Food bodies and their significance for obligate ant-association in the tree genus Macaranga (Euphorbiaceae)

FIALA, B. & MASCHWITZ, U., 1992. Food bodies and their significance for obligate ant-association in the tree genus Macaranga (Euphorbiaceae). The production of extrafloral nectar and food bodies plays an important role in many tropical ant-plant mutualisms. In Malaysia, a close association exists between ants and some species of the pioneer tree genus Macaranga (Euphorbiaceae). Macaranga is a very diverse genus which exhibits all stages of interaction with ants, from facultative to obligatory associations. The ants nest inside the hollow internodes and feed mainly on food bodies provided by the plants. Food body production had previously been reported only in myrmecophytic Macaranga species, where it is usually concentrated on protected parts of the plants such as recurved stipules. We found that non-myrmecophytic Macaranga species also produce food bodies on leaves and stems, where they are collected by a variety of ants. Levels of food body production differ between facultatively and obligatorily ant-associated species but also among the various non-myrmecophytes. This may be related to the degree of interaction with ants. Food body production starts at a younger age in the myrmecophytic species than in the transitional or non-myrmeccophytic Macaranga. Although food bodies of the non-inhabited Macaranga species are collected by a variety of ants, there is no evidence of association with specific ant species. Our observations suggest that food bodies enhance the evolution of ant-plant interactions. Production of food bodies alone, however, does not appear to be the most important factor for the development of obligate myrmecophytism in Macaranga.     

Carbon and nitrogen contents of food bodies in three myrmecophytic species of Macaranga: implications for antiherbivore defense mechanisms

In Macaranga myrmecophytes, differences in the production of the food bodies (FBs), on which symbiont ants feed, may relate to the intensity of antiherbivore defense by the ants. Interspecific comparisons among Macaranga species on such a mutualistic cost give important information on their strategies and evolution of antiherbivore defense. In this study, the carbon and nitrogen contents of FBs as well as the production rate of FBs were measured in three Macaranga species, M. winkleri, M. trachyphylla, and M. beccariana. There were significant differences in the production rates of FBs among species; the investment in FBs was greater in the Macaranga species in which ant defenses were more intensive. The carbon and nitrogen contents of FBs were significantly different among the three species, although they did not match the intensity of ant defense; the nitrogen content, especially, was greatest in the species of least intensive ant defense. It is suggested that Macaranga plants may have differentiated in the dependence on ant defense by controlling the total amount of nitrogen of FBs, not simply by nitrogen content.     

Studies of a South East Asian ant-plant association: protection of Macaranga trees by Crematogaster borneensis

Summary In the humid tropics of SE Asia there are some 14 myrmecophytic species of the pioneer tree genus Macaranga (Euphorbiaceae). In Peninsular Malaysia a close association exists between the trees and the small, non-stinging myrmicine Crematogaster borneensis. These ants feed mainly on food bodies provided by the plants and have their colonies inside the hollow internodes. In a ten months field study we were able to demonstrate for four Macaranga species (M. triloba, M. hypoleuca, M. hosei, M. hulletti) that host plants also benefit considerably from ant-occupation. Ants do not contribute to the nutrient demands of their host plant, they do, however, protect it against herbivores and plant competition. Cleaning behaviour of the ants results in the removal of potential hervivores already in their earliest developmental stages. Strong aggressiveness and a mass recruiting system enable the ants to defend the host plant against many herbivorous insects. This results in a significant decrease in leaf damage due to herbivores on ant-occupied compared to ant-free myrmecophytes as well as compared to non-myrmecophytic Macaranga species. Most important is the ants' defense of the host plant against plant competitors, especially vines, which are abundant in the well-lit pioneer habitats where Macaranga grows. Ants bite off any foreign plant part coming into contact with their host plant. Both ant-free myrmecophytes and non-myrmecophytic Macaranga species had a significantly higher incidence of vine growth than specimens with active ant colonies. This may be a factor of considerable importance allowing Macaranga plants to grow at sites of strongest competition.     

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.     

Plants feed ants: food bodies of myrmecophytic Piper and their significance for the interaction with Pheidole bicornis ants

Several species of Piper (Piperaceae) live in symbiosis with Pheidole bicornis (Formicidae-Myrmicinae) on the southern Pacific slope of Costa Rica. These plants produce small single-celled food bodies (FBs) in leaf domatia, formed by the petiole bases and roofing leaf sheaths. In the present study the dependency of ants on FBs of Piper fimbriulatum as a food source was analysed by comparing the natural abundance of ¹³C and ¹⁵N in ants and FBs. Both '¹³C and '¹⁵N values were very similar between FBs and Pheidole bicornis ants but differed substantially between the plant and other ant species. Therefore we suggest that FBs are a main food source for Pheidole bicornis ants. To strengthen this suggestion, the chemical composition of FBs of four myrmecophytic Piper species was analysed, with special emphasis on the nutritional requirements of inhabiting Pheidole bicornis ants. Standard chemical methods were modified and combined to a novel analysis scheme by which all major FB constituents could be quantified from minute [3-10 mg dry mass (DM)] quantities. Piper FBs mainly consisted of lipids (41-48% of DM) and proteins (17-24% of DM). Soluble carbohydrates and amino acids proved to be quantitatively unimportant. N was predominantly stored as soluble protein and, thus, was easily available to the ants. FBs proved to be a high-energy food source (up to 23 kJ g^-1 DM), with a chemical composition that meets well the nutritional needs of the inhabiting ants.     

Pathogenesis-related proteins protect extrafloral nectar from microbial infestation

Plants in more than 300 genera produce extrafloral nectar (EFN) to attract carnivores as a means of indirect defence against herbivores. As EFN is secreted at nectaries that are not physically protected from the environment, and contains carbohydrates and amino acids, EFN must be protected from infestation by micro-organisms. We investigated the proteins and anti-microbial activity in the EFN of two Central American Acacia myrmecophytes ( A. cornigera and A. hindsii ) and two related non-myrmecophytes ( A. farnesiana and Prosopis juliflora ). Acacia myrmecophytes secrete EFN constitutively at high rates to nourish the ants inhabiting these plants as symbiotic mutualists, while non-myrmecophytes secrete EFN only in response to herbivore damage to attract non-symbiotic ants. Thus, the quality and anti-microbial protection of the EFN secreted by these two types of plants were likely to differ. Indeed, myrmecophyte EFN contained significantly more proteins than the EFN of non-myrmecophytes, and was protected effectively from microbial infestation. We found activity for three classes of pathogenesis-related (PR) enzymes: chitinase, β-1,3-glucanase and peroxidase. Chitinases and β-1,3-glucanases were significantly more active in myrmecophyte EFN, and chitinase at the concentrations found in myrmecophyte EFN significantly inhibited yeast growth. Of the 52 proteins found in A. cornigera EFN, 28 were annotated using nanoLC-MS/MS data, indicating that chitinases and glucanases contribute more than 50% of the total protein content in the EFN of this myrmecophyte. Our study demonstrates that PR enzymes play an important role in protecting EFN from microbial infestation.     

Interspecific variation in the defensive responses of ant mutualists to plant volatiles

In ant–plant mutualist systems, ants patrol their host plants and search for herbivores. Such patrolling can be inefficient, however, because herbivore activity is spatio-temporally unpredictable. It has been proposed that rapid and efficient systems of communication between ants and plants, such as volatile compounds released following herbivory, both elicit defensive responses and direct workers to sites of herbivore activity. We performed bioassays in which we challenged colonies of two Amazonian plant-ants, Azteca sp. and Pheidole minutula , with extracts of leaf tissue from (1) their respective host-plant species ( Tococa bullifera and Maieta guianensis , both Melastomataceae), (2) sympatric ant-plants from the Melastomataceae, and (3) two sympatric but non-myrmecophytic Melastomataceae. We found that ants of both species responded dramatically to host-plant extracts, and that these responses are greater than those to sympatric myrmecophytes. Azteca sp. also responded to non-myrmecophytes with an intensity similar to that of sympatric ant-plants. By contrast, the response of P. minutula to any non-myrmecophytic extracts was limited. These differences may be driven in part by interspecific differences in nesting behaviour; although P. minutula only nests in host plants, Azteca sp. will establish carton satellite nests on nearby plants. We hypothesize that Azteca sp. must therefore recognize and defend a wider array of species than P. minutula .  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 241–249.     

Molekulare Studien an Ameisenbäumen

Molecular systematic studies in Southeast Asian ant‐plants Myrmecophytes are plants that are permanently inhabited by ants. They provide nesting space and feed their partners, whereas the ants protect their hosts from herbivores and competitors such as climbers and lianas. The manifold relationships between tropical pioneer trees of the genus Macaranga and their partner ants of the genus Crematogaster constitute the most important and species‐rich mutualistic ant‐plant relationship of the Paleotropics. We use comparative DNA sequencing and molecular marker technologies to evaluate phylogenetic relationships among the about 30 myrmecophytic Macaranga species as well as their co‐evolution with ants. We also study the population genetics and historical biogeography of particular Macaranga species groups. Patterns of genetic diversity and differentiation in these pioneer tree species show interesting correlations with their reproductive biology and with characteristics of the increasingly fragmented pioneer habitats in the rainforests of Sundaland.     

Slippery ant-plants and skilful climbers: selection and protection of specific ant partners by epicuticular wax blooms in Macaranga (Euphorbiaceae)

 In many ant-plant species of the genus Macaranga in South-East Asia, conspicuous blooms of epicuticular wax crystals cover the stem surface. We found that many ant species were unable to walk on these surfaces. Only the specific ant partners of glaucous Macaranga host plants were capable of moving on the slippery stems without difficulty. Therefore, the epicuticular coatings of Macaranga myrmecophytes appear to have a selective function and protect the associated ants against competitors. The epicuticular aggregates function as a physical barrier; no evidence of chemical repellence was found. The extent to which ”foreign” ant species are excluded from a tree strongly depends on inclination, diameter and length of the glaucous stem sections. The particular growth form of some glaucous Macaranga ant-plants enhances the influence of the wax barriers. The ant associates of glaucous and glossy Macaranga ant-plants (genera Crematogaster and Camponotus) differ strongly in their capacity to adhere to the glaucous stems. For this reason, the wax blooms in Macaranga can act as an ecological isolation mechanism for the sympiotic ants. Within the genus Macaranga, we find a high correspondence between the occurrence of glaucousness and obligatory ant association (50% in ant-plants; 6.7% in non-myrmecophytes). The genus Macaranga thus represents one of the few cases known so far where epicuticular wax crystals are likely to have evolved in relation to insects. Received: 2 January 1997 / Accepted: 9 June 1997     

Evolution of myrmecophytism in western Malesian Macaranga (Euphorbiaceae)

Plants inhabited by ants (myrmecophytes) have evolved in a diversity of tropical plant lineages. Macaranga includes approximately 300 paleotropical tree species; in western Malesia there are 26 myrmecophytic species that vary in morphological specializations for ant association. The origin and diversification of myrmecophytism in Macaranga was investigated using phylogenetic analyses of morphological and nuclear ITS DNA characters and studies of character evolution. Despite low ITS variation, the combined analysis resulted in a well-supported hypothesis of relationships. Mapping myrmecophytism on all most parsimonious trees resulting from the combined analysis indicated that the trait evolved independently between two and four times and was lost between one and three times (five changes). This hypothesis was robust when tested against trees constrained to have three or fewer evolutionary transformations, although increased taxon sampling for the ITS analysis is required to confirm this. Mapping morphological traits on the phylogeny indicated that myrmecophytism was not homologous among lineages; each independent origin involved a suite of different specializations for ant-plant association. There was no evidence that myrmecophytic traits underwent sequential change through evolution; self-hollowing domatia evolved independently from ant-excavated domatia, and different food-body production types evolved in different lineages. The multiple origins of myrmecophytism in Macaranga were restricted to one small, exclusively western Malesian lineage of an otherwise large and nonmyrmecophytic genus. Although the evolution of aggregated food-body production and the formation of domatia coincided with the evolution of myrmecophytism in all cases, several morphological, ecological, and biogeographic factors appear to have facilitated and constrained this radiation of ant-plants.     

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.     

Ant-Repelling Pollinators of the Myrmecophytic <Emphasis Type="Italic">Macaranga winkleri</Emphasis> (Euphorbiaceae)

Many plants have mutualistic relationships with ants, whereby plants provide food and/or nesting sites for the symbiotic ants, and in turn the ants protect the host plants by excluding herbivores. While the ants are useful as guards, they may negatively affect host reproduction by excluding pollinators. Here we studied this potential conflict in the myrmecophytic Macaranga winkleri pollinated by the thrips Dolichothrips fialae. Behavioural responses of ant guards to pollinator thrips and their chemicals, and related chemical analyses, provide evidence that thrips deter ant-guards by secreting droplets containing ant-repelling n-decanoic acid from their anuses. This is the first report of insect pollinators repelling their host’s symbiotic guard ants to perform pollination. This is a novel strategy by which a plant host avoids interference with pollination by ant-guards in an ant–plant mutualism. The acquisition of a pollination system that is resistant to ant attacks may have facilitated the evolution of myrmecophytes in the genus Macaranga.     

Production of food bodies on the reproductive organs of myrmecophytic Macaranga species (Euphorbiaceae): effects on interactions with herbivores and pollinators

In protective ant–plant mutualisms, plants offer ants food (such as extrafloral nectar and/or food bodies) and ants protect plants from herbivores. However, ants often negatively affect plant reproduction by deterring pollinators. The aggressive protection that mutualistic ants provide to some myrmecophytes may enhance this negative effect in comparison to plant species that are facultatively protected by ants. Because little is known about the processes by which myrmecophytes are pollinated in the presence of ant guards, we examined ant interactions with herbivores and pollinators on plant reproductive organs. We examined eight myrmecophytic and three nonmyrmecophytic Macaranga species in Borneo. Most of the species studied are pollinated by thrips breeding in the inflorescences. Seven of eight myrmecophytic species produced food bodies on young inflorescences and/or immature fruits. Food body production was associated with increased ant abundance on inflorescences of the three species observed. The exclusion of ants from inflorescences of one species without food rewards resulted in increased herbivory damage. In contrast, ant exclusion had no effect on the number of pollinator thrips. The absence of thrips pollinator deterrence by ants may be due to the presence of protective bracteoles that limit ants, but not pollinators, from accessing flowers. This unique mechanism may account for simultaneous thrips pollination and ant defense of inflorescences.     

Caterpillars and fungal pathogens: two co-occurring parasites of an ant-plant mutualism

In mutualisms, each interacting species obtains resources from its partner that it would obtain less efficiently if alone, and so derives a net fitness benefit. In exchange for shelter (domatia) and food, mutualistic plant-ants protect their host myrmecophytes from herbivores, encroaching vines and fungal pathogens. Although selective filters enable myrmecophytes to host those ant species most favorable to their fitness, some insects can by-pass these filters, exploiting the rewards supplied whilst providing nothing in return. This is the case in French Guiana for Cecropia obtusa (Cecropiaceae) as Pseudocabima guianalis caterpillars (Lepidoptera, Pyralidae) can colonize saplings before the installation of their mutualistic Azteca ants. The caterpillars shelter in the domatia and feed on food bodies (FBs) whose production increases as a result. They delay colonization by ants by weaving a silk shield above the youngest trichilium, where the FBs are produced, blocking access to them. This probable temporal priority effect also allows female moths to lay new eggs on trees that already shelter caterpillars, and so to occupy the niche longer and exploit Cecropia resources before colonization by ants. However, once incipient ant colonies are able to develop, they prevent further colonization by the caterpillars. Although no higher herbivory rates were noted, these caterpillars are ineffective in protecting their host trees from a pathogenic fungus, Fusarium moniliforme (Deuteromycetes), that develops on the trichilium in the absence of mutualistic ants. Therefore, the Cecropia treelets can be parasitized by two often overlooked species: the caterpillars that shelter in the domatia and feed on FBs, delaying colonization by mutualistic ants, and the fungal pathogen that develops on old trichilia. The cost of greater FB production plus the presence of the pathogenic fungus likely affect tree growth.     

Change in biomass of symbiotic ants throughout the ontogeny of a myrmecophyte, Macaranga beccariana (Euphorbiaceae)

Macaranga myrmecophytes (ant-plants) provide their partner symbiotic ants (plant-ants) with food bodies as their main food, and they are protected by the plant-ants from herbivores. The amount of resource allocated to food bodies determines the plant-ant colony size and consequently determines the intensity of ant defense (anti-herbivore defense by plant-ants). As constraints in resource allocation change as plants grow, the plant-ant colony size is hypothesized to change with the ontogenesis of Macaranga myrmecophyte. To determine the ontogenetic change in the relative size of the plant-ant colony, we measured the dry weights of the whole plant-ant colony and all of the aboveground parts of trees at various ontogenetic stages for a myrmecophytic species (Macaranga beccariana) in a Bornean lowland tropical rain forest. Ant biomass increased as plant biomass increased. However, the rate of increase gradually declined, and the ant biomass appeared to reach a ceiling once trees began to branch. The ant/plant biomass ratio consistently decreased as plant biomass increased, with the rate of decrease gradually accelerating. We infer that the ontogenetic reduction in ant/plant biomass ratio is caused by an ontogenetic change in resource allocation to food rewards for ants related to the physiological changes accompanying the beginning of branching.     

Variations in abiotic defense within myrmecophytic and non-myrmecophytic species of Macaranga in a Bornean dipterocarp forest

We examined the interspecific variations in intensity of total abiotic (chemical and physical) defenses in five sympatric Macaranga (Euphorbiaceae) species, including three myrmecophytic species. The intensity of the total abiotic defense for each Macaranga species was estimated by measuring inhibiting effects on the growth performance of the common cutworm, Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) when the cutworm larvae were fed fresh leaves of each Macaranga species. Indices of the growth performance, number of dead larvae, pupal weight and length of larval period were obtained. We found that the intensities of total abiotic defense of the two non-myrmecophytic species were significantly stronger than those of the three myrmecophytic species, and that there was a significant difference in intensity even within the three myrmecophytic species. The former result supports the hypothesis that, unlike non-myrmecophytic species, myrmecophytic species cannot invest so many metabolic resources in abiotic defense, because they have to allocate nutrients to biotic defense (toward biotic defense agents). Moreover, the latter result suggests the possibility that the three sympatric myrmecophytes have different defense strategies, with a trade-off between abiotic and biotic defense, and/or with a trade-off between defense and other life-history traits such as growth and reproduction. Abiotic defense can be roughly separated into physical and chemical mechanisms. To assess the intensity of the physical defense of Macaranga leaves, we measured the leaf toughness of each species. In addition, to assess the intensity of the plants general chemical defense, cutworm larvae were reared on an artificial diet containing dry leaf powder of each Macaranga species, and their growth performances were compared. The estimated orders of intensity of both leaf toughness and general chemical defense coincided with that of the total abiotic factors measured by the growth performance of cutworm on fresh leaves. This suggests the presence of both physical defenses, represented by leaf toughness, and a general chemical defense affecting the intensity of the total abiotic defense in similar ways.     

Diversity, evolutionary specialization and geographic distribution of a mutualistic ant-plant complex: Macaranga and Crematogaster in South East Asia

The most conspicuous and species-rich ant-plant mutualism in the Malesian region is found in the important pioneer tree genus Macaranga , yet little is known about the identities or community ecology of the species involved. Our studies have revealed a far more complex system than previously thought. This paper presents the first extensive investigation in the whole distribution area of myrmecophytic Macaranga. All ant-inhabited species were restricted to the moister parts of SE Asia: Peninsular Malaysia, South and East Thailand, Sumatra and Borneo. We found a rather strict and similar altitudinal zonation of myrmecophytic Macaranga species in all regions. Here we focus on the majority of the 19 Macaranga species obligatorily associated with ants of the genus Crematogaster. We identified a total of 2163 ant queens which belonged to at least eight (morpho)species of the small subgenus Decacrema as well as to one non-Decacrema (probably from Atopogyne ). The ant species were not randomly distributed among the Macaranga species but distinct patterns of associations emerged. Despite common sympatric distribution of Macaranga species, in most cases a surprisingly high specificity of ant colonization was maintained which was, however, often not species-specific but groups of certain plant species with identical ant partners could be found. These colonization patterns usually but not always mirror existing taxonomic sections within the genus Macaranga. Possible mechanisms of specificity are discussed. The results are compared with other ant-plant mutualisms.     

Host‐plant use by two Orthomeria (Phasmida: Aschiphasmatini) species feeding on Macaranga myrmecophytes

Myrmecophytes depend on symbiotic ants (plant‐ants) to defend against herbivores. Although these defensive mechanisms are highly effective, some herbivorous insects can use myrmecophytes as their host‐plants. The feeding habits of these phytophages on myrmecophytes and the impacts of the plant‐ants on their feeding behavior have been poorly studied. We examined two phasmid species, Orthomeria alexis and O. cuprinus, which are known to feed on Macaranga (Euphorbiaceae) myrmecophytes in a Bornean primary forest. Our observations revealed that: (i) each phasmid species relied on two closely‐related myrmecophytic Macaranga species for its host‐plants in spite of their normal plant‐ant symbioses; and (ii) there was little overlap between their host‐plant preferences. More O. cuprinus adults and nymphs were found on new leaves, which were attended by more plant‐ants than mature leaves, while most adults and nymphs of O. alexis tended to avoid new leaves. In a feeding choice experiment under ant‐excluded conditions, O. alexis adults chose a non‐host Macaranga myrmecophyte that was more intensively defended by plant‐ants and was more palatable than their usual host‐plants almost as frequently as their usual host‐plant, suggesting that the host‐plant range of O. alexis was restricted by the presence of plant‐ants on non‐host‐plants. Phasmid behavior that appeared to minimize plant‐ant attacks is described.     

Macaranga ant-plants hide food from intruders: correlation of food presentation and presence of wax barriers analysed using phylogenetically independent contrasts

Many tropical ant-plants provide specialized ant partners with food, which may attract foreign ants parasitizing the mutualism. We present evidence for the ant-plant genus Macaranga , showing that ant competition has forced host plants to hide food resources and restrict access to the mutualists. In Macaranga myrmecophytes, the influence of ant competition strongly depends on the presence of slippery 'wax barriers'. Of all Macaranga ant-plant species, 50% have waxy stems that can be climbed only by the specific ant partners and not by other ant species. We compared the presentation of food (food bodies and extrafloral nectar) between waxy and non-waxy Macaranga host plants using traditional and phylogenetic comparative methods. Consistent with the hypothesized effect of ant competition, wax-free Macaranga host species had fewer extrafloral nectaries and more often produced food bodies under recurved or tubular stipules inaccessible to other ants; closed stipules were less persistent in waxy hosts. Several traits showed phylogenetic signal, but our finding of a more promiscuous food presentation in waxy Macaranga hosts was still supported by phylogenetic comparative analyses. We conclude that competition among ants is an important factor in the evolution of myrmecophytism, and that it has given rise to traits acting as protective filter mechanisms.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 177–193.     

Herbivory and assemblage structure of myrmecophytous understory plants and their associated ants in the central Amazon

Summary The species combinations of myrmecophytic plants were compared in three different, neighboring local central Amazon forest sites. The proportional contribution of myrmecophytes in each setting varied significantly, withMaieta guainensis being the most abundant in each locality. This pattern resulted in low site similarity values. Other recorded species wereHirtella physophora, Tachigalia myrmecophila, Duroia sp.,Tococa sp., andCordia nodosa. Little variability was found with respect to associated ants that inhabited the myrmecophytes, and mutual entropies indicated a high degree of mutualistic interactions. However, for the majority of myrmecophytes, no differences in herbivore damage levels could be attributed to the presence of ants, with onlyM. guianensis andT. myrmecophila demonstrating significantly lower damages when inhabited by ants. Their respective ant associates,Pheidole minitula andPseudomyrmex concolor, were thus the only plant-ants with a demonstrable ability to reduce the levels of herbivory in their host plant.