Non-structural carbohydrates mediate seasonal water stress across Amazon forests

Abstract

Non-structural carbohydrates (NSC) are major substrates for plant metabolism and have been implicated in mediating drought-induced tree mortality. Despite their significance, NSC dynamics in tropical forests remain little studied. We present leaf and branch NSC data for 82 Amazon canopy tree species in six sites spanning a broad precipitation gradient. During the wet season, total NSC (NSC_T) concentrations in both organs were remarkably similar across communities. However, NSC_T and its soluble sugar (SS) and starch components varied much more across sites during the dry season. Notably, the proportion of leaf NSC_T in the form of SS (SS:NSC_T) increased greatly in the dry season in almost all species in the driest sites, implying an important role of SS in mediating water stress in these sites. This adjustment of leaf NSC balance was not observed in tree species less-adapted to water deficit, even under exceptionally dry conditions. Thus, leaf carbon metabolism may help to explain floristic sorting across water availability gradients in Amazonia and enable better prediction of forest responses to future climate change.

Fig. 1. Location of sampled sites and monthly precipitation.

The map depicts mean annual precipitation in South America (mm year⁻¹). The Amazon basin is bounded by the black outline. Bar plots show the monthly precipitation for each site, blue represents precipitation >100 mm month⁻¹ and red ≤100 mm month⁻¹. Data for the map and bar plots are from WorldClim v2 (1970–2010, 30 s resolution).

Fig. 2. Species-mean total NSC (NSC_T) and variance partitioning into site and taxonomic components.

Concentrations of NSC_T and variance partitioning results are displayed separately for leaves (panels a–d) and branches (panels e–h) during the wet and dry seasons. Left hand panels: Each box encompasses the 25th to 75th percentiles; the median is indicated by the horizontal line with each box while external horizontal lines indicate the 10th and 90th percentiles; dots indicate outliers. Sites are ordered and colour-coded from left to right from driest to wettest; red to yellow boxes represent the seasonal sites and two blue boxes the aseasonal sites; n indicates the number of species sampled in each site. Differences among sites were tested using Kruskal–Wallis. Sites with different letters are statistically distinguishable (p < 0.05, post hoc Mann–Whitney–Wilcoxon Rank Sum test using Bonferroni correction is indicated by small letters). Right hand panels: Partitioning of total variance of NSC_T, starch and soluble sugars into genetic (family/genus/species), environmental (site) and error (residual) components; for the variance partitioning analysis, values were log1p-transformed prior to analysis.

Fig. 3. Seasonal variation of total NSC (NSC_T), starch and soluble sugars (SS) across Amazon forests.

Sites are ordered from left to right, from driest to wettest site. Panels a, c and e represent leaves and panels b, d and f represent branches. Red boxes denote the dry season and blue boxes denote the wet season. Each box encompasses the 25th to 75th percentiles; the median is indicated by the horizontal line with each box while external horizontal lines indicate the 10th and 90th percentiles; dots indicate outliers. Number of species sampled in each site are the same in the dry and wet season and are as follows: Ken = 9, Fec = 14, Man = 13, Tam = 21. To test for differences between season within site we used paired sample Wilcoxon tests.

Fig. 4. Relationship between leaf NSC and water status, and distributions of species-level seasonal shifts in leaf NSC allocation.

Relationship between a leaf SS:NSC_T (proportion of leaf NSC_T in the form of soluble sugars) and midday leaf water potential (Ψ_MD); c leaf starch and Ψ_MD. Distributions of species-level seasonal shifts in b leaf SS:NSC_T allocation (SS:NSC_{T Wet}− SS:NSC_{T Dry}) and d starch allocation (starch _wet − starch _dry). In the panel a and c the SS:NSC_T, starch and Ψ_MD represent mean of all species sampled in each site in the dry season, except in the two sites where there is no dry season (monthly precipitation ≤ 100 mm month⁻¹). Vertical and horizontal bars denote one standard error of the mean. The relationship between SS:NSC_T, starch and Ψ_MD was fitted using standardised major axis (SMA) regression. In the panel b and d sites are ordered from top to bottom from drier to wettest. Long vertical black line denotate the mean ΔSS:NSC_T and starch, each dot represents one species. Values to the left of the blue line denote species that increased SS:NSC_T and starch in the dry season while those to the right of the line increased SS:NSC_T and starch in the wet season.