Processes and mechanisms of coastal woody-plant mortality

Abstract

Observations of woody plant mortality in coastal ecosystems are globally widespread, but the overarching processes and underlying mechanisms are poorly understood. This knowledge deficiency, combined with rapidly changing water levels, storm surges, atmospheric CO₂ , and vapor pressure deficit, creates large predictive uncertainty regarding how coastal ecosystems will respond to global change. Here, we synthesize the literature on the mechanisms that underlie coastal woody-plant mortality, with the goal of producing a testable hypothesis framework. The key emergent mechanisms underlying mortality include hypoxic, osmotic, and ionic-driven reductions in whole-plant hydraulic conductance and photosynthesis that ultimately drive the coupled processes of hydraulic failure and carbon starvation. The relative importance of these processes in driving mortality, their order of progression, and their degree of coupling depends on the characteristics of the anomalous water exposure, on topographic effects, and on taxa-specific variation in traits and trait acclimation. Greater inundation exposure could accelerate mortality globally; however, the interaction of changing inundation exposure with elevated CO₂ , drought, and rising vapor pressure deficit could influence mortality likelihood. Models of coastal forests that incorporate the frequency and duration of inundation, the role of climatic drivers, and the processes of hydraulic failure and carbon starvation can yield improved estimates of inundation-induced woody-plant mortality.

Keywords: carbon starvation; climate change; coastal; hydraulic failure; hypoxia; mortality; salinity; sea level rise.

FIGURE 1

Woody‐plant mortality in coastal ecosystems leads to large‐scale ghost forest formation globally. (a) Mangrove (Avicennia marina and Rhizophora stylosa) mortality in Australia (N. Duke). (b) Loblolly pine (Pinus taeda) mortality, Maryland, USA (M. Kirwan). (c) Sitka spruce (Picea sitchensis) mortality, Washington, USA (Nicholas Ward). (d) Mangrove (Avicennia germinans) mortality in Florida, USA (Ken Krauss).

FIGURE 2

The global distribution of reported coastal mortality events resulting in ghost forests. Regions of mangrove forests are highlighted in green. Map updated with new observations, primarily from non‐mangrove systems, from Sippo et al. (2018).

FIGURE 3

The interacting factors, drivers, mechanisms, and processes that cause coastal forest mortality under increasing seawater exposure. In this schematic, predisposing factors and drivers that occur before inundation (outer spiral) set the stage for subsequent mortality during and after inundation event(s). Pre‐disposing factors include site characteristics such as freshwater access, with drivers such as rising VPD, and mechanisms such as salt toxicity, all contributing to the processes of hydraulic failure and carbon starvation. The order of presentation of factors represents a hypothesis regarding the chronology of mechanisms and impacts. The osmotic phase (Munns & Termaat, 1986) and associated increasing risk of hydraulic failure begins as soon as saline and hypoxic conditions start upon inundation, with the ionic phase requiring more time to manifest as salts accumulate in the crown. Carbon starvation starts initially upon stomatal closure due to the associated reduction in photosynthesis. We note that increasing embolism and stomatal closure typically coincide (Rodriguez‐Dominguez & Brodribb, 2020) but are shown separately for clarity.

FIGURE 4

A mechanistic framework for coastal forest mortality from hypoxia and salinity. Abnormally prolonged or repeated exposure to hypoxia or high salinity results in significant reductions in belowground hydraulic conductance due to root death and osmotically induced reductions in the water potential gradient from soil to root. Reduced belowground conductance results in declining water supply to the foliated crown, increasing embolism and subsequently hydraulic failure. Reductions in water flow to the crown simultaneously induce carbon starvation through multiple mechanisms. Decreased foliar water potential reduces stomatal conductance while increasing foliar salt concentrations cause reduced photosynthetic capacity, turgor, and direct ion toxicity to cellular structure, all leading to decreased photosynthesis and hence increased risk of carbon starvation. Carbon starvation feeds back on itself through mortality of foliage via a negative carbon balance, leading to crown dieback and hence reduced whole‐plant photosynthetic capacity. Ultimately, the combination of these factors increases the likelihood of both hydraulic failure and carbon starvation.

FIGURE 5

Declining tree carbon uptake promotes carbon starvation. Sitka spruce (Picea Sitchensis) trees exposed to seawater inundation exhibit strong declines in (a) photosynthetic capacity (the slope of photosynthesis versus internal CO₂ concentration), (b) the fraction of their crowns that are foliated, and (c) starch concentrations in the foliage, branches, stems and roots. Combined, the decline in both photosynthetic capacity and in crown leaf area result in a significant decline in starch concentrations, which is the primary storage pool of carbon. As trees approach death the starch concentrations reach zero, which is rarely seen except for in studies that force carbon starvation (Quirk et al., ; Sevanto et al., ; Weber et al., 2018). Data used to create these figures are from Li et al. (2021) and Zhang, McDowell, et al. (2021).

FIGURE 6

Hypothesized responses of mortality to rising hypoxia and salinity and the influence of rising CO₂, VPD, and droughts. (a) As the cumulative duration of exposure to elevated hypoxia and salinity increases, hydraulic failure should be the first process to manifest because of the immediate declines in belowground hydraulic conductance that subsequently promote increased embolism, crown dieback, and eventual mortality. Carbon starvation will increase in likelihood at a slower rate because of the buffering capacity of stored carbohydrates but can become a dominant driver of mortality due to the large declines in whole‐plant photosynthetic potential. (b) Glycophytes are more sensitive to hypoxia and salinity than halophytes, however, their responses to elevated CO₂ and VPD are similar. Elevated CO₂ can mitigate mortality likelihood at low levels of hypoxia and salinity, but these benefits are lost with rising hypoxia and salinity. The relative range of exposure shown in panel (b) allows for a range of exposure at across taxa, topography, soil depths, and climate among other variables that could drive variation in any convergence. Elevated VPD, in contrast, will increase mortality likelihood throughout the range of hypoxia and salinity, regardless of vegetation‐type.