An ecological transcriptome approach to capture the molecular and physiological mechanisms of mass flowering in Shorea curtisii.

Climatic factors have commonly been attributed as the trigger of general flowering, a unique community-level mass flowering phenomenon involving most dipterocarp species that forms the foundation of Southeast Asian tropical rainforests. This intriguing flowering event is often succeeded by mast fruiting, which provides a temporary yet substantial burst of food resources for animals, particularly frugivores. However, the physiological mechanism that triggers general flowering, particularly in dipterocarp species, is not well understood largely due to its irregular and unpredictable occurrences in the tall and dense forests. To shed light on this mechanism, we employed ecological transcriptomic analyses on an RNA-seq dataset of a general flowering species, Shorea curtisii (Dipterocarpaceae), sequenced from leaves and buds collected at multiple vegetative and flowering phenological stages. We assembled 64,219 unigenes from the transcriptome of which 1,730 and 3,559 were differentially expressed in the leaf and the bud, respectively. Differentially expressed unigene clusters were found to be enriched with homologs of Arabidopsis thaliana genes associated with response to biotic and abiotic stresses, nutrient level, and hormonal treatments. When combined with rainfall data, our transcriptome data reveals that the trees were responding to a brief period of drought prior to the elevated expression of key floral promoters and followed by differential expression of unigenes that indicates physiological changes associated with the transition from vegetative to reproductive stages. Our study is timely for a representative general flowering dipterocarp species that occurs in forests that are under the constant threat of deforestation and climate change as it pinpoints important climate sensitive and flowering-related homologs and offers a glimpse into the cascade of gene expression before and after the onset of floral initiation.

Attitudes and preferences of wildlife and their relationship with childhood nature experience amongst residents in a tropical urban city.

How people relate to biodiversity and whether they are supportive of conservation programs and policies has implications on global and local biodiversity conservation efforts. Nature experiences in childhood has been shown to be strongly correlated to positive attitudes towards nature and wildlife in adulthood. In this study, we examined wildlife experience, attitudes and willingness to coexist with 26 vertebrates and invertebrates amongst residents in a highly urbanized tropical city, Singapore. A total of 1004 respondents were surveyed and their childhood nature experience and various socioeconomic variables were obtained. The animals were grouped by their likeability and preferred habitat from the respondents' answers. Three main groups of animals were discerned - unfavorable animals, mammals, and favorable animals. Singapore residents generally had high direct experiences of animals that are common in urban settings, for both favorable and unfavorable animals, such as butterflies, dragonflies, crows and bees, but low direct experiences of forest-dependent wildlife. Animals that were well-liked and acceptable near homes include the common urban ones and some forest-dependent ones, while animals that were disliked included stinging insects (bees and hornets) and reptiles (snakes and water monitors). Structured equation modelling showed that both childhood nature experience and wildlife experience had strong effects on wildlife likeability and habitat preference. The apparent mismatch between greening policies and people's willingness to coexist with wildlife may be problematic as urban development further encroaches on forest habitats, and this study highlights the importance of preserving forest habitats so that young children and adults have opportunities to be exposed to them. Supplementary Information: The online version contains supplementary material available at 10.1007/s11252-022-01280-1.

Impacts of climate change on reproductive phenology in tropical rainforests of Southeast Asia.

In humid forests in Southeast Asia, many species from dozens of plant families flower gregariously and fruit synchronously at irregular multi-year intervals1-4. Little is known about how climate change will impact these community-wide mass reproductive events. Here, we perform a comprehensive analysis of reproductive phenology and its environmental drivers based on a monthly reproductive phenology record from 210 species in 41 families in Peninsular Malaysia. We find that the proportion of flowering and fruiting species decreased from 1976 to 2010. Using a phenology model, we find that 57% of species in the Dipterocarpaceae family respond to both drought and low-temperature cues for flowering. We show that low-temperature flowering cues will become less available in the future in the RCP2.6 and 8.5 scenarios, leading to decreased flowering opportunities of these species in a wide region from Thailand to the island of Borneo. Our results highlight the vulnerability of and variability in phenological responses across species in tropical ecosystems that differ from temperate and boreal biomes.

Distance- and density-dependent leaf dynamics of seedlings of a tropical rainforest tree.

Parental distance and plant density dependence of seedling leaf turnover and survival was examined to investigate predictions of the Janzen-Connell hypothesis. The focal study species, Shorea macroptera is a canopy tree species in a lowland rain forest in peninsular Malaysia. We found that the peak of the distribution of plants shifted from 3-6 m to 6-9 m during the course of the change from seedling to sapling stage. The leaf demography of the seedlings was influenced by their distance from the adult tree and also by the seedling density. Although significant density- and distance dependence in leaf production was not detected, seedling leaf loss decreased with distance from the parent tree and with seedling density. Similarly, leaf damage was not found to be distance- or density-dependent, but net leaf gain of seedlings increased with distance from the parent tree. Although no significant distance- or density-dependence was evident in terms of leaf damage, significant distance dependence of the net leaf gain was found. Thus, we concluded that positive distance dependence in the leaf turnover of seedlings may gradually contribute to a shift in the distribution pattern of the progeny through reductions in growth and survivorship.

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.

Effects of childhood experience with nature on tolerance of urban residents toward hornets and wild boars in Japan.

Urban biodiversity conservation often aims to promote the quality of life for urban residents by providing ecosystem services as well as habitats for diverse wildlife. However, biodiversity inevitably brings some disadvantages, including problems and nuisances caused by wildlife. Although some studies have reported that enhancement of nature interaction among urban children promotes their affective attitude toward of favorable animals, its effect on tolerance toward problem-causing wildlife is unknown. In this study, we assessed the tolerance of 1,030 urban residents in Japan toward hornets and wild boar, and analyzed the effects of childhood experience with nature on tolerance using a structural equation model. The model used sociodemographic factors and childhood nature experience as explanatory variables, affective attitude toward these animals as a mediator, and tolerance as a response variable. The public tolerance toward hornets and boars was low; over 60% of the respondents would request the removal of hornets and wild boar from nearby green spaces by government services, even when the animals had not caused any damage. Tolerance was lower in females and elderly respondents. Childhood experience with nature had a greater influence on tolerance than did sociodemographic factors in the scenario where animals have not caused any problems; however, its effect was only indirect via promoting positive affective attitude toward wildlife when the animals have caused problems. Our results suggest that increasing people's direct experience with nature is important to raise public tolerance, but its effect is limited to cases where wildlife does not cause any problems. To obtain wider support for conservation in urban areas, conservationists, working together with municipal officials, educators and the media, should provide relevant information on the ecological functions performed by problem-causing wildlife and strategies for avoiding the problems that wildlife can cause.

Spatiotemporal dynamics of urban green spaces and human-wildlife conflicts in Tokyo.

Although urban green spaces are increasingly important both for humans and wildlife, an increase in urban green spaces may also increase human-wildlife conflicts in urban areas. However, few studies have examined the relationship between the size of green spaces and the level of conflicts with wildlife in multiple taxa, including invertebrates and vertebrates. To better understand current pest statistics and predict changes that will occur as the area of green spaces increases, we analysed a dataset compiling the number of pest consultations in 53 metropolitan districts in Tokyo over a 20-year period and its relationships with the area of green space. Stinging insects (e.g., wasps) made up over 50% of pest consultations, followed (in order) by rats and other nuisance animals (e.g., snakes). The number of consultations per unit population did not correlate, or was even negatively correlated, with the proportions of green spaces (mainly forest) for many indoor pests, but did positively correlate for some outdoor pests, such as wasps and snakes. Therefore, wasps and snakes can increase when urban green spaces increase. Because even minor nuisances are relevant for urban lifestyles, considerations of ways to minimise conflicts with wildlife are critical for urban green space management.

Satellite-based characterization of climatic conditions before large-scale general flowering events in Peninsular Malaysia.

General flowering (GF) is a unique phenomenon wherein, at irregular intervals, taxonomically diverse trees in Southeast Asian dipterocarp forests synchronize their reproduction at the community level. Triggers of GF, including drought and low minimum temperatures a few months previously has been limitedly observed across large regional scales due to lack of meteorological stations. Here, we aim to identify the climatic conditions that trigger large-scale GF in Peninsular Malaysia using satellite sensors, Tropical Rainfall Measuring Mission (TRMM) and Moderate Resolution Imaging Spectroradiometer (MODIS), to evaluate the climatic conditions of focal forests. We observed antecedent drought, low temperature and high photosynthetic radiation conditions before large-scale GF events, suggesting that large-scale GF events could be triggered by these factors. In contrast, we found higher-magnitude GF in forests where lower precipitation preceded large-scale GF events. GF magnitude was also negatively influenced by land surface temperature (LST) for a large-scale GF event. Therefore, we suggest that spatial extent of drought may be related to that of GF forests, and that the spatial pattern of LST may be related to that of GF occurrence. With significant new findings and other results that were consistent with previous research we clarified complicated environmental correlates with the GF phenomenon.

Geographical pattern and environmental correlates of regional-scale general flowering in Peninsular Malaysia.

In South-East Asian dipterocarp forests, many trees synchronize their reproduction at the community level, but irregularly, in a phenomenon known as general flowering (GF). Several proximate cues have been proposed as triggers for the synchronization of Southeast Asian GF, but the debate continues, as many studies have not considered geographical variation in climate and flora. We hypothesized that the spatial pattern of GF forests is explained by previously proposed climatic cues if there are common cues for GF among regions. During the study, GF episodes occurred every year, but the spatial occurrence varied considerably from just a few forests to the whole of Peninsular Malaysia. In 2001, 2002 and 2005, minor and major GF occurred widely throughout Peninsular Malaysia (GF2001, GF2002, and GF2005), and the geographical patterns of GF varied between the episodes. In the three regional-scale GF episodes, most major events occurred in regions where prolonged drought (PD) had been recorded prior, and significant associations between GF scores and PD were found in GF2001 and GF2002. However, the frequency of PD was higher than that of GF throughout the peninsula. In contrast, low temperature (LT) was observed during the study period only before GF2002 and GF2005, but there was no clear spatial relationship between GF and LT in the regional-scale episodes. There was also no evidence that last GF condition influenced the magnitude of GF. Thus, our results suggest that PD would be essential to trigger regional-scale GF in the peninsula, but also that PD does not fully explain the spatial and temporal patterns of GF. The coarse relationships between GF and the proposed climatic cues may be due to the geographical variation in proximate cues for GF, and the climatic and floristic geographical variations should be considered to understand the proximate factors of GF.

Non-density dependent pollen dispersal of Shorea maxwelliana (Dipterocarpaceae) revealed by a Bayesian mating model based on paternity analysis in two synchronized flowering seasons.

Pollinator syndrome is one of the most important determinants regulating pollen dispersal in tropical tree species. It has been widely accepted that the reproduction of tropical forest species, especially dipterocarps that rely on insects with weak flight for their pollination, is positively density-dependent. However differences in pollinator syndrome should affect pollen dispersal patterns and, consequently, influence genetic diversity via the mating process. We examined the pollen dispersal pattern and mating system of Shorea maxwelliana, the flowers of which are larger than those of Shorea species belonging to section Mutica which are thought to be pollinated by thrips (weak flyers). A Bayesian mating model based on the paternity of seeds collected from mother trees during sporadic and mass flowering events revealed that the estimated pollen dispersal kernel and average pollen dispersal distance were similar for both flowering events. This evidence suggests that the putative pollinators - small beetles and weevils - effectively contribute to pollen dispersal and help to maintain a high outcrossing rate even during sporadic flowering events. However, the reduction in pollen donors during a sporadic event results in a reduction in effective pollen donors, which should lead to lower genetic diversity in the next generation derived from seeds produced during such an event. Although sporadic flowering has been considered less effective for outcrossing in Shorea species that depend on thrips for their pollination, effective pollen dispersal by the small beetles and weevils ensures outcrossing during periods of low flowering tree density, as occurs in a sporadic flowering event.

Paternity analysis-based inference of pollen dispersal patterns, male fecundity variation, and influence of flowering tree density and general flowering magnitude in two dipterocarp species.

BACKGROUND AND AIMS: Knowledge of pollen dispersal patterns and variation of fecundity is essential to understanding plant evolutionary processes and to formulating strategies to conserve forest genetic resources. Nevertheless, the pollen dispersal pattern of dipterocarp, main canopy tree species in palaeo-tropical forest remains unclear, and flowering intensity variation in the field suggests heterogeneity of fecundity. METHODS: Pollen dispersal patterns and male fecundity variation of Shorea leprosula and Shorea parvifolia ssp. parvifolia on Peninsular Malaysian were investigated during two general flowering seasons (2001 and 2002), using a neighbourhood model modified by including terms accounting for variation in male fecundity among individual trees to express heterogeneity in flowering. KEY RESULTS: The pollen dispersal patterns of the two dipterocarp species were affected by differences in conspecific tree flowering density, and reductions in conspecific tree flowering density led to an increased selfing rate. Active pollen dispersal and a larger number of effective paternal parents were observed for both species in the season of greater magnitude of general flowering (2002). CONCLUSIONS: The magnitude of general flowering, male fecundity variation, and distance between pollen donors and mother trees should be taken into account when attempting to predict the effects of management practices on the self-fertilization and genetic structure of key tree species in tropical forest, and also the sustainability of possible management strategies, especially selective logging regimes.

Growth strategies differentiate the spatial patterns of 11 dipterocarp species coexisting in a Malaysian tropical rain forest.

We examined relationships between mortality rate, relative growth rate (RGR), and spatial patterns of three growth stages (small, medium, and large trees) for 11 dipterocarp species in the Pasoh 50-ha plot. Mortality rates for these species tended to be positively correlated with RGRs, although the correlation was significant only at the small-tree stage. Seven species with high growth and mortality rates exhibited peaks in spatial aggregation at small distances (<100 m) in small trees, but this aggregation disappeared in medium and large trees. In contrast, the other four species with low growth and mortality rates aggregated at large distances (>200 m) throughout the three growth stages in all but one species. Negative associations between different growth stages were observed only for the high-mortality species, suggesting density-dependent mortality. The high-mortality species showed habitat associations with topography, soil type, and the forest regeneration phase after gap formation, whereas the three low-mortality species only had associations with the forest regeneration phase. A randomization procedure revealed that these habitat associations explained little of their spatial aggregation. Our results suggest that the growth strategy has a large effect on the structuring of the spatial distribution of tree species through mortality processes.

Size-related flowering and fecundity in the tropical canopy tree species, Shorea acuminata (Dipterocarpaceae) during two consecutive general flowerings.

We monitored the reproductive status of all trees with diameters at breast height (dbh) >30 cm in a 40-ha plot at Pasoh, west Malaysia, and investigated the individual fecundity of 15 Shorea acuminata Dyer (Dipterocarpaceae) trees using seed-trapping methods during two consecutive general flowering periods in 2001 (GF2001) and 2002 (GF2002). The proportion of flowering trees was higher, and not dependent on size, in GF2002 (84.2%), than in GF2001 (54.5%), when flowering mainly occurred in trees with a dbh < or =70 cm. Fecundity parameters of individual trees per event varied widely (221,000-35,200,000 flowers, 0-139,000 mature seeds, and 1.04-177 kg total dry matter mass of fruit (TDM) per tree). Monotonic increases with increasing tree size were observed for flower production and TDM amongst trees up to 90 cm in dbh, but not for mature seed production or for any of these parameters amongst larger trees. The pattern of reproductive investment during the two consecutive reproductive events clearly differed between medium-sized and large trees; the former concentrated their reproductive investment in one of the reproductive events whereas the latter allocated their investment more evenly to both reproductive events. Our results suggest size-related differences in the resource allocation pattern for reproduction.

Delayed greening, leaf expansion, and damage to sympatric Shorea species in a lowland rain forest.

The function of delayed greening in the seedlings of canopy tree species in a lowland tropical rain forest was examined in terms of its potential defensive value against herbivory. To explore the ecological and evolutionary backgrounds for delayed greening, we chose eight sympatric congeneric (Shorea) dipterocarp species that were either normal-greening or delayed-greening species. Expansion and toughening of leaves took approximately 30 days for all species, and did not differ between the normal- and delayed-greening species. The main factors that affected leaf damage during expansion were insect herbivory and fungal infection. Levels of leaf damage were significantly lower for delayed-greening species than for normal-greening species, but proportions of heavily damaged leaves and leaf abscission during expansion did not differ. In addition, no significant difference was found in damage levels on leaves (aged 1-2 months) of naturally occurring seedlings between normal- and delayed-greening species. Therefore, delayed greening may effectively reduce the level of leaf damage in young expanding leaves, but may not necessarily reduce leaf abscission and damage to mature leaves. The existence of delayed greening could not be simply explained by the phylogenetic and ecological backgrounds of the trees. Consequently, delayed greening may have a function in reducing damage during expansion, but more information (such as knowledge of the secondary metabolites involved in this phenomenon) is needed to explain fully why these species exhibit delayed greening.

Temporal and spatial patterns of mass flowerings on the Malay Peninsula.

We propose a hypothesis to explain the temporal and spatial patterns of mass flowerings in dipterocarp tree species on the Malay Peninsula. The literature on these mass flowerings reveals that during 1980-2002 at least 11 flowerings occurred at irregular intervals of 1-6 yr in a lowland rain forest. Five of them were typical mass flowerings-a high density of flowering trees and the characteristic sequential flowering of Shorea species. The 11 flowerings were classified into two flowering times: spring and autumn. There is evidence that low temperature and drought triggered the flowerings. Therefore, the seasonality of mass flowerings is characterized by the annual patterns of rainfall and low temperature. In addition, changes in El Niño-Southern Oscillation (ENSO) may play important roles in determining the supra-annual occurrence of mass flowerings. Flowering surveys on the Malay Peninsula implied that regions with spring or autumn mass flowerings corresponded geographically to those regions that had one cool season (December-February) or two (December-February and June-August), respectively. This finding anticipates the seasonal pattern and geographical distribution of mass flowerings on the Malay Peninsula.