Kaoru Kitajima

Physiological and structural tradeoffs underlying the leaf economics spectrum

The leaf economics spectrum (LES) represents a suite of intercorrelated leaf traits concerning construction costs per unit leaf area, nutrient concentrations, and rates of carbon fixation and tissue turnover. Although broad trade-offs among leaf structural and physiological traits have been demonstrated, we still do not have a comprehensive view of the fundamental constraints underlying the LES trade-offs. Here, we investigated physiological and structural mechanisms underpinning the LES by analysing a novel data compilation incorporating rarely considered traits such as the dry mass fraction in cell walls, nitrogen allocation, mesophyll CO2 diffusion and associated anatomical traits for hundreds of species covering major growth forms. The analysis demonstrates that cell wall constituents are major components of leaf dry mass (18-70%), especially in leaves with high leaf mass per unit area (LMA) and long lifespan. A greater fraction of leaf mass in cell walls is typically associated with a lower fraction of leaf nitrogen (N) invested in photosynthetic proteins; and lower within-leaf CO2 diffusion rates, as a result of thicker mesophyll cell walls. The costs associated with greater investments in cell walls underpin the LES: long leaf lifespans are achieved via higher LMA and in turn by higher cell wall mass fraction, but this inevitably reduces the efficiency of photosynthesis.

Globally, functional traits are weak predictors of juvenile tree growth, and we do not know why

Additional co-authors: Herve Jactel, Xuefei Li, Kaoru Kitajima, Julia Koricheva, Cristina Martinez-Garza, Christian Messier, Alain Paquette, Christopher Philipson, Daniel Piotto, Lourens Poorter, Juan M. Posada, Catherine Potvin, Kalle Rainio, Sabrina E. Russo, Mariacarmen Ruiz-Jaen, Michael Scherer-Lorenzen, Campbell O. Webb, S. Joseph Wright, Rakan A. Zahawi, andnAndy Hector

The Ecophysiology of Leaf Lifespan in Tropical Forests: Adaptive and Plastic Responses to Environmental Heterogeneity

Leaf lifespan , the time from leaf expansion to shedding, exhibits wide variation and is a key integrator of relationships with photosynthetic rate, leaf mass per area (LMA), and leaf nitrogen among coexisting tropical tree species. We present a hierarchical view of sources of variation in leaf lifespan in tropical forests, emphasizing the importance of substantial within-species variation, which has rarely been addressed. Interspecific variation in leaf lifespan is positively correlated with LMA, varying from short-lived, low-LMA leaves to long-lived, high-LMA leaves of species associated with resource-rich versus resource-depleted habitats, respectively. Phenotypic responses of leaf lifespan and LMA to light show counter-gradient variation: with acclimation to shade, leaf lifespan increases, and LMA decreases, but both increase with adaptation to shade. In contrast, phenotypic responses to soil fertility are predicted to show co-gradient variation: both leaf lifespan and LMA increase with declining fertility both inter- and intraspecifically. We present new data analyses supporting these predictions, but the interactive effects of light and soil resources can produce complex phenotypic responses. Future studies of leaf lifespan should devote more attention to within-species variation to better quantify and explain how leaf lifespan is central to trade-offs generating the contrasting ecological strategies of tropical tree species.

Variations of leaf longevity in tropical moist forests predicted by a trait‐driven carbon optimality model

Leaf longevity (LL) varies more than 20-fold in tropical evergreen forests, but it remains unclear how to capture these variations using predictive models. Current theories of LL that are based on carbon optimisation principles are challenging to quantitatively assess because of uncertainty across species in the ageing rate: the rate at which leaf photosynthetic capacity declines with age. Here, we present a meta-analysis of 49 species across temperate and tropical biomes, demonstrating that the ageing rate of photosynthetic capacity is positively correlated with the mass-based carboxylation rate of mature leaves. We assess an improved trait-driven carbon optimality model with inxa0situLL data for 105 species in two Panamanian forests. We show that our model explains over 40% of the cross-species variation in LL under contrasting light environment. Collectively, our results reveal how variation in LL emerges from carbon optimisation constrained by both leaf structural traits and abiotic environment.

Implications of life span variation within a leaf cohort for evaluation of the optimal timing of leaf shedding

Summary nLeaf life span (LLS) has been intensively studied as a key functional trait, and it is thought to have evolved and acclimates so as to optimize carbon balance or nitrogen use. However, empirical studies have produced inconsistent results in support of the theoretical predictions of optimal LLS. nHow rapidly daily carbon gain declines with leaf age is a critical parameter in the theories of optimal LLS, and it is often estimated from empirical data on the mean daily carbon gain of surviving leaves at each age class. We predict that such statistical approach should result in overestimation of daily carbon gain at the mean LLS, especially when LLS variation is large in the leaf cohort. nThis prediction is supported by simple simulations; daily carbon gain linearly declines to zero at the death of each individual leaf within a cohort (Case 1), and daily carbon gain linearly declines to zero at the cohort mean LLS (t¯) (Case 2). In addition, variance in the initial carbon gain is considered, with the inverse relationship between the initial carbon gain and LLS but other assumptions are same as in the Case 1 (Case 3). Under the Cases 1 and 3, the mean daily carbon gain of surviving leaves at (t¯) is always positive, and it increases with increasing LLS variance within a cohort. Under the Case 2, the mean daily carbon gain of surviving leaves at (t¯) is zero regardless of variation in LLS, but this case is unrealistic as some leaves with negative carbon balance are assumed to survive for long-time when LLS variability is large. nPublished data on multiple species demonstrate a positive relationship of photosynthetic capacity at (t¯) with LLS variability as predicted by our simulation under the Cases 1 and 3. This strongly suggests that the age-related decline of carbon gain may be underestimated in many previous studies that neglect within-cohort variation in LLS. nIn conclusion, we call attention to the importance of LLS variations within a leaf cohort, which should be considered in empirical test of the theories of optimal LLS.

Leaf trait variations associated with habitat affinity of tropical karst tree species

Abstract Karst hills, that is, jagged topography created by dissolution of limestone and other soluble rocks, are distributed extensively in tropical forest regions, including southern parts of China. They are characterized by a sharp mosaic of water and nutrient availability, from exposed hilltops with poor soil development to valleys with occasional flooding, to which trees show species‐specific distributions. Here we report the relationship of leaf functional traits to habitat preference of tropical karst trees. We described leaf traits of 19 tropical tree species in a seasonal karst rainforest in Guangxi Province, China, 12 species in situ and 13 ex situ in a non‐karst arboretum, which served as a common garden, with six species sampled in both. We examined how the measured leaf traits differed in relation to species’ habitat affinity and evaluated trait consistency between natural habitats vs. the arboretum. Leaf mass per area (LMA) and optical traits (light absorption and reflectance characteristics between 400 and 1,050 nm) showed significant associations with each other and habitats, with hilltop species showing high values of LMA and low values of photochemical reflectance index (PRI). For the six species sampled in both the karst forest and the arboretum, LMA, leaf dry matter content, stomatal density, and vein length per area showed inconsistent within‐species variations, whereas some traits (stomatal pore index and lamina thickness) were similar between the two sites. In conclusion, trees specialized in exposed karst hilltops with little soils are characterized by thick leaves with high tissue density indicative of conservative resources use, and this trait syndrome could potentially be sensed remotely with PRI.

Plant–soil interactions maintain biodiversity and functions of tropical forest ecosystems

Tropical forests are characterized by high biodiversity and aboveground biomass growing on strongly weathered soils. However, the distribution of plant species and soils are highly variable even within a tropical region. This paper reviews existing and novel knowledge on soil genesis, plant and microbial physiology, and biogeochemistry. Typically, forests in Southeast Asia are dominated by dipterocarps growing on acidic Ultisols from relatively young parent material. In the Neotropics and Africa, forests contain abundant legume trees growing on Oxisols developed in the older parent materials on stable continental shields. In Southeast Asia, the removal of base cations from the surface soil due to leaching and uptake by dipterocarp trees result in intensive acidification and accumulation of exchangeable Al3+, which is toxic to most plants. Nutrient mining by ectomycorrhizal fungi and efficient allocation within tree organs can supply phosphorus (P) for reproduction (e.g., mast fruiting) even on P-limited soils. In the Neotropics and Africa, nitrogen (N) fixation by legume trees can ameliorate N or P limitation but excess N can promote acidification through nitrification. Biological weathering [e.g., plant silicon (Si) cycling] and leaching can lead to loss of Si from soil. The resulting accumulation of Al and Fe oxides in Oxisols that can reduce P solubility through sorption and lead to limitation of P relative to N. Thus, geographical variation in geology and plant species drives patterns of soil weathering and niche differentiation at the global scale in tropical forests.

Decomposing leaf mass into photosynthetic and structural components explains divergent patterns of trait variation within and among plant species

Across the global flora, photosynthetic and metabolic rates depend more strongly on leaf area than leaf mass. In contrast, intraspecific variation in these rates is strongly mass-dependent. These contrasting patterns suggest that the causes of variation in leaf mass per area (LMA) may be fundamentally different within vs. among species. We used statistical methods to decompose LMA into two conceptual components – ‘photosynthetic’ LMAp (which determines photosynthetic capacity and metabolic rates, and also affects optimal leaf lifespan) and ‘structural’ LMAs (which determines leaf toughness and potential leaf lifespan) using leaf trait data from tropical forest sites in Panama and a global leaf-trait database. Statistically decomposing LMA into LMAp and LMAs provides improved predictions of trait variation (photosynthesis, respiration, and lifespan) across the global flora, and within and among tropical plant species in Panama. Our analysis shows that most interspecific LMA variation is due to LMAs (which explains why photosynthetic and metabolic traits are area-dependent across species) and that intraspecific LMA variation is due to changes in both LMAp and LMAs (which explains why photosynthetic and metabolic traits are mass-dependent within species). Our results suggest that leaf trait variation is multi-dimensional and is not well-represented by the one-dimensional leaf economics spectrum.