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Interpreting, Measuring, and Modeling Soil Respiration

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Interpreting, Measuring, and Modeling Soil Respiration Biogeochemistry (2005) 73: 3–27 Ó Springer 2005 DOI 10.1007/s10533-004-5167-7 -1 Interpreting, measuring, and modeling soil respiration MICHAEL G. RYAN1,2,* and BEVERLY E. LAW3 1US Department of Agriculture-Forest Service, Rocky Mountain Research Station, 240 West Pros- pect Street, Fort Collins, CO 80526, USA; 2Affiliate Faculty, Department of Forest, Rangeland and Watershed Stewardship and Graduate Degree Program in Ecology, Colorado State University Fort Collins, CO 80523, USA; 3Department of Forest Science, Oregon State University, 328 Richardson Hall, Corvallis, OR 97331, USA; *Author for correspondence (e-mail: mgryan@fs.fed.us) Key words: Belowground carbon allocation, Carbon cycling, Carbon dioxide, CO2, Infrared gas analyzers, Methods, Soil carbon, Terrestrial ecosystems Abstract. This paper reviews the role of soil respiration in determining ecosystem carbon balance, and the conceptual basis for measuring and modeling soil respiration. We developed it to provide background and context for this special issue on soil respiration and to synthesize the presentations and discussions at the workshop. Soil respiration is the largest component of ecosystem respiration. Because autotrophic and heterotrophic activity belowground is controlled by substrate availability, soil respiration is strongly linked to plant metabolism, photosynthesis and litterfall. This link dominates both base rates and short-term fluctuations in soil respiration and suggests many roles for soil respiration as an indicator of ecosystem metabolism. However, the strong links between above and belowground processes complicate using soil respiration to understand changes in ecosystem carbon storage. Root and associated mycorrhizal respiration produce roughly half of soil respiration, with much of the remainder derived from decomposition of recently produced root and leaf litter. Changes in the carbon stored in the soil generally contribute little to soil respiration, but these changes, together with shifts in plant carbon allocation, determine ecosystem carbon storage belowground and its exchange with the atmosphere. Identifying the small signal from changes in large, slow carbon pools in flux dominated by decomposition of recent material and autotrophic and mycorrhizal respiration is a significant challenge. A mechanistic understanding of the belowground carbon cycle and of the response of different components to the environment will aid in identifying this signal. Our workshop identified information needs to help build that understanding: (1) the mechanisms that control the coupling of canopy and belowground processes; (2) the responses of root and heterotrophic respiration to environment; (3) plant carbon allocation patterns, particularly in different forest developmental stages, and in response to treatments (warming, CO2, nitrogen additions); and (4) coupling measurements of soil respiration with aboveground processes and changes in soil carbon. Multi-factor experiments need to be sufficiently long to allow the systems to adjust to the treatments. New technologies will be necessary to reduce uncertainty in estimates of carbon allocation, soil carbon pool sizes, and different responses of roots and microbes to environmental conditions. Introduction Belowground processes exert a large control on terrestrial carbon cycling. Plants send an estimated 35–80% of the carbon fixed in photosynthesis belowground for root production and respiration, mycorrhizae, and root exudates (Raich and Nadelhoffer 1989; Davidson et al. 2002a; Giardina et al. 4 2003; Ryan et al. 2004), and also transfer about 10% of annual photosyn- thesis to aboveground litter (Raich and Nadelhoffer 1989). The carbon stored in litter and labile and recalcitrant soil carbon pools is a large fraction of the carbon stored in the ecosystem in forests (30–90%, Dixon 1994; Sun et al. in press) and in grasslands (>90%). In forests, the carbon stored in roots (mostly woody support structures) is also a large pool – about 20% of aboveground biomass (Jackson and Chittenden 1981; Misra et al. 1998). Changes in the belowground carbon pools can have a major impact on carbon storage in terrestrial ecosystems and change carbon flux to the atmosphere. CO2 efflux from the litter surface originating as plant and microbial respi- ration reflects this large belowground activity. This ‘soil respiration’ is the main pathway for carbon moving from the ecosystem to the atmosphere and can strongly influence net carbon uptake from the atmosphere, or net ecosystem production (NEP) – the balance between photosynthesis (GPP) and ecosystem respiration. Eddy covariance studies have shown that on average, 80% of GPP is respired back to the atmosphere (Law et al. 2002) and that 70% of eco- system respiration in temperate forests is from soil (Goulden et al. 1996; Law et al. 1999; Janssens et al. 2001). Respiration may be more important than photosynthesis in controlling interannual variability in NEP (Valentini et al. 2000). The CO2 produced at the soil surface results from several respiratory pro- cesses, making modeling and interpretation of data complicated. About half the soil respiration is derived from metabolic activity to support and grow roots and associated mycorrhizae (Hanson et al. 2000; Ho¨gberg et al. 2001). Most of the remainder is associated with heterotrophic respiration from microbial communities using recently produced organic material as an energy substrate (Trumbore 2000; Giardina et al. 2004). Only a small fraction (10%) of soil respiration is derived from decomposition of older, more recalcitrant carbon compounds (Gaudinski et al. 2000; Trumbore 2000; Giardina et al. 2004). The proportion of soil respiration from autotrophic and heterotrophic contributions may vary seasonally and among ecosystems (Hanson et al. 2000). Across a range of studies, the heterotrophic contribution varied from 10 to 95% and averaged 54% annually and 40% during the growing season (Hanson et al. 2000). Because of its major role in carbon loss from ecosystems, soil respiration has received much recent attention, and the number of studies of soil respiration has increased rapidly. However, this flurry of studies has uncovered many new problems and opportunities. How can we untangle the components of this complex flux to understand the underlying processes that contribute to it? What are the short-term and long-term controls over the component fluxes and how do we model them so that we can predict changes in carbon stored in the ecosystem and atmosphere? How do we make unbiased measurements? Would standardizing measurements and accompanying information yield broader understanding? 5 We convened a workshop in October, 2003 to address these conceptual, measurement, and modeling issues (Hibbard et al. 2004). The purpose of this introductory paper is to provide background and context for measuring and modeling soil respiration and belowground processes, and to synthesize and expand upon some of the ideas discussed at the workshop. Our objectives are to discuss: (1) the conceptual basis for using measurements of soil respiration to understand terrestrial ecosystem carbon cycling; (2) how observations can be used to assess ecosystem carbon fluxes; (3) how biological processes control CO2 production (the timescales and magnitude of the fluxes from different components); (4) how wind and rain can decouple measured fluxes from bio- logical production; (5) potential biases in measurement and sampling tech- niques; (6) experiments to define the controls over soil respiration; (7) modeling soil respiration; and (8) protocols for sampling, measurement, and reporting soil CO2 fluxes (Appendix). Our paper is organized according to these objec- tives. It focuses on what we view as the background and critical issues for advancing understanding of soil respiration in ecosystem science, and is not intended to be an extensive review of the topic. For recent reviews and syn- theses, see Raich and Potter (1995), Jackson et al. (1997), Gill and Jackson (2000), Hanson et al. (2000), Rustad et al. (2001), Davidson et al. (2002a), Pendall et al. (2004), and Hibbard et al. (this issue). Conceptual basis for measurements of soil respiration to understand terrestrial ecosystem carbon cycling Soil respiration is the major pathway for carbon exiting terrestrial ecosystems, and in many models and syntheses it has been treated as strictly a heterotrophic process, responding to temperature or moisture (for example, Kicklighter et al. 1994; Raich and Potter 1995). However, we now know that plant metabolism (Ho¨gberg et al. 2001) or the decomposition of recently produced organic material (Trumbore 2000; Giardina and Ryan 2002; Giardina et al. 2004) generates most of the ‘soil’ respiration and that soil respiration strongly reflects plant metabolism (Ekblad and Ho¨gberg 2001; Bowling et al. 2002). Changes in the recalcitrant soil carbon stocks – the largest C pools in soil and the soil pools most important to changes in ecosystem carbon storage and atmospheric CO2 – contribute only a minor portion of soil CO2 efflux at any point in time (Trumbore 2000; Giardina et al. 2004). These insights suggest that soil respi- ration is a good indicator of ecosystem metabolism but a poor indicator of changes in ecosystem carbon storage. Measurements of soil respiration have great potential as an indicator of ecosystem metabolism and fine-scale process. Integrated measurements can be used to estimate belowground carbon allocation (Giardina and Ryan 2002), and can be coupled with estimates of canopy photosynthesis
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