Rhizosphere activity in an old-growth forest reacts rapidly to changes in soil moisture and shapes whole-tree carbon allocation

Abstract

Drought alters carbon (C) allocation within trees, thereby impairing tree growth. Recovery of root and leaf functioning and prioritized C supply to sink tissues after drought may compensate for drought-induced reduction of assimilation and growth. It remains unclear if C allocation to sink tissues during and following drought is controlled by altered sink metabolic activities or by the availability of new assimilates. Understanding such mechanisms is required to predict forests’ resilience to a changing climate. We investigated the impact of drought and drought release on C allocation in a 100-y-old Scots pine forest. We applied 13CO2 pulse labeling to naturally dry control and long-term irrigated trees and tracked the fate of the label in above- and belowground C pools and fluxes. Allocation of new assimilates belowground was ca. 53% lower under nonirrigated conditions. A short rainfall event, which led to a temporary increase in the soil water content (SWC) in the topsoil, strongly increased the amounts of C transported belowground in the nonirrigated plots to values comparable to those in the irrigated plots. This switch in allocation patterns was congruent with a tipping point at around 15% SWC in the response of the respiratory activity of soil microbes. These results indicate that the metabolic sink activity in the rhizosphere and its modulation by soil moisture can drive C allocation within adult trees and ecosystems. Even a subtle increase in soil moisture can lead to a rapid recovery of belowground functions that in turn affects the direction of C transport in trees.

Drought alters the carbon footprint of trees in soils—tracking the spatio‐temporal fate of 13C‐labelled assimilates in the soil of an old‐growth pine forest

“…This reduction in demand in turn feeds back on photosynthesis (Gessler & Grossiord, 2019; Hagedorn et al, 2016). In our experiment conducted under a natural moderate drought, the whole crown assimilation of the 13 C tracer as well as leaf‐level photosynthesis remained unaffected by irrigation (Joseph et al, 2020), which indicates that a limited sink activity in the rhizosphere was primarily responsible for the reduced rhizosphere respiration in dry soils. This conclusion is corroborated by the relatively greater incorporation of recent assimilates into microbial biomass (as compared to respiratory activity in the rhizosphere) in dry compared to irrigated soils (46 vs. 31%), signifying that the metabolization of assimilates is most strongly constrained by water.Our results show that intermittent precipitation events can strongly alter the dynamics and allocation patterns of recent assimilates from tree canopies into the soil.…”

“…Overall 10 approximately 100‐year‐old pine trees were pulse‐labelled, five of them growing under naturally dry conditions and five under irrigation. Adapted from Joseph et al (2020)…”

“…The fraction of 13 C taken up by trees being respired from the soil was calculated by dividing 13 C excess of soil‐respired CO 2 by this value. The total recovery of 13 C in various compartments of tree biomass, CO 2 fluxes from tree canopy, stems and soil was 75% of the amount of 13 C assimilated (Joseph et al, 2020).…”

“…Especially limited knowledge exists in mature forests where these processes are difficult to quantify, and timescales of C metabolization within trees and the C transfer among tree compartments can range between days and decades (Herrera‐Ramírez et al, 2020). Up to 50% of recent tree photosynthates are assumed to be transferred within a few days from trees into the belowground compartment (Epron et al, 2011; Högberg et al, 2008; Joseph et al, 2020), where they fuel root processes and soil microbial communities living in close association with the roots (Epron et al, 2012; Hagedorn et al, 2016). In mature trees, phloem transport leads to distinct time lags in plant–soil coupling (Dannoura et al, 2011; Kuzyakov & Gavrichkova, 2010) and a substantial fraction of assimilates is intermediately stored in the wood parenchyma before it is used for respiratory processes (Muhr et al, 2013).…”

Photosynthetic acclimation and sensitivity to short- and long-term environmental changes

“…times when water is available in higher amounts. Such rapid responses to precipitation were demonstrated by Joseph et al (2020), who found a strong increase in carbon allocation to belowground tissues in the control plots of the same forest system after a precipitation event.…”