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.

Limited stomatal regulation of the largest-size class of Dryobalanops aromatica in a Bornean tropical rainforest in response to artificial soil moisture reduction.

The physiological response of trees to drought is crucial for understanding the risk of mortality and its feedbacks to climate under the increase in droughts due to climate change, especially for the largest trees in tropical rainforests because of their large contribution to total carbon storage and water use. We determined the response of the mean canopy stomatal conductance per unit leaf area (gs) and whole-tree hydraulic conductance (Gp) of the largest individuals (38-53 m in height) of a typical canopy tree species in a Bornean tropical rainforest, Dryobalanops aromatica C.F.Gaertn., to soil moisture reduction by a 4-month rainfall exclusion experiment (REE) based on the measurements of sap flux and leaf water potentials at midday and dawn. In the mesic condition, the gs at vapor pressure deficit (D) = 1 kPa (gsref) was small compared with the reported values in various biomes. The sensitivity of gs to D (m) at a given gsref (m/gsref) was ≥ 0.6 irrespective of soil moisture conditions, indicating intrinsically sensitive stomatal control with increasing D. The REE caused greater soil drought and decreased the mean leaf water potentials at midday and dawn to the more negative values than the control under the relatively dry conditions due to natural reduction in rainfall. However, the REE did not cause a greater decrease in gs nor any clear alteration in the sensitivity of gs to D compared with the control, and induced greater decreases in Gp during REE than the control. Thus, though the small gs and the sensitive stomatal response to D indicate the water saving characteristics of the studied trees under usual mesic conditions, their limited stomatal regulation in response to soil drought by REE and the resulting decline in Gp might suggest a poor resistance to the unusually severe drought expected in the future.

Unravelling proximate cues of mass flowering in the tropical forests of South-East Asia from gene expression analyses.

Elucidating the physiological mechanisms of the irregular yet concerted flowering rhythm of mass flowering tree species in the tropics requires long-term monitoring of flowering phenology, exogenous and endogenous environmental factors, as well as identifying interactions and dependencies among these factors. To investigate the proximate factors for floral initiation of mast seeding trees in the tropics, we monitored the expression dynamics of two key flowering genes, meteorological conditions and endogenous resources over two flowering events of Shorea curtisii and Shorea leprosula in the Malay Peninsula. Comparisons of expression dynamics of genes studied indicated functional conservation of FLOWERING LOCUS T (FT) and LEAFY (LFY) in Shorea. The genes were highly expressed at least 1 month before anthesis for both species. A mathematical model considering the synergistic effect of cool temperature and drought on activation of the flowering gene was successful in predicting the observed gene expression patterns. Requirement of both cool temperature and drought for floral transition suggested by the model implies that flowering phenologies of these species are sensitive to climate change. Our molecular phenology approach in the tropics sheds light on the conserved role of flowering genes in plants inhabiting different climate zones and can be widely applied to dissect the flowering processes in other plant species.

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.

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.

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.

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.

Mangrove crab intestine and habitat sediment microbiomes cooperatively work on carbon and nitrogen cycling.

Mangrove ecosystems, where litter and organic components are degraded and converted into detrital materials, support rich coastal fisheries resources. Sesarmid (Grapsidae) crabs, which feed on mangrove litter, play a crucial role in material flow in carbon-rich and nitrogen-limited mangrove ecosystems; however, the process of assimilation and conversion into detritus has not been well studied. In this study, we performed microbiome analyses of intestinal bacteria from three species of mangrove crab and five sediment positions in the mud lobster mounds, including the crab burrow wall, to study the interactive roles of crabs and sediment in metabolism. Metagenome analysis revealed species-dependent intestinal profiles, especially in Neosarmatium smithi, while the sediment microbiome was similar in all positions, albeit with some regional dependency. The microbiome profiles of crab intestines and sediments were significantly different in the MDS analysis based on OTU similarity; however, 579 OTUs (about 70% of reads in the crab intestinal microbiome) were identical between the intestinal and sediment bacteria. In the phenotype prediction, cellulose degradation was observed in the crab intestine. Cellulase activity was detected in both crab intestine and sediment. This could be mainly ascribed to Demequinaceae, which was predominantly found in the crab intestines and burrow walls. Nitrogen fixation was also enriched in both the crab intestines and sediments, and was supported by the nitrogenase assay. Similar to earlier reports, sulfur-related families were highly enriched in the sediment, presumably degrading organic compounds as terminal electron acceptors under anaerobic conditions. These results suggest that mangrove crabs and habitat sediment both contribute to carbon and nitrogen cycling in the mangrove ecosystem via these two key reactions.

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.

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.

Accurate estimation of nitrogen concentration in deciduous tree leaves in a field study using a portable non-destructive nitrogen detector.

A non-destructive nitrogen (N) detector [Agriexpert PPW-3000 (PPW-3000)] is a useful device for rapid and non-destructive measurement of leaf N content. However, some studies find a poor correlation between the PPW-3000 reading and the actual leaf N content; the R2 value of the approximate equation was low. To improve the accuracy of N estimation, we determined the approximate equation taking into account the leaf development stage (maturing and mature leaves) and leaf flush type (early and late leaves). For the leaf development stage, we determined approximate equations for maturing leaves (Ya), mature leaves (Yb), and "maturing+mature" leaves (Yc) in species having simultaneous leaf emergence. The resulting accuracy of Ya, Yb, and Yc was quite high. For leaf flush species, we determined approximate equations for early leaves (Y1), late leaves (Y2), and "early+late" leaves (Y3) in species having heterophyllous leaf emergence. The accuracy of Y1 and Y2 was relatively high, but that of Y3 was low. We conclude that, when using a PPW-3000, we can determine an approximate equation for maturing and mature leaves jointly, but should treat early and late leaves separately.

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.

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.

Reproductive success and distance to conspecific adults in the sparsely distributed tree Kalopanax pictus.

To understand how a sparsely distributed species can maintain viable populations, and with a particular interest in distance-dependent reproductive success, we investigated the ovule survival and the factors that determine the survival for sparsely distributed Kalopanax pictus (Araliaceae) in a temperate forest landscape around the Ogawa Forest Reserve, central Japan. We found 154 potentially mature trees (>20 cm diameter at breast height) in a 600-ha site. The year 2000 was a mass flowering year for K. pictus; 96.8% of the trees examined flowered in that year; however, this was less than half of the trees that flowered in other years. The flowers of K. pictus include protandrous inflorescences, which bloom on individual tress in midsummer when few other tree species bloom. We conducted pollination experiments with out-crossed, self-pollinated, bagged, and control inflorescences. Results suggest that self-pollination is limited, partially by low self-compatibility and partially by protandry. Ovule survival from the flower to the seed stages was not dependent on the temporal flowering density of conspecific adults. The flowering habit and presence of effective pollinators may allow K. pictus to avoid the negative effects of sparse distribution on pollination efficiency. However, ovule survival during the ovary development stage depended on infection by a species-specific fungus, Mycosphaerella acanthopanacis. The fungus damages leaves, and the infection intensity depends on the distance between conspecific K. pictus adults. Thus, an advantage of sparse distribution in K. pictus is disease avoidance, whereas its disadvantages are overcome by pollination efficiency.