The distribution patterns of tropical ectomycorrhizal (ECM) fungi along altitudinal gradients remain largely unknown. Furthermore, despite being an iconic site for biodiversity research, virtually nothing is known about the diversity and spatial patterns of fungi on Mt Kinabalu and neighbouring mountain ranges. We carried out deep DNA sequencing of soil samples collected between 425 and 4000 m above sea level to compare richness and community composition of ECM fungi among altitudinal forest types in Borneo. In addition, we tested whether the observed patterns are driven by habitat or by geometric effect of overlapping ranges of species (mid-domain effect). Community composition of ECM fungi was strongly correlated with elevation. In most genera, richness peaked in the mid-elevation montane forest zone, with the exception of tomentelloid fungi, which showed monotonal decrease in richness with increasing altitude. Richness in lower-mid- and mid-elevations was significantly greater than predicted under the mid-domain effect model. We provide the first insight into the composition of ECM fungal communities and their strong altitudinal turnover in Borneo. The high richness and restricted distribution of many ECM fungi in the montane forests suggest that mid-elevation peak richness is primarily driven by environmental characteristics of this habitat and not by the mid-domain effect.
Tree mortality rates appear to be increasing in moist tropical forests (MTFs) with significant carbon cycle consequences. Here, we review the state of knowledge regarding MTF tree mortality, create a conceptual framework with testable hypotheses regarding the drivers, mechanisms and interactions that may underlie increasing MTF mortality rates, and identify the next steps for improved understanding and reduced prediction. Increasing mortality rates are associated with rising temperature and vapor pressure deficit, liana abundance, drought, wind events, fire and, possibly, CO2 fertilization-induced increases in stand thinning or acceleration of trees reaching larger, more vulnerable heights. The majority of these mortality drivers may kill trees in part through carbon starvation and hydraulic failure. The relative importance of each driver is unknown. High species diversity may buffer MTFs against large-scale mortality events, but recent and expected trends in mortality drivers give reason for concern regarding increasing mortality within MTFs. Models of tropical tree mortality are advancing the representation of hydraulics, carbon and demography, but require more empirical knowledge regarding the most common drivers and their subsequent mechanisms. We outline critical datasets and model developments required to test hypotheses regarding the underlying causes of increasing MTF mortality rates, and improve prediction of future mortality under climate change.
What causes individual tree death in tropical forests remains a major gap in our understanding of the biology of tropical trees and leads to significant uncertainty in predicting global carbon cycle dynamics. We measured individual characteristics (diameter at breast height, wood density, growth rate, crown illumination and crown form) and environmental conditions (soil fertility and habitat suitability) for 26 425 trees ≥ 10 cm diameter at breast height belonging to 416 species in a 52-ha plot in Lambir Hills National Park, Malaysia. We used structural equation models to investigate the relationships among the different factors and tree mortality. Crown form (a proxy for mechanical damage and other stresses) and prior growth were the two most important factors related to mortality. The effect of all variables on mortality (except habitat suitability) was substantially greater than expected by chance. Tree death is the result of interactions between factors, including direct and indirect effects. Crown form/damage and prior growth mediated most of the effect of tree size, wood density, fertility and habitat suitability on mortality. Large-scale assessment of crown form or status may result in improved prediction of individual tree death at the landscape scale.
Plant functional traits regulate ecosystem functions but little is known about how co-occurring gradients of land use and edaphic conditions influence their expression. We test how gradients of logging disturbance and soil properties relate to community-weighted mean traits in logged and old-growth tropical forests in Borneo. We studied 32 physical, chemical and physiological traits from 284 tree species in eight 1 ha plots and measured long-term soil nutrient supplies and plant-available nutrients. Logged plots had greater values for traits that drive carbon capture and growth, whilst old-growth forests had greater values for structural and persistence traits. Although disturbance was the primary driver of trait expression, soil nutrients explained a statistically independent axis of variation linked to leaf size and nutrient concentration. Soil characteristics influenced trait expression via nutrient availability, nutrient pools, and pH. Our finding, that traits have dissimilar responses to land use and soil resource availability, provides robust evidence for the need to consider the abiotic context of logging when predicting plant functional diversity across human-modified tropical forests. The detection of two independent axes was facilitated by the measurement of many more functional traits than have been examined in previous studies.
Mitochondrial respiration and tricarboxylic acid (TCA) cycle activity are required during salt stress in plants to provide ATP and reductants for adaptive processes such as ion exclusion, compatible solute synthesis and reactive oxygen species (ROS) detoxification. However, there is a poor mechanistic understanding of how salinity affects mitochondrial metabolism, particularly respiratory substrate source. To determine the mechanism of respiratory changes under salt stress in wheat leaves, we conducted an integrated analysis of metabolite content, respiratory rate and targeted protein abundance measurements. Also, we investigated the direct effect of salt on mitochondrial enzyme activities. Salt-treated wheat leaves exhibit higher respiration rate and extensive metabolite changes. The activity of the TCA cycle enzymes pyruvate dehydrogenase complex and the 2-oxoglutarate dehydrogenase complex were shown to be directly salt-sensitive. Multiple lines of evidence showed that the γ-aminobutyric acid (GABA) shunt was activated under salt treatment. During salt exposure, key metabolic enzymes required for the cyclic operation of the TCA cycle are physiochemically inhibited by salt. This inhibition is overcome by increased GABA shunt activity, which provides an alternative carbon source for mitochondria that bypasses salt-sensitive enzymes, to facilitate the increased respiration of wheat leaves.
Although fine roots are important components of the global carbon cycle, there is limited understanding of root structure-function relationships among species. We determined whether root respiration rate and decomposability, two key processes driving carbon cycling but always studied separately, varied with root morphological and chemical traits, in a coordinated way that would demonstrate the existence of a root economics spectrum (RES). Twelve traits were measured on fine roots (diameter ≤ 2 mm) of 74 species (31 graminoids and 43 herbaceous and dwarf shrub eudicots) collected in three biomes. The findings of this study support the existence of a RES representing an axis of trait variation in which root respiration was positively correlated to nitrogen concentration and specific root length and negatively correlated to the root dry matter content, lignin : nitrogen ratio and the remaining mass after decomposition. This pattern of traits was highly consistent within graminoids but less consistent within eudicots, as a result of an uncoupling between decomposability and morphology, and of heterogeneity of individual roots of eudicots within the fine-root pool. The positive relationship found between root respiration and decomposability is essential for a better understanding of vegetation-soil feedbacks and for improving terrestrial biosphere models predicting the consequences of plant community changes for carbon cycling.
Phyllanthus balgooyi (Phyllanthaceae), one of > 20 nickel (Ni) hyperaccumulator plant species known in Sabah (Malaysia) on the island of Borneo, is remarkable because it contains > 16 wt% Ni in its phloem sap, the second highest concentration of Ni in any living material in the world (after Pycnandra acuminata (Sapotaceae) from New Caledonia with 25 wt% Ni in latex). This study focused on the tissue-level distribution of Ni and other elements in the leaves, petioles and stem of P. balgooyi using nuclear microprobe imaging (micro-PIXE). The results show that in the stems and petioles of P. balgooyi Ni concentrations were very high in the phloem, while in the leaves there was significant enrichment of this element in the major vascular bundles. In the leaves, cobalt (Co) was codistributed with Ni, while the distribution of manganese (Mn) was different. The highest enrichment of calcium (Ca) in the stems was in the periderm, the epidermis and subepidermis of the petiole, and in the palisade mesophyll of the leaf. Preferential accumulation of Ni in the vascular tracts suggests that Ni is present in a metabolically active form. The elemental distribution of P. balgooyi differs from those of many other Ni hyperaccumulator plant species from around the world where Ni is preferentially accumulated in leaf epidermal cells.
*Three Bornean pitcher plant species, Nepenthes lowii, N. rajah and N. macrophylla, produce modified pitchers that 'capture' tree shrew faeces for nutritional benefit. Tree shrews (Tupaia montana) feed on exudates produced by glands on the inner surfaces of the pitcher lids and defecate into the pitchers. *Here, we tested the hypothesis that pitcher geometry in these species is related to tree shrew body size by comparing the pitcher characteristics with those of five other 'typical' (arthropod-trapping) Nepenthes species. *We found that only pitchers with large orifices and lids that are concave, elongated and oriented approximately at right angles to the orifice capture faeces. The distance from the tree shrews' food source (that is, the lid nectar glands) to the front of the pitcher orifice precisely matches the head plus body length of T. montana in the faeces-trapping species, and is a function of orifice size and the angle of lid reflexion. *Substantial changes to nutrient acquisition strategies in carnivorous plants may occur through simple modifications to trap geometry. This extraordinary plant-animal interaction adds to a growing body of evidence that Nepenthes represents a candidate model for adaptive radiation with regard to nitrogen sequestration strategies.
How tropical trees flower synchronously near the equator in the absence of significant day length variation or other meteorological cues has long been a puzzle. The rubber tree (Hevea brasiliensis) is used as a model to investigate this phenomenon. The annual cycle of solar radiation intensity is shown to correspond closely with the flowering of the rubber tree planted near the equator and in the subtropics. Unlike in temperate regions, where incoming solar radiation (insolation) is dependent on both day length and radiation intensity, insolation at the equator is due entirely to the latter. Insolation at the upper atmosphere peaks twice a year during the spring and autumn equinoxes, but the actual solar radiation that reaches the ground is attenuated to varying extents in different localities. The rubber tree shows one or two flowering seasons a year (with major and minor seasons in the latter) in accordance with the solar radiation intensity received. High solar radiation intensity, and in particular bright sunshine (as distinct from prolonged diffuse radiation), induces synchronous anthesis and blooming in Hevea around the time of the equinoxes. The same mechanism may be operational in other tropical tree species.
Drought regimes can be characterized by the variability in the quantity of rainfall and the duration of rainless periods. However, most research on plant response to drought has ignored the impacts of rainfall variation, especially with regard to the influence of nonstructural carbohydrates (NSCs) in promoting drought resistance. To test the hypothesis that these components of drought differentially affect NSC dynamics and seedling resistance, we tracked NSC in plant tissues of tropical tree seedlings in response to manipulations of the volume and frequency of water applied. NSC concentrations decreased in woody tissues under infrequent-high watering but increased under no watering. A faster decline of growth relative to stomatal conductance in the no watering treatment was consistent with NSC accumulation as a result of an uncoupling of growth and photosynthesis, while usage of stored NSCs in woody tissues to maintain function may account for the NSC decline under infrequent-high watering. NSCs, and specifically stem NSCs, contributed to drought resistance under severe water deficits, while NSCs had a less clear role in drought resistance to variability in water availability. The contrasting response of NSCs to water variability and deficit indicates that unique processes support seedling resistance to these components of drought.
A comparative study of four Malayan ferns, Christensenia aesculifolia (Bl.) Maxon, Tectaria singaporeana (Wall.) Ching, Abacopteris multilineata (Wall.) Ching and Hymenophyllum polyanthos Sw. from shady habitats and another four, Dicranopteris linearis (Burm.) Und., Lygodium scandens (L.) Sw., Blechnum orientate Linn, and Stenochlaena palustris (Burm.) Bedd. from sunlit habitats showed that the total chlorophyll content expressed on a gram fresh weight basis was greater in the shade ferns. There was little difference in the chlorophyll content between the sun and shade ferns when it was expressed on a per unit leaf area basis. The protein and protohaem content was greater in the sun ferns. Measurements of the in vitro photochemical activities of the photosystems I and II in isolated chloroplasts by means of an oxygen electrode showed higher rates in the sun ferns. As determined by spectrophotometric analysis, the photosynthetic cytochrome content from isolated chloroplasts was greater in the sun ferns. The results indicate that the sun ferns have physiological characteristics favouring greater capacity for photosynthesis. Mitochondria isolated from the sun ferns showed faster rates of electron transport using exogenous NADH as substrate.
Eucalyptus is characterized by high foliar concentrations of plant secondary metabolites with marked qualitative and quantitative variation within a single species. Secondary metabolites in eucalypts are important mediators of a diverse community of herbivores. We used a candidate gene approach to investigate genetic associations between 195 single nucleotide polymorphisms (SNPs) from 24 candidate genes and 33 traits related to secondary metabolites in the Tasmanian Blue Gum (Eucalyptus globulus). We discovered 37 significant associations (false discovery rate (FDR) Q < 0.05) across 11 candidate genes and 19 traits. The effects of SNPs on phenotypic variation were within the expected range (0.018 < r(2) < 0.061) for forest trees. Whereas most marker effects were nonadditive, two alleles from two consecutive genes in the methylerythritol phosphate pathway (MEP) showed additive effects. This study successfully links allelic variants to ecologically important phenotypes which can have a large impact on the entire community. It is one of very few studies to identify the genetic variants of a foundation tree that influences ecosystem function.
Oil palm breeding involves crossing dura and pisifera palms to produce tenera progeny with greatly improved oil yield. Oil yield is controlled by variant alleles of a type II MADS-box gene, SHELL, that impact the presence and thickness of the endocarp, or shell, surrounding the fruit kernel. We identified six novel SHELL alleles in noncommercial African germplasm populations from the Malaysian Palm Oil Board. These populations provide extensive diversity to harness genetic, mechanistic and phenotypic variation associated with oil yield in a globally critical crop. We investigated phenotypes in heteroallelic combinations, as well as SHELL heterodimerization and subcellular localization by yeast two-hybrid, bimolecular fluorescence complementation and gene expression analyses. Four novel SHELL alleles were associated with fruit form phenotype. Candidate heterodimerization partners were identified, and interactions with EgSEP3 and subcellular localization were SHELL allele-specific. Our findings reveal allele-specific mechanisms by which variant SHELL alleles impact yield, as well as speculative insights into the potential role of SHELL in single-gene oil yield heterosis. Future field trials for combinability and introgression may further optimize yield and improve sustainability.
Arbuscular mycorrhizal fungi (AMF) and ectomycorrhizal fungi (EMF) produce contrasting plant-soil feedbacks, but how these feedbacks are constrained by lithology is poorly understood. We investigated the hypothesis that lithological drivers of soil fertility filter plant resource economic strategies in ways that influence the relative fitness of trees with AMF or EMF symbioses in a Bornean rain forest containing species with both mycorrhizal strategies. Using forest inventory data on 1245 tree species, we found that although AMF-hosting trees had greater relative dominance on all soil types, with declining lithological soil fertility EMF-hosting trees became more dominant. Data on 13 leaf traits and wood density for a total of 150 species showed that variation was almost always associated with soil type, whereas for six leaf traits (structural properties; carbon, nitrogen, phosphorus ratios, nitrogen isotopes), variation was also associated with mycorrhizal strategy. EMF-hosting species had slower leaf economics than AMF-hosts, demonstrating the central role of mycorrhizal symbiosis in plant resource economies. At the global scale, climate has been shown to shape forest mycorrhizal composition, but here we show that in communities it depends on soil lithology, suggesting scale-dependent abiotic factors influence feedbacks underlying the relative fitness of different mycorrhizal strategies.
Leaf respiration in the dark (Rdark ) is often measured at a single time during the day, with hot-acclimation lowering Rdark at a common measuring temperature. However, it is unclear whether the diel cycle influences the extent of thermal acclimation of Rdark , or how temperature and time of day interact to influence respiratory metabolites. To examine these issues, we grew rice under 25°C : 20°C, 30°C : 25°C and 40°C : 35°C day : night cycles, measuring Rdark and changes in metabolites at five time points spanning a single 24-h period. Rdark differed among the treatments and with time of day. However, there was no significant interaction between time and growth temperature, indicating that the diel cycle does not alter thermal acclimation of Rdark . Amino acids were highly responsive to the diel cycle and growth temperature, and many were negatively correlated with carbohydrates and with organic acids of the tricarboxylic acid (TCA) cycle. Organic TCA intermediates were significantly altered by the diel cycle irrespective of growth temperature, which we attributed to light-dependent regulatory control of TCA enzyme activities. Collectively, our study shows that environmental disruption of the balance between respiratory substrate supply and demand is corrected for by shifts in TCA-dependent metabolites.
Leaf venation networks evolved along several functional axes, including resource transport, damage resistance, mechanical strength, and construction cost. Because functions may depend on architectural features at different scales, network architecture may vary across spatial scales to satisfy functional tradeoffs. We develop a framework for quantifying network architecture with multiscale statistics describing elongation ratios, circularity ratios, vein density, and minimum spanning tree ratios. We quantify vein networks for leaves of 260 southeast Asian tree species in samples of up to 2 cm2 , pairing multiscale statistics with traits representing axes of resource transport, damage resistance, mechanical strength, and cost. We show that these multiscale statistics clearly differentiate species' architecture and delineate a phenotype space that shifts at larger scales; functional linkages vary with scale and are weak, with vein density, minimum spanning tree ratio, and circularity ratio linked to mechanical strength (measured by force to punch) and elongation ratio and circularity ratio linked to damage resistance (measured by tannins); and phylogenetic conservatism of network architecture is low but scale-dependent. This work provides tools to quantify the function and evolution of venation networks. Future studies including primary and secondary veins may uncover additional insights.
The relative importance of tree mortality risk factors remains unknown, especially in diverse tropical forests where species may vary widely in their responses to particular conditions. We present a new framework for quantifying the importance of mortality risk factors and apply it to compare 19 risks on 31 203 trees (1977 species) in 14 one-year periods in six tropical forests. We defined a condition as a risk factor for a species if it was associated with at least a doubling of mortality rate in univariate analyses. For each risk, we estimated prevalence (frequency), lethality (difference in mortality between trees with and without the risk) and impact ('excess mortality' associated with the risk, relative to stand-level mortality). The most impactful risk factors were light limitation and crown/trunk loss; the most prevalent were light limitation and small size; the most lethal were leaf damage and wounds. Modes of death (standing, broken and uprooted) had limited links with previous conditions and mortality risk factors. We provide the first ranking of importance of tree-level mortality risk factors in tropical forests. Future research should focus on the links between these risks, their climatic drivers and the physiological processes to enable mechanistic predictions of future tree mortality.
Chilling restrains the distribution of mangroves. We tested whether foliar phosphorus (P) fractions and gene expression are associated with cold tolerance in mangrove species. We exposed seedlings of six mangrove populations from different latitudes to favorable, chilling and recovery treatments, and measured their foliar P concentrations and fractions, photochemistry, nighttime respiration, and gene expression. A Kandelia obovata (KO; 26.45°N) population completely and a Bruguiera gymnorhiza (Guangxi) (BGG; 21.50°N) population partially (30%) survived chilling. Avicennia marina (24.29°N), and other B. gymnorhiza (26.66°N, 24.40°N, and 19.62°N) populations died after chilling. Photosystems of KO and photosystem I of BGG were least injured. During chilling, leaf P fractions, except nucleic acid P in three populations, declined and photoinhibition and nighttime respiration increased in all populations, with the greatest impact in B. gymnorhiza. Leaf nucleic acid P was positively correlated with photochemical efficiency during recovery and nighttime respiration across populations for each treatment. Relatively high concentrations of nucleic acid P and metabolite P were associated with stronger chilling tolerance in KO. Bruguiera gymnorhiza exhibited relatively low concentrations of organic P in favorable and chilling conditions, but its partially survived population showed stronger compensation in nucleic acid P and Pi concentrations and gene expression during recovery.
Leaf structure plays an important role in photosynthesis. However, the causal relationship and the quantitative importance of any single structural parameter to the overall photosynthetic performance of a leaf remains open to debate. In this paper, we report on a mechanistic model, eLeaf, which successfully captures rice leaf photosynthetic performance under varying environmental conditions of light and CO2 . We developed a 3D reaction-diffusion model for leaf photosynthesis parameterised using a range of imaging data and biochemical measurements from plants grown under ambient and elevated CO2 and then interrogated the model to quantify the importance of these elements. The model successfully captured leaf-level photosynthetic performance in rice. Photosynthetic metabolism underpinned the majority of the increased carbon assimilation rate observed under elevated CO2 levels, with a range of structural elements making positive and negative contributions. Mesophyll porosity could be varied without any major outcome on photosynthetic performance, providing a theoretical underpinning for experimental data. eLeaf allows quantitative analysis of the influence of morphological and biochemical properties on leaf photosynthesis. The analysis highlights a degree of leaf structural plasticity with respect to photosynthesis of significance in the context of attempts to improve crop photosynthesis.