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Premise Leaf phenology is an essential developmental process in trees and an important component in understanding climate change. However, little is known about the regulation of leaf phenology in tropical trees. Methods To understand the regulation by temperature of leaf phenology in tropical trees, we performed daily observations of leaf production under rainfall‐independent conditions using saplings of Shorea leprosula and Neobalanocarpus heimii, both species of Dipterocarpaceae, a dominant tree family of Southeast Asia. We analyzed the time‐series data obtained using empirical dynamic modeling (EDM) and conducted growth chamber experiments. Results Leaf production by dipterocarps fluctuated in the absence of fluctuation in rainfall, and the peaks of leaf production were more frequent than those of day length, suggesting that leaf production cannot be fully explained by these environmental factors, although they have been proposed as regulators of leaf phenology in dipterocarps. Instead, EDM suggested a causal relationship between temperature and leaf production in dipterocarps. Leaf production by N. heimii saplings in chambers significantly increased when temperature was increased after long‐term low‐temperature treatment. This increase in leaf production was observed even when only nighttime temperature was elevated, suggesting that the effect of temperature on development is not mediated by photosynthesis. Conclusions Because seasonal variation in temperature in the tropics is small, effects on leaf phenology have been overlooked. However, our results suggest that temperature is a regulator of leaf phenology in dipterocarps. This information will contribute to better understanding of the effects of climate change in the tropics.

Large‐scale conversion of tropical forests into oil palm monocultures has led to dramatic losses of biodiversity and ecosystem functions. While ecological restoration is urgently needed in many oil palm landscapes, there is a lack of scientific knowledge of sustainable management strategies. We established experimental tree islands of varying sizes (25 m² to 1,600 m²) and diversity levels (1, 2, 3 and 6 species) in an oil palm plantation in Sumatra, Indonesia. Six native multi‐purpose tree species including Archidendron pauciflorum (Jengkol), Durio zibethinus (Durian), Parkia speciosa (Petai), Shorea leprosula (Meranti), Peronema canescens (Sungkai) and Dyera polyphylla (Jelutung) were planted between living and felled oil palms. Here, we analyse the controlling factors of tree growth and survival during the first 4 years at the level of local neighbourhood and tree island. We found a significant effect of diversity levels on tree productivity, that is, basal area was higher in multi‐species than in single‐species tree islands. This overyielding was attributed to enhanced tree growth, while mortality had no effect. In the local neighbourhood, tree species richness had a positive effect on tree growth during the first year only, indicating that selection and dominance of well‐performing species at high level of diversity are most likely driving overyielding. Trees grew better away from living oil palms, suggesting tree‐palm competition. Proximity to felled oil palms increased growth especially during the first years, during which the planted trees might have benefited from the additional available space and resources. Despite positive edge effects from the conventional oil palm management in the surrounding, tree island size had an overall positive effect on tree growth. Synthesis and applications. We planted native trees in an oil palm landscape following a tree island pattern. The establishment success differed widely among the six planted species. The selection of particular species is a decisive factor to foster a positive relationship between diversity and tree growth. Planting larger tree islands (e.g. 1,600 square metres) is a better option to enhance tree growth, but tree‐palm competition implies a trade‐off between tree growth and palm oil production in the tree islands.

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.

In a unique phenomenon restricted to the ever wet forests of Southeast Asia, hundreds of species from dozens of plant families reproduce synchronously at irregular, multi-year intervals. The proximate environmental cues that synchronize these general flowering events have not been evaluated systematically because there have been no long-term, high temporal resolution, species-level records from the region. We present 13 years of weekly flowering records for five Shorea species as well as daily temperature and rainfall records from the Pasoh Forest Reserve, Peninsular Malaysia. We constructed models to evaluate hypothesized relationships between flowering and cool temperature, drought, and additive and synergistic effects of cool temperature and drought for each species. Model parameters include periods of time for floral cue accumulation and flower development and temperature and/or rainfall thresholds required for floral initiation. Parameters estimated using flowering observations from 2001 to 2011 were used to forecast flowering for 2011–2014. We show that drought and cool temperatures acting synergistically best explain the timing of flowering events for all Shorea species in the section Mutica and forecast the largest general flowering event accurately. Periods estimated for signal accumulation ranged from 54 to 90 days among species. Periods estimated for flowers to develop ranged between 43 and 96 days and closely followed the interspecific sequence of flowering in the Shorea species. Drought and temperature thresholds also varied among species, with Shorea maxwelliana requiring the most severe drought and Shorea leprosula the lowest temperatures. Synthesis. Our results indicate that cool temperatures and low rainfall occurring on seasonal time-scales of about 2–3 months rather than brief cold snaps or brief droughts best explain general flowering in Shorea species at the Pasoh Forest Reserve. Low rainfall is equally likely in winter (December–February) and summer (July–August) and cool temperatures are most likely in winter at Pasoh, which explains why general flowering events are restricted to spring and fall, with more frequent and stronger flowering in spring. In addition, species-specific sensitivity to environmental cues suggests that future climate change will have differential impacts on the frequency of reproduction, with potential consequences for regeneration of these dominant species of lowland tropical forests.

Tropical rainforests in South-East Asia have been affected by climatic fluctuations during past glacial eras. To examine how the accompanying changes in land areas and temperature have affected the genetic properties of rainforest trees in the region, we investigated the phylogeographic patterns of a widespread dipterocarp species, Shorea leprosula. Two types of DNA markers were used: expressed sequence tag-based simple sequence repeats and chloroplast DNA (cpDNA) sequence variations. Both sets of markers revealed clear genetic differentiation between populations in Borneo and those in the Malay Peninsula and Sumatra (Malay/Sumatra). However, in the south-western part of Borneo, genetic admixture of the lineages was observed in the two marker types. Coalescent simulation based on cpDNA sequence variation suggested that the two lineages arose 0.28-0.09 million years before present and that following their divergence migration from Malay/Sumatra to Borneo strongly exceeded migration in the opposite direction. We conclude that the genetic structure of S. leprosula was largely formed during the middle Pleistocene and was subsequently modified by eastward migration across the subaerially exposed Sunda Shelf.

Summary 1. Masting, the production of large seed crops at intervals of several years, is a reproductive adaptation displayed by many tree species. The predator satiation hypothesis predicts that starvation of seed predators between mast years and satiation during mast years decreases seed predation and thus enhances tree regeneration. 2. Mast fruiting comes at demographic costs such as missed reproduction opportunities and increased density-dependence of recruits, but it remains unknown if predator satiation constitutes a sufficiently large benefit for masting to evolve as a viable life-history strategy. So far, no studies have quantified the net fitness consequences of masting. 3. Using a long-term demographic data set of the dipterocarp Shorea leprosula in a Malaysian forest, we constructed stochastic matrix population models and performed a demographic cost–benefit analysis. 4. For observed values of mast frequency and seed predation rates, we show that strict masting strongly increases fitness compared with fruiting annually. Model results also show that the demographic costs of mast fruiting are very low compared to the demographic losses due to seed predation in a scenario of annual fruiting. Finally, we find that mast fruiting would still be selected for even at low levels of seed predation and when including additional costs such as decreased adult growth rates, limiting crop size and density-dependent seedling survival. 5. Synthesis. Our results are consistent with the predictions of the predator satiation hypothesis: mast fruiting increases fitness for a range of seed predation levels. Under seed predation pressure annually fruiting species are at a strong disadvantage and as a result a mast fruiting strategy may swiftly confer a fitness advantage. Our study shows that demographic modelling allows the weighing of fitness benefits and costs of life-history phenomena such as strict masting.

Simple sequence repeats (SSRs) derived from expressed sequence tags (ESTs) are valuable markers because they represent transcribed regions and often transferable to related taxa. Here, we report the development and characterization of EST-SSRs from Shorea leprosula. Fifty-four sequences containing SSRs were identified in 2003 unigenes assembled from 3159 ESTs. Twenty-four EST-SSRs were developed, of which four gave multiple amplifications, five were found to be monomorphic and 15 showed polymorphism, with allele numbers ranging from two to 17 in a single Pasoh Forest Reserve population of 24 individuals. The observed and expected heterozygosities ranged from 0.05 to 0.91 and from 0.16 to 0.93, respectively. Cross-species transferability of the 15 loci to 36 species within Dipterocarpaceae revealed between four and 14 loci that gave positive amplification and 10 loci were found to be transferable to more than 15 species.

Summary 1 Interspecific and intraspecific competition in seedling banks may be important determinants of regeneration success in some groups of canopy trees, e.g. dipterocarps in south-east Asian tropical rain forests, and the outcomes of these competitive interactions may contribute to the maintenance of the high levels of plant diversity. 2 We present the results of an experiment examining the effects of seedling bank diversity within canopy gaps on seedling growth, architecture and levels of insect herbivore defoliation over 18 months. Within each of six experimental canopy gaps, we planted two conspecific blocks of Shorea leprosula (Dipterocarpaceae) seedlings and two heterospecific blocks of S. leprosula seedlings amongst four other dipterocarp species with differing growth rates and palatability to herbivores. 3 The growth allocation patterns of S. leprosula differed according to whether they were planted among conspecifics or heterospecifics. Although S. leprosula seedlings grew taller in conspecific stands, their above ground biomass did not differ between planting treatments, due to increased branching and leaf area in seedlings in the heterospecific stands. 4 Shorea leprosula displayed the lowest levels of antiherbivore defences and sustained the greatest levels of defoliation of all species studied. Despite an increase of almost 60% in leaf damage in conspecific vs. heterospecific stands, neither biomass nor survival of S. leprosula seedlings differed between stands over the 18-month growth period. 5 The important effects of neighbourhood composition on the growth and herbivory of S. leprosula seedlings, suggest that diversity of seedling banks can be an important determinant of regeneration success and, thus, forest dynamics. Neighbourhood composition may have similar impacts on competitive outcomes and biomass allocation patterns in other ecological communities.

The mating system in a natural population of Shorea leprosula from Malaysian lowland dipterocarp forest was quantified by allozyme analysis using the multi-locus mixed-mating model. The population was found to be predominantly outcrossed (tm = 0.837 ± 0.066). Variation in individual multi-locus outcrossing rates (range = 0.55–1.00) may have reflected variation in individual self-compatibility, heterogeneity in the pollen pool, differences in the mating neighborhood of individuals, or population substructure. Departure from the mixed-mating model was evident from the differences in pollen and ovule allele frequencies. Pollen pool heterogeneity and significant levels of biparental mating (tm − ts = 0.127, P < 0.01) indicated that the population was most probably genetically substructured. The inbreeding coefficient based on Wright's fixation index for maternal trees (Fa = −0.078) was lower than that obtained for progenies (Fe = 0.089), suggesting considerable selection against selfed progenies duri...

Shorea leprosula is an important timber tree in Southeast Asia. From a genomic library enriched for dinucleotide (CT) repeats, 20 polymorphic microsatellite markers were developed for this species. Polymorphism of these loci was evaluated in a sample of 24 adult individuals from a natural population. The number of alleles ranged from five to 15, and the observed heterozygosity ranged from 0.333 to 0.875. Probability of paternity exclusion, in the case where the mother is known, ranged from 0.285 to 0.784. These markers were also characterized for applicability in S. parvifolia ; 16 loci were successfully cross-amplified and showed high levels of polymorphism.

Analyses of the spatial distribution pattern, spatial genetic structure and of genetic diversity were carried out in two tropical tree species with contrasting breeding systems and different ploidy levels using a 50-ha demographic plot in a lowland dipterocarp forest in Peninsular Malaysia. Shorea leprosula is a diploid and predominantly outcrossed species, whereas S. ovalis ssp. sericea is an autotetraploid species with apomictic mode of reproduction. Genetic diversity parameters estimated for S. leprosula using microsatellite were consistently higher than using allozyme. In comparisons with S. leprosula and other tropical tree species, S. ovalis ssp. sericea also displayed relatively high levels of genetic diversity. This might be explained by the lower pressure of genetic drift due to tetrasomic inheritance, and for autotetraploids each locus can accommodate up to four different alleles and this allows maintenance of more alleles at individual loci. The observed high levels of genetic diversity in S. ovalis ssp. sericea can also be due to a random retention of more heterogeneous individuals in the past, and the apomictic mode of reproduction might be an evolutionary strategy, which allows the species to maintain high levels of genetic diversity. The spatial distribution pattern analyses of both species showed significant levels of aggregation at small and medium but random distribution at the big diameter-class. The decrease in magnitude of spatial aggregation from small- to large-diameter classes might be due to compensatory mortality during recruitment and survival under competitive thinning process. Spatial genetic structure analyses for both species revealed significant spatial genetic structure for short distances in all the three diameter-classes. The magnitude of spatial genetic structure in both species was observed to be decreasing from smaller- to larger-diameter classes. The high spatial genetic structuring observed in S. ovalis ssp. sericea at the small-diameter class is due primarily to limited seed dispersal and apomictic mode of reproduction. The similar observation in S. leprosula, however, can be explained by limited seed and pollen dispersal, which supports further the fact that the species is pollinated by weak fliers, mainly of Thrips and Megalurothrips in the lowland dipterocarp forest.

The survival of dipterocarp seedlings in the understorey of south-east Asian rain forests is limited by their ability to maintain a positive carbon balance. Photosynthesis during sunflecks is an important component of carbon gain. Field measurements demonstrated that Shorea leprosula seedlings in a rain forest understorey received a high proportion of daily photon flux density at temperatures supra-optimal for photosynthesis (72% at ≥ 30 ∞ C, 14% at ≥ 35 ∞ C). To investigate the effect of high temperatures on photosynthesis during sunflecks, gas exchange and chlorophyll fluorescence measurements were made on seedlings grown in controlled environment conditions either, under uniform, saturating irradiance (approximately 539 m mol m - 2 s - 1 ) or, shade/fleck sequences (approximately 30 m m m mol m - - 2 s - 1

The survivorship of dipterocarp seedlings in the deeply shaded understorey of South-east Asian rain forests is limited by their ability to maintain a positive carbon balance. Photosynthesis during sunflecks is an important component of carbon gain. To investigate the effect of elevated CO 2 upon photosynthesis and growth under sunflecks, seedlings of Shorea leprosula were grown in controlled environment conditions at ambient or elevated CO 2 . Equal total daily photon flux density (PFD) ( ~ ~ ~ 7·7 mol m - - 2 d - 1 ) was supplied as either uniform irradiance ( ~ ~ ~ 170 m mol m - 2 s - 1 ) or shade/ fleck sequences ( ~ 30 m m m mol m - 2 s - 1 / ~ ~ ~ 525 m mol m - 2 s - 1 ). Photosynthesis and growth were enhanced by elevated CO 2 treatments but lower under flecked irradiance treatments. Acclimation of photosynthetic capacity occurred in response to elevated CO 2 but not flecked irradiance. Importantly, the relative enhancement effects of elevated CO 2 were greater under sunflecks (growth 60%, carbon gain 89%) compared with uniform irradiance (growth 25%, carbon gain 59%). This was driven by two factors: (1) greater efficiency of dynamic photosynthesis (photosynthetic induction gain and loss, post-irradiance gas exchange); and (2) photosynthetic enhancement being greatest at very low PFD. This allowed improved carbon gain during both clusters of lightflecks (73%) and intervening periods of deep shade (99%). The relatively greater enhancement of growth and photosynthesis at elevated CO 2 under sunflecks has important potential consequences for seedling regeneration processes and hence forest structure and composition.

Dipterocarps dominate the canopy of lowland tropical rain forest in South-east Asia. Seedlings of these species form diverse assemblages on the forest floor where low irradiance severely limits their growth. Further growth depends largely upon the increased irradiance that can occur with the creation of canopy gaps. However, the response of dipterocarp seedlings to increased irradiance and their subsequent establishment in the canopy may be influenced by the availability of other resources, such as nutrient availability. We investigated the influence of nitrogen supply on aspects of the photosynthetic physiology and growth of seedlings of four dipterocarp species (Shorea leprosula, Shorea johorensis, Shorea oleosa and Dryobalanops lanceolata) growing under low irradiance, during transfer from low to high irradiance, and during subsequent growth at high irradiance. All four species increased growth and photosynthetic capacity in response to N-supply at high irradiances but not at low irradiance approximating that which can be expected to occur in the forest understorey. When seedlings grown at low irradiances and varying N-supply were exposed to a large increase in irradiance, all species showed some degree of initial photodamage (measured through chlorophyll fluorescence), the extent of which was similar between species but differed markedly depending on the pre-exposure growth irradiance and N-supply. Greater photodamage occurred in seedlings grown at lower compared with higher N-supply and irradiance. Despite these initial difference in the extent of this photodamage, all seedlings demonstrated a similar capacity to recover from damage. However, the alterations in the photosynthetic physiology of leaves during this recovery differed between species and depended on N-supply. Under high N-supply all species apart from S. oleosa increased photosynthetic capacity per unit chlorophyll following exposure to high irradiance by increasing photosynthetic capacity per unit leaf area while, under low N-supply, an increase in photosynthetic capacity per unit leaf only occurred in D. lanceolata. Our results suggest that variations in N-availability may have a much greater impact on the relative competitiveness of dipterocarp seedlings during the regenerative phase following canopy gap formation than physiological differences between seedlings. Our results demonstrate a potentially significant role for N-availability in the regeneration dynamics and distribution of canopy-dominating dipterocarp species.

Interspecific ecophysiological differences in response to different light environments are important to consider in regeneration behavior and forest dynamics. The diurnal changes in leaf gas exchange and chlorophyll fluorescence of two dipterocarps, Shorea leprosula (a high light-requiring) and Neobalanocarpus heimii (a low light-requiring), and a pioneer tree species (Macaranga gigantea) growing in open and gap sites were examined. In the open site, the maximum net photosynthetic rate (Pn), photosystem II (PSII) quantum yield (δ; F/Fm′), and relative electron transport rate (r-ETR) through PSII at a given photosynthetic photon flux density (PPFD) was higher in S. leprosula and M. gigantea than in N. heimii, while non-photochemical quenching (NPQ) at a given PPFD was higher in N. heimii. The maximum values of net photosynthetic rate (Pn) in M. gigantea and S. leprosula was higher in the open site (8–11 μmol m−2 s−1) than in the gap site (5 μmol m−2 s−1), whereas that in N. heimii was lower in the open site (2 μmol m−2 s−1) than in the gap site (4 μmol m−2 s−1), indicating that N. heimii was less favorable to the open site. These data provide evidence to support the hypothesis that ecophysiological characteristics link with plant’s regeneration behavior and successional status. Although Pn and stomatal conductance decreased at midday in M. gigantea and S. leprosula in the open site, both r-ETR and leaf temperature remained unchanged. This indicates that stomatal closure rather than reduced photochemical capacity limited Pn in the daytime. Conversely, there was reduced r-ETR under high PPFD conditions in N. heimii in the open site, indicating reduced photochemical capacity. In the gap site, Pn increased in all leaves in the morning before exposure to direct sunlight, suggesting a relatively high use of diffuse light in the morning.

summary The development of mycorrhizal infection on seedlings of the dipterocarp. Shorea leprosula (Miq.). was followed for 7 months after germination at three sites in West Malaysia. Arbuscular mycorrhizal infection was not observed, Seedling roots had well-developed ectomycorrhizal sheaths, but no Hartig net, 20 d after germination, i.e. before the leaves had formed. By 2 months a range of ectomycorrhizal types with well-developed Hartig nets were present. Twenty-three types were recognized, of which 15 were common to alt three sites, and 20 to two sites. Individual seedlings never had more than five types and normally had line or two types only. The majority of ectomycorrhizas were formed by relatively few fungi and the six most abundant types at each site accounted for 77–92%, of the mycorrhizas. On the basis of the frequency of types (i.e. number of seedlings having mycorrhizas of a given type), and the number of times that a type contributed more than 40% of the mycorrhizas on a given seedling it was possible to recognize group of 12 dominant types. At each site new types were encountered at each harvest, and the number of types per harvest also increased. As well as fungi entering the mycorrhizal community as time progressed there was clear evidence that some fungi were lost or declined in relative abundance. Over the study period the level of infection fell at the two sites at which it was initially greatest. Although the community of mycorrhizal fungi was broadly similar at all three sites, overall level of infection, total number of types and number of types per seedling were highest at the site which appeared to have experienced the least disturbance and at which there were the greatest number of adult S. Ieprosula trees.