Ecosystem BVOC fluxes during drought and recovery trace ecohydrological responses of the vegetation and soil microbial interactions - insights from an ecosystem-scale isotope labelling experiment

Severe droughts endangers ecosystem functioning worldwide and can impact ecosystem-atmosphere exchange of water and carbon fluxes as well as biogenic volatile organic compound (BVOC) emissions. However, mechanisms driving alterations in ecosystem-atmosphere exchange of BVOCs during drought and recovery remain poorly understood. To disentangle complex ecosystem dynamics we imposed a 9.5-week drought on the Biosphere 2 tropical rainforest, a thirty-year old enclosed forest. We traced ecosystem scale interactions through a whole-ecosystem labelling approach in the Biosphere 2 Tropical Rainforest, the B2 Water, Atmosphere, and Life Dynamics (B2WALD) experiment. We analysed total ecosystem exchange, soil and leaf fluxes of H₂O, CO₂ and BVOCs, and their stable isotopes over five months. To trace changes in soil-plant-atmosphere interactions we labelled the ecosystem with a ¹³CO₂-isotope.

Drought sequentially propagated through the vertical forest strata, with a rapid increase in vapor pressure deficit, the driving force of tree water loss, in the top canopy layer and early dry-down of the upper soil layer but delayed depletion of deep soil moisture. Gross primary production (GPP), ecosystem respiration (Reco), and evapotranspiration (ET) declined rapidly during early drought and moderately under severe drought. Interactions between plants and soil led to distinct patterns in the relative abundance of atmospheric BVOC concentrations as the drought progressed, serving as a diagnostic indicator of ecosystem drought stress, with isoprene indicating the onset of ET and GPP reduction and hexanal indicating their final decline under severe drought. Net uptake of isoprene and monoterpenes by the soil was influenced by both overlying atmospheric concentrations and soil moisture. During drought, the concentration normalized soil uptake capacity of monoterpenes increased relative to isoprene. This indicated greater persistence of monoterpene scavenging by soils under drought when plant monoterpene emissions were highest.

Ecosystem ¹³CO₂-pulse-labeling showed that drought enhanced the mean residence times of freshly assimilated carbon- indicating down-regulation of carbon cycling velocity and delayed transport form leaves to trunk and roots. Despite reduced ecosystem carbon uptake and total VOC emissions, plants continued to allocate a similar proportion of fresh carbon to de novo VOC synthesis, as incorporation of 13C into both isoprene and monoterpenes remained high. Maintaining carbon allocation into VOC synthesis demonstrates the fundamental role of these compounds in protecting plants from heat stress and photooxidative damage. VOC uptake increased immediately upon rain rewetting.

These data highlight the importance of quantifying drought impacts on forest functioning beyond the intensity of (meteorological) drought, but also taking dynamics response of hydraulic regulation of different vegetation compounds and soil microbial activity of the forest into account.

Werner et al. 2021, Science 374, 1514 (2021), DOI: 10.1126/science.abj6789