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A Global Relationship Between the Heterotrophic and Autotrophic Components of Soil Respiration?

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A Global Relationship Between the Heterotrophic and Autotrophic Components of Soil Respiration? 中国科技论文在线 http://www.paper.edu.cn Global Change Biology (2004) 10, 1756–1766, doi: 10.1111/j.1365-2486.2004.00816.x A global relationship between the heterotrophic and autotrophic components of soil respiration? BEN BOND-LAMBERTY*, CHUANKUAN WANG*w and S T I T H T . G O W E R * *Department of Forest Ecology and Management, University of Wisconsin-Madison, 1630 Linden Drive, Madison, WI 53706, USA wEcology Program, Northeast Forestry University, Harbin 150040, China Abstract Soil surface CO2 flux (RS) is overwhelmingly the product of respiration by roots (autotrophic respiration, RA) and soil organisms (heterotrophic respiration, RH). Many studies have attempted to partition RS into these two components, with highly variable results. This study analyzes published data encompassing 54 forest sites and shows that 2 RA and RH are each strongly (R 40.8) correlated to annual RS across a wide range of forest ecosystems. Monte Carlo simulation showed that these correlations were significantly stronger than any correlation introduced as an artefact of measurement method. Biome type, measurement method, mean annual temperature, soil drainage, and leaf habit were not significant. For sites with available data, there was a significant 2 (R 5 0.56) correlation between total detritus input and RH, while RA was unrelated to net primary production. We discuss why RA and RH might be related to each other on large scales, as both ultimately depend on forest carbon balance and photosynthate supply. Limited data suggest that these or similar relationships have broad applicability in other ecosystem types. Site-specific measurements are always more desirable than the application of inferred broad relationships, but belowground measurements are difficult and expensive, while measuring RS is straightforward and commonly done. Thus the relationships presented here provide a useful method that can help constrain estimates of terrestrial carbon budgets. Keywords: autotrophic respiration, carbon cycling, heterotrophic respiration, Monte Carlo simulation, root respiration, soil CO2 flux Received 14 October 2003; revised version received 3 February 2004 and accepted 12 March 2004 into its heterotrophic and autotrophic source fluxes Introduction (Singh & Gupta, 1977; Hanson et al., 2000). Such a The processes controlling the sources and dynamics of partitioning constitutes a gross simplification of the soil surface CO2 flux (RS) remain poorly understood. sources of RS – and as such is probably unable to This flux is the second largest in the global carbon cycle, capture processes controlling turnover of the large contributing 20–40% of atmospheric CO2 annual input pools with slow turnover that ultimately control carbon (Raich & Schlesinger, 1992) with marked temporal storage and net ecosystem production – but is none- variation (Savage & Davidson, 2001, Raich et al., theless a highly useful one. 2002). At smaller scales, RS comprises a large percen- The partitioning of RS is an important issue in forest tage of ecosystem respiration (Lavigne et al., 1997; Law ecosystem ecology, carbon cycling, plant physiology, et al., 1999, Janssens et al., 2001), the variability of which soil science, and global climate change modelling. Root can determine forest carbon balance (Goulden et al., and microbial respiration may respond differently to 1998; Valentini et al., 2000). RS is overwhelmingly the temperature (Boone et al., 1998; Pregitzer et al., 2000; product of respiration by roots (autotrophic respiration, Epron et al., 2001), implying different flux behaviours at RA) and soil decomposers (heterotrophic respiration, a variety of time scales and in different plant species RH), and there have been many efforts to partition it (Kuzyakov & Domanski, 2000). This is important because the balance between soil organic matter decay Correspondence: Ben Bond-Lamberty, tel. 1 1 608 262 6369, and CO2 fertilization effects may drive future changes fax 1 1 608 262 9922, e-mail: [email protected] in the global carbon cycle (Jenkinson, 1991; Melillo et al., 1756 r 2004 Blackwell Publishing Ltd 转载 中国科技论文在线 http://www.paper.edu.cn SOIL AUTOTROPHIC AND HETEROTROPHIC CO2 FLUX 1757 2002), as the global soil organic matter pool contains limitations of estimating RA and RH from measure- twice the C of the atmosphere (Post et al., 1982). Plant ments of annual RS. This paper focuses primarily on fine roots play important roles in terrestrial carbon and forest RS because forests comprise 50% of the global nutrient cycling (Hendricks et al., 1993), and accurate land surface, with an even greater share of terrestrial measurements of RS and RA can help constrain NPP (Melillo et al., 1993), and more data on RS and RC estimates of carbon allocation to these roots (Nadelhof- have been published for forests than for any other fer & Raich, 1992). In addition, while measurements of ecosystem type (Hanson et al., 2000). net primary production (NPP) subsume RA losses, knowledge of heterotrophic fluxes is required to Methods calculate net ecosystem production and permit com- parison of process- and biomass-based estimates with We collected studies in the scientific literature that net ecosystem exchange derived from eddy covariance estimated autotrophic and heterotrophic sources of RS. techniques. Thus the contribution of each RS compo- We used only studies that (i) partitioned RS into its nent must be known to understand the effects of global heterotrophic and autotrophic component fluxes, or change on net exchange of CO2 between terrestrial otherwise calculated RC, and (ii) reported annual (not ecosystems and the atmosphere. simply growing season) RS flux for one or more field Belowground measurements are difficult to perform, study sites. If a study did not report annual RS but was and values of 10–90% for the root contribution (RC, performed at an intensively studied site for which these defined here as RA/RS)toRS have been reported for data were available (e.g., the BOREAS NSA tower site both forest and nonforest ecosystems (Hanson et al., in Manitoba, Canada), the study was included. Data 2000). Much of this variability may be caused by from a study of RS and RC for a boreal black spruce problems associated with different methods used to (Picea mariana (Mill.) BSP) chronosequence (Bond- estimate RC, rather than any underlying variability Lamberty, 2004 (in press)) were included; annual RS between ecosystems, species, or developmental stages has been published for these sites (Wang et al., 2002). (Ho¨gberg et al., 2001), as the complexity, cost, and We focused on undisturbed forests or tree plantations disturbance associated with experimental treatments and thus excluded several studies (Edwards & Ross- complicate field and laboratory measurements (Kuzya- Todd, 1983; Gordon, 1987; Toland & Zak, 1994) kov & Domanski, 2000). Another difficulty is that comparing recent clearcuts to intact forests, all of which microbial respiration is influenced by root exudates reported essentially no root contribution to RS (i.e., (Kuzyakov, 2002). Here we follow many previous RC 5 0% for intact forest). This is improbable, and we studies in using the terms ‘root respiration’ and believe that the high disturbance associated with such ‘autotrophic respiration’ interchangeably, as there is clearcuts justified excluding these studies. In addition, no standard practice to include rhizospheric respiration the RA values reported by Ryan et al. (1997) for the in microbial soil respiration or in autotrophic root BOREAS NSA research site exceeded reported RS at this respiration (Hanson et al., 2000); a clean separation of site, and were significantly different from a number of the two sources may not be possible, or even realistic. other studies using similar techniques at the same site We acknowledge that there are heterotrophic contribu- (Steele et al., 1997; Dioumaeva et al., 2002). These data tions to ‘root’ or ‘autotrophic’ respiration, e.g., the respi- were thus excluded; we did not exclude data from other ration in the rhizosphere of symbiotic mycorrhizal fungi sites reported by Ryan et al. (1997) using the same and other microorganisms (Kelting et al., 1998), but in a techniques (but doing so would not have significantly meta-analysis such as this study, there was no practical changed our results). Finally, one study (Thierron & way to correct for this. Thus, we simply used RA or RH Laudelout, 1996) with extremely high reported values values reported by authors, making no attempt to for RS and RC was excluded after model fitting, as an correct for varying definitions of ‘root respiration.’ outlier test (Chatterjee & Price, 1991) using it and the This paper examines published estimates of RS and reduced data set was highly significant (Y* 5 817, RC, the annual root contribution to RS, and discusses YPRED 5 191, SE(YPRED) 5 105, T53 5 5.96, Bonferroni- relationships between RS and its two major source adjusted Po0.001). We did not exclude studies based fluxes, RA and RH. This is equivalent to testing the on measurement method (e.g., low readings possibly hypothesis that there is a global correlation between the associated with alkali absorbents) (Raich & Nadelhof- RA and RH components of RS. We discuss the biological fer, 1989). and statistical underpinnings of such a relationship, Thirty-one boreal, cold temperate, warm temperate, show why these variables are significantly more and tropical forest studies were used for the final correlated than can be explained simply as an artefact analyses, with data from 54 total sites, 47 of them being of measurement method, and outline the uses and unique (Table 1). Techniques used to separate RA from r 2004 Blackwell Publishing Ltd, Global Change Biology, 10, 1756–1766 中国科技论文在线 http://www.paper.edu.cn 1758 B. BOND-LAMBERTY et al. Table 1 Studies used in the analysis presented here, with values reported for total soil surface CO2 flux (RS), its autotrophic (RA) À2 À1 and heterotrophic (RH) subcomponents (all in g Cm yr , and/or root contribution to RS (RC, equal to RA/RS) Study Method Location Habit Soil Age RS RA RH RC (%) Boreal Bond-Lamberty et al.
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