Macaranga Myrmecophytes Research Articles

アリ-オオバギ共生系の多様性 : 生物群集への波及効果( 生物間相互作用と群集構造:生態化学量論、間接効果、そして進化)

アリ-オオバギ共生系の多様性 : 生物群集への波及効果( 生物間相互作用と群集構造:生態化学量論、間接効果、そして進化)

Various chemical strategies to deceive ants in three Arhopala species (lepidoptera: Lycaenidae) exploiting Macaranga myrmecophytes.

Macaranga myrmecophytes (ant-plants) are generally well protected from herbivore attacks by their symbiotic ants (plant-ants). However, larvae of Arhopala (Lepidoptera: Lycaenidae) species survive and develop on specific Macaranga ant-plant species without being attacked by the plant-ants of their host species. We hypothesized that Arhopala larvae chemically mimic or camouflage themselves with the ants on their host plant so that the larvae are accepted by the plant-ant species of their host. Chemical analyses of cuticular hydrocarbons showed that chemical congruency varied among Arhopala species; A. dajagaka matched well the host plant-ants, A. amphimuta did not match, and unexpectedly, A. zylda lacked hydrocarbons. Behaviorally, the larvae and dummies coated with cuticular chemicals of A. dajagaka were well attended by the plant-ants, especially by those of the host. A. amphimuta was often attacked by all plant-ants except for the host plant-ants toward the larvae, and those of A. zylda were ignored by all plant-ants. Our results suggested that conspicuous variations exist in the chemical strategies used by the myrmecophilous butterflies that allow them to avoid ant attack and be accepted by the plant-ant colonies.

Congruence of microsatellite and mitochondrial DNA variation in acrobat ants (Crematogaster subgenus Decacrema, Formicidae: Myrmicinae) inhabiting Macaranga (Euphorbiaceae) myrmecophytes.

A previously reported mitochondrial DNA (mtDNA) phylogeny of Crematogaster (subgenus Decacrema) ants inhabiting Macaranga myrmecophytes indicated that the partners diversified synchronously and their specific association has been maintained for 20 million years. However, the mtDNA clades did not exactly match morphological species, probably owing to introgressive hybridization among younger species. In this study, we determined the congruence between nuclear simple sequence repeat (SSR, also called microsatellite) genotyping and mtDNA phylogeny to confirm the suitability of the mtDNA phylogeny for inferring the evolutionary history of Decacrema ants. Analyses of ant samples from Lambir Hills National park, northeastern Borneo, showed overall congruence between the SSR and mtDNA groupings, indicating that mtDNA markers are useful for delimiting species, at least at the local level. We also found overall high host-plant specificity of the SSR genotypes of Decacrema ants, consistent with the specificity based on the mtDNA phylogeny. Further, we detected cryptic genetic assemblages exhibiting high specificity toward particular plant species within a single mtDNA clade. This finding, which may be evidence for rapid ecological and genetic differentiation following a host shift, is a new insight into the previously suggested long-term codiversification of Decacrema ants and Macaranga plants.

How Do Scale Insects Settle into the Nests of Plant-Ants on Macaranga Myrmecophytes? Dispersal by Wind and Selection by Plant-Ants

This report elucidates the process of settlement by Coccus scale insects into Crematogaster plant-ant nests formed inside the hollow stems of a myrmecophytic species, Macaranga bancana, in a tropical rain forest. We collected wafting scale insect nymphs from the canopy using sticky traps and characterized the DNA sequence of the trapped nymphs. In addition, we experimentally introduced first-instar nymphs of both symbiotic and nonsymbiotic scale insects to M. bancana seedlings with newly formed plant-ant colonies. Nymphs of symbiotic species were generally carried by ants into their nests within a few minutes of introduction. Most nymphs of nonsymbiotic species were thrown to the ground by ants. Our results suggest that in Crematogaster–Macaranga myrmecophytism, symbiotic coccids disperse by wind onto host plant seedlings at the nymphal stage, and plant-ants actively carry the nymphs landing on seedlings into their nests in discrimination from nonsymbiotic scale insects.

Host-plant use by twoOrthomeria(Phasmida: Aschiphasmatini) species feeding onMacarangamyrmecophytes

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.

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.

Effects of symbiotic coccid on the plant-ant colony growth in the myrmecophyte Macaranga bancana

Macaranga (Euphorbiaceae) myrmecophytes provide their partner ants (plant-ants) with hollow stems used as nesting spaces, as well as food bodies as food rewards. In return, they benefit from the anti-herbivore defense of the ants. The plants harbor not only ants but also specific honeydew-producing coccids, which live inside the ant nests in the hollow stems. Although the honeydews are fed by the plant-ants, their effect on the growth of plant-ant colonies is undetermined. In this study, we investigated how such myrmecophilous coccids, Coccus spp. affect the colony growth of plant-ants, Crematogaster spp. on the myrmecophytic species M. bancana. We compared the growth of plant-ant colonies on seedlings from which coccids were experimentally excluded with that on seedlings into which specific myrmecophilous coccids were experimentally introduced. Foundress queens in 14 of 16 coccid-excluded seedlings died by the time we dissected the seedlings 235-637 days after the seedlings were transplanted in a meshed nursery. In contrast, those on 12 of 17 coccid-introduced seedlings survived during that period, with the survival rate of queens differing significantly between treatments. This result suggests that the symbiotic coccids provide nutrients that facilitate the colony growth of plant-ants inhabiting Macaranga myrmecophytes.

Species-specific Leaf Volatile Compounds of Obligate Macaranga Myrmecophytes and Host-specific Aggressiveness of Symbiotic Crematogaster Ants

Macaranga myrmecophytes harbor species-specific Crematogaster ants that defend host trees from herbivores. We examined ant aggressive behaviors when artificially damaged leaf pieces from another tree were offered to four sympatric species of obligate Macaranga myrmecophytes. The ants showed aggressive behavior in response to leaf pieces regardless of the leaf species; however, aggressiveness was higher when conspecific leaf pieces were offered than when nonhost species were offered. Thus, ants can recognize leaf damage and distinguish among damaged leaf species. Chemical analyses of volatile compounds emitted from damaged leaves that may induce ant defense showed that the composition of the minor compounds differed among the four Macaranga species, although there were many compounds in common.

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.

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.

Species specificity in settling-plant selection by foundress ant queens in Macaranga–Crematogaster myrmecophytism in a Bornean dipterocarp forest

Previous studies have demonstrated that the obligate myrmecophytism between Macaranga ant-plants and Crematogaster plant-ants is highly species specific, although multiple Macaranga species can coexist in a microhabitat. However, the species specificity has been described based on the study of trees with established plant-ant colonies. We studied how the process of settling into the partner Macaranga seedlings by single foundress Crematogaster queens contributes to species specificity. By sampling seedlings of three sympatric Macaranga myrmecophytes species in the field, we tested two hypotheses. The first is that foundresses correctly select their specific partner plant species when they settle into seedlings. The second hypothesis is that the seasons in which seedlings available for settling by foundresses appear are segregated among the Macaranga species, and the seasons in which foundress queens settle are synchronized to the appearance of seedlings of specific partner species; thus species specificity is consequently generated. Our results support the former hypothesis but not the latter: we always observed foundresses settling species-specific host plants, and seedlings suitable for settling were always available in each Macaranga species.

Difference in Intensity of Ant Defense among Three Species ofMacarangaMyrmecophytes in a Southeast Asian Dipterocarp Forest1

ABSTRACTTo examine interspecific variation in the intensity of ant defense among three sympatric species of obligate myrme‐cophytes ofMacaranga(Euphorbiaceae), we measured the ratio of ant biomass to plant biomass, ant aggressiveness to artificial damage on host plants, and increase in herbivore damage on host plants when symbiont ants were removed. Increase in herbivore damage from two‐ and four‐week ant exclusion varied significantly among the three species. The decreasing order of vulnerability to herbivory wasM. winkleri, M. trachyphylla, andM. beccariana.The antip/ant biomass ratio (= rate of the dry weight of whole ant colonies to the dry weight of whole aboveground plant parts) and ant agressiveness also varied significantly among the three species; the orders of both the ant/plant biomass ratio and ant aggressiveness were the same as in the herbivory increase. These results indicated that the intensity of ant defense differs predictably among sympatric species of obligate myrmecophytes onMacaranga.In addition to the interspecific difference in the total intensity of ant defense, when symbiont ants were excluded, both patterns of within‐plant variation in the amount of herbivore damage and compositions of herbivore species that caused the damage differed among species. This suggests that the threeMacarangaspecies have different systems of ant defense with reference to what parts of plant tissue are protected and what herbivorous species are avoided by ant defense. Thus, it is important to consider the interspecific variation in ant defense amongMacarangaspecies to understand the herbivore community onMacarangaplants and the mechanisms that promote the coexistence of multipleMacarangamyrmecophytes.

Difference in Intensity of Ant Defense among Three Species of Macaranga Myrmecophytes in a Southeast Asian Dipterocarp Forest1

Difference in Intensity of Ant Defense among Three Species of Macaranga Myrmecophytes in a Southeast Asian Dipterocarp Forest1

Camponotus (Colobopsis)(Mayr 1861) andMacaranga(Thouars 1806): a specific two-partner ant-plant system from Malaysia

Within the paleotropical tree genus Macaranga (Thouars 1806) (Euphorbiaceae), the majority of ant-plant species are associated with specialized Crematogaster (Lund 1831) partner ants from the subgenus Decacrema (Myrmicinae). We have now discovered a completely different myrmecophytic system in which an ant species of the Formicinae lives in symbiosis with the peat swamp forest tree Macaranga puncticulata (Gage 1922). M. puncticulata twigs develop spacious cavities (domatia). An undescribed Camponotus (Colobopsis) (Mayr 1861) species of the C. saundersi-group was the dominant ant inhabitant (65% of the investigated plants) at forest sites, but this species, provisionally named C. (Colobopsis) sp. 1, was only rarely found at open stands. Another 29 opportunistic stem-nesting ant species were collected less frequently. None of them were Crematogaster (Decacrema) ants. C. (Colobopsis) sp. 1 has never been found to nest away from M. puncticulata. The mated queens are capable of locating young M. puncticulata plants and of chewing entrance holes into the domatia. In contrast to all the other obligate plant-ants associated with Macaranga, C. (Colobopsis) sp. 1 never cultivates any trophobionts, neither inside nor outside the domatia. Instead of taking up honey dew from coccids, the ants obtain carbohydrates from extrafloral nectaries along the leaf margins of M. puncticulata. This food source is an uncommon trait within Macaranga myrmecophytes. The association of C. (Colobopsis) sp. 1 with M. puncticulata is therefore the first record of a two-partner ant-plant system without endophytic coccids in the genus Macaranga.

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.