Global Change Biology (2012) 18, 2532–2545, doi: 10.1111/j.1365-2486.2012.02721.x
Net ecosystem exchange modifies the relationship between the autotrophic and heterotrophic components of soil respiration with abiotic factors in prairie grasslands N U R I A G O M E Z - C A S A N O V A S * , R O S E R M A T A M A L A † , D A V I D R . C O O K ‡ and MIQUEL A. GONZALEZ-MELER* *Department of Biological Sciences, University of Illinois at Chicago, Chicago, IL USA, †Biosciences Division, Argonne National Laboratory, Argonne, IL USA, ‡Environmental Science Division, Argonne National Laboratory, Argonne, IL USA
Abstract We investigated the relationships of net ecosystem carbon exchange (NEE), soil temperature, and moisture with soil respiration rate and its components at a grassland ecosystem. Stable carbon isotopes were used to separate soil respiration into autotrophic and heterotrophic components within an eddy covariance footprint during the 2008 and 2009 growing seasons. After correction for self-correlation, rates of soil respiration and its autotrophic and heterotrophic components for both years were found to be strongly influenced by variations in daytime NEE – the amount of C retained in the ecosystem during the daytime, as derived from NEE measurements when photosynthetically active radiation was above 0 lmol m2 s1. The time scale for correlation of variations in daytime NEE with fluctuations in respiration was longer for heterotrophic respiration (36–42 days) than for autotrophic respiration (4–6 days). In addition to daytime NEE, autotrophic respiration was also sensitive to soil moisture but not soil temperature. In contrast, heterotrophic respiration from soils was sensitive to changes in soil temperature, soil moisture, and daytime NEE. Our results show that – as for forests – plant activity is an important driver of both components of soil respiration in this tallgrass prairie grassland ecosystem. Heterotrophic respiration had a slower coupling with plant activity than did autotrophic respiration. Our findings suggest that the frequently observed variations in the sensitivity of soil respiration to temperature or moisture may stem from variations in the proportions of autotrophic and heterotrophic components of soil respiration. Rates of photosynthesis at seasonal time scales should also be considered as a driver of both autotrophic and heterotrophic soil respiration for ecosystem flux modeling. Received 24 August 2011; revised version received 16 March 2012 and accepted 28 March 2012
Introduction Soil respiration returns carbon (C) back to the atmosphere (about 80 Pg C yr1) and represents one of the largest C fluxes in the terrestrial biosphere (Schlesinger, 1977; Raich et al., 2002). Therefore, small changes in soil respiration rates can have major impacts on annual Present address: Nuria Gomez-Casanovas, Institute for Genomic Biology, University of Illinois at Urbana-Champaign, 1206 W. Gregory Drive, Urbana, IL 61801, USA Correspondence: Miquel A. Gonzalez-Meler, tel. + 312 355 3928, fax + 231 413 2435, e-mail:
[email protected] The submitted manuscript has been created by UChicago Argonne, LLC, Operator of Argonne National Laboratory (“Argonne”). Argonne, a U.S. Department of Energy Office of Science laboratory, is operated under Contract No. DE-AC02-06CH11357. The U.S. Government retains for itself, and others acting on its behalf, a paid-up nonexclusive, irrevocable worldwide license in said article to reproduce, prepare derivative works, distribute copies to the public, and perform publicly and display publicly, by or on behalf of the Government.
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increases in the concentration of atmospheric CO2 (Valentini et al., 2000; Gonzalez-Meler & Taneva, 2004; Schulze, 2006). Despite the importance of soil CO2 efflux on ecosystem C budgets, the underlying biophysical factors controlling the autotrophic and heterotrophic components of soil respiration are poorly understood. This limits our capacity for predicting responses and feedbacks of terrestrial ecosystems to current and future changes in climate (Ryan & Law, 2005). Soil respiration consists of two major flux components: (1) autotrophic respiration integrates the respiration of root systems and root-associated microorganisms, whereas (2) heterotrophic respiration includes the respiration of free-living microorganisms in the soil. The components of soil respiration are known to vary greatly in time and space and across ecosystems (Trumbore, 2006). This variation can be due to the relative contributions of belowground components to soil CO2 efflux, as well as the differential responses of belowground components to abiotic (soil temperature, moisture, © 2012 Blackwell Publishing Ltd
N E E A N D A U T O - A N D H E T E R O T R O P H I C S O I L R E S P I R A T I O N 2533 and oxygen supply) and biotic (vegetation type, plant productivity, and microbial community) factors (Ho¨gberg et al., 2001; Ryan & Law, 2005; Tang et al., 2005; Trueman & Gonzalez-Meler, 2005; Borken et al., 2006; Davidson & Janssens, 2006; Scott-Denton et al., 2006; Trumbore, 2006; Hartley et al., 2007; Bru¨ggemann et al., 2011; Taneva & Gonzalez-Meler, 2011). Partitioning soil respiration into its components becomes essential for elucidating the extent to which biotic and abiotic factors contribute to C oxidative processes in soils. Variations in soil respiration and, to a lesser extent, its autotrophic and heterotrophic components have often been correlated with changes in soil temperature and moisture (Lloyd & Taylor, 1994; Davidson et al., 1998; Kirschbaum, 2000; Janssens et al., 2001; Hibbard et al., 2005; Martin & Bolstad, 2005; Ryan & Law, 2005; Davidson & Janssens, 2006; Bahn et al., 2009). Some studies have shown that soil respiration does not always respond to soil temperature or moisture in a predictable manner (Craine et al., 1999; Ho¨gberg et al., 2001; Wan & Luo, 2003; Tang et al., 2005; Davidson & Holbrook, 2009; Phillips et al., 2011; Taneva & GonzalezMeler, 2011). This, in part, may be the consequence of a recently documented link between concurrent plant activity and variations in soil respiration rates (Craine et al., 1999; Ekblad & Ho¨gberg, 2001; Ho¨gberg et al., 2001; Janssens et al., 2003; Wan & Luo, 2003; CurielYuste et al., 2004; Tang et al., 2005; Trueman & Gonzalez-Meler, 2005; Davidson et al., 2006; Carbone & Trumbore, 2007; Bahn et al., 2009; Kuzyakov & Gavrichkova, 2010; Mencuccini & Ho¨ltta¨, 2010). If plant activity influences soil respiration and its components at different time scales, interpretations of the temperature and moisture sensitivities of soil respiration become difficult (Janssens et al., 2003; CurielYuste et al., 2004; Tang et al., 2005; Trumbore, 2006; Davidson & Holbrook, 2009; Bahn et al., 2010; Bru¨ggemann et al., 2011; Taneva & Gonzalez-Meler, 2011). Photosynthesis and soil respiration interactions have been documented in both forests and grasslands (Vargas et al., 2010, 2011). However, developing a quantitative relationship that includes differential control by plant activity on the autotrophic and heterotrophic components of soil respiration has proven difficult (Hibbard et al., 2005; Bond-Lamberty & Thomson, 2010; Vargas et al., 2011; Taneva & Gonzalez-Meler, 2011), in part, because the mechanistic interactions between plants and soil organisms are not understood (Trueman & Gonzalez-Meler, 2005; Vargas et al., 2011). To date, only forests have shown lagging effects of photosynthesis rates on soil respiration variations within days (Bahn et al., 2008, 2009; BhupinderpalSingh et al., 2003; Tang et al., 2005; Vargas et al., 2010). © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2532–2545
These effects are largely attributed to variations in root respiration. The lack of similar results in grasslands is, in part, due to paucity of data, but more importantly may reveal more complex interactions between the components of soil respiration and changes in temperature or photosynthesis. Although, it is evident that photosynthesis can provide an immediate C source for soil respiration in grasslands (Bahn et al., 2009; Vargas et al., 2011), no studies have shown effects of photosynthesis on separated autotrophic and heterotrophic fluxes in an ecosystem at seasonal time scales. Mixed grasslands (C3 and C4 plants) present a good opportunity to study the dynamics of the autotrophic and heterotrophic components of soil CO2 flux, because these soil respiratory components can be separated on the basis of differences in the natural abundance of 13C derived from decomposition of soil organic matter vs. recent photosynthate. We used a mixed grasslands system to investigate net ecosystem C exchange, soil temperature, and soil moisture effects on soil respiration and its autotrophic and heterotrophic flux components during the growing season by combining eddy covariance flux measurements with continuous measurements of soil respiration. Our main objective was to investigate the relationships of plant activity and environmental factors with total soil, autotrophic, and heterotrophic respiration in grasslands. We also investigated whether variations in total soil, autotrophic, and heterotrophic respiration were in phase with or lagged behind the variations in the biophysical factors over two growing seasons.
Materials and methods
Site description The study site is a restored tallgrass prairie located at the Fermi National Accelerator Laboratory (Batavia, IL, USA). The site had been cultivated for over 100 years before it was restored to prairie in 1990 using native tallgrass prairie vegetation (Betz, 1986; Betz et al., 1996; Matamala et al., 2008). At the time of the study, dominant vegetation consisted of native and nonnative C3 forbs and grasses with some contribution of C4 grasses. The site topography has gradual variations in elevation of less than 3 m. Soils are predominantly silty loams and silty clay loams belonging to the Mundelein soil series. The prairie is burned biannually; during the study it was burned in the spring of 2009.
Eddy covariance measurements Continuous measurements of CO2, water, and energy exchange were made with the eddy covariance technique, a micrometeorological method that measures the net exchange
2534 N . G O M E Z - C A S A N O V A S et al. of a scalar between the biosphere and the atmosphere (Baldocchi, 2003). The CO and H2O fluxes were measured at 3.76 m above the ground, at a rate of 10 Hz, using an open-path CO2/H2O infrared gas analyzer (LI–7500, LICOR, Inc., Lincoln, NE, USA). Wind speed, wind direction, and energy fluxes were measured with a three-dimensional sonic anemometer (R3, Gill Instruments, Ltd., Lymington, UK). The site contributes to the AmeriFlux network (site US-IB2), and calibration of instruments and data handling were in accordance with AmeriFlux standards (http://public.ornl.gov/ameriflux/ sop.shtml). Thirty-minute average fluxes of CO , H2O, and sensible heat and momentum were calculated after application of accepted data corrections (Webb et al., 1980; McMillen, 1988; Massman, 2000; Fuehrer & Friehe, 2002; Finnigan et al., 2003; Loescher et al., 2005; Grelle & Burba, 2007; Ruppert et al., 2006). The 30– min averages were inspected for outliers, and gaps of 1 h or less were filled by linear interpolation. Longer data gaps were filled with 30–min averages derived from all good data from the applicable 30-d period (Moffat et al., 2007). Daily net ecosystem exchange (NEE) was derived from 30–min-average CO fluxes for 48 periods daily (Baldocchi, 2003), from May 18 through November 1 in 2008 and from May 1 through November 1 in 2009. Incoming radiation measurements – obtained every second using a photosynthetically active radiation (PAR) sensor (LICOR LI–190SA Quantum Sensor) installed in the same eddy covariance tower – were averaged every 30 min for a total of 48 periods in a day. Daytime NEE was derived from all 30–min-average CO flux periods when PAR was above 0 lmol m2 s1 (Wilson & Baldocchi, 2001; Drake et al., 2008). Growing season daytime NEE was calculated as the sum of daytime NEE values for the defined time periods. Measurements of soil temperature and moisture were made by using soil probes inserted at a depth of 2.5 cm (REBS STP1 Soil Temperature Probe; REBS SMP1 Soil Moisture Probe) at 1-s time steps. Soil moisture and temperature measurements were averaged every 30 min, for a total of 48 periods in a day, as for NEE and PAR. Because of a transformer failure, NEE was not collected at all times during August 2008. Data gap-filled as in Moffat et al. (2007) were used for the analyses.
Soil respiration measurements Soil respiration was measured continuously every 30 min in four random locations within the footprint of the tower by using an automated infrared gas analyzer (LICOR LI-8100) connected to a multiplexer system (LICOR LI–8150). Chambers (LICOR LI–8100–104), 20.3 cm in diameter, were delimited by polyvinyl chloride (PVC) collars that were permanently inserted 10 cm into the soil after removal of aboveground vegetation. Each collar was measured at least once every 30 min. Less than 15% of the soil respiration data over the two growing seasons required gap filling by a smoothing approach using a 3-days moving average (as in Myklebust et al., 2008). After averaging of data for the four automated chambers, daily and daytime soil respiration rates were calculated similar to NEE.
Separation of the autotrophic and heterotrophic components of soil respiration by using natural abundance isotopes Total soil respiration was separated isotopically into its autotrophic (respiration of roots and root-associated organisms) and heterotrophic (oxidative activity of free-living soil organisms) components. The C3 and C4 mixed crop and the site vegetation history (i.e., corn rotation agriculture) provide isotopically distinct signals of respired CO originating from plant roots and soil organic matter that can be used in a twosource mixing model to separate these two respiration components from CO2 efflux, as follows: d13 CRsoil ¼ ð1 fÞd13 CRoot þ ðfÞd13 CSoil
ð1Þ
Here, d13CRsoil is the d13C of soil-respired CO , d13CRoot and d13CSoil are the d13C values for root-respired and root-free-soilrespired CO2, and f is the fraction of the soil respiration originating from heterotrophs. The d13CRsoil was measured at least once every 3 weeks from May through November using the Keeling plot approach (Keeling, 1958; Pataki et al., 2003) as in Taneva & GonzalezMeler (2011). In brief, an infrared gas analyzer connected to a soil respiration chamber (LICOR LI–6400-09) was used to collect gas samples from 24 PVC soil collars (10–cm diameter) placed across the site. To prevent pressure differences at the time of sampling and minimize kinetic fractionation by soil CO advection, the extracted gas volume was replaced by a similar volume of air transferred to an inflatable balloon inside the chamber (Taneva & Gonzalez-Meler, 2011; Midwood & Millard, 2011). Because the d13CRsoil obtained by the Keeling plot approach was not different from that for nearby collars (Taneva & Gonzalez-Meler, 2011), each collar was sampled once to (1) ensure steady-state CO2 conditions in the soil pore space, (2) minimize kinetic fractionation due to soil CO2 diffusion and extraction, and (3) increase the spatial representativeness of d13CRsoil (Cerling et al., 1991; Pataki et al., 2003; Olsson et al., 2005; Trueman & Gonzalez-Meler, 2005; Bowling et al., 2008; Nickerson & Risk, 2009; Kayler et al., 2010). Gas samples were collected in 125–mL evacuated flasks after passage through a magnesium perchlorate water trap. Gas samples were collected when the CO concentration inside the chamber was 400–700 lL L1 and the CO2 concentrations differed by at least 50 lL L1 among samples (Flanagan et al., 1999; Pataki et al., 2003; Olsson et al., 2005). The CO2 from gas samples was purified by cryogenic distillation within 24 h after collection and was passed through a gas chromatograph connected to a Delta Plus XL mass spectrometer (Finnegan, Bremen, and Germany) operated in continuous-flow mode. Keeling plots were constructed by plotting the d13C of CO2 in any given gas sample obtained at each collar with the inverse of the CO2 concentration of each gas sample. (See Fig. S1 in supplemental information for an example.) The extrapolated y-intercept obtained using a linear regression Model I represented the d13CRsoil. To ensure linearity, only those y-intercepts from linear regressions with r2 > 0.98 were used to partition soil respiration (Pataki et al., 2003; Trueman & Gonzalez-Meler, 2005; Nickerson & Risk, 2009). © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2532–2545
N E E A N D A U T O - A N D H E T E R O T R O P H I C S O I L R E S P I R A T I O N 2535 Because d13CRsoil can vary from daytime to nighttime, two sets of Keeling plots were generated for each day of measurements. Nighttime d13CRsoil measurements were made 2–4 h before dawn, and daytime d13CRsoil measurements were made at about noon, over a 3–h period. Each set of Keeling plots consisted of at least 3 plots constructed using > 5 points for each sampling time. The d13CRoot- and d13CSoil-respired-CO2 end members were measured by soil incubation at field conditions every time a Keeling plot was made (Hymus et al., 2005; Trueman & Gonzalez-Meler, 2005; Millard et al., 2008; Taneva & GonzalezMeler, 2008, 2011). Soil samples were composited from 6 to 9 punch-type soil cores taken near the collars to a depth of 15 cm. Either rinsed root material or root-free soil was incubated in a free-CO2 air chamber, where the accumulated respired CO2 from the sample was collected. These root and root-free soil incubations were done at soil field conditions (temperature and moisture) within 2 h after sampling to minimize substrate effects. Although incubations can affect soil respiration rates, the isotopic compositions of respired CO2 from roots (d13CRoot) and soils (d13CSoil) are often preserved for 3 h and 14 h after sampling, respectively (Millard et al., 2008; data not shown). An assumption of this method is that substrates used for respiration by roots and bulk soil heterotrophs remain unchanged during sample preparation and analyses with respect to in situ conditions. Respired CO2 from these incubations was collected in a 125–mL flask through a water trap (Hymus et al., 2005; Trueman & Gonzalez-Meler, 2005) and distilled cryogenically before passage through a gas chromatograph (to separate N20) to a Delta Plus XL isotope ratio mass spectrometer (Finnegan) operated in continuous-flow mode. Values for fd (the fraction of heterotrophic respiration during daytime) and fn (the fraction of heterotrophic respiration during nighttime) were calculated from Eqn. 1 for each Keeling plot measurement day. Heterotrophic respiration flux for a given day was calculated by multiplying fd by each 30–min total soil respiration average flux period when PAR > 0 or by multiplying fn by each 30–min total soil respiration average flux period when PAR = 0. To obtain continuous measurements for the growing seasons, we applied the same fd and fn values to one previous week and one succeeding week from the day when Keeling plots were made, while weather and NEE conditions were similar. The autotrophic soil respiration flux was determined similarly using (1 fd) and (1 fn). Variability in the partitioning of soil respiration into its autotrophic and heterotrophic components, determined with a first-order Taylor series approximation as described by Phillips & Gregg (2001), accounted for the variability in the d13C of soil-respired CO2 from the root and the root-free soil end members. The statistical difference between the end members was examined by analysis of variance (ANOVA) after checking for normality and homoscedasticity (P < 0.05) using Mystat v.12 (Systat Software, Inc., Chicago, IL, USA).
Statistical analyses We used one-way ANOVA to test for differences in soil moisture and temperature, daytime NEE, and soil respiration and its © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2532–2545
components between the 2008 and 2009 growing seasons. Within each growing season, time lags for biotic factors (daytime NEE) and abiotic factors (moisture, temperature) vs. soil respiration and its components were investigated using Mystat to perform a Fourier-type cross-correlation function analysis for up to 100 days (Bowling et al., 2002; Tang et al., 2005; Vargas et al., 2010). We used simple regression analysis (SRA) to investigate the influence of soil moisture, temperature, and daytime NEE on soil respiration and its autotrophic and heterotrophic components, after transformation of the data to ensure the normality and homogeneity of variances (Schroeder et al., 1986). In addition, we used a general linear model (GLM) to calculate the coefficient of determination (r2) and, thus account for the effects of the abiotic (soil temperature and moisture) vs. biotic (daytime NEE) factors on soil respiration and its autotrophic and heterotrophic components. Daytime NEE, along with soil respiration and its autotrophic and heterotrophic components, were independent variables measured separately, thus avoiding issues often associated with auto-correlated variables (DeLucia et al., 2007). To discount for self-correlation (as NEE flux also contains the soil respiration flux), we used daytime NEE as the unique variable and soil respiration, or its components, as the common variable (as the components are contained in both NEE and soil respiration measurements) to estimate the self-correlation coefficient (rSC, Vickers et al., 2009). The self-correlation coefficient was then used to correct the coefficient of determination (r2) and to obtain the so-called “true” correlation coefficients used for data comparisons (Vickers et al., 2009) at both daily and monthly time scales. These tests and analyses were implemented using Statgraphics Plus 5.0 (Statistical Graphics Corporation, Rockville, MD, USA).
Results
Climatic variables and daytime NEE Mean soil temperature was similar (P = 0.1, ANOVA) for the growing seasons of 2008 (18.2 ± 0.3 °C) and 2009 (18.8 ± 0.3 °C; Fig. 1A). Soil temperature maximums were 24.3 °C in mid-August 2008 and 26.5 °C and 25.7 °C in mid-June and mid-August 2009, respectively (Fig. 1A). Mean soil volumetric water content was also similar (P = 0.9, ANOVA) for the 2008 (0.37 ± 0.01 cm3 cm3) and 2009 (0.36 ± 0.01 cm3 cm3) growing seasons (Fig. 1B). Growing season cumulative precipitation was higher in 2008 (807 mm) than in 2009 (550 mm; Fig. 1B). Daily NEE was negative (i.e.,photosynthetic C uptake > respiratory C losses) from the beginning of May through mid-September for both years (Fig. 2). Throughout the two growing seasons, daily NEE values decreased from May to June, reaching most negative values by early June (–9.7 g C m2 day1 in 2008 and – 10.0 g C m2 day1 in 2009), then progressively
2536 N . G O M E Z - C A S A N O V A S et al.
(A)
(A)
(B) (B)
Fig. 1 Diurnal averages of soil temperature at 2.5 cm depth (A), volumetric soil water content at 2.5 cm depth (B, dots), and cumulative rainfall (B, triangles) during the 2008 and 2009 growing seasons. Because of instrument failure, data for August 5–26, 2008, were extracted from a nearby (~ 1 km) fully instrumented site.
(C)
Fig. 3 Daily soil (A, s), autotrophic (B, r), and heterotrophic (C, &) respiration rates over the 2008 and 2009 growing seasons. Autotrophic and heterotrophic components were calculated from soil respiration using a two-end-member mixing model, as explained in Materials and Methods. Fig. 2 Daily (daytime + nighttime; filled circles) and daytime (open circles) NEE during the 2008 and 2009 growing seasons. Data for August 5–26, 2008, are averages of NEE and daytime NEE values from the 2005, 2007, and 2009 growing seasons.
increasing until the end of the growing season in October (Fig. 2). Growing season NEE was –413 g C m2 in 2008 and –579 g C m2 in 2009 (P < 0.05, ANOVA; Fig. 2). Growing season daytime NEE was about 28%
higher in 2009 (–806 g C m2) than in 2008 (–628 g C m2, P < 0.05; Fig. 2) and followed growing season patterns similar to those of daily NEE.
Soil respiration flux and its autotrophic and heterotrophic components Daily rates of soil respiration exhibited temporal variability during both growing seasons (Fig. 3A). In © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2532–2545
N E E A N D A U T O - A N D H E T E R O T R O P H I C S O I L R E S P I R A T I O N 2537 general, these rates increased from May to June. After reaching a maximum in mid-June, they declined progressively until the end of the growing season (Fig. 3A). Cumulative growing season soil respiration flux was not different between the two growing seasons. The isotopic composition of soil-respired CO2 (d13CRsoil; determined by Keeling plots) was not different during daytime vs. nighttime periods for most of the 2008 and 2009 growing seasons (Table 1). Daytime and nighttime d13CRsoil values were different only at the end of June and the beginning of July for both growing seasons (P < 0.05, ANOVA; Table 1). In 2008 and 2009, respired CO2 values for d13CRoot and d13CSoil were significantly different from each other during both daytime and nighttime (P < 0.05, ANOVA; Fig. 4), allowing their use as end members (Eqn. 1). The isotopic composition of the root-free soil end member (d13CSoil) decreased from –25.0 ± 0.8& in May to –26.0 ± 0.1& in November during 2008 and from –25.3 ± 0.2& in May to –26.3 ± 0.1& in November in 2009 (Fig. 4). Daytime and nighttime values of the d13CRoot end member were more depleted than the d13CSoil end member for both the 2008 and 2009 growing seasons (P < 0.05, ANOVA; Fig. 4). The proportion of the autotrophic component in soil respiration was 48% for the 2008 growing season and 52% for the 2009 growing season (Table 1). This proportion, however, varied during the growing season. Autotrophic respiration from soils represented as much as 74% of soil respiration in June, but declined to 25% by end of the growing season (Table 1). Although the
Fig. 4 The isotopic composition of root-respired CO2 (d13CRoot; open symbols) and root-free-soil-respired CO2 (d13CSoil; closed symbols) during the 2008 and 2009 growing seasons. The d13CRoot and the d13CSoil end members were determined from root- and root-free-soil-respired CO2 field incubations. Measurements were made during either daytime (s) or nighttime (r). Values shown are means ± standard error of the mean of 3–6 replicates. Asterisks denote statistical differences between d13CRoot and d13CSoil (P < 0.05; ANOVA).
proportion of autotrophic respiration to soil respiration was similar for most of the growing seasons of 2008 and 2009, striking differences were seen during the month of August (Table 1). In 2008, the autotrophic component represented 29% of total soil respiration in August, whereas during 2009 it represented 55% of total soil respiration (Table 1). Conversely, the contribution of
Table 1 The d13C of soil-respired CO2 (d13CRsoil) and the percentage contribution of autotrophic respiration to soil respiration (in parentheses) for the 2008 and 2009 growing seasons. The percentage contribution of autotrophic respiration was estimated using Eqn. 1 and data from Fig. 4. The d13C of soil-respired CO2 (d13CRsoil obtained as a Keeling plot) is shown for the daytime (D) and nighttime (N) periods. Isotope values shown are means ± standard errors of at least four replicates. N/A indicates no data for that day and period. Asterisks denote statistical differences between d13C values of soil-respired CO2 measured during daytime and nighttime periods (P < 0.05) 2008 Julian Day June 10 July 1 July 23 August 21
September 9 October 30
2009
D N D N D N D N D N D N
d13C Soil-Respired CO2 –28.15 ± 0.22 (73.9 ± 8) –28.20 ± 0.14 (74.2 ± 6.2) –27.80 ± 0.24*(70.6 ± 6.7) –27.07 ± 0.03 (70.8 ± 9.7) –27.87 ± 0.22*(62.6 ± 9.3) –27.07 ± 0.16 (63.5 ± 8.4) –26.51 ± 0.10 (26.6 ± 10) –26.64 ± 0.16 (28.9 ± 12) –26.44 ± 0.08 (24.2 ± 26.4) –26.41 ± 0.03 (27.5 ± 10.6) –26.86 ± 0.07 (27.4 ± 3.5) N/A
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2532–2545
Julian Day May 20 June 25 July 18 September 6
September 27 October 24
D N D N D N D
d13C Soil-Respired CO2 –27.08 ± 0.10 (66.5 ± 10.3) –26.88 ± 0.10 (63.8 ± 8.9) –27.38 ± 0.09*(74.3 ± 11.4) –26.75 ± 0.11 (70 ± 16.3) –27.73 ± 0.19 (67.3 ± 15.9) –27.45 ± 0.13 (66.7 ± 18.2) –27.40 ± 0.12 (55.4 ± 20.6)
N D N D N
–27.05 ± 0.18 (46.5 ± 17.7) –26.62 ± 0.07 (22.2 ± 31.4) N/A –26.60 ± 0.014 (25.8 ± 50.8) N/A
2538 N . G O M E Z - C A S A N O V A S et al. the heterotrophic component of soil respiration was relatively low at the beginning of the growing season (May-June) and increased to 74% by November of both years (Table 1). The autotrophic component of soil respiration exhibited higher rates during the growing season in 2009 (3.1 ± 0.2 g C m2 day1) than in 2008 (2.4 ± 0.1 g C m2 day1; P < 0.05, ANOVA; Fig. 3B). Heterotrophic soil respiration rates were similar for both the 2008 and 2009 growing seasons (2.4 ± 0.1 g C m2 day1 and 2.2 ± 0.1 g C m2 day1; P = 0.16, ANOVA; Fig. 3C). The autotrophic component of soil respiration showed a consistent pattern for the two growing seasons studied, reaching maximum steady values during July and August, but declining progressively after that and reaching very low values at the end of the growing season (< 0.2 g C m2 day1; Fig. 3B). Rates of heterotrophic soil respiration reached a maximum value during September for both years (3.5 and 3.8 g C m2 day1 for 2008 and 2009, respectively; Fig. 3C). Minimum rates of heterotrophic soil respiration were observed at the beginning of the growing season, during the month of May (0.9 and 0.7 g C m2 day1 for 2008 and 2009, respectively; Fig. 3C).
Relationships between components of soil respiration and abiotic and biotic factors Soil temperature and daily rates of soil respiration were moderately correlated for both the 2008 and 2009 growing seasons (Table 2). Soil temperature variations explained more of the variation in the rates of heterotrophic respiration in 2008 than in 2009 (Table 2; Fig. 5), but they did not explain much of the variation in the autotrophic component of soil respiration (Table 2; Fig. 5). In contrast, soil moisture strongly influenced total soil respiration and its autotrophic component, particularly during the growing season of 2008 (Table 2; Fig. 6). In 2009, this relationship was weaker than in 2008, and soil moisture explained variations in the rates of heterotrophic soil respiration only poorly (Table 2; Fig. 6). After correction for self-correlation (Vickers et al., 2009), soil respiration and its autotrophic and heterotrophic components were significantly correlated with daytime NEE, although at different time scales (Table 2; Fig. 7). During the growing seasons of 2008 and 2009, fluctuations in daytime NEE values caused the rates of soil and autotrophic respiration to vary
Fig. 5 The relationships between the autotrophic (r; top panels) and heterotrophic (&; bottom panels) components of soil respiration and soil temperature during the 2008 (filled symbols) and 2009 (open symbols) growing seasons. Coefficients of determination are shown in Table 2. © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2532–2545
N E E A N D A U T O - A N D H E T E R O T R O P H I C S O I L R E S P I R A T I O N 2539
Fig. 6 The relationships between the autotrophic (r; top panels) and heterotrophic (&; bottom panels) components of soil respiration and volumetric soil water content during the 2008 (filled symbols) and 2009 (open symbols) growing seasons. Coefficients of determination are shown in Table 2.
4–8 days later and the rates of heterotrophic respiration to vary more than a month later (Table 2; Fig. 7). Daytime NEE was correlated with the daily rates of soil, autotrophic, and heterotrophic respiration, after accounting for the time lag and even after adjusting for self-correlation (soil respiration r2SC = 0.14 and 0.19 in 2008 and 2009, respectively; autotrophic respiration r2SC = 0.12 and 0.14 in 2008 and 2009, respectively; and heterotrophic respiration r2SC = 0.01 for both years), particularly in 2008 (Table 2). The proportion of variation explained by daytime NEE over abiotic factors depended on the soil respiration component, ranging from 22% to 31% in 2008 and from 16% to 32% in 2009, as shown by the GLM analysis (Table 2).
Discussion In this study, we investigated daytime NEE, soil temperature, and soil moisture controls on soil respiration and its autotrophic and heterotrophic components in a tallgrass prairie. Within a growing season, soil respiration was correlated with daytime NEE (dominated by plant photosynthesis) and, to a lesser extent, by soil © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2532–2545
temperature and moisture. Variations in daytime NEE explained variations in both the autotrophic and heterotrophic components of soil respiration. In addition, rates of heterotrophic soil respiration varied with soil temperature, whereas the autotrophic component of soil respiration also appeared to be correlated with changes in soil moisture (Table 2). These results suggest that the sensitivity of soil respiration to abiotic factors (temperature and moisture) may be a function of the proportions of the autotrophic and heterotrophic components of soil respiration at any given time. Results also document that plant photosynthetic activity drives not only the more obvious soil autotrophic component but also the soil heterotrophic components, although at different time scales. Daytime NEE was highly correlated with rates of soil respiration (Table 2). As daytime NEE flux of grasslands is dominated by plant photosynthesis (Wilson & Baldocchi, 2001; Drake et al., 2008), these results are in agreement with forest studies in which soil respiration depended strongly on plant photosynthetic activity over both short (Ekblad & Ho¨gberg, 2001; Ho¨gberg et al., 2001; Janssens et al., 2003; Curiel-Yuste et al.,
0.58 0.39 0.24 0.35 0.43 42 0.82 0.54 0.13 0.71 36
0.50
0.61 0.65 0.45 0.33 0.34 0.34 0.24 0.07 0.40 0.63 8 6 0.82 0.86 0.60 0.55 0.67 0.62 0.35 0.18 0.71 0.75
Soil Temperature T
6 4
Soil Respiration Autotrophic Respiration Heterotrophic Respiration
Abiotic & biotic factors Abioticfactors Abiotic factors Daytime NEE
Soil Moisture
GLM analysis SRA analysis
Abiotic & biotic factors
T
Daytime NEE
Soil Temperature
Soil Moisture
GLM analysis SRA analysis 2009 2008
Table 2 The lag time (T, in days) of total soil respiration and its autotrophic and heterotrophic components vs. daytime NEE, the true coefficients of determination (i.e., observed coefficients, r2, minus self-correlation coefficients, r2SC; P < 0.01) derived from the relationships between total soil respiration and its autotrophic and heterotrophic components with soil temperature, soil moisture, and daytime NEE (SRA analysis), and the true coefficients of determination (adjusted by r2SC; r2; P < 0.01) derived from the combined effect of abiotic factors (soil temperature and moisture) and biotic factors (daytime NEE) on soil respiration and its components (GLM analysis)
2540 N . G O M E Z - C A S A N O V A S et al. 2004; Trueman & Gonzalez-Meler, 2005; Davidson et al., 2006; Carbone & Trumbore, 2007; Carbone & Vargas, 2008; Kuzyakov & Gavrichkova, 2010; Mencuccini & Ho¨ltta¨, 2010; Vargas et al., 2010) and long time scales (Raich & Schlesinger, 1992). However, the relationships between plant activity and soil respiration in this grassland were not linear, as a 28% increase in daytime NEE during the 2009 season (Fig. 2) resulted in lower correlation with soil respiration rates than in 2008, when NEE was lower (Table 2). In fact, all biotic and abiotic factors explained more than 80% of the variation in soil respiration and its components during the growing season of 2008, whereas it explained roughly 60% during 2009 (Table 2). This nonlinearity suggests uncoupling between aboveground plant activity and belowground ecosystem fluxes. Ford et al. (2012) showed that increased annual precipitation in temperate grasslands ecosystems resulted in an increased C allocation to roots. As 2008 had higher rainfall in the growing season than did 2009 (Fig. 1B), plants might have allocated proportionally more C to belowground tissues during 2008, increasing the sensitivity of soil fluxes to daytime NEE that year (Table 2). This might have increased autotrophic respiration from soils, which represented roughly 50% of overall soil respiration during the growing season, as seen in other studies (Dugas et al., 1999; Hanson et al., 2000; Subke et al., 2006). However, the proportion of autotrophic respiration in soil respiration ranged from > 60% early in the growing season to 20% late in the growing season. The autotrophic and heterotrophic components of soil respiration might have different sensitivities to biotic and abiotic controlling factors (e.g., Tang et al., 2005; Taneva & Gonzalez-Meler, 2011). For instance, autotrophic respiration from soils slowed more at lower soil moisture values (0.30 cm3 cm3) than did the heterotrophic component (> 0.40 cm3 cm3; Fig. 6). During the course of the experiment, 40% of the days experienced conditions of soil moisture above 0.40 cm3 cm3. Soil aggregation and structure, along with soil moisture, are major determinants of soil C accrual rates in these prairies (O’Brien et al., 2010). High soil moisture conditions, along with other edaphic factors (texture, pore size, etc.), might determine the availability of oxygen to roots and decomposers, thus affecting respiration rates (Davidson et al., 1998). In contrast with soil moisture, heterotrophic soil respiration was more sensitive than the autotrophic component to soil temperature (Table 2). These results contrast with some similar forest studies (Boone et al., 1998; Epron et al., 2001; Koch et al., 2007), but they are in agreement with many other studies, including those in grasslands (Luo et al., 2001; Ba¨th & Wallander, 2003; © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2532–2545
N E E A N D A U T O - A N D H E T E R O T R O P H I C S O I L R E S P I R A T I O N 2541
Fig. 7 The relationships between the autotrophic (r; top panels) and heterotrophic (&; bottom panels) components of soil respiration with daytime NEE during the 2008 (filled symbols) and 2009 (open symbols) growing seasons. Coefficients of determination are shown in Table 2.
Hartley et al., 2007; Heinemeyer et al., 2007; Bahn et al., 2009; Ho¨gberg, 2010; Vicca et al., 2010; Wei et al., 2010). The lack of apparent sensitivity of the autotrophic component of soil respiration to temperature is in contrast with the vast amount of resources invested to belowground biomass and the large proportion of autotrophic respiration in soils (Table 2). Substrate supply to roots and rapid thermal acclimation of root respiration activity and capacity might explain these observations (Atkin & Tjoelker, 2003; Gonzalez-Meler & Taneva, 2004). In addition, the sensitivity of the heterotrophic component of soil respiration to temperature could be caused, in part, by the availability of soil C substrates (Kirschbaum, 2004; Eliasson et al., 2005; Hartley et al., 2007; Vicca et al., 2009; Bru¨ggemann et al., 2011). The availability of respiratory substrates from recently formed photosynthate might influence the components of soil respiration (Fig. 7), but not necessarily to the same extent. For example, prairie plant dynamics, where C3 and C4 plants substitute for each other during the growing season, could reduce impacts of temperature on autotrophic respiration by ensuring that active root systems are present through© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2532–2545
out the season, while influencing heterotrophic respiration through variations in substrate quality and availability (O’Brien et al., 2010, 2012). A similar situation could explain the lack of an apparent response of soil heterotrophic respiration to experimental air warming for most of the growing season (Suseela et al., 2012). Therefore, seasonal responses of soil respiration to abiotic factors can also depend on the proportion of auto- and heterotrophic components of soil respiration. Consistent with these observations was a strong relationship between daytime NEE and autotrophic soil respiration, with a lag time of 4–6 days (Table 2). A similar time lag between plant photosynthesis and soil respiration has been shown previously for forests (e.g., Bowling et al., 2002) and has been explained as the time required for phloem sap to reach belowground tissues (Davidson & Holbrook, 2009; Kuzyakov & Gavrichkova, 2010; Mencuccini & Ho¨ltta¨, 2010). Although the time lag between daytime NEE and soil respiration might be shorter in herbaceous species than in forests (12–24 h; Kuzyakov & Gavrichkova, 2010), this was not the case for our study (4–6 days) and for
2542 N . G O M E Z - C A S A N O V A S et al. the other very few field studies in perennial grasslands (e.g., Carbone & Trumbore, 2007). The time lag discrepancy between this study and other studies with herbaceous plants might result from the time needed for CO to diffuse from roots to the soil surface (Stoy et al., 2007). This diffusion could be impeded by the poorly drained characteristics of the clayey soil at our study site. In grasslands, the supply of photosynthate to distant roots via phloem might not be a limiting factor for the autotrophic component of soil respiration (reviewed by Kuzyakov & Gavrichkova, 2010), as root respiration is thought to be driven by energy demand (Bingham & Farrar, 1988), and high levels of nonstructural carbohydrates often result in down-regulation of root respiration capacity (e.g., Millenaar et al., 2002). The relationships between daytime NEE and root respiration seen in our study are, therefore, likely driven by the competition between shoots and roots for nutrients to meet energy demands (e.g., Lejay et al., 2008), root growth patterns (e.g., Millenaar et al., 2001), total root mass (Kucera & Kirkham, 1971), nonstructural carbohydrates (e.g., Carbone & Trumbore, 2007), exudates (Badri & Vivanco, 2009), nonphosphorylating pathways (Rachmilevitch et al., 2007), or abiotic constraints (e.g., Atkin et al., 2009). These factors would effectively vary the sink strength of belowground tissues affecting the C allocation patterns of grassland plants. This was the case for the growing season of 2008, where high precipitation levels could have resulted in greater belowground C allocation (as described in Ford et al., 2012) than in 2009. The strength of the relationship between abiotic and biotic factors and soil respiration and its components could also be the result of changes in plant C allocation patterns, which could affect plant respiration rates (Cannell & Thornley, 2000; Thornley & Cannell, 2000). Evidence from this can be seen in some forest studies. In a loblolly pine plantation, autotrophic respiration was controlled by substrate supply from photosynthesis at the beginning of the growing season, when energy demand was low; however, substrate supply could not meet the demand from root tissues in midsummer (Drake et al., 2008), when net photosynthesis was at its maximum (Scha¨fer et al., 2003). Therefore, root respiration would be more highly correlated with daytime NEE at low NEE values (as in 2008) than at high NEE values (2009; Table 2; Fig. 7). This is because substrate supply to root respiration is likely to be less under lower photosynthetic rates; that is, if root respiration is limited by substrate, increases in substrate supply due to higher daytime NEE should increase autotrophic respiration. Other factors such as rootshoot ratios, storage of carbohydrates, exudation rates,
and symbiotic associations might further explain the lower true correlation coefficients of 2009 vs. 2008. Plant photosynthetic activity can also modulate the heterotrophic component of soil respiration (Table 2; Fig. 7) at monthly time scales. For example, heterotrophic soil respiration lagged daytime NEE by 36–42 days (Table 2). In a tulip poplar plantation, heterotrophic respiration of C pools that were at least 3 years old was dramatically inhibited 10 days after tree coppicing (Trueman & Gonzalez-Meler, 2005). Similar short-time dependencies have now been documented in other forests for even decadal soil C substrates (e.g., Taneva & Gonzalez-Meler, 2011). These results suggest a direct or indirect C dependency of decomposers on recent assimilates that might be afforded by exudates or the turnover of fine roots, microbial biomass, or even soil aggregates. Microbial biomass turnover in grasslands has been reported to be 7–27 days, depending on the soil conditions (Ocio et al., 1991; Ostle et al., 2003) affecting the time lag between microbial growth (which might respond to rhizodeposits) and the amount of dead microbial biomass available for other heterotrophic respiration components (Leake et al., 2006; Jones et al., 2009). Increased substrate availability at the end of the growing season due to plant senescence and root mortality could also explain increases in heterotrophic respiration during this period (Fig. 3C; Table 1), when daytime NEE declined sharply (Fig. 2). Plant roots can modulate microbial activity, growth, and diversity through exudation and rhizodeposition rates (Badri & Vivanco, 2009; Ladygina & Hedlund, 2010). Plant C substrates leached to soils can also stimulate the mineralization of older soil organic matter through the so-called “priming effect” (Kuzyakov and Cheng, 2001, 2004; Kuzyakov, 2002; Fontaine et al., 2007). Together, these plant substrate dependencies of soil decomposers and the time scales at which they operate, although not fully understood, can have a substantial impact on the ability of soils to store carbon. We conclude that the autotrophic and heterotrophic components of soil respiration were affected by daytime NEE at different time scales. In addition, the autotrophic component of soil respiration was sensitive to soil moisture, whereas heterotrophic respiration from soils was also sensitive to soil temperature. Plant photosynthetic activity (the major driver of daytime NEE) is an important factor determining rates of soil respiration, its autotrophic and heterotrophic components, and its temperature and moisture sensitivities in prairie grasslands. Ecosystem models should consider these primary effects of NEE on soil respiration and its components to detect the true sensitivity of ecosystem fluxes to climate forcing factors. © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2532–2545
N E E A N D A U T O - A N D H E T E R O T R O P H I C S O I L R E S P I R A T I O N 2543 Acknowledgments The “Measurement of Carbon Fluxes and Stocks in Midwest Agricultural Land and Restored Grasslands” project is supported by the U S Department of Energy, Office of Science, Office of Biological and Environmental Research, Terrestrial Ecosystem Science Division, under contract DE-AC0206CH11357. We thank Fermilab National Environmental Research Park coordinator Rod Walton and Fermilab Road and Grounds personnel, especially Michael Becker and Robert Lootens, for maintenance of the site; J Sarsfield, R. Bourgart, S. Kirt, and T. Vugteveen (Argonne) for assistance in the sampling and processing of vegetation and soils; and J. LugoPerez and M. Sandor (University of Illinois at Chicago) for their help in isotope measurements at the University’s stable isotope laboratory.
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Supporting Information Additional Supporting Information may be found in the online version of this article: Figure S1. Data for daytime 10 June 2008 sampling, are shown below as an example of a typical Keeling plot constructed to determine the d13C of soil-respired CO during this study at any given time. Data points show the relationship between the inverse of the concentration of CO in the headspace of the soil respiration chamber (x-axis) vs. the d13C of the air collected from the headspace chamber (y-axis) at a given CO concentration. Each headspace air sample was collected from a different PVC collar, when the CO concentration inside the soil respiration chamber was 400-700 µL L-1 and the CO2 concentration differed by at least 50 µL L-1 from that for the previous sample. The data points were fitted to a linear regression Model I. The extrapolated y-intercept represents the d13C of soil-respired CO (d13CRsoil). For this linear regression, the slope was 7194 ± 308, the y-intercept was 28.25 ± 0.1 and the r2 = 0.9950.
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