Quantifying the wood-wide web: Tracing 13C-labeled photosynthate from temperate trees to ectomycorrhizal fungi indicates extensive belowground sharing of carbohydrates

Erik A. Hobbie, Earth Systems Research Center, University of New Hampshire, Durham, NH, Sonja G. Keel, Climate and Agriculture Group, Agroecology and Environment, Agroscope, Zurich, Switzerland, Katharina Steinmann, 3Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Birmensdorf, Switzerland, Markus Wilhelm, Verein für Pilzkunde Basel, Basel, Switzerland, Matthias Saurer, Forest Dynamics, WSL Birmensdorf, Zürich, Switzerland; PSI, Villigen, Switzerland, Christian Körner, Institute of Botany, University of Basel, Basel, Switzerland and Rolf T. W. Siegwolf, Swiss Federal Institute for Forest, Snow and Landscape Research (WSL), Switzerland

δBackground/Question/Methods
Although there is great interest in the ‘wood-wide web’, how carbon moves from plants to ectomycorrhizal fungi and then through shared pathways has primarily been studied in seedlings, rather than mature trees. Here, we used isotopic data generated during the Free-Air CO2 Experiment from 2001-2005 near Basel, Switzerland to study carbon movement through ectomycorrhizal networks. In the study, canopies of a 550-m2 cluster of 14 deciduous trees were labeled with 13C-depleted CO2 for five seasons. We traced the movement of that carbon for four growing seasons into ectomycorrhizal sporocarps collected under CO2-labeled trees (elevated treatment), and at 0-6 m, 6-12 m, and greater than 12 m distance (ambient) from the labeled trees. We could then use patterns of 13C:12C ratios (expressed as δ13C) and C/N in sporocarps across these treatments to infer whether amino acids or carbohydrates were primarily transported within mycorrhizal networks. Fungal carbohydrates (CHO) and protein (pro) will differ in δ13C depending on source region, with δ13Cpro-amb > δ13CCHO-amb > δ13Cpro-elev > δ13CCHO-elev and C/NCHO > C/Npro.
Results/Conclusions
Sporocarps derived 54±4%, 24±5%, and 12±5% of their carbon from labeled trees in the elevated, 0-6 m, and 6-12 m treatments, respectively, with an average transport distance of 13 meters for carbon. However, low plant productivity in the cool and cloudy summer of 2004 reduced carbon transport so that carbon from labeled trees was not detected in the 6-12 m treatment. In this study, sporocarp δ13C correlated positively with C/N within the elevated CO2 treatment and negatively elsewhere, reflecting that high-δ13C carbohydrates from the surrounding ambient zone contributed to sporocarps under elevated CO2. We calculated that 52% to 65% of carbohydrates and 26% to 0% of protein carbon was derived from trees from outside the elevated CO2 zone. These patterns accordingly indicated that 1) carbohydrates rather than amino acids were preferentially transferred between regions differing in source δ13C, 2) this transfer can be quantified using the natural 13C depletion of fossil fuel-derived CO2, and 3) the average transport distance of carbon of 13 meters was decreased with lower plant productivity. This approach provides a powerful tool in 13C labeling studies to examine belowground fungal networks and their spatial extent.