below-ground carbon cycling
Globally, the flux of carbon (C) to below-ground in terrestrial ecosystems exceeds C emitted to the atmosphere through combustion of fossil fuels by an order of magnitude (c. 60 vs. 6 Gt C year−1; Giardina et al. 2005), and exerts a large influence on soils and ecosystems by regulating soil organic C formation and decomposition, and associated soil physical, chemical and biological properties. Despite the magnitude of below-ground C flux, it remains the least understood C flux in terrestrial ecosystems (Clark et al. 2001; Gower et al. 2001; Giardina et al. 2005; Litton, Raich & Ryan 2007). This uncertainty is particularly problematic when modelling the role of forests in global C cycling, as forests account for the majority of terrestrial primary productivity and C storage (Jobbágy & Jackson 2000; Geider et al. 2001).
In forest ecosystems, the annual total of canopy photosynthesis (gross primary production; GPP) is partitioned between component fluxes to above- and below-ground production and respiration. Importantly, the balance between net primary productivity (NPP) and heterotrophic respiration regulates C storage in terrestrial vegetation and soils (Pendall et al. 2004), and this balance may be sensitive to changes in climate (Cox et al. 2000). The sensitivity of C allocation (GPP and component fluxes; the partitioning of GPP to above- or below-ground, to plant respiration or biomass production, and to short-lived or long-lived tissues) to climate change will in part determine whether the sink strength of forests changes in response to a warming climate, because any trade-offs in C allocation will impact detrital C availability and C storage in both short- and long-lived pools. In particular, climate-driven changes in below-ground C flux and partitioning have the potential to feedback positively or negatively on climate by slowing or accelerating the accumulation of greenhouse gases in the atmosphere.
While terrestrial ecosystems exert a large influence on the global C cycle (Cox et al. 2000), fundamental aspects of C allocation remain poorly quantified (Giardina et al. 2005; Litton et al. 2007). Critical questions remaining in terrestrial C cycle science include: (i) how much of GPP do forests partition below-ground and what is the ultimate fate of this C; and (ii) how will climate change impact both the overall partitioning of GPP to below-ground C flux, and the partitioning of below-ground C flux to production vs. respiration?
Prior syntheses have identified positive relationships across diverse forests between mean annual temperature (MAT) and above-ground net primary production (ANPP), and between MAT and total below-ground carbon flux (TBCF) (Giardina et al. 2005; Raich et al. 2006). These findings suggest that total C inputs to soils will increase with warming but TBCF includes C used for both autotrophic respiration and below-ground net primary production (BNPP), and only the latter contributes directly to soil organic C formation. Raich et al. (2006) identified an increase in TBCF with increasing MAT in moist tropical forests. However, soil organic C storage decreased across a similar MAT gradient, suggesting that an increase in the total flux of C to below-ground with climate change may not lead to increased soil C storage.
How the partitioning of TBCF to production vs. respiration varies with temperature is unknown and unlikely to be straightforward. For example, autotrophic respiration may show a strong, short-term response to experimentally manipulated temperature. However, this appears to be a transient response where plant respiration rapidly acclimates to warmer temperatures (see King et al. 2006), including below-ground (Bryla, Bouma & Eissenstat 1997; Dewar, Medlyn & McMurtrie 1999). Further, the fraction of GPP used for plant respiration appears to show little or no response to experimentally manipulated temperatures (Gifford 1994; Tjoelker, Oleksyn & Reich 1999; Atkin, Scheurwater & Pons 2007). Moreover, where seasonal changes in temperature have been used to quantify the relationship between respiration and temperature, phenological changes in GPP may confound patterns (Fitter et al. 1999; Högberg et al. 2001).
Increasingly sophisticated approaches have been employed to examine how the distribution of plant and animal species, the timing of life-history events, and the structure of ecosystems may change in response to modern climate change (Root et al. 2003; Walther et al. 2005). However, enormous logistical hurdles and a lack of adequate methodologies, particularly for quantifying below-ground processes, have constrained efforts to predict the impact of climate change on the physiological and biogeochemical process rates that control terrestrial C storage (Pendall et al. 2004; Giardina et al. 2005; Litton et al. 2007). Multiple studies have demonstrated that below-ground processes are tightly coupled to forest canopy physiology (Ekblad & Högberg 2001; Högberg et al. 2001; Giardina et al. 2004; Högberg & Read 2006), and across large scales to above-ground C fluxes (Litton et al. 2007). However, the fate of C allocated below-ground, especially C that ultimately resides in longer lived pools, has rarely been quantified in response to environmental change (Giardina et al. 2005).
Efforts to quantify the role that forest ecosystems play in global C cycling under a changing climate are largely accomplished with the use of terrestrial ecosystem models (e.g. Cox et al. 2000; Schimel et al. 2000; Thornton et al. 2002; Ise & Moorcroft 2006). Yet confidence in resulting scenarios is constrained by the high uncertainty of underlying climate–process relationships (Giardina & Ryan 2000; Grace & Rayment 2000; Holland et al. 2000) and an incomplete understanding of C allocation in forests (Friedlingstein et al. 1999; Landsberg 2003; Litton et al. 2007). While MAT is predicted to rise by 1·8–4·0 °C over the next 100 years (IPCC 2007), the effects of this rise in temperature on below-ground C flux and partitioning are largely unknown (Giardina et al. 2005).
flux and partitioning of gpp to tbcf and bnpp
Raich & Nadelhoffer (1989) proposed a mass balance approach that relies on conservation of mass to estimate TBCF (originally termed ‘TRCA’ and/or ‘TBCA’), which includes coarse and fine root production, coarse and fine root respiration, root exudates and plant C used by mycorrhizae (Raich & Nadelhoffer 1989; Giardina & Ryan 2002; Litton et al. 2007). Based on conservation of mass, the total flux of C below-ground (i.e. TBCF) will either alter below-ground C storage (e.g. a net change in the storage of soil C or root C), or will be lost from the system (e.g. autotrophic or heterotrophic respiration). This approach to quantifying TBCF has been examined across a wide diversity of ecosystem types, and the required assumptions tested under diverse conditions. See Giardina & Ryan (2002) for a more complete discussion of terminology and methods for quantifying TBCF in forest ecosystems.
The fraction of TBCF that is not used for autotrophic respiration is often termed BNPP, which includes coarse and fine root production, root mortality and losses to herbivory, root exudation, and mycorrhizal growth and turnover. Root exudates and mycorrhizae are likely to be a large portion of BNPP in most ecosystems (Fogel & Hunt 1979; Sylvia 1998; Hobbie 2006). However, most studies of BNPP do not account for these components (Giardina et al. 2005; Litton et al. 2007), and their contribution to BNPP remains poorly quantified (Eissenstat et al. 2000; Stevens, Jones & Mitchell 2002; Wells, Glenn & Eissenstat 2002). In general, BNPP estimates include sequential coring, sequential coring coupled with analysis of root production, and loss and survivorship from mini-rhizotron imagery. For a more complete discussion of terminology and methods pertaining to BNPP see Giardina et al. (2005) and Litton et al. (2007).
Litton et al. (2007) presented a global data set of annual forest C budgets that documents a decrease in partitioning to TBCF (TBCF : GPP) as GPP increases – presumably as below-ground resource supply also increases. While GPP and its components increase globally with increasing MAT (Giardina et al. 2005; Raich et al. 2006; Luyssaert et al. 2007), we are not aware of any study that has examined how the partitioning of GPP (e.g. TBCF : GPP) varies across a broad range of MATs. The fraction of TBCF that is BNPP is also poorly quantified, yet both of these ratios are critical to efforts seeking to correctly model ecosystem C cycling. In the past, efforts to estimate stand level carbon use efficiency (CUE) and BNPP have often assumed that c. 50% of TBCF is BNPP (e.g. Law, Ryan & Anthoni 1999; Giardina et al. 2003; Vitousek 2004; Newman, Arthur & Muller 2006). Moreover, while some terrestrial ecosystem models have dynamic, albeit simplified, C allocation schemes that vary partitioning to below-ground based on water and/or nutrient availability (e.g. 3-PG; Landsberg & Waring 1997), many models assume a constant CUE of c. 50% (Delucia et al. 2007; Litton et al. 2007).
Available data to justify these assumptions are conspicuously lacking (Clark et al. 2001; Giardina et al. 2005). Nadelhoffer & Raich (1992) looked at a variety of ecosystems where fine root production had been estimated using the N budget technique, and estimated that c. 33% of TBCF goes to fine root production. McDowell et al. (2001) estimated that BNPP accounted for 53–63% of TBCF in Pseudotsuga menziesii forests but fine root and mycorrhizal production, which accounted for most of BNPP, were not directly quantified. Based on central tendency of relationships between TBCF and ANPP, and between BNPP and ANPP, Giardina et al. (2005) identified that BNPP was c. 50% of TBCF. Because TBCF can account for 21–75% of GPP (Litton et al. 2007), uncertainty surrounding the fraction of TBCF that is BNPP severely constrains efforts to accurately model terrestrial C cycling and ecosystem C balance.
Ecosystems are dynamic, with C allocation patterns and below-ground process rates dependent upon a multitude of factors such as species composition, stand age, climate and nutrient supply (Pendall et al. 2004; Giardina et al. 2005; Litton et al. 2007). To date, a paucity of available data has prevented detailed analyses of how climate change will impact stand level C budgets. Here, we examine global-scale patterns of GPP, TBCF, BNPP, partitioning of GPP to TBCF (TBCF : GPP) and partitioning of TBCF to BNPP (BNPP : TBCF) across a global MAT gradient to examine how they vary with temperature.
We hypothesized that partitioning of GPP to below-ground (TBCF : GPP) will increase with increasing MAT because both TBCF and ANPP have been shown to increase with temperature but the slope is steeper for TBCF (Giardina et al. 2005; Raich et al. 2006). Based on C allocation theory and a recent global analysis (see Litton et al. 2007), the most likely mechanism explaining an increase in partitioning to TBCF with increasing MAT is that as MAT increases, below-ground limitations to GPP (e.g. nutrients, water) become more important than above-ground limitations (e.g. light, temperature) (Fig. 1). This proposed mechanism is compatible with MAT driven increases in both above- and below-ground resource supply. How increasing MAT affects the balance between above- and below-ground resource limitations to GPP has not been examined in forest ecosystems, and is outside the scope of this analysis. Nonetheless, a better understanding of how climate variables impact C allocation patterns in forests is clearly warranted. We also hypothesized that partitioning of TBCF to production (BNPP : TBCF) will approximate 0·50 across a wide range of MAT, as originally proposed by Giardina et al. (2005).
Because below-ground processes are likely to respond simultaneously to a suite of factors, including MAT and water availability, we also explored how below-ground C flux and partitioning respond to mean annual precipitation (MAP), and whether MAT, MAP or their interaction is the most important variable for explaining observed global patterns. Changes in temperature and/or precipitation, in turn, are likely to have both direct and indirect impacts on nutrient supply, an important determinant of GPP and its partitioning (Litton et al. 2007). However, the impact of nutrient supply on below-ground C processes was outside of the scope of this analysis. Global observational analyses like that used here are unable to control for all factors that influence the variable of interest – in this case the effect of MAT on below-ground C processes. However, we contend that these analyses provide compelling insights into global-scale processes and their drivers and, as such, help to identify important areas of future research.