Extrafloral nectaries in the genus Macaranga (Euphorbiaceae) in Malaysia: comparative studies of their possible significance as predispositions for myrmecophytism

Some species of the paleotropical tree genus Macaranga (Euphorbiaceae) live in close association with ants. The genus comprises the full range of species from those not regularly inhabited by ants to obligate myrmecophytes. In Malaysia (Peninsular and Borneo) 23 of the 52 species are known to be ant-associated (44%). The simplest structural adaptation of plants to attract ants are extrafloral nectaries. We studied the distribution of extrafloral nectaries in the genus Macaranga to assess the significance of this character as a possible predisposition for the evolution of obligate myrmecophytism. All species have marginal glands on the leaves. However, only the glands of non- myrmecophytic species function as nectaries, whereas liquids secreted by these glands in myrmecophytic species did not contain sugar. Some non-myrmecophytic Macaranga and transitional Macaranga species in addition have extrafloral nectaries on the leaf blade near the petiole insertion. All obligatorily myrmecophytic Macaranga species, however, lack additional glands on the lamina. The non-myrmecophytic species are visited by a variety of different ant species, whereas myrmecophytic Macaranga are associated only with one specific ant-partner. Since these ants keep scale insects in the hollow stems, reduction of nectary production in ant-inhabited Macaranga seems to be biologically significant. We interpret this as a means of (a) saving the assimilates and (b) stabilization of maintenance of the association's specificity. Competition with other ant species for food rewards is avoided and thereby danger of weakening the protective function of the obligate ant- partner for the plant is reduced. A comparison with other euphorb species living in the same habitats as Macaranga showed that in genera in which extrafloral nectaries are widespread, no myrmecophytes have evolved. Possession of extrafloral nectaries does not appear to be essential for the development of symbiotic ant-plant interactions. Other predispositions such as nesting space might have played a more important role.     

Differences in Survival and Growth Among Tropical Rain Forest Pioneer Tree Seedlings in Relation to Canopy Openness and Herbivory

Although differences in canopy openness, herbivory and their interaction may promote species coexistence, how these factors affect pioneer tree species and potentially limit growth, and survival has been poorly studied, particularly in tropical South Asia. We monitored the effect of canopy openness and herbivore damage on seedling survival and growth of 960 individuals of six pioneer tree species: Dillenia triquetra, Macaranga indica, Macaranga peltata, Schumacheria castaneifolia, Trema orientalis, and Wendlandia bicuspidata. Seedlings were placed in four gap‐understory positions—center, outer gap edge, inner forest edge, and understory—in four large, natural gaps within the Sinharaja World Heritage Reserve, Sri Lanka. Canopy openness positively affected survival probability beyond the 550‐d experiment, while herbivory decreased survival and was highest in understory conditions. The relative order of species survival stayed fairly consistent between gap‐understory positions and followed their known shade tolerance rankings. When averaged across all experimental conditions, T. orientalis had the lowest survival probability estimate beyond the 550‐d experiment (0.05), but the greatest capacity for growth where it successfully established, while the species with highest averaged survival probability (0.79), D. triquetra, showed the lowest growth. One species, W. bicuspidata, responded positively to herbivory by re‐sprouting. Coexistence of D. triquetra, T. orientalis, and W. bicuspidata can be explained by a trade‐off among species in survival, growth, and response to herbivory. In addition to variation in canopy light environment, herbivory may be important in determining pioneer species distribution through fine‐scale niche partitioning and should be carefully considered in reforestation efforts.     

鼎湖血桐种群生物学及遗传多样性初步研究

采用点格局分析、径级结构分析以及微卫星筛选等方法,对鼎湖山保护区20hm2永久样地中的鼎湖血桐进行了种群生物学及遗传多样性研究。结果表明:鼎湖血桐是一种r-对策型阳生植物,种群年龄结构呈金字塔型;植株受光照不足的胁迫,种群大部分个体聚集分布于光照充足的林窗中;通过磁珠富集法筛选出鼎湖血桐特异性微卫星引物13对,其中2对具备多态性,多态百分率为15.4%,多态信息含量在0～0.3734之间,平均期望杂合度为0.0756,远低于同属其它植物。研究表明鼎湖血桐对环境变化的适应范围较窄,遗传多样性较低,应对其种质资源进行多样性评估与保护。     

Isolation, DNA topoisomerase-II inhibition, and cytotoxicity of three new terpenoids from the bark of Macaranga tanarius

One new pimarane-type diterpenoid (1) and two new taraxerane-based triterpenoids (2 and 3) were isolated from the bark of Macaranga tanarius, along with seven known compounds. Their structures were identified by spectroscopic methods including NMR and MS analyses. Compounds 1-5 were tested for their in vitro inhibition of DNA topoisomerase II, as well as for their cytotoxicities against human lung carcinoma A549 cells (Table 3). The triterpenoids 2-5 showed strong activities in both assays, but the diterpenoid 1 was only moderately active.     

Microsatellite markers for the palaeotropic pioneer tree genus Macaranga (Euphorbiaceae) and their cross‐species transferability

We developed primer sequences for five polymorphic microsatellite loci in the tropical ant‐plant genus Macaranga (Euphorbiaceae). Population genetic parameters were determined on the basis of 30 individuals from each of two Macaranga species in Borneo. Allele numbers per locus ranged from three to 13. Expected and observed heterozygosities ranged from 0.160 to 0.850 and from 0.130 to 0.700, respectively. Four of the five primer pairs cross‐amplify polymorphic PCR products in a wide range of Macaranga species.     

Comparison of the physiology, morphology, and leaf demography of tropical saplings with different crown shapes

Branch architecture, leaf photosynthetic traits, and leaf demography were investigated in saplings of two woody species, Homolanthus caloneurus and Macaranga rostulata, co-occurring in the understory of a tropical mountain forest. M. rostulata saplings have cylindrical crowns, whereas H. caloneurus saplings have flat crowns. Saplings of the two species were found not to differ in area-based photosynthetic traits and in average light conditions in the understory of the studied site, but they do differ in internode length, leaf emergence rate, leaf lifespan, and total leaf area. Displayed leaf area of H. caloneurus saplings, which have the more rapid leaf emergence, was smaller than that of M. rostulata saplings, which have a longer leaf lifespan and larger total leaf area, although M. rostulata saplings showed a higher degree of leaf overlap. Short leaf lifespan and consequent small total leaf area would be linked to leaf overlap avoidance in the densely packed flat H. caloneurus crown. In contrast, M. rostulata saplings maintained a large total leaf area by producing leaves with a long leaf lifespan. In these understory saplings with a different crown architecture, we observed two contrasting adaptation strategies to shade which are achieved by adjusting a suite of morphological and leaf demographic characters. Each understory species has a suite of morphological traits and leaf demography specific to its architecture, thus attaining leaf overlap avoidance or large total leaf area.     

Phylogenetic patterns in larval host plant and ant association of Indo-Australian Arhopalini butterflies (Lycaenidae: Theclinae)

The Oriental butterfly genus Arhopala is by far the most species‐rich genus within the subfamily Theclinae. We investigated whether biotic interactions with larval host plants or ants are phylogenetically constrained in the evolutionary history of Arhopala, by collating available information on the ecology of Arhopala from the literature as well as from personal observations, and analysing and interpreting these data rigorously in a phylogenetic context. Larvae of all species in the sister‐group of Arhopala and Flos feed on Fabaceae. However, the predominant feeding preference of Arhopala s.l., with the exception of a particular monophyletic and species‐rich group, called ‘Group A’, appears to be centred on Fagaceae, with additional records of Dipterocarpaceae feeding. The preference for Fagaceae has strong phylogenetic inertia, as indicated by T‐PTP tests designed to test for phylogenetic signal. Adding all available life‐history data, using the phylogeny presented before as scaffolding, further increased the phylogenetic signal in host plant data. Feeding on Fabaceae (mainly in the outgroup) and Euphorbiaceae also showed significant phylogenetic signal, but feeding on Dipterocarpaceae did not and was found scattered across the phylogeny. Except for the Dipterocarpaceae, phylogenetic signal in feeding preferences was very clear, even despite uneven taxon sampling and apparent lability in host plant use. Ant association also demonstrated historical constraint, but based on the phylogenetic hypothesis presented here it was not clear whether increased ant association intimacy emerged independently various times in Group A, as well as in several basal groups. Our finding of distinct phylogenetic patterns in the host plant and to a lesser degree in ant association data contradicts the hypothesis that life‐history traits are very labile in the Lycaenidae. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 84 , 225–241.     

Absolute configuration of (+)-pinoresinol 4-O-[6″-O-galloyl]-β-d-glucopyranoside, macarangiosides E, and F isolated from the leaves of Macaranga tanarius

A lignan glucoside, (+)-pinoresinol 4-O-[6″-O-galloyl]-β-d-glucopyranoside (1), and two megastigmane glucosides, named macarangiosides E and F (2, 3), together with 15 known compounds (4–18) were isolated from leaves of Macaranga tanarius (L.) Müll.-Arg. (Euphorbiaceae). Their structures were elucidated by spectroscopic and chemical analyses. In addition, the absolute stereochemistry of macarangiosides B and C isolated previously from the same plant was also determined for the first time. Compounds 1 and 2 were galloylated on glucose and possessed potent DPPH radical-scavenging activity.     

A chloroplast genealogy of myrmecophytic Macaranga species (Euphorbiaceae) in Southeast Asia reveals hybridization, vicariance and long-distance dispersals

Macaranga (Euphorbiaceae) includes about 280 species with a palaeotropic distribution. The genus not only comprises some of the most prominent pioneer tree species in Southeast Asian lowland dipterocarp forests, it also exhibits a substantial radiation of ant-plants (myrmecophytes). Obligate ant-plant mutualisms are formed by about 30 Macaranga species and 13 ant species of the genera Crematogaster or Camponotus. To improve our understanding of the co-evolution of the ants and their host plants, we aim at reconstructing comparative organellar phylogeographies of both partners across their distributional range. Preliminary evidence indicated that chloroplast DNA introgression among closely related Macaranga species might occur. We therefore constructed a comprehensive chloroplast genealogy based on DNA sequence data from the noncoding ccmp2, ccmp6, and atpB-rbcL regions for 144 individuals from 41 Macaranga species, covering all major evolutionary lineages within the three sections that contain myrmecophytes. A total of 88 chloroplast haplotypes were identified, and grouped into a statistical parsimony network that clearly distinguished sections and well-defined subsectional groups. Within these groups, the arrangement of haplotypes followed geographical rather than taxonomical criteria. Thus, up to six chloroplast haplotypes were found within single species, and up to seven species shared a single haplotype. The spatial distribution of the chloroplast types revealed several dispersals between the Malay Peninsula and Borneo, and a deep split between Sabah and the remainder of Borneo. Our large-scale chloroplast genealogy highlights the complex history of migration, hybridization, and speciation in the myrmecophytes of the genus Macaranga. It will serve as a guideline for adequate sampling and data interpretation in phylogeographic studies of individual Macaranga species and species groups.     

Origin of caulinary ant domatia and timing of their onset in plant ontogeny: evolution of a key trait in horizontally transmitted ant-plant symbioses

Many ant plants possess caulinary domatia, hollow and usually swollen stems. What are the evolutionary origins of this key trait of ant‐plant symbioses? In a single lineage, myrmecophytes often differ in the timing of the first appearance of domatia. What processes have led to diversification in the timing of expression of domatia in ontogeny? We suggest that an approach based on the analysis of leaf‐ stem size correlations, that appear general in trees, can supply answers to both these questions. Traits associated with increased primary diameter of twigs may have facilitated the evolution of domatia. Among lineages, differences in stem diameter may help to explain why domatia appeared in some, and not in others. Within species, because twig primary diameter increases over plant ontogeny, initially ants may have colonized only plants at later stages of development, whose twigs had reached a minimum size. We thus postulate that expression of domatia later in development is the primitive condition in lineages with domatia, and that increasing specialization of ants and plants enhanced both the probability of establishment and ant protection, favouring precocity of onset of domatia and other myrmccophytic characters. In the language of heterochrony, these characters are affected by prc‐displacement.