Is tree root respiration more sensitive than heterotrophic respiration to changes in soil temperature?


Most of the return CO2 flux from terrestrial ecosystems back to the atmosphere comes from the soil (Raich & Schlesinger, 1992). This flux comprises two major components: autotrophic respiration from roots and their microbial symbionts (especially mycorrhizal fungi); and heterotrophic respiration by microorganisms decomposing litter and soil organic matter (e.g. Hanson et al., 2000). The two components are difficult to partition in situ, and consequently their controls have been difficult to study. However, several studies have suggested that the autotrophic component should be more sensitive to changes in temperature (e.g. Boone et al., 1998), a driver of particular interest in model predictions of potential effects of climate on soil activity (e.g. Zhou et al., 2010). This suggestion was not supported by a laboratory mesocosm study, in which the autotrophic and heterotrophic components could be separated (Bååth & Wallander, 2003). Likewise, when girdling of the trees was used to partition components of soil respiration in a boreal forest (Högberg et al., 2001; Bhupinderpal-Singh et al., 2003), autotrophic respiration did not appear to be more sensitive to changes in soil temperature, but the data heightened the role of seasonality in carbon (C) allocation with greater allocation to roots in late season. Other, subsequent, studies also pointed out the role of substrate supply to roots and mycorrhizal fungi as a key driver of soil autotrophic respiration (Yuste et al., 2004; Heinemeyer et al., 2007).

Recently, Zhou et al. (2010) cited the tree-girdling study (Högberg et al., 2001; Bhupinderpal-Singh et al., 2003) in support of yet another claim that soil autotrophic respiration is more sensitive to temperature than is soil heterotrophic respiration. Let me illustrate why the data from this tree-girdling experiment do not support their claim.

In 2001, the second year of the girdling experiment, a cold air mass occurred in the middle of the summer, which caused the soil temperature in the horizon containing most of the fine tree roots to decrease by 5.5°C during a period of 20 d (Bhupinderpal-Singh et al., 2003). In the tree-girdled plots, in which all soil respiration is heterotrophic respiration, the activity clearly declined, as expected (Fig. 1). A similar decline in soil respiration was seen in the control plots, in which soil respiration also includes the autotrophic component. However, the autotrophic activity, calculated as the difference in soil respiration between control plots and plots with girdled trees, did not decline at all (Fig. 1). The calculated contribution of the autotrophic activity is not independent from the measured heterotrophic activity, but the estimated contribution of the autotrophic activity was highest, c. 65%, at the end of the cold period, suggesting that heterotrophic activity was more sensitive to temperature. This occurred during a time when the allocation of C shifts from aboveground tree components to roots (Hansen et al., 1997), to the effect that the decline in temperature had no apparent effect on the rate of the soil autotrophic respiration. Strong support for this proposition is provided by a recent 13CO2-labelling experiment in boreal pine forest, in which the below-ground C allocation was 500% higher in late summer than in early summer, although soil temperature only increased from 9.1 to 11.5°C (Högberg et al., 2010).

Figure 1.

 Relations between the autotrophic and heterotrophic components of soil respiration and soil temperature (at a soil depth of 5 cm) in a boreal pine forest (data from Bhupinderpal-Singh et al., 2003). Measurements from the beginning (17 May 2001) to the end (12 October 2001) of the season are numbered consecutively (1–8). The red arrows show the responses to a decline in soil temperature in the middle of the summer.

Thus, the large increase in soil autotrophic respiration during the summer in temperate and boreal forests should not be attributed solely to the increase in soil temperature, which results in unreasonably high estimates of Q10 (the Q10 temperature coefficient gives the rate of change of a process as a consequence of increasing the temperature by 10°C). Models must acknowledge that soil autotrophic respiration is also driven by the strong seasonality in tree belowground C allocation.