Tree mortality after a spring fire: the role of reduced live leaf area in depletion of early growing season bole NSC

This scientific commentary refers to “Nonstructural carbohydrates explain post-fire tree mortality and recovery patterns” by Reed and Hood (doi: 10.1093/treephys/tpad155).

Prescribed fire is used as a tool to achieve various ecological objectives in fire-adapted ecosystems (Ryan et al. 2013). These objectives often include targeted mortality of encroaching species to minimize the risk of catastrophic wildfire (Ryan et al. 2013). Achieving mortality of some species while protecting others requires a foundational understanding of how different species respond to different types of fire at different times of year.

Fire practitioners rely on operational models of postfire tree mortality to make decisions about forest treatment prescriptions. These models all rely on an empirical relationship between mortality and flame-length or scorch height derived from field data in the 1980s (Ryan and Reinhardt 1988; Reinhardt et al. 1997; Reinhardt and Crookston 2003; Hood et al. 2007; Andrews 2013). These empirical models may not hold up as mortality thresholds shift under compound disturbance (Kane et al. 2017) or as we move into no-analog future conditions with climate change (Lalor et al. 2023). Such cases where nonlinear responses are common require that fire-effects models transition from empirical to mechanistic approaches that capture fundamental physiological processes to project postfire mortality (O’Brien et al. 2018). Understanding fire-induced mortality mechanisms, and their relationships to phenology as it shifts with climate change, will be critical to managing ecosystems in an uncertain future.

As with mortality from drought (Hammond et al. 2019) and herbivory (Barker Plotkin et al. 2021), research suggests that delayed postfire mortality may result from sufficiently high loss of hydraulic conductivity (Michaletz et al. 2012; West et al. 2016; Bär et al. 2018; Partelli-Feltrin et al. 2021) or low nonstructural carbohydrate (NSC) content (Varner et al. 2009; Partelli-Feltrin et al. 2023), resulting from heat damage to the water and carbon uptake and transport systems (Hood et al. 2018; Bär et al. 2019). Nonstructural carbohydrates are those carbohydrates, not bound in structural biomass, that play critical roles in growth, metabolism, osmoregulation, transport, storage and defense (Dietze et al. 2014). Reed and Hood (2023) provide the first evidence of NSC declines as a mechanistic link between fire-induced crown scorch (discoloration of foliage and buds after fire) and subsequent postfire mortality under low-severity prescribed fire.

This work is a critical step toward informing mechanistic simulation of postfire tree mortality under a changing climate. The authors assessed crown-injury (a common metric of fire severity and tree survival; Varner et al. 2021) and collected and analyzed NSC in needles, branch phloem and main stem (bole) phloem of ponderosa pine at seven timepoints, from prefire to 16 months postfire. They found that postfire NSC was reduced in all burned trees relative to unburned controls and did not recover to control levels in trees that eventually died. The authors also found a negative relationship between crown-scorch and bole phloem NSCs, which did not recover in trees that died, supporting the hypothesis that NSC decline provides the mechanistic link between crown-scorch and mortality.

Of particular note is the large and significant reduction in bole phloem starch at the third sampling timepoint postfire (T3) in burned trees that died relative to those that survived, and the subsequent reduction in bole phloem soluble sugars at the fourth postfire sampling timepoint (T4; Fig. 1a). These time points correspond to the beginning and end of the observed new needle growth period, respectively, and suggest that bole phloem starch accumulation and subsequent soluble sugar availability is critical to postburn recovery and survival. The authors demonstrate that both bole phloem starch at T3 and soluble sugars at T4 are negatively related to crown scorch (Fig. 1b), where trees that died experienced >75% crown scorch and concomitant reductions in mean bole phloem starch and soluble sugars of ~85% relative to trees that survived. It is worth noting here that tree stature likely played a role in crown scorch extent, as surviving burned trees had greater overall height, diameter and bark thickness, and lower observed crown scorch relative to smaller trees that died. The differences in crown scorch between trees that died and survived at the second postfire sampling timepoint (T2), the time point at which daily minimum air temperatures increase above 0 °C, are visually apparent (Fig. 1c) and highlight the extensive damage to previous years’ needles in trees that died, which likely inhibited assimilation by previous years’ needles and/or allocation to bole phloem NSC in the time period between spring thaw and new needle growth (Fig. 1a).

Figure 1.

Growing season reductions in bole phloem NSCs associated with extensive crown scorch portend post-fire mortality. (a) Burned trees that die show reductions in bole phloem starch during the pre-budburst assimilation period (T2–3) and soluble sugars during the new needle growth period (T3–4) relative to surviving burned and unburned control trees. Vertical dashed line indicates date of fire. T2, T3 and T4 indicate the second, third and fourth postfire sampling points associated with daily minimum air temperature rising above 0 °C, and the start and end of new needle growth, respectively. Boxes highlight the largest measured differences between trees that died and survived in mean bole phloem starch (T3) and soluble sugars (T4) used in panel (b) regressions against T2 crown scorch. (b) Bole phloem NSC declined with increasing crown scorch, and all trees that died had >75% crown scorch at T2 and starch and soluble sugars below 30 and 55 mg g⁻¹ at T3 and T4, respectively. (c) Photos of crown scorch at T2 from a burned tree that died (left) and one that survived (right) illustrating extent of foliage damage and likely impacts to pre-budburst assimilation and/or allocation to bole phloem NSC. Figure components are adapted from Reed & Hood (2023).

The observed dynamics of bole phloem starch and soluble sugars (Fig. 1a) are consistent with previous studies demonstrating that, in pine species, stem starch peaks at the beginning of the growing season, and concentrations of sugars are higher during winter than summer (Michelot et al. 2012; Gruber et al. 2013; Dietze et al. 2014; Schoonmaker et al. 2021). However, the role of that starch and subsequently accumulated soluble sugars requires further research. A meta-analysis showing consistently significant seasonal variation of stem starch and soluble sugars (Martínez-Vilalta et al. 2016) suggests the importance of carbon mobilized from stem pools in seasonal carbohydrate dynamics, but its role remains to be defined. The seasonal dynamics observed here in unburned and surviving trees may indicate temporary storage of recent assimilate as bole phloem starch before bud-burst, which is then mobilized and depleted to support either local growth and respiration, or transport to other sinks, such as shoot growth and needle expansion (Peltier et al. 2023). This is consistent with the authors’ observation that, though all burned trees had surviving buds and flushed new needles, those new needles had lower NSC concentrations in trees that died than those that survived, and many new needles died by the end of the first growing season postfire, perhaps due to insufficient metabolite availability.

Other studies that have measured seasonal fluctuations in both pine bole phloem and xylem NSC show early spring declines in xylem NSC corresponding with an increase in phloem NSC at the time of shoot expansion (Schoonmaker et al. 2021). If, consistent with Schoonmaker et al. (2021), the source of the seasonal increase in bole phloem starch of unburned and surviving trees was in fact the xylem rather than new assimilates, this could suggest that bole phloem NSC declines in dying trees were due to inhibited xylem NSC translocation (De Schepper et al. 2013; Pfautsch et al. 2015) resulting some form of crown-scorch-associated hydraulic limitation (e.g. transpiration inhibition, foliage cavitation, vascular dysfunction; Lodge et al. 2018; Hillabrand et al. 2019; Varner et al. 2021). Though previous work evaluating sapflux response to fire found no relationship with crown scorch (O’Brien et al. 2010), scorch levels were much lower with only one tree experiencing scorch comparable to burned trees that died in this study. Similarly, though studies evaluating transpiration response to insect-, drought- or fire-induced defoliation often see upregulation in surviving foliage (Niccoli et al. 2023), at higher levels of defoliation comparable to those observed here, canopy level transpiration declines (Pataki et al. 1998; Schäfer et al. 2014; McIntire et al. 2021). Indeed, extensive defoliation may impact translocation of NSC through loss of a sufficient water potential gradient (Paljakka et al. 2017). Elevated leaf water potentials in a recent study that attributed fire-induced mortality of Pinus ponderosa saplings to phloem death and associated NSC declines (Partelli-Feltrin et al. 2023) suggest such a loss of pressure gradients. In the current study, while there were no visible signs of heat-killed cambium prior to mortality or when the dead trees were cut, evidence that evergreen trees can store enough stem NSC to re-foliate two-thirds of the crown (Hoch et al. 2003) points to a likely role for hydraulic inhibition of NSC translocation. Additionally, the smaller stature of burned trees that died likely corresponds, not only to lower live leaf area, but also to smaller, shallower root systems with reduced access to water stores, further inhibiting recovery. The absence of hydraulic data in this study prevents further speculation, but highlights the need for further research that integrates the interactions between carbon and hydraulic limitations from fire.

Whatever the source or function, the absence of a bole phloem starch pool and subsequent soluble sugars, derived either from bole phloem starch hydrolysis or assimilation from newly flushed needles, appears critical to postburn survival. These results highlight the importance of considering phenology in prescribed fire timing, as well as the mechanisms underlying delayed postfire mortality as phenology shifts with climate change. For instance, assuming bole starch accumulated from recent assimilate is used to support subsequent growth of new needles, if the timing of bud-burst shifts earlier in the growing season, there may be less time for sufficient starch stores to accumulate, and greater postfire mortality may result. Reed and Hood (2023) provide a critical step toward developing a mechanistic model that accounts for phenology by linking fire-induced injury to seasonally dependent impacts on water and carbon uptake/transport systems to subsequent recovery or mortality (Dickman et al. 2023). Such a process-based approach will be necessary to capture the physiology underlying live fuel conditions and postfire survival under drought and warming, enabling climate-smart decision-making.

Funding

L.T.D. was supported by the Laboratory Directed Research and Development program of Los Alamos National Laboratory, Los Alamos, NM, USA under project numbers 20230509ECR and 20220024DR.

Conflict of interest

None declared.

Data availability

No new data were generated or analyzed in support of this research.