Changes in carbon and nitrogen metabolism during seawater-induced mortality of Picea sitchensis trees

Abstract

Increasing seawater exposure is causing mortality of coastal forests, yet the physiological response associated with seawater-induced tree mortality, particularly in non-halophytes, is poorly understood. We investigated the shifts in carbon and nitrogen metabolism of mature Sitka-spruce trees that were dying after an ecosystem-scale manipulation of tidal seawater exposure. Soil porewater salinity and foliar ion concentrations increased after seawater exposure and were strongly correlated with the percentage of live foliated crown (PLFC; e.g., crown ‘greenness’, a measure of progression to death). Co-occurring with decreasing PLFC was decreasing photosynthetic capacity, N-investment into photosynthesis, N-resorption efficiency, and non-structural carbohydrate (NSC, soluble sugars and starch) concentrations, with the starch reserves depleted to near zero when PLFC dropped below 5%. Combined with declining PLFC, these changes subsequently decreased total carbon gain and thus exacerbated the carbon starvation process. This study suggests that an impairment in carbon and N metabolism during the mortality process after seawater exposure is associated with the process of carbon starvation, and provides critical knowledge necessary to predict sea-level rise impacts on coastal forests.

The influence of increasing atmospheric CO2, temperature, and vapor pressure deficit on seawater‐induced tree mortality

“…soil capacity, soil texture), tree height, DBH, and leaf width (Sumida et al, 2013;Zhang et al, 2020) (Supporting Information Table S1). From 2018 to the end of 2019, we monitored individual tree's PLFC, gas exchange (including photosynthesis rate A, and leaf level transpiration E L ), predawn water potential Ψ predawn , and midday water potential Ψ midday every 2-3 months; for details, see Li et al (2021), Zhang et al (2021b), P. Zhang et al (2021). We conducted measurements of A-C i curves from 14 trees within our PLFC gradient in October 2019 to estimate the maximum carboxylation rate V c,max.25 and maximum electron transport rate J max.25 at 25°C (Li et al, 2021).…”

“…; nonhalophytic species) along a c . 800 m transect from downstream to upstream along the floodplain, with an associated shift in tidal influence (Yabusaki et al ., 2020, Li et al ., 2021; P. Zhang et al ., 2021). The trees were selected to cover a broad range of the percentage of live foliated crown (PLFC).…”

“…These processes are dependent on plant stress related to C and water depletion (McDowell et al, 2016(McDowell et al, , 2022 and involve mechanisms associated with root function, embolism vulnerability, osmotic regulation, photosynthesis, nonstructural carbohydrates (NSCs) concentrations, and other critical functions (e.g. nitrogen (N)-resorption efficiency and N investment into photosynthesis; Li et al, 2021). The negative impacts of rising seawater exposure on each of these mechanisms should logically promote C starvation through reductions in NSC availability, and hydraulic failure through increased xylem embolism.…”

Severe declines in hydraulic capacity and associated carbon starvation drive mortality in seawater exposed Sitka-spruce (Picea sitchensis) trees

“…Photosynthetic capacity became particularly low (Li et al 2021), due in large part to ion toxicity impacts from elevated foliar sodium (Figure S5) (Munns, 2002, Negrão et al 2017. The low photosynthetic capacity has implications for our interpretation of the large decline in crown-scale Δ as a measure of declining stomatal conductance (Wang et al 2019).…”

“…Increasing PLFC as trees approached death, combine with the low photosynthetic capacity at the individual leaf-level (Li et al 2021), should result in a decline in photosynthate production and hence growth and NSC storage. BAI declined strongly with declining PLFC (R 2 =0.77, p<0.001), such that annual growth approached zero at PLFC<40% (figure 6(a)).…”