Figures
Abstract
The flux of carbon dioxide (CO2) between terrestrial ecosystems and the atmosphere may ameliorate or exacerbate climate change, depending on the relative responses of ecosystem photosynthesis and respiration to warming temperatures, rising atmospheric CO2, and altered precipitation. The combined effect of these global change factors is especially uncertain because of their potential for interactions and indirectly mediated conditions such as soil moisture. Here, we present observations of CO2 fluxes from a multi-factor experiment in semi-arid grassland that suggests a potentially strong climate – carbon cycle feedback under combined elevated [CO2] and warming. Elevated [CO2] alone, and in combination with warming, enhanced ecosystem respiration to a greater extent than photosynthesis, resulting in net C loss over four years. The effect of warming was to reduce respiration especially during years of below-average precipitation, by partially offsetting the effect of elevated [CO2] on soil moisture and C cycling. Carbon losses were explained partly by stimulated decomposition of soil organic matter with elevated [CO2]. The climate – carbon cycle feedback observed in this semiarid grassland was mediated by soil water content, which was reduced by warming and increased by elevated [CO2]. Ecosystem models should incorporate direct and indirect effects of climate change on soil water content in order to accurately predict terrestrial feedbacks and long-term storage of C in soil.
Citation: Pendall E, Heisler-White JL, Williams DG, Dijkstra FA, Carrillo Y, Morgan JA, et al. (2013) Warming Reduces Carbon Losses from Grassland Exposed to Elevated Atmospheric Carbon Dioxide. PLoS ONE 8(8): e71921. https://doi.org/10.1371/journal.pone.0071921
Editor: Carl J. Bernacchi, University of Illinois, United States of America
Received: March 4, 2013; Accepted: July 3, 2013; Published: August 19, 2013
This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Funding: This project was supported by the United States Department of Agriculture Agricultural Research Service Climate Change, Soils & Emissions Program, USDA-CSREES Soil Processes Program (Grant no. 2008-35107-18655), United States Department of Energy’s Office of Science (BER), through the Terrestrial Ecosystem Science program and the Western Regional Center of the National Institute for Climatic Change Research at Northern Arizona University, and by NSF (DEB# 1021559). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Models predict declining C sequestration in the coming century [1], [2], [3] as ecosystem respiration (Reco) is preferentially stimulated over ecosystem photosynthesis (Peco), but experimental tests for these predictions are lacking [4]. Experimental manipulations of single global change factors have greatly improved our understanding of ecological processes that regulate C exchange [5], [6]. Photosynthesis is stimulated by elevated [CO2] due to increased biochemical forcing and improved water use efficiency [7], but the magnitude of these mechanisms varies both within and across ecosystems [8]. Warming has been shown to increase, decrease, and have no effect on C assimilation [6] – responses that are tied to enzymatic reaction rates, plant photosynthetic acclimation, potential changes in growing season length, and resource availability. On a physiological level, Reco, composed of both autotrophic (Ra) and heterotrophic (Rh) respiration, responds more strongly to temperature than does photosynthesis [9], underpinning model predictions that ecosystem C storage will gradually decrease in a future warmer world [1], [10]. Multifactor climate change experiments are needed to test the predictions of global C cycle models and identify the strength of interactive effects on ecosystem C uptake and loss [4].
Recent modeling and meta-analysis studies suggest that the combination of warming and elevated [CO2] will increase biomass and soil respiration in grassland [11], [12], but this does not address what mechanisms underlie the responses. Furthermore, only six experiments in the meta-analysis combined these treatments in natural ecosystems, and of those, just one reported measurements of Rh, which is a key determinant of long-term climate – C cycle feedbacks. Biomass and respiration responses to elevated [CO2] are known to be mediated by indirect effects of soil water enhancement [8], [13], whereas warming-induced drying may counteract the effects of moisture on C cycling. These emergent, ecosystem-level properties are not well represented in meta-analyses or simulation models, because virtually no experimental data exists to validate the models.
Since 2006, we have conducted a global change experiment in a temperate semi-arid native grassland in southeastern Wyoming, USA to study the combined impacts of elevated [CO2] and warming on ecosystem C dynamics and C balance. The Prairie Heating And CO2 Enrichment (PHACE) experiment combines a full-factorial manipulation of these global change conditions and a supplemental irrigation treatment across 25 replicate plots (n = 5 per treatment type). Previous research at PHACE demonstrated that elevated [CO2] and warming together enhanced net primary production (NPP), especially in C4 grasses [14], but the gross and net CO2 fluxes, and therefore feedbacks to climate change, are still in question.
We hypothesized that soil water availability (SWC) would mediate treatment effects on gross CO2 fluxes and Rh, such that 1) elevated [CO2] alone (referred to as the Ct treatment) would stimulate Reco more than Peco due to enhanced Rh, leading to net C losses, compared to the ambient (ct) treatment [13], [15]; 2) warming alone (cT treatment) would stimulate Peco and suppress Reco relative to ambient conditions, as soil moisture limits Rh, leading to net C gains relative to ambient conditions [6]; and that 3) elevated [CO2] plus warming (CT treatment) would lead to no stimulation or suppression of Reco or Peco relative to ambient conditions, because SWC is the same in this treatment as ambient [14]. We further hypothesized that CO2 fluxes in the irrigated (ct-i) treatment would follow a similar pattern to the elevated [CO2] treatment because SWC was manipulated to match that of the Ct treatment.
Materials and Methods
Experimental Manipulation and Field Site
The Prairie Heating and CO2 Enrichment (PHACE) experiment is located in a northern mixed grass prairie (NMP) ecosystem at the United States Department of Agriculture Agricultural Research Service (USDA-ARS) High Plains Grasslands Research Station in Cheyenne, Wyoming, USA, with full approval by HPGRS management. The vegetation is dominated by the C3 grass Pascopyrum smithii (Rydb.) A Love and the C4 grass Bouteloua gracilis (H.B.K) Lag, and other abundant species include the C3 grass Hesperostipa comata Trin and Rupr., the sedge Carex eleocharis L. Bailey, and the sub-shrub Artemisia frigida Willd. No protected species were sampled during this research. Mean annual precipitation is 384 mm and mean maximum and minimum air temperatures are 17.5°C in July and −2.5°C in January, respectively. The soil is a fine-loamy, mixed, mesic Aridic Argiustoll.
In 2005, 25 circular plots were established ca. 3.4 m in diameter and surrounded by an impermeable barrier that was buried to 60 cm soil depth. Free-Air CO2 Enrichment [16] began in 2006 and elevates [CO2] to 600 µmol mol−1, and warming began in 2007 with infrared heaters that elevate plant canopy temperatures 1.5 and 3.0°C during the day and night, respectively [17], in a full factorial design with 5 replicates for each of the 4 combinations (ct, ambient CO2 and ambient temperature; cT, ambient CO2 and elevated temperature; Ct, elevated CO2 and ambient temperature; and CT, elevated CO2 and elevated temperature). Five plots were exposed to ambient CO2 and temperature and received periodic irrigations to maintain soil water content (SWC) similar to that in elevated CO2 plots (referred to as ct-i in figures). These plots received 20-mm irrigations five times in 2007 (7 June, 20 June, 11 July, 21 September, and 15 November), three times in 2008 (26 June, 18 July, and 19 September), three times in 2009 (17 July, 10 August, and 28 September), and three times in 2010 (1 July, 22 July, and 20 August).
Continuous Measurement of Soil Moisture
Within each plot, volumetric soil moisture was measured at 10 and 20 cm soil depths (EnviroSMART probe; Sentek Sensor Technologies, Stepney, Australia) and logged (via CR10X data loggers; Campbell Scientific, Logan, Utah, USA) hourly from 2007–2010. We calculated soil water content (SWC; cm H2O) for the 0–10 cm and 10–20 cm soil depths and summed the amounts to arrive at SWC for the upper 0–20 cm of the soil profile.
Ecosystem C Flux Measurements
We used a static chamber method [18] to measure ecosystem C fluxes on ca. 50 days between May 2006 and October 2010 through a combination of mid-day and diurnal sampling campaigns. Flux measurements occurred every 2–4 weeks during the growing season, with diurnal sampling campaigns at approximately 6 week intervals and midday campaigns during the intervening periods. Both net ecosystem exchange (NEE) and ecosystem respiration (Reco) were measured, and ecosystem photosynthesis (Peco) was calculated according to Peco = NEE − Reco. For each diurnal, NEE and Reco were measured 5 times over the course of 24 hours (at ca. 0400, 0900, 1300, 1600, and 2100 hours). We used a Lexan polycarbonate (GE plastics, Pittsfield, MA) chamber fitted with 2 circulating fans, a Q190 photosynthetically active radiation sensor (LI-COR, Lincoln, NE), and an open-path LI-7500 infrared gas analyzer (LI-COR) for measuring [CO2]. Two chambers were used in tandem so that the sampling time period was constrained to ≤2 hours. NEE was measured for 2 minutes, and then an opaque cover was placed over the chamber to block light and eliminate photosynthesis to measure Reco for the next 2 minutes.
Ecosystem CO2 fluxes were calculated after applying a correction for water vapor dilution [19]. Comparisons of CO2 fluxes between the two chambers on a subset of the plots revealed no significant offset from a 1∶1 line, with a correlation coefficient of 0.96, indicating no chamber bias. For each diurnal field campaign, integrations of daily NEE, Peco, and Reco were calculated using linear interpolation between measurement points to calculate hourly C balance, summed over 24-hours and presented as g C m−2 day−1.
We used simple linear regression to establish scaling relationships between mid-day and daily C fluxes [18] (Figures S1, S2). This allowed us to scale frequent mid-day measurements to daily sums of C uptake or loss (g m−2 day−1). Because daily NEE cannot be directly estimated from mid-day NEE, we used the equation NEEdaily = Pecodaily+Recodaily (where Pecodaily and Recodaily were first estimated by linear regression). We arrived at growing season (May – October) Peco, Reco and net ecosystem production (NEP) values by using linear interpolation to estimate daily net C fluxes for all days between measurement dates and then summing all daily data for each season. This simple gap-filling method to estimate seasonal carbon fluxes allowed us to make nearly simultaneous measurements at 25 plots during 50 campaigns. Our measurements were representative of climatic conditions encountered within the field site. This temporal variability did not interact significantly with the climate change treatments [18], so the summation method does not affect the outcome of statistical tests.
Heterotrophic Respiration and Soil C
In early May of 2008, we established root exclusion plots, a standard method for separating soil respiration into root and microbial components [20]. We installed root barriers to 25 cm depth and applied glyphosate, a broad-spectrum herbicide, to a small area of each plot. PVC rings 25-cm in diameter were inserted 8-cm deep into the soil and a standard static chamber method [21] was used to analyze CO2 efflux from headspace samples collected at weekly to biweekly intervals. Syringes were used to collect headspace air three-four times over a 45 minute period, which were analyzed for CO2 by gas chromatography (Varian 3800 gas chromatograph equipped with thermal conductivity and flame ionization detectors, Varian Instruments, Sunnyvale, CA, USA). Soil C concentrations were determined on root-free, acidified (1 N H3PO4) soil samples collected by coring plots in mid-July with a Costech elemental analyzer (Cernusco, Italy).
Methodological Limitations
Ecosystem-scale flux measurements are required to quantify net C storage on land, and partitioning the net CO2 flux into its gross components of ecosystem respiration and photosynthesis demonstrates the physiological control over C storage. We acknowledge the potential for artifacts associated with our chamber techniques, including short-term light-enhanced dark respiration [22] and offsets between light and dark microbial respiration [23]. While increased recognition of these leaf-level phenomena demonstrates a role in ecosystem-scale C cycling, their contribution to fluxes reported here is estimated to be <10%, and within the error of the measurements, because aboveground biomass is only about 20% of total biomass [14], and ecosystem respiration is contributed by approximately equal parts of soil organic matter decomposition and root respiration.
Statistical Analyses
We used a repeated measures mixed effects model with CO2 level, temperature level, and year to test for main and interactive effects of global change treatments on cumulative annual carbon fluxes (Peco, Reco, and NEP). To determine whether C fluxes in response to elevated [CO2] and irrigation were similar, a single factor ANOVA with irrigation as the main effect was used. When necessary, data were log-transformed to meet assumptions of normality and equal variance (soil C). Throughout the text, we characterize significant results according to P≤0.05 and numerical values are presented with standard error of the mean (SEM).
Results
Under present ambient conditions, our data suggest that the semi-arid grassland of the PHACE experiment site ranged from being a slight C sink to a slight source to the atmosphere over 2006–2010; with growing season (April–October) net ecosystem production (NEP, the sum of NEE) losses averaging +33 g m−2 over this period (Fig. 1C; positive fluxes indicate mass transfer from the ecosystem to the atmosphere, and negative fluxes indicate mass transfer from the atmosphere to the ecosystem). Elevated [CO2] reduced net C uptake in 2006, and caused significantly greater net C losses than ambient in 2009 and 2010 (Fig. 1C; ANOVAR P<0.01 in all 3 years; n = 5). No significant elevated [CO2] effects on NEP were observed in 2007–2008. Warming alone never affected NEP, but when combined with elevated [CO2], led to significant net C loss in 2007 (Fig. 1C; ANOVAR P = 0.02; n = 5); consistent net C losses were observed from CT treatment from 2007 through 2010.
Growing season sums (April–October, 2006–2010) for A) gross ecosystem production (Peco), B) ecosystem respiration (Reco) and heterotrophic respiration (Rh) inset white bars, and C) net ecosystem production (NEP) for control and global change treatments at the Prairie Heating and CO2 Enrichment Experiment in Cheyenne, WY USA. Negative (–) values indicate C uptake and positive (+) values indicate C efflux. Treatment codes are: ct = ambient [CO2] and temperature, cT = ambient [CO2] and warming, Ct = elevated [CO2] and ambient temperature, and CT = elevated [CO2] and warming. Statistically significant main and interactive treatment effects (within a given year) along with p-values are indicated (n = 5 for all measurements).
Elevated [CO2] enhanced C cycling by stimulating both gross fluxes, Peco and Reco, from 2006–2008 (Fig. 1), years in which both average and below-average annual precipitation were experienced [14]. During these first three years of the experiment, Peco was stimulated by 19–40%, and Reco by 13–42% (Table 1). Beginning in 2009, however, elevated [CO2] ceased to stimulate Peco but continued to stimulate Reco. This continued stimulation of Reco led to NEP losses that averaged 93 g m−2 per growing season (Fig. 1; Table 1). These cumulative CO2 losses did not lead to measurable net changes in soil C storage or concentrations during 2006–2010.
Throughout the experiment, soil water content (SWC) was increased in elevated [CO2] plots on average by 21% during the growing season (Fig. 2), owing to reduced stomatal conductance and transpiration under elevated [CO2] [8]. We evaluated the influence of this indirect SWC effect on C fluxes by frequently irrigating an additional set of non-CO2 treated plots (n = 5) and maintaining SWC close to that observed under elevated [CO2] (Fig. 2). Both the seasonal pattern of daily Peco (Fig. 3) and the annual Peco response were nearly identical in elevated [CO2] and irrigated plots in all years of the experiment (Fig. 3; Table 1). Further, the addition of 60 mm of water to irrigated plots did not stimulate Peco in 2009 and 2010 (Table 1, Fig. 3), indicating that water availability under ambient conditions did not limit Peco in these two wetter years. This suggests that stimulation of Peco by elevated [CO2] was primarily due to enhanced soil water availability rather than biochemical forcing, and that elevated [CO2] alleviates water limitations that might otherwise constrain Peco.
Mean monthly soil water content (SWC, 0–20 cm) for ambient and global change treatments (2007–2010). Treatment codes are ct = ambient temperature and ambient [CO2]; cT = elevated temperature and ambient [CO2]; Ct = ambient temperature and elevated [CO2]; and CT = elevated temperature and elevated [CO2]; ct-i = ambient temperature and ambient [CO2]+irrigation.
Cumulative effects of global changes on gross ecosystem production (Peco; g m−2 yr−1) and ecosystem respiration (Reco; g m−2 yr−1) in 2007–2010 at the Prairie Heating and CO2 Enrichment Experiment (PHACE) in Cheyenne, WY USA. Treatment effects are differences from ambient values for each year of the experiment with increases in fluxes expressed as “stimulation” and decreases in fluxes expressed as “suppression.” Data are expressed as cumulative across the growing season with the CO2 effect in blue, warming effect in red, CO2×warming interactive effect in purple, and irrigation effect in green. Daily precipitation amounts are depicted in the bottom panel. Both annual and growing season precipitation totals (in parentheses) are included for each year.
Seasonal trends for Reco under elevated [CO2] were similar to the shallow irrigation treatment in 2007–2008 (Fig. 3), suggesting that SWC was important in stimulating Reco during those years of average moisture. However, in 2009–2010, the seasonal trends and cumulative fluxes diverged between elevated [CO2] and irrigation treatments (Fig. 3; Table 1), suggesting that other mechanisms, in addition to SWC, drove the Reco response to elevated [CO2].
Warming suppressed C cycling by reducing Reco, especially during dry years of 2007 (P<0.01) and 2010 (P = 0.03) (Fig. 1; Table 1). In 2007, the suppression of Reco by warming alone was sufficient to enhance net C uptake, but when warming was combined with elevated [CO2], net C losses were enhanced (Fig. 1; [CO2]×temperature interaction, P = 0.02). The warming treatment decreased growing season SWC by 15% on average during 2007–2010 compared to ambient (Fig. 2). Cumulative Peco was not affected by warming (Fig. 1A; Table 1), although it was stimulated early in the wet growing season of 2010 (Fig. 3) when SWC was highest (Fig. 2). This stimulatory effect of warming, however, was quickly reversed as soil water was depleted below levels observed in ambient treatment plots. These opposing responses, within a single growing season, emphasize the role of water availability in mediating C assimilation responses to warming.
Elevated [CO2] led to both gains and losses of C (depending on the year), but when elevated [CO2] was combined with warming, only net C loss was observed (Fig. 1C). This was driven by consistent enhancement of Reco with elevated [CO2] (Fig. 1B) combined with a neutral response of Peco (Fig. 1A). From 2007–2010, Reco was stimulated by an average of 111%, resulting in a net efflux of 259 g C m−2 over 4 years under elevated [CO2] plus warming, compared to ambient conditions. Compared to NEP under ambient conditions, 545 g m−2 of C (237% increase) were lost from the ecosystem with elevated [CO2] plus warming during 2007–2010 (Fig. 1C).
We tested for the possibility of enhanced decomposition at PHACE by measuring respiration from root exclusion plots beginning in 2008. Elevated [CO2] was observed to stimulate decomposition, or Rh, by 145% averaged over the last three years of the experiment (Fig. 1B, white bars), but Ra (estimated as the difference between Reco and Rh) was not significantly affected by any treatment. Soil moisture in root exclusion plots was not affected by elevated [CO2], and was less affected by warming compared to plots with intact vegetation [24]. Therefore the stimulation of Rh by elevated [CO2] may have mainly been driven by increased C substrate in the form of dissolved organic C [25] and/or fine root biomass [14].
Discussion
Our measurements of net CO2 exchange (NEE) and its components of ecosystem CO2 uptake (Peco) and release (Reco) in future climate conditions indicated consistent, inter-annual net CO2 loss in a semi-arid grassland in response to the combined global changes of elevated [CO2] and warming. This result is in contrast to our third hypothesis that the combined treatment would not be different than ambient conditions, and to a recent modeling study indicating net C uptake with elevated [CO2] and warming in other grasslands [12]. This positive feedback to climate change arose due to the prolonged stimulation of Reco and the absence of consistent Peco stimulation by elevated [CO2], in agreement with our first hypothesis. The main effect of warming was to dampen the CO2 loss, particularly in dry years, but Peco was never stimulated by warming, and net C gain never occurred, in opposition to our second hypothesis. While it has been suggested that part of the terrestrial C sink is due to recent warming and lengthening of the growing season [26] our results agree with evidence from climate and remote sensing data [27], suggesting that these changes do not necessarily lead to greater C uptake and assimilation when integrated over the growing season.
Our results indicate that indirect effects of both warming and elevated [CO2] on soil moisture strongly affected Reco. Soil water availability is an important driver of soil and ecosystem respiration – which are comparable in our ecosystem due to the short vegetation stature – especially in water limited environments [28]. A modeling study suggested that precipitation was the dominant environmental influence over Rs in drylands [29], which contrasts somewhat with our findings that added irrigation sometimes stimulated and sometimes suppressed Reco (Table 1; Figure 3). The same modeling study suggests that in simulated future climate, warming will increase the effect of elevated [CO2] by additional stimulation of Rs [29]. This positive effect of combined warming and elevated [CO2] was observed in a mesic herbaceous ecosystem [30]. By contrast, our results suggest warming suppressed the effect of elevated [CO2] on Reco, probably due to soil drying (Table 1; Figure 2).
The importance of substrate availability in the enhancement of respiration by elevated [CO2] was inferred from the larger stimulation of Reco than in the irrigated plots (Figure 3). Stimulation of Peco by elevated [CO2] in the initial years of this experiment, and subsequently greater above- and belowground biomass production [14], may have increased substrate availability [25], [31] to stimulate decomposition by an enhanced priming effect [32]. This is consistent with findings from a CO2 enrichment experiment in a similar grassland where increased belowground C availability was much more important than soil moisture in stimulating soil respiration [33]. Further, increased labile soil C has often been associated with increased Rs in elevated [CO2] experiments [13], [34], [35]. If labile C inputs lead to priming of soil organic matter decomposition (Rh) [13], C losses may be increased with elevated [CO2] [15], [36]. In our experiment, increased supply of C substrates belowground from a larger root system also stimulated microbial activity [25], contributing to the enhanced Rh associated with elevated [CO2]. Our work demonstrates that the considerable stocks of C stored in grassland soils will be vulnerable to future global changes if Rh is broadly stimulated by elevated [CO2] (Figure 1). However, soil C contents did not change over the 5-year duration of our study.
Warming at PHACE stimulates soil microbial temperature sensitivity at optimal moisture conditions [37], indicating that both elevated [CO2] and warming can have the potential to diminish C sequestration in grassland soils. However, drier soils in the field may offset the enhanced temperature sensitivity we observed in the laboratory. The drying effect of warming clearly should be taken into account in modeling studies, some of which still predict enhanced Rh with warming, even in dryland ecosystems [29].
We expected to observe more consistent stimulation of C uptake (Peco) by elevated [CO2], although ample soil moisture availability can suppress the stimulatory effect of elevated [CO2] on biomass growth [14]. Variable C uptake is expected in grassland ecosystems, which are characteristically water-limited and experience high interannual variability in precipitation [38]. Warming suppressed the enhancement of Peco by elevated [CO2] in 2007 with a significant interaction (Figure 1), probably due to reduction of moisture availability (Figure 3). Our experiment indicated relatively small effects of climate change on gross C uptake in comparison to gross C losses, indicating a continued need to improve understanding of respiratory process responses to climate change [39]. These findings underscore the need for continued measurements of interacting climate change factors and moisture mediated responses of ecosystem C metabolism to elevated [CO2] and warming [12], [40].
Supporting Information
Figure S1.
Relationship between midday and daily measurements of ecosystem respiration. Individual data points reflect pairs of midday measurements and daily sums for a given treatment during diurnal field campaigns conducted in 2007–2010.
https://doi.org/10.1371/journal.pone.0071921.s001
(TIF)
Figure S2.
Relationship between midday and daily measurements of ecosystem photosynthesis. Individual data points reflect pairs of midday measurements and daily sums for a given treatment during diurnal field campaigns conducted in 2007–2010.
https://doi.org/10.1371/journal.pone.0071921.s002
(TIF)
Acknowledgments
We thank D. Smith for installation and operation of the PHACE experiment, E. Hardy for assistance in installation, F. Miglietta for advice and help on the installation of the FACE system, and B. Kimball for advice and help on the installation of the infrared heating system. Technical assistance in the field and/or laboratory was provided by S. Bachman, A. Brennan, J. Newcomb, H. Munn, M. Wood, B. Mitra, D. Bronson, M. Taylor, E. Bladyka, J. Chen, K. Tylka, A. Eden, A. Jacobs and M. Smith. E. Ainsworth and C. Bernacchi provided feedback on the manuscript. Mention of commercial products is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA.
Author Contributions
Conceived and designed the experiments: JAM EP DGW. Performed the experiments: JHW EP DGW DRL FAD YC. Analyzed the data: JHW EP. Wrote the paper: EP JHW DGW JAM FAD YC.
References
- 1. Cox PM, Betts RA, Jones CD, Spall SA, Totterdell IJ (2000) Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408: 750–750.
- 2.
Piao SL, Ciais P, Friedlingstein P, de Noblet-Ducoudre N, Cadule P, et al.. (2009) Spatiotemporal patterns of terrestrial carbon cycle during the 20th century. Global Biogeochemical Cycles 23.
- 3. Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440: 165–173.
- 4. Luo Y, Melillo J, Niu S, Beier C, Clark JS, et al. (2011) Coordinated approaches to quantify long-term ecosystem dynamics in response to global change. Global Change Biology 17: 843–854.
- 5. Pataki DE, Ellsworth DS, D ER, Gonzalez-Meler M, King J, et al. (2003) Tracing changes in ecosystem function under elevated carbon dioxide conditions. BioScience 53: 805–818.
- 6. Luo YQ (2007) Terrestrial carbon-cycle feedback to climate warming. Annual Review of Ecology Evolution and Systematics 38: 683–712.
- 7. Nowak RS, Ellsworth DS, Smith SD (2004) Functional responses of plants to elevated atmospheric CO2 - do photosynthetic and productivity data from FACE experiments support early predictions? New Phytologist 162: 253–280.
- 8. Morgan JA, Pataki DE, Korner C, Clark H, Del Grosso S, et al. (2004b) Water relations in grassland and desert ecosystems exposed to elevated atmospheric CO2. Oecologia 140: 11–25.
- 9. Kirschbaum MUF (2000) Will changes in soil organic carbon act as a positive or negative feedback on global warming? Biogeochemistry 48: 21–51.
- 10. Heimann M, Reichstein M (2008) Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451: 289–292.
- 11. Dieleman WIJ, Vicca S, Dijkstra FA, Hagedorn F, Hovenden MJ, et al. (2012) Simple additive effects are rare: a quantitative review of plant biomass and soil process responses to combined manipulations of CO2 and temperature. Global Change Biology 18: 2681–2693.
- 12. Luo Y, Gerten D, Le Maire G, Parton WJ, Weng E, et al. (2008) Modeled interactive effects of precipitation, temperature, and CO2 on ecosystem carbon and water dynamics in different climatic zones. Global Change Biology 14: 1986–1999.
- 13.
Pendall E, Del Grosso S, King JY, LeCain DR, Milchunas DG, et al.. (2003) Elevated atmospheric CO2 effects and soil water feedbacks on soil respiration components in a Colorado grassland. Global Biogeochemical Cycles 17.
- 14. Morgan JA, LeCain DR, Pendall E, Blumenthal DM, Kimball BA, et al. (2011) C(4) grasses prosper as carbon dioxide eliminates desiccation in warmed semi-arid grassland. Nature 476: 202–U101.
- 15. Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proceedings of the National Academy of Sciences of the United States of America 104: 4990–4995.
- 16. Miglietta F, Hoosbeek MR, Foot J, Gigon F, Hassinen A, et al. (2001) Spatial and temporal performance of the MiniFACE (Free Air CO2 Enrichment) system on bog ecosystems in northern and central Europe. Environmental Monitoring and Assessment 66: 107–127.
- 17. Kimball BA (2005) Theory and performance of an infrared heater for ecosystem warming. Global Change Biology 11: 2041–2056.
- 18. Bachman S, Heisler-White JL, Pendall E, Williams DG, Morgan JA, et al. (2010) Elevated carbon dioxide alters impacts of precipitation pulses on ecosystem photosynthesis and respiration in a semi-arid grassland. Oecologia 162: 791–802.
- 19. Jasoni RL, Smith SD, Arnone JA (2005) Net ecosystem CO2 exchange in Mojave Desert shrublands during the eighth year of exposure to elevated CO2. Global Change Biology 11: 749–756.
- 20. Hanson PJ, Edwards NT, Garten CT, Andrews JA (2000) Separating root and soil microbial contributions to soil respiration: A review of methods and observations. Biogeochemistry 48: 115–146.
- 21. Livingston GP, Hutchinson GL, Spartalian K (2006) Trace gas emission in chambers: A non-steady-state diffusion model. Soil Science Society of America Journal 70: 1459–1469.
- 22. Atkin OK, Evans JR, Siebke K (1998) Relationship between the inhibition of leaf respiration by light and enhancement of leaf dark respiration following light treatment. Australian Journal of Plant Physiology 25: 437–443.
- 23. Ayub G, Smith RA, Tissue DT, Atkin OK (2011) Impacts of drought on leaf respiration in darkness and light in Eucalyptus saligna exposed to industrial-age atmospheric CO2 and growth temperature. New Phytologist 190: 1003–1018.
- 24. Carrillo Y, Dijkstra FA, Pendall E, Morgan JA, Blumenthal DM (2012) Controls over Soil Nitrogen Pools in a Semiarid Grassland Under Elevated CO2 and Warming. Ecosystems 15: 761–774.
- 25. Carrillo Y, Pendall E, Dijkstra FA, Morgan JA, Newcomb JM (2011) Response of soil organic matter pools to elevated CO(2) and warming in a semi-arid grassland. Plant and Soil 347: 339–350.
- 26. Nemani RR, Keeling CD, Hashimoto H, Jolly WM, Piper SC, et al. (2003) Climate-driven increases in global terrestrial net primary production from 1982 to 1999. Science 300: 1560–1563.
- 27. Angert A, Biraud S, Bonfils C, Henning CC, Buermann W, et al. (2005) Drier summers cancel out the CO2 uptake enhancement induced by warmer springs. Proceedings of the National Academy of Sciences of the United States of America 102: 10823–10827.
- 28. Parton W, Morgan J, Smith D, Del Grosso S, Prihodko L, et al. (2012) Impact of precipitation dynamics on net ecosystem productivity. Global Change Biology 18: 915–927.
- 29. Shen WJ, Reynolds JF, Hui DF (2009) Responses of dryland soil respiration and soil carbon pool size to abrupt vs. gradual and individual vs. combined changes in soil temperature, precipitation, and atmospheric [CO2]: a simulation analysis. Global Change Biology 15: 2274–2294.
- 30. Wan S, Norby RJ, Ledford J, Weltzin JF (2007) Responses of soil respiration to elevated CO2, air warming, and changing soil water availability in a model old-field grassland. Global Change Biology 13: 2411–2424.
- 31. Fontaine S, Barot S, Barre P, Bdioui N, Mary B, et al. (2007) Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450: 277–U210.
- 32. Kuzyakov Y (2010) Priming effects: Interactions between living and dead organic matter. Soil Biology & Biochemistry 42: 1363–1371.
- 33. Adair EC, Reich PB, Trost JJ, Hobbie SE (2011) Elevated CO2 stimulates grassland soil respiration by increasing carbon inputs rather than by enhancing soil moisture. Global Change Biology 17: 3546–3563.
- 34. Pendall E, King JY (2007) Soil organic matter dynamics in grassland soils under elevated CO2: Insights from long-term incubations and stable isotopes. Soil Biology & Biochemistry 39: 2628–2639.
- 35. Dijkstra FA, Hobbie SE, Reich PB, Knops JMH (2005) Divergent effects of elevated CO2, N fertilizattion, and plant diversity on soil C and N dynamics in a grassland field experiment. Plant and Soil 272: 41–52.
- 36. Hungate BA, Holland EA, Jackson RB, Chapin FSI, Mooney HA, et al. (1997) The fate of carbon in grasslands under carbon dioxide enrichment. Nature 388: 576–579.
- 37. Nie M, Pendall E, Bell CW, Gasch C, Raut S, et al. (2012) Positive climate feedbacks of soil microbial communities in a semi-arid grassland. Ecology Letters 16: 234–241.
- 38. Knapp AK, Smith MD (2001) Variation among biomes in temporal dynamics of aboveground primary production. Science 291: 481–484.
- 39. Pendall E, Bridgham S, Hanson P, Hungate B, Kicklighter D, et al. (2004a) Belowground Process Responses to Elevated CO2 and Temperature: A Discussion of Observations, Measurement Methods, and Models. New Phytologist 162: 311–322.
- 40. Dijkstra FA, Blumenthal D, Morgan JA, Pendall E, Carrillo Y, et al. (2010) Contrasting effects of elevated CO(2) and warming on nitrogen cycling in a semiarid grassland. New Phytologist 187: 426–437.