Soil organisms are almost exclusively fuelled by energy derived from plant photosynthesis. Litter from above- and below-ground plant parts feed heterotrophic organisms, chiefly bacteria and fungi, with typical time lags of months to centuries between photosynthesis and the decomposition of the organic matter. An equally large flux of C is, however, allocated below ground by the plants within h to months to sustain an autotrophic soil component consisting of plant roots, their symbiotic mycorrhizal fungi, and a rich flora of other microorganisms dependent on labile C compounds exuded by the roots (Hanson et al., 2000; van Hees et al., 2005; Högberg & Read, 2006). The heterotrophic pathway, particularly the early stages of decomposition of above-ground litter, is the most thoroughly studied, because inputs of above-ground litter can be easily manipulated and their degradation can be readily observed (Berg & McClaugherty, 2003). Processes further down in the soil are more difficult to follow (Wardle et al., 2004). This is especially true for the activity of mycorrhizal roots, which is disrupted if the C supply from the plant canopy is severed by sampling of the soil (Söderström & Read, 1987; Högberg et al., 2001).
Despite the mounting interest in the C cycle, the fate of the plant C distributed through roots to soil organisms has mainly been followed in detail in micro- or mesocosms, or in short-stature ecosystems such as grasslands (Ostle et al., 2000, 2007; Leake et al., 2006; Bahn et al., 2009). An important advance has been the application of C isotopes (Staddon, 2004). For example, small trees have been labelled with the radioactive 14C to study C allocation patterns (Horwath et al., 1994; Carbone et al., 2007) and patches of forest or model systems with trees have been labelled with very low tracer amounts of the stable 13C in studies of the effects of elevated CO2 concentrations (Lin et al., 1999; Matamala et al., 2003; Körner et al., 2005). Pulse-labelling with 14C enables a much higher temporal resolution than so-called FACE (free-air carbon dioxide enrichment) experiments, in which the degree of isotopic enrichment is relatively small and the ecosystems become slowly labelled with 13C. Indeed, Horwath et al. (1994) were able to demonstrate a 250% higher below-ground 14C allocation to roots and the return soil CO2 efflux in the late as compared with the early season, which is in agreement with other results from studies of the physiology of trees in temperate and boreal climates (Hansen et al., 1997; Waring & Running, 1998; Kagawa et al., 2006). Recently, a few studies have demonstrated the possibility of high-tracer level pulse-labelling with 13C of trees directly in forest field settings (Högberg et al., 2008; Plain et al., 2009). In these studies, single trees (Plain et al., 2009) or a patch of a forest (Högberg et al., 2008) were labelled over a period of a few hours. The latter study demonstrated significant labelling of the cytoplasm of soil microorganisms, but labelling was not high enough to study incorporation of tracer C in phospholipid fatty acids (PLFAs), biomarkers for different groups of microorganisms.
No previous study has been designed to follow in situ the rapid translocation of C to different groups of soil organisms via the autotrophic pathway in a forest ecosystem. We therefore lack a detailed picture of how a large amount of photosynthetically fixed C, an amount several times larger than all anthropogenic C emissions (Schimel, 1995), is distributed among groups of soil organisms and how this varies seasonally and in response to the ongoing N eutrophication (Vitousek et al., 1997; Aber et al., 1998) of forests. This paucity of knowledge limits our understanding of the future roles of these organisms in overall ecosystem functioning. With regard to climate change, much attention has recently been paid to potential direct effects on soil biota of higher temperatures and changes in soil moisture, but less attention has been shown to possible indirect effects on soil biota of climate-related changes in plant below-ground C allocation (Högberg & Read, 2006). For example, the production season of sporocarps of ectomycorrhizal (ECM) (Gange et al., 2007) fungi in Britain became longer during the period 1950–2005, which was primarily attributed to direct effects of changes in temperature and moisture. However, changes in the seasonality of C supply from the tree hosts to the fungi could also be involved. Moreover, N eutrophication is expected to lead to a reduction in tree below-ground C allocation (Waring & Running, 1998; Mäkeläet al., 2008). Indeed, several studies have reported decreases in ECM fungal sporocarp production and mycelium in response to N additions (Wallenda & Kottke, 1998; Nilsson & Wallander, 2003), and in a tree-girdling experiment the autotrophic soil respiratory component appeared twice as high in nonfertilized as compared with N-fertilized spruce forest (Olsson et al., 2005), but the implied reductions in tree below-ground C allocation have not been quantified directly in the field. Hence, we do not know how important this effect may be.
Here, we report results of a large-scale 13C tracer pulse-chase experiment in a boreal 14-yr-old Pinus sylvestris forest ecosystem, which allowed a highly resolved analysis of the C flux from trees to different groups of soil organisms. We addressed two major questions: first, how large is the difference in below-ground C allocation between the early and late seasons; and second, how much does added N affect the below-ground allocation of C?