No evidence of carbon storage usage for seed production in 18 dipterocarp masting species in a tropical rain forest.

Most canopy species in lowland tropical rain forests in Southeast Asia, represented by Dipterocarpaceae, undergo mast reproduction synchronously at community level during a general flowering event. Such events occur at irregular intervals of 2-10 years. Some species do not necessarily participate in every synchronous mast reproduction, however. This may be due to a lack of carbohydrate resources in the trees for masting. We tested the hypothesis that interspecific differences in the time required to store assimilates in trees for seed production are due to the frequency of masting and/or seed size in each species. We examined the relationship between reproductive frequency and the carbon accumulation period necessary for seed production, and between the seed size and the period, using radiocarbon analysis in 18 dipterocarp canopy species. The mean carbon accumulation period was 0.84 years before seed maturation in all species studied. The carbon accumulation period did not have any significant correlation with reproductive frequency or seed size, both of which varied widely across the species studied. Our results show that for seed production, dipterocarp masting species do not use carbon assimilates stored for a period between the masting years, but instead use recent photosynthates produced primarily in a masting year, regardless of the masting interval or seed size of each species. These findings suggest that storage of carbohydrate resources is not a limiting factor in the masting of dipterocarps, and that accumulation and allocation of other resources is important as a precondition for participation in general flowering.

Convergence in phosphorus constraints to photosynthesis in forests around the world.

Tropical forests take up more carbon (C) from the atmosphere per annum by photosynthesis than any other type of vegetation. Phosphorus (P) limitations to C uptake are paramount for tropical and subtropical forests around the globe. Yet the generality of photosynthesis-P relationships underlying these limitations are in question, and hence are not represented well in terrestrial biosphere models. Here we demonstrate the dependence of photosynthesis and underlying processes on both leaf N and P concentrations. The regulation of photosynthetic capacity by P was similar across four continents. Implementing P constraints in the ORCHIDEE-CNP model, gross photosynthesis was reduced by 36% across the tropics and subtropics relative to traditional N constraints and unlimiting leaf P. Our results provide a quantitative relationship for the P dependence for photosynthesis for the front-end of global terrestrial C models that is consistent with canopy leaf measurements.

Water uptake patterns of tropical canopy trees in Borneo: species-specific and temporal variation and relationships with aboveground traits.

Root water uptake depth and its temporal variation are important determinants of tree mortality, resource partitioning and drought resistance; however, their effects on tropical trees remain poorly understood. In this study, we investigated interspecific differences in water uptake depth and its temporal variation using stable isotope analysis and examined the relationships between water uptake depth and aboveground traits in a humid aseasonal tropical rainforest in Borneo. Species-specific differences in water uptake depth were examined for six dominant dipterocarp species. Temporal variation in water uptake depth for various canopy trees was assessed in three periods with different soil moisture conditions. We then examined the relationships between water uptake depth and aboveground traits including wood density, maximum tree height, flowering frequency and growth rate. Dipterocarpus globosus appeared to be more reliant on deep water resources than the other dipterocarp species. Water uptake from the soil layers varied among the three sampling periods. Trees generally utilized deeper soil water during the second driest sampling period, when temperatures were lowest. During the driest and wettest sampling periods, species with higher flowering frequencies tended to preferentially uptake deep soil water. These results suggest that low temperature and soil moisture promote increased deep soil water uptake in the study region. Dynamic relationships between water uptake patterns and aboveground tree traits may be related to resource partitioning among co-existing species.

Verification of our empirical understanding of the physiology and ecology of two contrasting plantation species using a trait database.

The effects of climate change on forest ecosystems take on increasing importance more than ever. Information on plant traits is a powerful predictor of ecosystem dynamics and functioning. We reviewed the major ecological traits, such as foliar gas exchange and nutrients, xylem morphology and drought tolerance, of Cryptomeria japonica and Chamaecyparis obtusa, which are major timber species in East Asia, especially in Japan, by using a recently developed functional trait database for both species (SugiHinokiDB). Empirically, C. obtusa has been planted under drier conditions, whereas C. japonica, which grows faster but thought to be less drought tolerant, has been planted under wetter conditions. Our analysis generally support the empirical knowledge: The maximum photosynthetic rate, stomatal conductance, foliar nutrient content and soil-to-foliage hydraulic conductance were higher in C. japonica than in C. obtusa. In contrast, the foliar turgor loss point and xylem pressure corresponding to 50% conductivity, which indicate drought tolerance, were lower in C. obtusa and are consistent with the drier habitat of C. obtusa. Ontogenetic shifts were also observed; as the age and height of the trees increased, foliar nutrient concentrations, foliar minimum midday water potential and specific leaf area decreased in C. japonica, suggesting that nutrient and water limitation occurs with the growth. In C. obtusa, the ontogenetic shits of these foliar traits were less pronounced. Among the Cupressaceae worldwide, the drought tolerance of C. obtusa, as well as C. japonica, was not as high. This may be related to the fact that the Japanese archipelago has historically not been subjected to strong dryness. The maximum photosynthetic rate showed intermediate values within the family, indicating that C. japonica and C. obtusa exhibit relatively high growth rates in the Cupressaceae family, and this is thought to be the reason why they have been selected as economically suitable timber species in Japanese forestry. This study clearly demonstrated that the plant trait database provides us a promising opportunity to verify out empirical knowledge of plantation management and helps us to understand effect of climate change on plantation forests by using trait-based modelling.

Vertical distribution of radiocesium concentrations among crown positions and year-to-year variation in four major tree species after the Fukushima Daiichi Nuclear Power Plant accident.

To evaluate the distribution of radiocesium (137Cs) among crown positions in trees after the Fukushima Daiichi Nuclear Power Plant accident, we collected foliage and branch samples from different crown positions of four major tree species (Chamaecyparis obtusa, Cryptomeria japonica, Pinus densiflora, and Quercus serrata) from 2011 to 2019 in northeast Japan. We divided the samples into current-year and more than 1-year-old groups (called old foliage and old branches), which sometimes included directly contaminated parts. The 137Cs activity concentration in dry foliage and branches was measured using a germanium semiconductor detector. There were complex differences in the relative 137Cs activity concentration among species and organ types (i.e., foliage and branches) among crown positions. The relative 137Cs activity concentration in current-year foliage was higher in the upper crowns of C. obtusa, but higher in lower crown positions in C. japonica. No differences among crown positions were observed in P. densiflora and Q. serrata. In current-year branches, the relative 137Cs concentration in Q. serrata was similar among crown positions but higher in the upper crown in P. densiflora. The concentrations in old foliage and old branches in all species tended to be higher in the lower crown. The factors causing these interspecific and organ type differences among crown positions may be related to the organ turnover rate, dilution effect due to different growth rates, and potassium distribution within the crown. No year-to-year variation was observed in most foliage and branches in all species, except for current-year branches of Q. serrata, old foliage in C. japonica and P. densiflora, and old branches in P. densiflora. Our long-term data on the interspecific and inter-organ patterns of contamination, focusing on variation among crown positions and year-to-year trends, might help to improve the estimation of 137Cs deposition and dynamics in polluted forest ecosystems.

Seasonal changes in radiocesium and potassium concentrations in current-year shoots of saplings of three tree species in Fukushima, Japan.

We studied seasonal changes in radiocesium (137Cs) activity and potassium concentrations in current-year leaves and branches of Pinus densiflora (naturally regenerated saplings), Cryptomeria japonica (planted saplings) and Quercus serrata (planted saplings and coppice shoots) in Fukushima, Japan. We collected current-year shoots from 10 individuals of each species over two growing seasons at intervals of 1-4 months, between June 2016 and December 2017. For the deciduous species Q. serrata, we also collected dead leaves that remained attached to branches in December to investigate reabsorption of 137Cs. All collected shoots were divided into leaves and branches, oven-dried, and ground; dry weights of each sample were recorded. 137Cs activity concentrations were measured using a germanium semiconductor detector. Potassium concentrations were quantified using inductively coupled plasma optical emission spectrometry (ICP-OES). Increases in dry weight were observed in both leaves and branches between May/June and August; growth then slowed considerably and virtually ceased after October. Clear seasonal changes in 137Cs activity concentrations were observed in both 2016 and 2017, regardless of tree species. Concentrations were higher in young leaves and branches during May and June, then decreased and changed relatively little from August to winter. Reduced 137Cs activity concentrations in dead leaves of Q. serrata were observed only in December 2017 (approximately 15% lower than in October). This reduction may indicate reabsorption of 137Cs in leaves prior to shedding. The changes in potassium concentrations were similar to those in 137Cs in both years. Potassium concentrations were higher in young leaves than in mature leaf and branch samples collected later in the year. A reduction of about 50% in the potassium concentrations in dead leaves of Q. serrata was also observed in December. A positive relationship between 137Cs and potassium concentrations in leaves and branches was observed in all species, except for planted Q. serrata. This relationship may indicate that 137Cs moves in tree shoots with potassium. Leaf and branch weight correlated negatively with 137Cs and potassium concentrations. Reduced concentrations may indicate dilution of these elements as a result of biomass increases over the growing season. Our results imply that irrespective of species, 137Cs exhibits seasonal variations resulting from dilution; these variations correspond with trends in potassium, with higher levels in young organs and decreased levels in older organs.

Isotopic evidence for oligotrophication of terrestrial ecosystems.

Human societies depend on an Earth system that operates within a constrained range of nutrient availability, yet the recent trajectory of terrestrial nitrogen (N) availability is uncertain. Examining patterns of foliar N concentrations and isotope ratios (δ15N) from more than 43,000 samples acquired over 37 years, here we show that foliar N concentration declined by 9% and foliar δ15N declined by 0.6-1.6‰. Examining patterns across different climate spaces, foliar δ15N declined across the entire range of mean annual temperature and mean annual precipitation tested. These results suggest declines in N supply relative to plant demand at the global scale. In all, there are now multiple lines of evidence of declining N availability in many unfertilized terrestrial ecosystems, including declines in δ15N of tree rings and leaves from herbarium samples over the past 75-150 years. These patterns are consistent with the proposed consequences of elevated atmospheric carbon dioxide and longer growing seasons. These declines will limit future terrestrial carbon uptake and increase nutritional stress for herbivores.

Effects of rainfall exclusion on leaf gas exchange traits and osmotic adjustment in mature canopy trees of Dryobalanops aromatica (Dipterocarpaceae) in a Malaysian tropical rain forest.

Climate change exposes vegetation to unusual levels of drought, risking a decline in productivity and an increase in mortality. It still remains unclear how trees and forests respond to such unusual drought, particularly Southeast Asian tropical rain forests. To understand leaf ecophysiological responses of tropical rain forest trees to soil drying, a rainfall exclusion experiment was conducted on mature canopy trees of Dryobalanops aromatica Gaertn.f. (Dipterocarpaceae) for 4 months in an aseasonal tropical rain forest in Sarawak, Malaysia. The rainfall was intercepted by using a soft vinyl chloride sheet. We compared the three control and three treatment trees with respect to leaf water use at the top of the crown, including stomatal conductance (gsmax), photosynthesis (Amax), leaf water potential (predawn: Ψpre; midday: Ψmid), leaf water potential at turgor loss point (πtlp), osmotic potential at full turgor (π100) and a bulk modulus of elasticity (ε). Measurements were taken using tree-tower and canopy-crane systems. During the experiment, the treatment trees suffered drought stress without evidence of canopy dieback in comparison with the control trees; e.g., Ψpre and Ψmid decreased with soil drying. Minimum values of Ψmid in the treatment trees decreased during the experiment, and were lower than πtlp in the control trees. However, the treatment trees also decreased their πtlp by osmotic adjustment, and the values were lower than the minimum values of their Ψmid. In addition, the treatment trees maintained gs and Amax especially in the morning, though at midday, values decreased to half those of the control trees. Decreasing leaf water potential by osmotic adjustment to maintain gs and Amax under soil drying in treatment trees was considered to represent anisohydric behavior. These results suggest that D. aromatica may have high leaf adaptability to drought by regulating leaf water consumption and maintaining turgor pressure to improve its leaf water relations.

Ecological distribution of leaf stomata and trichomes among tree species in a Malaysian lowland tropical rain forest.

The vertical structure of a tropical rain forest is complex and multilayered, with strong variation of micro-environment with height up to the canopy. We investigated the relation between morphological traits of leaf surfaces and tree ecological characteristics in a Malaysian tropical rain forest. The shapes and densities of stomata and trichomes on the abaxial leaf surfaces and their relation with leaf characteristics such as leaf area and leaf mass per area (LMA) were studied in 136 tree species in 35 families with different growth forms in the tropical moist forest. Leaf physiological properties were also measured in 50 canopy and emergent species. Most tree species had flat type (40.4 %) or mound type (39.7 %) stomata. In addition, 84 species (61.76 %) in 22 families had trichomes, including those with glandular (17.65 %) and non-glandular trichomes (44.11 %). Most leaf characteristics significantly varied among the growth form types: species in canopy and emergent layers and canopy gap conditions had higher stomatal density, stomatal pore index (SPI), trichome density and LMA than species in understory and subcanopy layers, though the relation of phylogenetically independent contrasts to each characteristic was not statistically significant, except for leaf stomatal density, SPI and LMA. Intrinsic water use efficiency in canopy and emergent tree species with higher trichome densities was greater than in species with lower trichome densities. These results suggest that tree species in tropical rain forests adapt to a spatial difference in their growth forms, which are considerably affected by phylogenetic context, by having different stomatal and trichome shapes and/or densities.

Height-related changes in leaf photosynthetic traits in diverse Bornean tropical rain forest trees.

Knowledge of variations in morphophysiological leaf traits with forest height is essential for quantifying carbon and water fluxes from forest ecosystems. Here, we examined changes in leaf traits with forest height in diverse tree species and their role in environmental acclimation in a tropical rain forest in Borneo that does not experience dry spells. Height-related changes in leaf physiological and morphological traits [e.g., maximum photosynthetic rate (Amax), stomatal conductance (gs), dark respiration rate (Rd), carbon isotope ratio (δ(13)C), nitrogen (N) content, and leaf mass per area (LMA)] from understory to emergent trees were investigated in 104 species in 29 families. We found that many leaf area-based physiological traits (e.g., A(max-area), Rd, gs), N, δ(13)C, and LMA increased linearly with tree height, while leaf mass-based physiological traits (e.g., A(max-mass)) only increased slightly. These patterns differed from other biomes such as temperate and tropical dry forests, where trees usually show decreased photosynthetic capacity (e.g., A(max-area), A(max-mass)) with height. Increases in photosynthetic capacity, LMA, and δ(13)C are favored under bright and dry upper canopy conditions with higher photosynthetic productivity and drought tolerance, whereas lower R d and LMA may improve shade tolerance in lower canopy trees. Rapid recovery of leaf midday water potential to theoretical gravity potential during the night supports the idea that the majority of trees do not suffer from strong drought stress. Overall, leaf area-based photosynthetic traits were associated with tree height and the degree of leaf drought stress, even in diverse tropical rain forest trees.

Chemical composition of desert willow (Salix psammophila) grown in the Kubuqi Desert, Inner Mongolia, China: bark extracts associated with environmental adaptability.

Bark of desert willow (Salix psammophila, Spsa) grown in Inner Mongolia was successively extracted with n-hexane, diethyl ether, acetone, methanol, and hot water to examine chemical components associated with its environmental adaptability to desert conditions. The yield of n-hexane extract (5.0% based on dry bark), mainly composed of wax, was higher than those of acetone and methanol extracts (3.7% and 4.2%, respectively), whereas the yields of n-hexane extract (1.4%) from willow bark grown in humid areas were much lower than those of acetone (17.4% and 19.9%) and methanol (12.5% and 14.0%) extracts. Unlike other willow bark samples, Spsa bark contained a certain amount of sugar alcohols. In particular, we identified arabinitol (0.21%), which has not previously been reported as a major component of extracts of willow bark. The high content of wax and sugar alcohol would be associated with the ability of Spsa to survive in desert conditions. Accumulation of wax on the outer bark surface would reduce water loss, while sugar alcohols might improve freezing tolerance.

Change in biomass of symbiotic ants throughout the ontogeny of a myrmecophyte, Macaranga beccariana (Euphorbiaceae).

Macaranga myrmecophytes (ant-plants) provide their partner symbiotic ants (plant-ants) with food bodies as their main food, and they are protected by the plant-ants from herbivores. The amount of resource allocated to food bodies determines the plant-ant colony size and consequently determines the intensity of ant defense (anti-herbivore defense by plant-ants). As constraints in resource allocation change as plants grow, the plant-ant colony size is hypothesized to change with the ontogenesis of Macaranga myrmecophyte. To determine the ontogenetic change in the relative size of the plant-ant colony, we measured the dry weights of the whole plant-ant colony and all of the aboveground parts of trees at various ontogenetic stages for a myrmecophytic species (Macaranga beccariana) in a Bornean lowland tropical rain forest. Ant biomass increased as plant biomass increased. However, the rate of increase gradually declined, and the ant biomass appeared to reach a ceiling once trees began to branch. The ant/plant biomass ratio consistently decreased as plant biomass increased, with the rate of decrease gradually accelerating. We infer that the ontogenetic reduction in ant/plant biomass ratio is caused by an ontogenetic change in resource allocation to food rewards for ants related to the physiological changes accompanying the beginning of branching.

Abortion of reproductive organs as an adaptation to fluctuating daily carbohydrate production.

Excess flower production is a common phenomenon in hermaphrodite plants. The tropical pioneer shrub Melastoma malabathricum (Melastomataceae) frequently aborts not only young ovaries just after flowering, but also flower buds and developed ovaries. We tested a hypothesis that the excess production of reproductive organs and their abortion in this species is an adaptation to environmental fluctuations over shorter time scales than had previously been reported in other plants. To calculate the daily demand for carbohydrate and water by reproductive organs at the level of individual plants, we measured the respiration and transpiration of the reproductive organs at various stages and monitored their growth and abortion. To determine the daily supply of carbohydrate and water, we measured the photosynthetic productivity of leaf area, solar radiation and rainfall. The daily carbohydrate demands of the reproductive organs were significantly correlated with total photosynthetic productivity per leaf area during the previous 1, 3 and 5 days, but no correlations were found between the demands for water and accumulated rainfall or radiation. The daily abortion rates of the population were also correlated with demand for carbohydrates on the previous day per total photosynthetic productivity per leaf area. In brief, it was considered that this species produced and grew more reproductive organs when more resources were supplied and that the abortion occurred when demands for carbohydrate were large. Therefore our hypothesis was supported. We concluded that this reproductive strategy was an adaptation for pioneers characterized by continuous reproduction in aseasonal tropics. In our study, the adaptive consequence of excess production was determined by measuring natural environmental fluctuation.

Ecological distribution of homobaric and heterobaric leaves in tree species of Malaysian lowland tropical rainforest.

Tree species can generally be classified into two groups, heterobaric and homobaric leafed species, according to whether bundle-sheath extensions (BSEs) are found in the leaf (heterobaric leaf) or not (homobaric leaf). In this study, we study whether the leaf type is related to the growth environment and/or life form type, even in a tropical rain forest, where most trees have evergreen leaves that are generally homobaric. Accordingly, we investigated the distribution of leaf morphological differences across different life forms of 250 tree species in 45 families in a tropical rainforest. In total, 151 species (60%) in 36 families had homobaric leaves, and 99 species (40%) in 21 families had heterobaric leaves. We found that the proportion of heterobaric and homobaric leaf species differed clearly across taxonomic groups and life form types, which were divided into five life form types by their mature tree heights (understory, subcanopy, canopy, and emergent species) and as canopy gap species. Most understory (94%) and subcanopy (83%) species such as Annonaceae had homobaric leaves. In contrast, heterobaric leaf trees appeared more frequently in the canopy species (43%), the emergent species (96%) (such as Dipterocarpaceae), and the canopy gap species (62%). Our results suggest that tree species in the tropical rainforest adapt to spatial differences in the environmental conditions experienced at the mature height of each tree species, such as light intensity and vapor pressure difference, by having differing leaf types (heterobaric or homobaric) because these types potentially have different physiological and/or mechanical functions.

Changes in photosynthesis and leaf characteristics with tree height in five dipterocarp species in a tropical rain forest.

Variations in leaf photosynthetic, morphological and biochemical properties with increasing plant height from seedlings to emergent trees were investigated in five dipterocarp species in a Malaysian tropical rain forest. Canopy openness increased significantly with tree height. Photosynthetic properties, such as photosynthetic capacity at light saturation, light compensation point, maximum rate of carboxylation and maximum rate of photosynthetic electron transport, all increased significantly with tree height. Leaf morphological and biochemical traits, such as leaf mass per area, palisade layer thickness, nitrogen concentration per unit area, chlorophyll concentration per unit dry mass and chlorophyll to nitrogen ratio, also changed significantly with tree height. Leaf properties had simple and significant relationships with tree height, with few intra- and interspecies differences. Our results therefore suggest that the photosynthetic capacity of dipterocarp trees depends on tree height, and that the trees adapt to the light environment by adjusting their leaf morphological and biochemical properties. These results should aid in developing models that can accurately estimate carbon dioxide flux and biomass production in tropical rain forests.

Interspecific variation of photosynthesis and leaf characteristics in canopy trees of five species of Dipterocarpaceae in a tropical rain forest.

Photosynthetic rate, nitrogen concentration and morphological properties of canopy leaves were studied in 18 trees, comprising five dipterocarp species, in a tropical rain forest in Sarawak, Malaysia. Photosynthetic rate at light saturation (Pmax) differed significantly across species, varying from 7 to 18 micro mol m(-2) s(-1). Leaf nitrogen concentration and morphological properties, such as leaf blade and palisade layer thickness, leaf mass per area (LMA) and surface area of mesophyll cells per unit leaf area (Ames/A), also varied significantly across species. Among the relationships with leaf characteristics, Pmax had the strongest correlation with leaf mesophyll parameters, such as palisade cell layer thickness (r2 = 0.76, P < 0.001) and Ames/A (r2 = 0.73, P < 0.001). Leaf nitrogen concentration and Pmax per unit area also had a significant but weaker correlation (r2 = 0.46, P < 0.01), whereas Pmax had no correlation, or only weakly significant correlations, with leaf blade thickness and LMA. Shorea beccariana Burck, which had the highest P(max) of the species studied, also had the thickest palisade layer, with up to five or more layers. We conclude that interspecific variation in photosynthetic capacity in tropical rain forest canopies is influenced more by leaf mesophyll structure than by leaf thickness, LMA or leaf nitrogen concentration.