Discussion
We found that drought reduced survival and growth for seedlings of 16 tree species from a wet tropical forest region in India (Western Ghats), but species varied substantially in their responses. Interspecific variation in survival and growth with drought was primarily explained by anatomical traits that mediate water use. Generally, species with fewer stomata and smaller xylem show lower decline in performance, growth and survival under drought condition. Variation in photosynthetic performance under drought stress correlated best with anatomical traits related to water use and gas exchange (Figure 3). Growth constituted a distinct axis as compared to survival and photosynthesis for variation in species’ drought response (Appendix Figure A9), but the overall variation in performance among species was explained by composite phenotypes determined by soft traits. Species from more seasonal sites showed larger proportional decline in photosynthetic performance under drought (Figure 1c), but species affinity to seasonality conditions did not explain variation in drought response in terms of growth or survival.
Different aspects of species’ drought performance were regulated by different traits, but stomata and xylem traits emerged as consistently important. Seedling survival in well-watered conditions improved with larger xylem and stomata (Figure 1a, b). Larger xylem also correlated with faster growth (Figure 2d) in well-watered conditions indicating that survival under well-watered conditions improves with traits that allow moving larger volumes of water for carbon assimilation. Accordingly, species with larger xylem also had higher photosynthetic rates (Figure 3a). The benefit of larger xylem for survival eroded in dry conditions (Figure 2a), indicating that species that move more water through their conduits may be disadvantaged during drought, consistent with larger xylem being more vulnerable to embolism and cavitation (Hoffmann et al. 2011, Skelton et al. 2015, Santiagoet al. 2018).
Greater stomatal density increased growth (Figure 2e) and photosynthesis (Figure 3b) in well-watered conditions, highlighting that tighter stomatal packing improved physiological function when resources were not limited (Medeiros et al. 2019). However, in drought conditions, species with larger, more densely packed stomates experienced substantially larger declines in photosynthesis (Figure 3 b, f, g) and growth (Figure 2e). Since smaller stomatal size did not correlate with higher stomatal density, stomatal size and density form different axes to regulate water-use (Anderegg et al. 2018)⁠. Stomatal area fraction (SAF = SD*SS) showed results consistent with stomatal density (Appendix Figure A3).
Species with lower specific root length, i.e., ones that proportionally invested more in root length than area, had higher survival when water was plenty, but experienced larger decline in survival in drought conditions (Appendix Table A9, l). Investing in below ground tissues may help maintain growth during drought by improving access to water (Joslinet al. 2000, Poorter & Markesteijn 2008, Paz et al. 2015, Chitra-Tarak et al. 2018)⁠. The relationship between drought response and organ-level allocation may be due to higher photosynthesis in species that invest more above-ground, suggesting coordination between root traits and stomata in regulating performance. However, photosynthetic rates in well-watered conditions did not vary with root mass fraction, or the length and area of roots. Moreover, these relationships remained similar in drought conditions even as average photosynthetic rates declined with water scarcity.
In general, trait values that supported better growth in well-watered conditions resulted in larger declines in growth with drought, suggesting a safety-efficiency trade-off with respect to water use (Choat et al. 2012)⁠. Species with larger xylem, suggesting higher hydraulic conductivity, also decreased photosynthesis during drought, but in this case, reduced photosynthesis translated to greater mortality suggesting carbon starvation with drought. Variability of trait effects on different aspects of performance was unsurprising when considering that survival and photosynthesis comprised distinct axes as compared to growth for variation among species (see PCA of species coefficients for performance variables, Appendix Figure A10). Moreover, different combinations of traits were possible and required to explain interspecific variation in the overall drought response represented by changes in survival, growth, and photosynthesis.
A few caveats temper interpretation of our results. Extrapolating from pot experiments to performance in field conditions merits caution. Plant size affects soil water depletion and transpiration rates when growing in a limited volume of soil, influencing comparisons among species (Comita & Engelbrecht 2014)⁠. Initial height, however, did not predict drought responses in our study. Secondly, in closed canopy forests, shade may buffer seedlings from drought if shaded conditions decrease evapotranspiration and/or maintain water in soil (Kupers et al. 2019)⁠. In addition, larger trees often transport water from deeper layers towards the surface (hydraulic redistribution) and increase water availability for seedlings to buffer drought stress. Alternatively, drought in natural settings may increase mortality due to other stressors such as nutrient limitation or herbivory, which we did not assess. Transplant experiments in the field will be needed to understand ‘real world’ implications of drought for seedling performance (Comita & Engelbrecht 2014)⁠.