cm

CS 5-15 cm

600 500 400 300 200 100 0 0

20

40

60

80

100

120

140 0

20

40

60

80

100

120

140

Incubation period (days) Fig. 2. Modeled cumulative CO2 efflux for a 130-day incubation period for whole soil (WS) and crushed soil (CS) collected from the fumigated (closed circles) and control (open circles) plots at FACTS-1. Values represent means  standard error (n ¼ 3).

2674

L. Taneva, M.A. Gonzalez-Meler / Soil Biology & Biochemistry 40 (2008) 2670–2677

asymptote of the curve) and the decay constant were obtained (Tables 2 and 3). The initial respiration rate (i.e., CO2 evolution at time 0) was higher for Cpost-tr in 0–5 cm WS (P < 0.05), while the residual respiration rates and the mineralization decay constants were not significantly different between Cpre-tr or Cpost-tr (P > 0.05; Table 2). There were no significant differences in any parameter between Cpre-tr and Cpost-tr in 5–15 cm CS (P > 0.1; Table 2). The only significant difference between Cpre-tr and Cpost-tr mineralization at 5–15 cm depth was in their residual respiration rate in WS (P < 0.05; Table 2). Cumulative efflux rates, calculated by using the specific mineralization rates of pre-treatment and post-treatment C, show that if all the soil C at the 0–5 cm depth was Cpost-tr, cumulative efflux would be 71% higher than if all the soil C consisted of Cpre-tr in WS and 86% in CS during a 130-day incubation (Fig. 5; Table 3). At the 5–15 cm depth, the specific respiration rate of Cpre-tr was higher than that of Cpost-tr and, therefore, during 130 days, soil composed entirely of Cpre-tr would respire 29% more C in WS and 24% more C in CS than soil composed entirely of Cpost-tr (Fig. 5; Table 3).

Table 1 Modeled cumulative efflux for a 130-day incubation of whole (WS) and crushed (CS) soil collected from the fumigated and control plots at FACTS-1 Soil treatment and depth

Efflux from ambient [CO2] (mg CO2-C)

Efflux from elevated [CO2] (mg CO2-C)

WS 0–5 cm CS 0–5 cm WS 5–15 cm CS 5–15 cm

1698  58 1666  172 503  32 459  30

2236  264 2445  333 538  34 515  97

Values represent means  standard error (n ¼ 3).

of C respired by WS was 7% higher under elevated [CO2], while CS respiration was 12% higher under elevated [CO2] (Table 1). 3.2. Mineralization of Cpre-tr and Cpost-tr The 13C signature of evolved CO2 at each sampling time was used to partition efflux during the incubation period into that derived from Cpre-tr and Cpost-tr (Fig. 3). In general, there was little variation in the isotopic composition of respired CO2 throughout the incubation period and at the two CO2 treatments (Fig. 3). Overall, mineralization rate of both Cpre-tr and Cpost-tr was higher in soil collected from 0–5 cm depth than 5–15 cm depth (P < 0.01; Fig. 4). Furthermore, the specific respiration rate of Cpost-tr (i.e., posttreatment CO2 evolved per unit of post-treatment soil C present in the sample) was higher than that of Cpre-tr (pre-treatment CO2 evolved per unit of pre-treatment soil C present in the sample) at 0– 5 cm, while the specific respiration rate of Cpre-tr was higher than that of Cpost-tr at 5–15 cm depth (P < 0.05). There were no significant differences in the mineralization of Cpre-tr between crushed and whole soil at either sampling depth (P > 0.5; Fig. 4). When fitting a second order exponential decay function to the mineralization data of pre-treatment and post-treatment C in WS and CS from each of the three fumigated plots at FACTS-1, the curve parameters giving the initial respiration rate, the residual rate (the

4. Discussion In this study, we found that in a temperate coniferous forest, mineral soil collected from plots exposed to elevated atmospheric [CO2] had higher respiration rates in the absence of concurrent plant activity than mineral soil from plots under ambient CO2 conditions. These differences in respiration rate were only significant in soil collected from the top 5 cm depth (Fig. 1). The difference in respiration rate between ambient and elevated CO2treated soils could be largely explained by higher initial respiration rates of soil collected from the CO2-fumigated plots (Fig. 1), as was the case in an incubation experiment with FACTS-1 soil collected in 1998 (Andrews et al., 2000). Similarly, in incubation experiments with soil collected from a grassland in Switzerland exposed to FACE, soil from CO2-treated plots had higher respiration rates

-20 -22

WS 0-5 cm

CS 0-5 cm

WS 5-15 cm

CS 5-15 cm

-24 -26 -28 -30

δ13C

-32 -34 -20 -22 -24 -26 -28 -30 -32 -34 0

20

40

60

80

100

120

140 0

20

40

60

80

100

120

140

Day since start of incubation Fig. 3. The 13C composition (d13C) of CO2 evolved from whole (WS; right panel) and crushed (CS; left panel) soil, collected from the fumigated (closed circles) and control (open circles) plots at FACTS-1. Values represent means  standard error (n ¼ 3).

L. Taneva, M.A. Gonzalez-Meler / Soil Biology & Biochemistry 40 (2008) 2670–2677

2675

250

WS 0-5cm

CS 0-5 cm

200

Post-tr C Pre-tr C

150

µg C g C-1 day-1

100 50 0 30

CS 5-15 cm

WS 5-15 cm 25 20 15 10 5 0 0

20

40

60

80

100

120

140 0

20

40

60

80

100

120

140

Incubation period (days) Fig. 4. Specific carbon mineralization rates of pre-treatment (open circles) and post-treatment (closed circles) C in whole (WS) and crushed soil (CS) from the fumigated plots at FACTS-1. Values represent means  standard error (n ¼ 3).

than soil from control plots (De Graaff et al., 2004; Bazot et al., 2006). Higher initial respiration rates in CO2-treated soil suggest either the presence of a larger labile C pool and/or greater accessibility of substrate under elevated [CO2]. Because mineralization constants in whole soil were similar under the ambient and elevated [CO2] treatments (data not shown), higher initial respiration rates under elevated [CO2] are likely to be the result of greater availability to decomposers of recently added C and not necessarily the result of changes in the chemical nature of mineralizable SOM between ambient and elevated [CO2]. If recently added C is more available to decomposers in field conditions under elevated [CO2], and if C inputs are sustained, the turnover of new C inputs could be accelerated, with the potential of reducing soil C accumulation at the ecosystem level at higher atmospheric [CO2]. We examined soil respiration rates from soils with all aggregates <2 mm intact (WS) and crushed soil with all macroaggregates disrupted (CS). Disruption of the physical protection of the mineral soil did not result in a difference in efflux rate in soil from this forest under ambient or elevated CO2 conditions at either depth. These

results are in contrast to other studies reporting increased respiration rates when aggregates were dispersed (Gregorich et al., 1989; Bossuyt et al., 2002; Grandy and Robertson, 2006) and indicate low levels of macroaggregate protection in the soil of this forest at 0–15 cm depth. However, marginally significant differences (P ¼ 0.07) in daily efflux rates between 0 and 5 cm CS and WS translated to higher modeled cumulative efflux rate in the crushed soil at that depth, suggesting that the amount of C that is physically protected in macroaggregates under elevated [CO2] in 0–5 cm deep soil may be slightly larger than that under ambient CO2 conditions after 8 years of CO2 fumigation. In contrast to these results, Jastrow et al. (2005) reported similar physical microaggregate protection mechanisms in soil under ambient and elevated [CO2] after 5 years of CO2 fumigation in a temperate deciduous forest. Previous studies have shown that microaggregates (20–250 mm in diameter) may play a more important role in long-term SOM protection and stability than macroaggregates (reviewed in Six et al., 2002). Crushing the soil in this study vs. standard methods of aggregate dispersal through sequential shaking may have left most of the smaller microaggregates intact. Further study is required to

Table 2 Comparison of the second-order exponential decay function parameters, describing the mineralization rate of pre-treatment and post-treatment carbon in whole (WS) and crushed (CS) soil collected from the fumigated plots at FACTS-1 WS

CS

Pre-tr C

Post-tr C

P

Pre-tr C

Post-tr C

P

0–5 cm Initial rate Residual rate Decay constant r2

105.7  18.0 10.2  1.5 0.286  0.029 0.96  0.02

187.1  17.6 16.6  2.2 0.258  0.013 0.96  0.01

0.03 0.08 0.45 –

108.3  14.1 11.3  1.2 0.379  0.048 0.99  0.01

174.4  38.3 17.3  4.0 0.207  0.087 0.96  0.03

0.2 0.29 0.18 –

5–15 cm Initial rate Residual rate Decay constant r2

18.6  0.9 4.0  0.3 0.290  0.052 0.95  0.01

20.0  3.3 2.8  0.1 0.439  0.041 0.94  0.02

0.72 0.03 0.09 –

18.4  3.8 3.2  0.6 0.139  0.023 0.95  0.01

20.0  4.4 2.3  0.7 0.169  0.013 0.96  0.003

0.79 0.36 0.33 –

Values are means  standard error (n ¼ 3). P-values were obtained from a two-tailed t-test.

2676

L. Taneva, M.A. Gonzalez-Meler / Soil Biology & Biochemistry 40 (2008) 2670–2677

Table 3 Modeled potential cumulative efflux form 100% pre-treatment or post-treatment carbon in whole (WS) and crushed (CS) soil collected from the fumigated plots at FACTS-1 Soil treatment and depth Pre-treatment C (mg CO2-C) Post-treatment (mg CO2-C) WS 0–5 cm CS 0–5 cm WS 5–15 cm CS 5–15 cm

1756  244 1839  226 605  45 568  87

3002  334 3416  485 427  27 434  112

Values represent means  SE (n ¼ 3).

evaluate the degree of microaggregate protection of recent C inputs in soil at FACTS-1 and the role of this form of physical protection in the storage capacity of these soils under elevated [CO2]. Using the ecosystem 13C tracer at FACTS-1, we were able to determine the contribution of pre-treatment (C assimilated by photosynthesis at least 8 years previously) and post-treatment C (C assimilated during the previous 8 years) to CO2 efflux during the incubation period from soil from the fumigated plots. The average fraction of Cpost-tr in respired CO2 from 0–5 cm deep WS was w51%, while its contribution to 0–5 cm CS was, on average, w55% during the incubation period. At 5–15 cm soil depth, the average contribution of Cpost-tr to soil CO2 efflux was lowerdapproximately 31% in both whole and crushed soil. Similar rates of Cpost-tr mineralization in WS and CS at each depth further indicate low levels of macroaggregate protection of recent inputs in soil from the CO2 treatment plots in this forest. The specific respiration of Cpost-tr was higher than that of Cpre-tr in the top 5 cm of soil, consistent with other reports of 13C partitioning of soil-respired CO2 in incubation experiments (De Graaff et al., 2004). Even though post-treatment C was assimilated by the ecosystem more recently than pre-treatment C, mineralization kinetics of Cpost-tr and Cpre-tr were similar (Table 2). The initial respiration rate of Cpost-tr was higher than that of Cpre-tr in 0–5 cm WS and CS, possibly due to a larger pool of recently added soil C, but their decay constants were similar (Table 2). In soil from the 5– 15 cm depth, initial respiration rates of Cpre-tr and Cpost-tr were

similar, as were the decay constants of C of these two different age groups. These results suggest that, in the absence of plant activity, the mineralization of soil C of different ages in this forest may be under similar biological and/or biochemical control. Furthermore, similar decomposition kinetics in 0–5 cm whole and crushed soil indicate that Cpost-tr and Cpre-tr are distributed almost equally among soil physical protection pools. Soil treatment (i.e. WS vs. CS) did not have an effect on the decomposition of Cpre-tr and Cpost-tr with depth (P > 0.4); however, the curve-fitting analyses indicate lower decay constants for 5–15 cm CS than were obtained for WS at this depth (Table 2). Therefore, crushing the soil exposed substrate of lower inherent decomposability to microbial attack, suggesting that physical protection has the potential to alter turnover time of Cpre-tr and Cpost-tr at 5–15 cm depth. De Graaff et al. (2004) and Six et al. (2001) found that in a grassland exposed to elevated [CO2], post-treatment C was mostly distributed among soil C pools with a fast turnover rate. Our results do not necessarily contradict these reports, as all the soil C pools contributing to CO2 efflux during this incubation experiment had relatively fast turnover rates. However, our results additionally suggest that older C contributes substantially to CO2 efflux from pools that have relatively short turnover times and that the C pools contributing to respired CO2 consist of a mixture of older and more recently added soil C. 5. Conclusions We studied soil C decomposition dynamics in an incubation experiment with soil collected from a temperate forest exposed to elevated [CO2] for 8 years. The results presented here indicate that soils from elevated [CO2] plots had a larger labile C pool at the 0– 5 cm depth than soils from the control plots. The decomposition kinetics of soil C of the two age classes examined here (up to 8 years old and older than 8 years) were similar, suggesting that in the absence of plant activity and the availability of particulate organic matter, the decomposition of C of different ages is under similar biological and/or biochemical control in this forest. Furthermore, similar decomposition kinetics in 0–5 cm whole and crushed soil

4000

WS 0-5

CS 0-5 cm

3000

2000

µg CO2-C

1000 Post-tr C Pre-tr C

0 700

WS 5-15 cm

CS 5-15 cm

600 500 400 300 200 100 0 0

20

40

60

80

100

120

140 0

20

40

60

80

100

120

140

Incubation period (days) Fig. 5. Potential cumulative mineralization of pre-treatment (open circles) and post-treatment (closed circles) C in whole (WS) and crushed soil (CS) collected from the fumigated plots at FACTS-1. Values represent means  standard error (n ¼ 3).

L. Taneva, M.A. Gonzalez-Meler / Soil Biology & Biochemistry 40 (2008) 2670–2677

indicate that C of these two age classes was distributed almost equally among soil physical protection pools. These results are consistent with those presented in (Taneva and Gonzalez-Meler, Submitted for Publication), where pre-treatment C respiration at FACTS-1 showed distinct diurnal (i.e. short-term) variability under field conditions. Due to the lack of a 13C tracer in the control plots at FACTS-1, we were not able to compare the cycling of soil C of different ages under elevated [CO2] to that under ambient CO2 conditions. However, if the higher initial rates of decomposition of post-treatment C seen in these experiments are sustained in the field, greater labile pool size of recently added C, and potentially faster cycling of this pool, may in part explain higher soil respiration rates and limited soil C accumulation under elevated [CO2] in this forest.

Acknowledgments This research was funded by NSF and DOE; LT was funded by a University of Illinois at Chicago Graduate Fellowship. We gratefully acknowledge the staff of Brookhaven National Laboratory and the Duke Forest for maintenance and operation of the FACTS-1 experiment. We thank Leah Simoni, Sergey Oleynik, and Matt Lorz for assistance in the laboratory and Alice Niederland for her help in the field. We thank Luca Borghesio for his help with statistical analyses. The FACTS-1 experiment is supported by the Office of Science (BER), US Department of Energy.

References Ainsworth, E.A., Rogers, A., 2007. The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant, Cell and Environment 30, 258–270. Allard, V., Robin, C., Newton, P.C.D., Lieffering, M., Soussana, J.-F., 2006. Short and long-term effects of elevated CO2 on Lolium perenne rhizodeposition and its consequences on soil organic matter turnover and plant N yield. Soil Biology & Biochemistry 38, 1178–1187. Andrews, J.A., Harrison, K.G., Matamala, R., Schlesinger, W.H., 1999. Separation of root respiration from total soil respiration using carbon-13 labeling during FACE. Soil Science Society of America Journal 63, 1429–1435. Andrews, J.A., Matamala, R., Westover, K.M., Schlesinger, W.H., 2000. Temperature effects on the diversity of soil heterotrophs and the delta 13C of soil-respired CO2. Soil Biology & Biochemistry 32, 699–706. Balesdent, J., Mariotti, A., 1996. Measurement of Soil Organic Matter Turnover Using 13 C Natural Abundance. Marcel Dekker, Inc., New York. Bazot, S., Ulff, L., Blum, H., Nguyen, C., Robin, C., 2006. Effects of elevated CO2 concentration on rhizodeposition from Lolium perenne grown on soil exposed to 9 years of CO2 enrichment. Soil Biology & Biochemistry 38, 729–736. Bernhardt, E.S., Barber, J.J., Pippen, J.S., Taneva, L., Andrews, J.A., Schlesinger, W.H., 2006. Long-term effects of free air CO2 enrichment (FACE) on soil respiration. Biogeochemistry 77, 91–116. Bossuyt, H., Six, J., Hendrix, P.F., 2002. Aggregate-protected carbon in no-tillage and conventional tillage agroecosystems using carbon-14 labeled plant residue. Soil Science Society of America Journal 66, 1965–1973. De Graaff, M.-A., Six, J., Harris, D., Blum, H., Van Kessel, C., 2004. Decomposition of soil and plant carbon from pasture systems after 9 years of exposure to elevated CO2: impact on C cycling and modeling. Global Change Biology 10, 1922–1935. DeGryze, S., Six, J., Paustian, K., Morris, S.J., Paul, E.A., Merckx, R., 2004. Soil organic carbon pool changes following land-use conversions. Global Change Biology 10, 1120–1132. DeLucia, E.H., Hamilton, J.G., Naidu, S.L., Thomas, R.B., Andrews, J.A., Finzi, A.C., Lavine, M., Matamala, R., Mohan, J.E., Hendrey, G.R., Schlesinger, W.H., 1999. Net carbon storage in an intact forest under experimental CO2 enrichment. Science 284, 1177–1179. Diaz, S., Grime, J.P., Harris, J., McPherson, E., 1993. Evidence of a feedback mechanism limiting plant response to elevated carbon dioxide. Nature 364, 616–617. Elliott, E.T., Coleman, D.C., 1988. Let the soil work for us. Ecological Bulletin 39, 23–32. Ellsworth, D.S., 1999. CO2 enrichment in a maturing pine forest: are CO2 exchange and water status in the canopy affected? Plant. Cell and Environment 22, 461–472. Grandy, A.S., Robertson, G.P., 2006. Initial cultivation of a temperate-region soil immediately accelerates aggregate turnover and CO2 and N2O fluxes. Global Change Biology 12, 1507–1520. Gregorich, E.G., Kachanoski, R.G., Voroney, R.P., 1989. Carbon mineralization in soil size fractions after various amounts of aggregate disruption. Journal of Soil Science 40, 649–659.

2677

Hendrey, G.R., Ellsworth, D.S., Lewin, K.F., Nagy, J., 1999. A free-air enrichment system for exposing tall forest vegetation to elevated atmospheric CO2. Global Change Biology 5, 293–309. Hoosbeek, M.R., Lukac, M., van Dam, D., Godbold, D.L., Velthorst, E.J., Biondi, F.A., Peressotti, A., Cotrufo, M.F., De Angelis, P., Scarascia-Mugnozza, G., 2004. More new carbon in the mineral soil of a poplar plantation under Free Air Carbon Enrichment (POPFACE): cause of increased priming effect? Global Biogeochemical Cycles 18, GB1040. doi:1010.1029/2003GB002127. Hungate, B.A., Jackson, R.B., Field, C.B., Chapin, F.S., 1996. Detecting changes in soil carbon in CO2 enrichment experiments. Plant and Soil 187, 135–145. Hymus, G.J., Maseyk, K., Valentini, R., Yakir, D., 2005. Large daily variation in 13Cenrichment of leaf-respired CO2 in two Quercus forest canopies. New Phytologist 167, 377–384. Jastrow, J.D., Boutton, T.W., Miller, R.M., 1996. Carbon dynamics of aggregateassociated organic matter estimated by 13C natural abundance. Soil Science Society of America Journal 60, 801–807. Jastrow, J.D., Miller, R.M., Matamala, R., Norby, R.J., Boutton, T.W., Rice, C.W., Owensby, C.E., 2005. Elevated atmospheric carbon dioxide increases soil carbon. Global Change Biology 11, 2057–2064. King, J.S., Hanson, P.J., Bernhardt, E.S., De Angelis, P., Norby, R.J., Pregitzer, K.S., 2004. A multiyear synthesis of soil respiration responses to elevated atmospheric CO2 from four forest FACE experiments. Global Change Biology 10, 1027–1042. Leavitt, S.W., Pendall, E., Paul, E.A., Brooks, T.J., Kimball, B.A., Pinter Jr., P.J., Johnson, H.B., Matthias, A.D., Wall, G.W., LaMorte, R.L., 2001. Stable-carbon isotopes and soil organic carbon in wheat under CO2 enrichment. New Phytologist 150, 305–314. Lichter, J., Barron, S.H., Finzi, A.C., Irving, K.F., Roberts, M.T., Stemmler, E.A., Schlesinger, W.H., 2005. Soil carbon sequestration and turnover in a pine forest after six years of atmospheric CO2 enrichment. Ecology 86, 1835–1847. Matamala, R., Schlesinger, W.H., 2000. Effects of elevated atmospheric CO2 on fine root production and activity in an intact temperate forest ecosystem. Global Change Biology 6, 967–979. Matamala, R., Gonzalez-Meler, M.A., Jastrow, J.D., Norby, R.J., Schlesinger, W.H., 2003. Impacts of fine root turnover on forest NPP and soil C sequestration potential. Science 302, 1385–1387. Montealegre, C.M., Van Kessel, C., Russelle, M.P., Sadowsky, M.J., 2002. Changes in microbial activity and composition in a pasture ecosystem exposed to elevated atmospheric CO2. Plant and Soil 243, 197–207. Moore, D.J., Aref, S., Ho, R., Pippen, J.S., Hamilton, J.G., DeLucia, E.H., 2006. Annual basal area increment and growth duration of Pinus taeda in response to eight years of free-air carbon dioxide enrichment. Global Change Biology 12, 1367–1377. Norby, R.J., DeLucia, E.H., Gielen, B., Calfapietra, C., Giardina, C.P., King, J.S., Ledford, J., McCarthy, H.R., Moore, D.J., Ceulemans, R., de Angelis, P., Finzi, A.C., Karnosky, D.F., Kubiske, M.E., Lukac, M., Pregitzer, K.S., Scarascia-Mugnozza, G., Schlesinger, W.H., Oren, R., 2005. Forest response to elevated CO2 is conserved across a broad range of productivity. Proceedings of the National Academy of Sciences USA 102, 18052–18056. Oades, J.M., 1984. Soil organic matter and structural stability, mechanisms and implications for management. Plant and Soil 76, 319–337. Robertson, G.P., Wedin, D., Groffman, P.M., Blair, J.M., Holland, E.A., Nadelhoffer, K.J., Harris, D., 1999. Soil Carbon and Nitrogen Availability: Nitrogen Mineralization, Nitrification, Soil Respiration Potentials. Oxford University Press, Inc., New York. Schlesinger, W.H., Lichter, J., 2001. Limited carbon storage in soil and litter of experimental forest plots under increased atmopsheric CO2. Nature 411, 466–469. Six, J., Elliott, E.T., Paustian, K., 1999. Aggregate and soil organic matter dynamics under conventional and no-tillage systems. Soil Science Society of America Journal 63, 1350–1358. Six, J., Elliott, E.T., Paustian, K., 2000. Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biology & Biochemistry 32, 2099–2103. Six, J., Carpentier, A., Van Kessel, C., Merckx, R., Harris, D., Horwath, W.R., Luscher, A., 2001. Impact of elevated CO2 on soil organic matter dynamics as related to changes in aggregate turnover and residue quality. Plant and Soil 234, 27–36. Six, J., Conant, R.T., Paul, E.A., Paustian, K., 2002. Stabilization mechanisms of soil organic matter: implications for C-saturation of soils. Plant and Soil 241, 155–176. Subke, J.-A., Hahn, V., Battipaglia, G., Linder, S., Buchmann, N., Cotrufo, M.F., 2004. Feedback interactions between needle litter decomposition and rhizosphere activity. Oecologia 139, 551–559. Submitted for Publication L. Taneva, M.A. Gonzalez-Meler. Temperature- and moisture-independent temporal variability in four soil respiration components in a temperate forest exposed to elevated [CO2], submitted. Taneva, L., Pippen, J.S., Schlesinger, W.H., Gonzalez-Meler, M.A., 2006. The turnover of carbon pools contributing to soil CO2 and soil respiration in a temperate forest exposed to elevated CO2 concentration. Global Change Biology 12, 983–994. Trueman, R.J., Gonzalez-Meler, M.A., 2005. Accelerated belowground C cycling in a managed agriforest ecosystem exposed to elevated carbon dioxide concentrations. Global Change Biology 11, 1258–1271. Van Groenigen, K.-J., Six, J., Harris, D., Blum, H., Van Kessel, C., 2003. Soil 13C-15N dynamics in an N2-fixing clover system under long-term exposure to elevated atmospheric CO2. Global Change Biology 9, 1751–1762. Zak, D.R., Pregitzer, K.S., Curtis, P.S., Teeri, J.A., Fogel, R., Randlett, D.L., 1993. Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles. Plant and Soil 151, 105–117.