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.     

Geographical and Seasonal Variation in the Richness of Ant-Plant Interactions in México1

The richness and seasonal variation of ant-plant interactions were compared in four habitats in México: lowland tropical dry forest (La Mancha, Veracruz), coastal sand dune matorral (San Benito, Yucatán), semiarid highland vegetation (Zapotitlán, Puebla), and lower montane humid forest (Xalapa, Veracruz). The effects of temperature and precipitation on the seasonal distribution of the number of ant-plant interactions differed among habitats. The general linear models fitted to the ant-plant interaction curves explained 78.8 percent of the variation for La Mancha, 80.1 percent for Zapotitlán, 18 percent for San Benito, and 29.5 percent for Xalapa. Even though rainfall is low in Zapotitlán and San Benito, minimum temperature was the most important factor accounting for the seasonal distribution and low number of interactions. At La Mancha, with milder minimum temperatures and higher water availability, temperature alone did not account for the seasonal distribution and number of interactions, whereas the effect of the precipitation × temperature interaction was highly significant. Xalapa exhibits the lowest temperatures and the highest precipitation, but the role of these factors was only marginal. We suggest that the vegetation at Xalapa, a mixture of tropical and temperate floristic elements, constrains ant-plant interactions due to a limited presence of nectaries. Also, ants are less abundant in cool and relatively aseasonal habitats. The other habitats have tropical floristic elements that are abundant and frequently have nectar-producing structures. We report considerable variation among habitats in the number and seasonal distribution of ant-plant interactions, and suggest that it is due to the effect of variation in environmental parameters, the richness of plants with nectaries in the vegetation, and habitat heterogeneity.     

Comparison between the anatomical and morphological structure of leaf blades and foliar domatia in the ant-plant Hirtella physophora (Chrysobalanaceae)

Background and Aims: Myrmecophytes, or ant-plants, are characterized by their abilityto shelter colonies of some ant species in hollow structures,or ant-domatia, that are often formed by hypertrophy of theinternal tissue at specific locations (i.e. trunk, branches,thorns and leaf pouches). In Hirtella physophora (Chrysobalanaceae),the focal species of this study, the ant-domatia consist ofleaf pouches formed when the leaf rolls over onto itself tocreate two spheres at the base of the blade. Methods: The morphological and anatomical changes through which foliarant-domatia developed from the laminas are studied for the firsttime by using fresh and fixed mature leaves from the same H.physophora individuals. Key results: Ant-domatia were characterized by larger extra-floral nectaries,longer stomatal apertures and lower stomatal density. The anatomicalstructure of the domatia differed in the parenchymatous tissuewhere palisade and spongy parenchyma were indistinct; chloroplastdensity was lower and lignified sclerenchymal fibres were morenumerous compared with the lamina. In addition, the domatiawere thicker than the lamina, largely because the parenchymatousand epidermal cells were enlarged. Conclusions: Herein, the morphological and anatomical changes that permitfoliar ant-domatia to be defined as a specialized leaf structureare highlighted. Similarities as well as structural modificationsin the foliar ant-domatia compared with the lamina are discussedfrom botanical, functional and mutualistic points of view. Theseresults are also important to understanding the reciprocal evolutionarychanges in traits and, thus, the coevolutionary processes occurringin insect–plant mutualisms.     

Are myrmecophytes always better protected against herbivores than other plants?

The present field study compared the degree of defoliation of three Guianian melastome, two myrmecophytes (i.e. plants sheltering ants in hollow structures) and Clidemia sp., a nonmyrmecophytic plant serving as a control. Maieta guianensis Aubl. hosted mostly Pheidole minutula Mayr whatever the area, whereas Tococa guianensis Aubl. hosted mostly Azteca bequaerti Wheeler along streams and Crematogaster laevis Mayr or Azteca sp. 1 in the understory where it never blossomed. Only Tococa , when sheltering A. bequaerti in what can be considered as a truly mutualistic relationship, showed significantly less defoliation than control plants. In the other associations, the difference was not significant, but P. minutula is mutualistic with Maieta because it furnishes some protection (exclusion experiments) plus nutrients (previous studies). When devoid of ants, Tococa showed significantly greater defoliation than control plants; therefore, it was deduced that Tococa probably lacks certain antidefoliator metabolites that control plants possess (both Tococa and control plants are protected by ground-nesting, plant-foraging ants, which is termed 'general myrmecological protection'). Consequently, plant-ants other than A. bequaerti probably also protect Tococa slightly, thus compensating for this deficiency and permitting it to live in the understory until treefall gaps provide the conditions necessary for seed production.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 91–98.     

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.     

Systematics, biogeography and host plant associations of the Pseudomyrmex viduus group (Hymenoptera: Formicidae), Triplaris- and Tac/Mga/t-inhabiting ants

The Pseudomyrmex viduus group is a Neotropical clade of arboreal ants containing 13 species, of which three are newly described here: P. insuavis, P. ultrix, and P. vitabilis. Most species inhabit the domatia of specialized ant-plants. The ants keep brood and scale insects (Coccoidea) in the plant cavities, and defend their nest sites much more aggressively than do generalist species of Pseudomyrmex nesting in dead twigs. Five species are obligate associates of trees in the genus Triplaris (Polygonaceae) and five taxa are restricted to Tachigali (Fabaceae: Caesalpinioideae). One species, P. viduus (F. Smith), is much less host-specific, inhabiting Cordia, Coussapoa, Ocotea, Pseudobombax, Pterocarpus, Sapium, Triplaris and other myrmecophytes. Nothing is known about the biology of P. vitabilis, a close relative of/?viduus. The last member of the species group, P. kuenckeli (Emery), is a non-specialist but aggressive species that nests in dead branches of various plants. A cladistic analysis indicates that this aggressive behaviour evolved before obligate associations with specialized ant-plants, and that the Triplaris and Tachigali inhabitants each form their own clade. P. viduus, which is nested within the Triplaris-associated clade, suggests a possible model for host plant evolution in these ants wherein shifts from one ant-plant to another involve an intermediate phase of expanded host plant use. At least nine other Pseudomyrmex species, from two different species groups (not closely related to the P. viduus group), have evolved specialized associations with Triplaris or Tachigali including five new species: P. crudelis, P. deminutus, P. eculeus. P. ferox and P. hospitalis. Although the P. viduus group is centred in the Amazon basin, the geographic ranges of most species do not coincide with the Pleistocene forest refugia proposed by Haffer and others. A consideration of the phylogenetic relationships, distribution patterns, and host plant specificity of the ants indicates that much of the diversification of the P. viduus group occurred before the Pleistocene, and that the interactions with Triplaris and Tachigali plants are also of Tertiary origin.