Fragmentation Genetics of Vateria indica: implications for management of forest genetic resources of an endemic dipterocarp

Tropical agro-forest landscapes are potentially valuable reserves of forest genetic resources for forestry and restoration of degraded forests. The Dipterocarpaceae is a dominant Southeast Asian family of tree species of global significance for the tropical timber industry. Very little information exists about how effective human modified landscapes are for conserving genetic diversity in dipterocarp species. This study provides a baseline for understanding how fragmented agro-forest landscapes in India sustain forest genetic resources in an endemic dipterocarp tree. We compare genetic diversity and fine-scale spatial genetic structure (FSGS) in the threatened tree species Vateria indica within an isolated and a continuous forest site in the Western Ghats, South India. We place these results in the context of dipterocarps from both the Seychelles and Borneo. Parentage analysis of 694 progeny using twelve nuclear microsatellite markers is applied to estimate pollen and seed dispersal. Using a nursery trial we evaluate effects of inbreeding on growth performance. Our results show that levels of FSGS, and gene dispersal are comparable between a small isolated and a large continuous site of V. indica. Realized long-distance pollen flow into the isolated patch appears to help maintaining genetic diversity. The nursery experiment suggests that selection favours outbred progeny. Individuals of V. indica in close proximity appear less related to each other than in another highly fragmented and endangered dipterocarp species from the Seychelles, but more related than in three dipterocarp species studied in continuous forest in Borneo. We discuss the wider implications of our findings in the context of conservation and restoration of dipterocarp forest genetic resources in fragmented populations.     

西双版纳龙脑香林与热带亚洲和中国热带北缘地区植物区系的关系

西双版纳龙脑香林只有与热带亚洲的龙脑香林完全一致的植物科的组成,绝大多数的属也与后者共有,特别是在乔木层的区系组成和数量特征上,二者很类似,表明西双版纳龙脑香林在植物区系性质上归属于热带亚洲龙脑香林,但为后者的一种北缘类型。与中国热带边缘地区的其它一些森林类型相比,西双版纳龙脑香林亦具有与它们基本一致的科的组成,但无论按在群落中的种数,按占科的世界区系百分比,还是按重要值指数,西双版纳龙脑香林中热带科均占有显著地位,并且包含有较高比例的热带亚洲分布属和种,故可认为它是中国热带北缘地区的森林类型中热带性强,在区系组成上接近热带亚洲龙脑香林而作为后者的一个部分的森林类型。     

Ecological considerations for using dipterocarps for restoration of lowland rainforest in Southeast Asia

The lowland dipterocarp forests of Southeast Asia support a substantial proportion of the world’s biodiversity. They are of considerable environmental and economic value at the local, regional and global scale, providing many goods and services to a growing population. The forests of this region are among the fastest disappearing in the world and restoration is urgently required. This paper provides a review of the ecological constraints to restoration of lowland dipterocarp forest in Southeast Asia. It focuses on the production of planting stock, the significance of site-species matching and post-planting site maintenance. It identifies gaps in our knowledge and highlights priority areas of research. Adopting a long-term view is essential for restoring as well as conserving the dipterocarp forests of Southeast Asia. An immediate strategy for the conservation and management of dwindling genetic resources of these important timber species is essential. This will provide the foundations for sourcing seed and production of planting material for longer term restoration. The importance of species-site matching, mycorrhizal fungi and post-planting maintenance for restoration are apparent. Financing is a major limiting factor to dipterocarp forest restoration. Trading in carbon, private finance and environmental markets afford considerable opportunities for restoring these forests providing their total value is recognised. Despite the wealth of ecological knowledge we already have for scientifically-informed forest restoration, without the backing of governments and corporate stakeholders, forest restoration will not gain the urgently required momentum.     

Predicting the terminal velocity of dipterocarp fruit

We measured the terminal velocity of helicopter‐like fruit from the Dipterocarpaceae family and present a model predicting the terminal velocities for all dipterocarp species in the Malesiana region. A ballistic model of seed dispersal using the observed terminal velocities predicted dispersal distances of 17–77 m under normal atmospheric conditions. These data are of applied use in parametizing models of species coexistence, forest regeneration and habitat connectivity in Southeast Asian tropical forests.     

Contrasting Diversity and Host Association of Ectomycorrhizal Basidiomycetes versus Root-Associated Ascomycetes in a Dipterocarp Rainforest

Root-associated fungi, including ectomycorrhizal and root-endophytic fungi, are among the most diverse and important belowground plant symbionts in dipterocarp rainforests. Our study aimed to reveal the biodiversity, host association, and community structure of ectomycorrhizal Basidiomycota and root-associated Ascomycota (including root-endophytic Ascomycota) in a lowland dipterocarp rainforest in Southeast Asia. The host plant chloroplast ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit (rbcL) region and fungal internal transcribed spacer 2 (ITS2) region were sequenced using tag-encoded, massively parallel 454 pyrosequencing to identify host plant and root-associated fungal taxa in root samples. In total, 1245 ascomycetous and 127 putative ectomycorrhizal basidiomycetous taxa were detected from 442 root samples. The putative ectomycorrhizal Basidiomycota were likely to be associated with closely related dipterocarp taxa to greater or lesser extents, whereas host association patterns of the root-associated Ascomycota were much less distinct. The community structure of the putative ectomycorrhizal Basidiomycota was possibly more influenced by host genetic distances than was that of the root-associated Ascomycota. This study also indicated that in dipterocarp rainforests, root-associated Ascomycota were characterized by high biodiversity and indistinct host association patterns, whereas ectomycorrhizal Basidiomycota showed less biodiversity and a strong host phylogenetic preference for dipterocarp trees. Our findings lead to the working hypothesis that root-associated Ascomycota, which might be mainly represented by root-endophytic fungi, have biodiversity hotspots in the tropics, whereas biodiversity of ectomycorrhizal Basidiomycota increases with host genetic diversity.     

Growth and survivorship of dipterocarp seedlings: differences in shade persistence create a special case of dispersal limitation

A series of growth experiments and observations on natural populations have been carried out on dipterocarp species of contrasting ecology growing in artificial gaps and the forest understorey. These studies have demonstrated that although differences exist between species in photosynthetic and growth responses to the high-light environment, competition for light in canopy gaps is highly asymmetrical and tends to reinforce any pre-existing dominance hierarchy. We propose that differences in seedling persistence in forest canopy shade are highly influenced by species-specific biotic and abiotic interactions. Our experiments suggest that as seedlings, dipterocarp species trade off traits which enhance persistence and growth in shade against those that enhance their ability to exploit gaps. Less competitive species survive for progressively longer periods of time after a gregarious fruiting event. This leads to significant shifts with time in the number of species present in the seedling bank and hence in the importance of interspecific competition in determining which species dominates regrowth in gaps. We propose that this special case of dispersal limitation is more likely to account for coexistence of dipterocarp species than differences in growth responses to gaps of different size, with stochastic and environmental variables interacting to determine species distribution and abundance.     

Tree Leaf Form in Brunei: A Heath Forest and a Mixed Dipterocarp Forest Compared1

Canopy‐top leaves of the dominant tree species from two 0.96‐ha plots in Brunei, northern Borneo, were sampled for structural and chemical analysis. Thirteen species from the mixed dipterocarp forest at Andulau and 14 from the lowland heath forest at Badas were studied. The heath‐forest species had significantly thicker leaves and were lower in nitrogen and ash concentration than those from the mixed dipterocarp forest. There were no significant differences between the two species groups in leaf mass per unit area (LMA), leaf fracture toughness, carbon concentration, 8¹³C, neutral detergent fiber concentration, sclerophylly index, and stomatal density. A significant negative correlation between %C and 8¹³C was found for the species from the mixed dipterocarp forest, but not those from the heath forest. The degree of sclerophylly measured in physical terms overlapped between the two sites to a considerable degree; however, all six species tested that were present in both plots had higher leaf fracture toughness in the heath forest. The possible reasons for the marked sclerophylly in the mixed dipterocarp forest are discussed.     

Habitat Associations and Community Structure of Dipterocarps in Response to Environment and Soil Conditions in Brunei Darussalam,Northwest Borneo

Plant habitat associations are well documented in Bornean lowland tropical forests, but few studies contrast the prevalence of associations across sites. We examined habitat associations and community composition of Dipterocarpaceae trees in two contrasting Bornean lowland mixed dipterocarp forests separated by approximately 100 km: Andulau (uniform topography, lower altitudinal range, sandy soils) and Belalong (highly dissected topography, higher altitudinal range, clay‐rich soils). Dipterocarpaceae trees ≥ 1 cm diameter at breast height (dbh) were censused in 20‐m wide belt transects established along topographic gradients at each site. Dipterocarp density, evenness, species richness, and diversity were significantly higher at Andulau than Belalong. Significant site associations (with either Andulau or Belalong) were detected for 19 (52%) of the 37 dipterocarp species tested. Dipterocarpaceae community composition at Belalong correlated with soil nutrient concentrations as well as measures of vegetation and topographic structure, but community composition at Andulau correlated with fewer habitat variables. Within each site, dipterocarp density, species richness, and diversity were consistently higher on ridges than in slopes and valleys. Significant within‐site associations to topographic habitats were less common at Andulau (10% of species tested) than at Belalong (15%). We conclude that edaphic and other environmental factors influence dipterocarp community composition at a local scale, and are more important drivers of community structure in the more variable environment at Belalong. Species richness and diversity of dipterocarps on small plots, however, were higher at Andulau, suggesting that factors other than environmental heterogeneity contribute to contrasts in dipterocarp tree species richness at small scales.     

Wood and bark anatomy of Muntingiaceae: A phylogenetic comparison within Malvales s. l.

Quantitative and qualitative data on wood and bark anatomy are given for Muntingia calabura L. and Dicraspidia donnell-smithii Standley. These data are compared with phylogenetic schemes, based on DNA analysis, in which Muntingiaceae belong to the “dipterocarp clade” within Malvales. The data are consistent with this hypothesis, although Muntingiaceae lack pit vestures in vessels, which are seen in the other malvalean families (Cistaceae, Dipterocarpaceae, Neuradaceae, Sarcolaenaceae, Thymeleaceae), and this may represent a loss of pit vestures. All families of the dipterocarp clade agree with both genera of Muntingiaceae in having tracheids as the imperforate tracheary element type (at least ancestrally), although fiber-tracheids also occur in some Dipterocarpaceae and Thymeleaceae. The large size of some malvalean families (with attendant greater diversity in character states) and a paucity of wood studies in those families make for difficulty in comparison of features such as axial parenchyma and ray types with those of Muntingiaceae; character states of these features are consistent with placement of Muntingiaceae in the dipterocarp clade of Malvales. Banded phloem fibers in bark of Muntingiaceae are much like those of other Malvales. Wood of Muntingiaceae is highly mesomorphic according to quantitative vessel features.     

Terpenoid Compositions and Botanical Origins of Late Cretaceous and Miocene Amber from China

The terpenoid compositions of the Late Cretaceous Xixia amber from Central China and the middle Miocene Zhangpu amber from Southeast China were analyzed by gas chromatography-mass spectrometry (GC-MS) to elucidate their botanical origins. The Xixia amber is characterized by sesquiterpenoids, abietane and phyllocladane type diterpenoids, but lacks phenolic abietanes and labdane derivatives. The molecular compositions indicate that the Xixia amber is most likely contributed by the conifer family Araucariaceae, which is today distributed primarily in the Southern Hemisphere, but widely occurred in the Northern Hemisphere during the Mesozoic according to paleobotanical evidence. The middle Miocene Zhangpu amber is characterized by amyrin and amyrone-based triterpenoids and cadalene-based sesquiterpenoids. It is considered derived from the tropical angiosperm family Dipterocarpaceae based on these compounds and the co-occurring fossil winged fruits of the family in Zhangpu. This provides new evidence for the occurrence of a dipterocarp forest in the middle Miocene of Southeast China. It is the first detailed biomarker study for amber from East Asia.     

Pollination biology in a lowland dipterocarp forest inSarawak, Malaysia. I. Characteristics of the plant-pollinator communityin a lowland dipterocarp forest

Flowerings and flower visitors were observed continuously in alowland dipterocarp forest in Sarawak, Malaysia, for 53 mo in1992-1996. Flower visitors of 270 plant species were observed orcollected, and pollinators were assessed by observing body contact tostigmas and anthers. We recognized 12 categories of pollination systems.Among them, plants pollinated by social bees included the largest numberof species (32%) and were followed by beetle-pollinated species(20%). Pollination systems were significantly related with somefloral characters (flowering time of day, reward, and floral shape), butnot with floral color. Based on the relationships between pollinatorsand floral characters, we described pollination syndromes found in alowland dipterocarp forest. The dominance of social bees and beetlesamong pollinators is discussed in relation to the general floweringobserved in dipterocarp forests of West Malesia. In spite of high plantspecies diversity and consequent low population densities of lowlanddipterocarp forests, long-distance-specific pollinators were uncommoncompared with theNeotropics.     

中国龙脑香科植物纪要

广义的龙脑香科是泛热带分布。中国有 5属 12种 ,其中 1种为引种栽培 ,产云南、广西、海南及西藏。本科分布北界在印度的喜马偕尔邦 ,在该地粗壮娑罗双Shorearobusta约达北纬 31°。《中国植物志》所报道见于我国的纤细龙脑香Dipterocarpusgracilis确实未见于我国。我国自然生长的东京龙脑香Dipterocarpusretusus依据毛被的多少可分为 2个变种 ,它们可能同时出现在同一林中。由于毛被多少不是区分种的可靠特征 ,因此将河内坡垒Hopeahongayanensis及多毛坡垒H mollissima两者都归并到狭叶坡垒H chinensis。鉴于雄蕊数目的不确定性 ,海南所产的Hopeaexalata与越南所产的H reticulata就视为同一种 ,而采用后者作为种名。版纳青梅Vaticaxishuangbannaensis与广西青梅V guangxiensis两者以叶脉数目来区分是不可靠的 ,也应视为同种而采用后者作为种名。经野外实地考察 ,望天树Parashoreachinensis仍应恢复其原来的学名。     

Photosynthetic characteristics of dipterocarp species planted on degraded sandy soils in southern Thailand

To elucidate whether dipterocarp species, dominant late-successional species of tropical forests in Southeast Asia, actually have a disadvantage when planted on open site in terms of their photosynthetic characteristics, we investigated photosynthesis in dipterocarp seedlings planted in the open on degraded sandy soils in southern Thailand. These species were compared with seedlings of Acacia mangium Willd., a fast-growing tropical leguminous tree, which is often planted on degraded open site in Southeast Asia. The dipterocarp seedlings had an irradiance-saturated net photosynthetic rate (P _N), stomatal conductance (g _s), carboxylation efficiency, and photosynthetic capacity comparable to or superior to those of A. mangium. In particular, seedlings of Dipterocarpus obtusifolius Teijsm. ex Miq. showed an irradian-ce-saturated P _N of 21 μmol m⁻² s⁻¹, a value higher than any previously reported for a dipterocarp species, accompanied by high g _s (0.7 mol m⁻² s⁻¹) and high photosynthetic capacity. Thus dipterocarp species do not necessarily have a disadvantage in terms of their photosynthetic characteristics on open sites with degraded sandy soils.     

龙脑香科植物AM真菌的初步研究

对我国云南和海南龙脑香科植物的天然原始林和人工林AM真菌资源进行了调查,对从46处龙脑香林采回的19种龙脑香科树种的根系和根际土壤样品,分别进行显微观察和分离AM真菌的孢子,发现在所调查的19个树种中,所有树种的根系都有不同程度的AM真菌的侵染,高者可达50%,平均为21%,其中在大多数根样中发现有泡囊生成;对土壤样品的分析,分离到大量的孢子,其孢子密度从7~132个/20ml土样不等,平均为58个。对所分离到的孢子进行鉴定,发现无梗囊霉属和球囊霉属的孢子占大多数,其频度和相对多度分别为33.25和46.89;18.04和30.80。研究结果表明,龙脑香科不仅仅能够形成外生菌根,而且也能象大多数热带林木一样能够广泛的形成丛枝菌根。     

Predicting dispersal of auto‐gyrating fruit in tropical trees: a case study from the Dipterocarpaceae

Seed dispersal governs the distribution of plant propagules in the landscape and hence forms the template on which density‐dependent processes act. Dispersal is therefore a vital component of many species coexistence and forest dynamics models and is of applied value in understanding forest regeneration. Research on the processes that facilitate forest regeneration and restoration is given further weight in the context of widespread loss and degradation of tropical forests, and provides impetus to improve estimates of seed dispersal for tropical forest trees. South‐East Asian lowland rainforests, which have been subject to severe degradation, are dominated by trees of the Dipterocarpaceae family which constitute over 40% of forest biomass. Dipterocarp dispersal is generally considered to be poor given their large, gyration‐dispersed fruits. However, there is wide variability in fruit size and morphology which we hypothesize mechanistically underpins dispersal potential through the lift provided to seeds mediated by the wings. We explored experimentally how the ratio of fruit wing area to mass (“inverse wing loading,” IWL) explains variation in seed dispersal kernels among 13 dipterocarp species by releasing fruit from a canopy tower. Horizontal seed dispersal distances increased with IWL, especially at high wind speeds. Seed dispersal of all species was predominantly local, with 90% of seed dispersing <10 m, although maximum dispersal distances varied widely among species. We present a generic seed dispersal model for dipterocarps based on attributes of seed morphology and provide modeled seed dispersal kernels for all dipterocarp species with IWLs of 1–50, representing 75% of species in Borneo.     

A Revised Conservation Assessment of Dipterocarps in Sabah

Borneo has experienced a rapid decline in the extent of forest cover, which has reduced the amount of habitat available for many plant and animal species. The precise impact of habitat loss on the conservation status of dipterocarp trees is uncertain. We use three contrasting techniques, the extent of occurrence, area of occupancy and ecological niche models derived using maxent , in conjunction with a current land‐use map of Sabah, to derive estimates of habitat loss and infer a regional IUCN Red List conservation status for 33 Sabah dipterocarp species. Estimates of habitat loss differed significantly according to the methods employed and between species on different habitat types. Proportion of habitat loss determined from the ecological niche models varied from 21 percent for Shorea micans to 99.5 percent for Dipterocarpus lamellatus. Thirty‐two of the 33 dipterocarp species analyzed in this study would have their Sabah populations classified as Threatened (equal to a habitat loss of > 30%) under the A2 IUCN Red List criterion. Dipterocarps that occur in lowland forests have experienced greater habitat loss than upland/lower montane or ultramafic species. In addition, species with the lowest predicted area within their historic distributions had the highest proportion of habitat lost, which provides a rationale for targeting conservation effort on the species with narrow distributions. We recommend the ecological niche modeling approach as a rapid assessment tool for reconstructing species’ historic distributions during conservation assessments of tropical trees.     

A Comparison of the Soil Water,Nutrient Status,and Litterfall Characteristics of Tropical Heath and Mixed‐Dipterocarp Forest Sites in Brunei1

Two of the main hypotheses to explain the distribution and special characteristics of tropical heath forest are nutrient and water limitation. A study was undertaken to investigate both factors on two sites under tropical heath forest (Badas Forest Reserve) and mixed‐dipterocarp forest (Andulau Forest Reserve) in Brunei. Soil water potentials were monitored at depths of 20, 50, and 90 cm over wet and dry periods for five months at each site. The results showed the mixed‐dipterocarp forest site to be drier at 50 cm depth compared to the tropical heath forest site. There was no significant difference in water potentials between sites at 20 or 90 cm. Nutrient concentrations in the soil solution were monitored at the same depths over a seven‐month period at the same sites. A 12‐month litterfall study was also undertaken to monitor nutrient returns from the canopy at each site. The results of both studies suggest that the tropical heath forest site is poorer in nitrogen, but richer in calcium, than the mixed‐dipterocarp forest site. The results for phosphorus are less clear, but do not suggest that its limitation is a significant factor at the tropical heath forest site compared to the mixed‐dipterocarp forest site. Phosphorus and magnesium concentrations in the soil solution showed a strong positive correlation with sliding 30‐day rainfall totals at both sites.     

Ectomycorrhizal fungi of the Philippines: a preliminary survey and notes on the geographic biodiversity of the Sclerodermatales

Basidiomata of putative ectomycorrhizal fungi have been collected from under pine or dipterocarp stands in Central Luzon in the Philippines. Over 100 collections are reported. Among the material, 75 taxa have been recognised and assigned to known genera or at least placed close to already documented European, Japanese or North American taxa. Formal identifications for 46 species are given along with comments on previous collections from South-East Asia. Species collected from under the native Pinus kesiya resemble the communities found under three-needled pines in North America and the West Himalayas, whereas those from dipterocarp forests were similar to communities found in Malaysia and Japan. Members of the Sclerodermatales were particularly common and are probably the pioneer colonizers of young seedlings in these ecosystems.     

Differences in the fruit maturation stages at which oviposition occurs among insect seed predators feeding on the fruits of five dipterocarp tree species

The seeds of dipterocarp trees are the main food resources for many species of weevils, bark beetles and small moths; however, for most seed‐eating insects on dipterocarp tropical trees, seed utilization patterns remain poorly investigated. This study aimed to determine the fruit maturation stages at which eggs are laid by different insect seed predators feeding on the seeds or fruits of the following five dipterocarp species: Dipterocarpus globosus, Dryobalanops aromatica, Shorea beccariana, S. acuta and S. curtisii, which reproduced during the same period. We investigated the occurrence frequencies of the insect seed predators at various growth stages by collecting both unfallen and fallen fruit on several occasions during the period of seed/fruit maturation in a tropical rainforest in Borneo from September to December 2013. Weevils and bark beetles were the dominant insect seed predators of the five tree species. One or two weevil species of Alcidodes, Damnux and/or Nanophyes preyed on the seeds of each of the five tree species, and one bark beetle species, Coccotrypes gedeanus, preyed on the seeds of all five tree species. Many larvae, pupae and adults of each weevil species were found in pre‐dispersal (unfallen) fruit, whereas bark beetles at various growth stages were found in post‐dispersal (fallen) fruit. These results suggested that, among the dominant insect seed predators of the five dipterocarp species, weevil species oviposit on pre‐dispersal fruit and begin their larval growth before seed dispersal, whereas the oviposition and larval development of bark beetle species occurs in post‐dispersal fruit.     

Leaf litter decomposition rates in degraded and fragmented tropical rain forests of Borneo

Previously extensive tracts of primary rain forest have been degraded by human activities, and we examined how the effects of forest disturbance arising from habitat fragmentation and commercial selective logging affected ecosystem functioning in these habitats by studying leaf litter decomposition rates in litter bags placed on the forest floor. The rain forests of Borneo are dominated by trees from the family Dipterocarpaceae, and we compared leaf litter decomposition rates of three dipterocarp species at eight forest fragment sites (area 3–3529 ha) that had different histories of disturbance pre‐fragmentation: four fragments had been selectively logged prior to fragmentation and four had been formed from previously undisturbed forest. We compared these logged and unlogged forest fragments with sites in continuous forest that had been selectively logged (two sites) and fully protected and undisturbed (two sites). After 120 d, undisturbed continuous forest sites had the fastest rates of decomposition (52% mass loss). Forest fragments formed from unlogged forest (32% mass loss) had faster decomposition rates than logged forest fragments (28% mass loss), but slower rates than continuous logged forest (39% mass loss). Leaves of a light‐demanding species (Parashorea malaanonan) decomposed faster than those of a shade‐tolerant species (Hopea nervosa), but decomposition of all three dipterocarp species that we studied responded similarly to logging and fragmentation effects. Reduced decomposition rates in logged and fragmented forest sites may affect nutrient cycling and thus have detrimental consequences for forest regeneration. Conservation management to improve forest quality should be a priority, particularly in logged forest fragments.