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.     

Carbon and nitrogen contents of food bodies in three myrmecophytic species of <Emphasis Type="Italic">Macaranga</Emphasis>: 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. Received: January 19, 2001 / Accepted: December 23, 2001     

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.     

Diversity of ant-plant interactions: protective efficacy in Macaranga species with different degrees of ant association

The pioneer tree Macaranga in SE Asia has developed manyfold associations with ants. The genus comprises all stages of interaction with ants, from facultative relationships to obligate myrmecophytes. Only myrmecophytic Macaranga offer nesting space for ants and are associated with a specific ant partner. The nonmyrmecophytic species are visited by a variety of different ant species which are attracted by extrafloral nectaries (EFN) and food bodies. Transitional Macaranga species like M. hosei are colonized later in their development due to their stem structure. Before the colonization by their specific Crematogaster partner the young plants are visited by different ant species attracted by EFN. These nectaries are reduced and food body production starts as soon as colonization becomes possible. We demonstrated earlier that obligate ant partners can protect their Macaranga plants against herbivore damage and vine cover. In this study we focused on nonspecific interactions and studied M. tanarius and M. hosei, representing a non-myrmecophyte and a transitional species respectively. In ant exclusion experiments both M. tanarius and M. hosei suffered significantly higher mean leaf damage than controls, 37% versus 6% in M. hosei, 16% versus 7% in M. tanarius. M. tanarius offers both EFN and food bodies so that tests for different effects of these two food rewards could be conducted. Plants with food bodies removed but with EFN remaining had the lowest mean increase of herbivore damage of all experimental groups. Main herbivores on M. hosei were mites and caterpillars. Many M. tanarius plants were infested by a shootborer. Both Macaranga species were visited by various ant species, Crematogaster spp. being the most abundant. We found no evidence for any specific relationships. The results of this study strongly support the hypothesis that non-specific, facultative associations with ants can be advantageous for Macaranga plants. Food bodies appear to have lower attractive value for opportunistic ants than EFN and may require a specific dietary adaptation. This is also indicated by the fact that food body production in the transitional M. hosei does not start before stem structure allows a colonization by the obligate Crematogaster species. M. hosei thus benefits from facultative association with a variety of ants until it produces its first domatia and can be colonized by its obligate mutualist.     

Ants on plants: a meta-analysis of the role of ants as plant biotic defenses

We reviewed the evidence on the role of ants as plant biotic defenses, by conducting meta-analyses for the effects of experimental removal of ants on plant herbivory and fitness with data pooled from 81 studies. Effects reviewed were plant herbivory, herbivore abundance, hemipteran abundance, predator abundance, plant biomass and reproduction in studies where ants were experimentally removed (n = 273 independent comparisons). Ant removal exhibited strong effects on herbivory rates, as plants without ants suffered almost twice as much damage and exhibited 50% more herbivores than plants with ants. Ants also influenced several parameters of plant fitness, as plants without ants suffered a reduction in biomass (−23.7%), leaf production (−51.8%), and reproduction (−24.3%). Effects were much stronger in tropical regions compared to temperate ones. Tropical plants suffered almost threefold higher herbivore damage than plants from temperate regions and exhibited three times more herbivores. Ant removal in tropical plants resulted in a decrease in plant fitness of about 59%, whereas in temperate plants this reduction was not statistically significant. Ant removal effects were also more important in obligate ant–plants (=myrmecophytes) compared to plants exhibiting facultative relationships with hemiptera or those plants with extrafloral nectaries and food bodies. When only tropical plants were considered and the strength of the association between ants and plants taken into account, plants with obligate association with ants exhibited almost four times higher herbivory compared to plants with facultative associations with ants, but similar reductions in plant reproduction. The removal of a single ant species increased plant herbivory by almost three times compared to the removal of several ant species. Altogether, these results suggest that ants do act as plant biotic defenses, but the effects of their presence are more pronounced in tropical systems, especially in myrmecophytic plants. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. N. P. de U. Barbosa, L. Diniz, Y. Oki and F. Pezzini contributed equally to this work and are listed in alphabetical order.     

Effects of food rewards offered by ant–plant Macaranga on the colony size of ants

Myrmecophytes (ant–plants) have special hollow structures (domatia) in which obligate ant partners nest. As the ants live only on the plants and feed exclusively on plant food bodies, sap-sucking homopterans in the domatia, and/or the homopterans honeydew, they are suitable for the study of colony size regulation by food. We examined factors regulating ant colony size in four myrmecophytic Macaranga species, which have strictly species-specific association with Crematogaster symbiont ants. Intra- and interspecific comparison of the plants showed that the ant biomass per unit food biomass was constant irrespective of plant developmental stage and plant species, suggesting that the ant colony size is limited by food supply. The primary food offered by the plants to the ants was different among Macaranga species. Ants in Macaranga beccariana and Macaranga bancana relied on homopterans rather than food bodies, and appeared to regulate the homopteran biomass and, as a consequence, regulate the ants own biomass. In contrast, ants in Macaranga winkleri and Macaranga trachyphylla relied primarily on food bodies rather than homopterans, and the plants appeared to manipulate the ant colony size. Per capita plant investment in ants (ant dry weight plant dry weight^–1) was different among the four Macaranga species. The homoptera-dependent M. beccariana and M. bancana harbored lower biomass of ants than the food-body dependent M. winkleri, suggesting that energy loss is involved in the homoptera-interposing symbiotic system which has one additional trophic level. The plants investment ratio to the ants generally decreased as plants grew. The evolution of the plant reward-offering system in ant–plant–homopteran symbioses is discussed with an emphasis on the role of homopterans.     

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.     

Reduced chemical defence in ant‐plants? A critical re‐evaluation of a widely accepted hypothesis

Since its original formulation by Janzen in 1966, the hypothesis that obligate ant‐plants (myrmecophytes) defended effectively against herbivores by resident mutualistic ants have reduced their direct, chemical defence has been widely adopted. We tested this hypothesis by quantifying three classes of phenolic compounds (hydrolysable tannins, flavonoids, and condensed tannins) spectrophotometrically in the foliage of 20 ant‐plant and non‐ant‐plant species of the three unrelated genera Leonardoxa,Macaranga and Acacia (and three other closely related Mimosoideae from the genera Leucaena, Mimosa and Prosopis). We further determined biological activities of leaf extracts of the mimosoid species against fungal spore germination (as measure of pathogen resistance), seed germination (as measure of allelopathic activity), and caterpillar growth (as measure of anti‐herbivore defence).
Condensed tannin content in three of four populations of the non‐myrmecophytic Leonardoxa was significantly higher than in populations of the myrmecophyte. In contrast, we observed no consistent differences between ant‐plants and non‐ant‐plants in the Mimosoideae and in the genus Macaranga, though contents of phenolic compounds varied strongly among different species in each of these two plant groups. Similarly, among the investigated Mimosoideae, biological activity against spore or seed germination and caterpillar growth varied considerably but showed no clear relation with the existence of an obligate mutualism with ants. Our results did not support the hypothesis of ‘trade‐offs’ between indirect, biotic and direct, chemical defence in ant‐plants.
A critical re‐evaluation of the published data suggests that support for this hypothesis is more tenuous than is usually believed. The general and well‐established phenomenon that myrmecophytes are subject to severe attack by herbivores when deprived of their ants still lacks an explanation. It remains to be studied whether the trade‐off hypothesis holds true only for specific compounds (such as chitinases and amides whose cost may be the direct negative effects on plants’ ant mutualists), or whether the pattern of dramatically reduced direct defence of ant‐plants is caused by classes of defensive compounds not yet studied.     

Reduced ant defenses in <Emphasis Type="Italic">Macaranga</Emphasis> myrmecophytes (Euphorbiaceae) infested with a winged phasmid <Emphasis Type="Italic">Orthomeria cuprinus</Emphasis>

Macaranga is a tree genus that includes many species of myrmecophytes, which are plants that harbor ant colonies within hollow structures known as domatia. The symbiotic ants (plant–ants) protect their host plants against herbivores; this defense mechanism is called ‘ant defense’. A Bornean phasmid species Orthomeria cuprinus feeds on two myrmecophytic Macaranga species, Macaranga beccariana and Macaranga hypoleuca, which are obligately associated with Crematogaster ant species. The phasmids elude the ant defense using specialized behavior. However, the mechanisms used by the phasmid to overcome ant defenses have been insufficiently elucidated. We hypothesized that O. cuprinus only feeds on individual plants with weakened ant defenses. To test the hypothesis, we compared the ant defense intensity in phasmid-infested and non-infested M. beccariana trees. The number of plant–ants on the plant surface, the ratio of plant–ant biomass to tree biomass, and the aggressiveness of plant–ants towards experimentally introduced herbivores were significantly lower on the phasmid-infested trees than on the non-infested trees. The phasmid nymphs experimentally introduced into non-infested trees, compared with those experimentally introduced into phasmid-infested trees, were more active on the plant surface, avoiding the plant–ants. These results support the hypothesis and suggest that ant defenses on non-infested trees effectively prevent the phasmids from remaining on the plants. Thus, we suggest that O. cuprinus feeds only on the individual M. beccariana trees having decreased ant defenses, although the factors that reduce the intensity of the ant defenses remain unclear.     

Competition hierarchy and plant defense in a guild of ants on tropical Passiflora

In facultative ant–plant interactions, ants may compete with each other for food provided by extrafloral nectar (EFN) plants. We studied resource competition and plant defense in a guild of ants that use the same EFN resource provided by two species of Passiflora in a seasonal rain forest in tropical China. At least 22 ant species were recorded using the EFN resource, although some of those species were rare. Among these ants, Paratrechina sp.1 and Dolichoderus thoracicus were more aggressive than other species. Ant aggressiveness measured as ant behavioral dominance index (BDI) was positively correlated with ant abundance on the Passiflora species studied. Ant BDI was also positively correlated to the protection that ants provided against herbivory. In Passiflora siamica, the number of workers patrolling on the plants did negatively correlate with average leaf loss per plant. We conclude that in this facultative Passiflora–ant system, plant defense upon herbivore was indeed influenced by the total number of ants present on plant and the aggressiveness of these ants.     

Interspecific variation and ontogenetic change in antiherbivore defense in myrmecophytic Macaranga species

The present study examined whether or not coexisting congeneric plant species have different defense strategies against herbivores, and the intensity of defense changes ontogenetically. We focused on nine myrmecophytic Macaranga species and estimated the intensity of non-biotic and biotic defense by the degree of leaf damage in ant-free and ant-occupied plants, respectively. Ant colonization of myrmecophytic Macaranga species occurred in the early stage of plant development (5–50 cm-tall seedlings). Following the colonization, damage by leaf eaters was minimized and stable during the ontogenetic development of the host plants due to protection by ants. In ant-free trees, however, herbivore damage was immense in seedlings and decreased as trees grew. Interspecific comparison of leaf damage and herbivore fauna supported that coexisting congeneric plants differ in their types of non-biotic (chemical/structural) defense: without ant protection, Macaranga beccariana, for example, was somewhat resistant to leaf eaters but susceptible to gall-makers, Macaranga trachyphylla was heavily infested by generalist leaf eaters, and Macaranga winkleri was exploited by ant-predatory birds. Despite these variations in chemical/structural defense, ant-colonized plants were generally well defended by ants against all kinds of herbivores. This suggests that the individual host-specific ant mutualists are well adapted to deter the chemically or structurally adapted herbivores. These results imply that in the history of diversification in the Macaranga–ant–herbivore system, a sequence of mutual counter adaptation took place not only between plants and herbivores but also between ants and herbivores.     

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.     

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.     

Ant Defense Versus Induced Defense in Lafoensia pacari (Lythraceae), a Myrmecophilous Tree of the Brazilian Cerrado1

We compared the effects of ant presence at extrafloral nectaries of Lafoensia pacari St. Hil. on herbivore damage and silicon accumulation. Plants that were accessible to ants experienced lower herbivory levels over the first 3 mo of the experiment. After 3 mo, most leaves were fully expanded with inactive extrafloral nectaries; by 6 mo there was no effect of ant access on herbivore damage. Along with experiencing higher herbivory, plants in the ant‐exclusion treatment had significantly higher silicon levels in their leaves, suggesting that silicon serves as an induced defense in this ant–plant–herbivore interaction.     

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.     

Species specificity in settling-plant selection by foundress ant queens in <Emphasis Type="Italic">Macaranga</Emphasis>–<Emphasis Type="Italic">Crematogaster</Emphasis> 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. Electronic Publication     

Plant defense, herbivory, and the growth of Cordia alliodora trees and their symbiotic Azteca ant colonies

The effects of herbivory on plant fitness are integrated over a plant??s lifetime, mediated by ontogenetic changes in plant defense, tolerance, and herbivore pressure. In symbiotic ant?Cplant mutualisms, plants provide nesting space and food for ants, and ants defend plants against herbivores. The benefit to the plant of sustaining the growth of symbiotic ant colonies depends on whether defense by the growing ant colony outpaces the plant??s growth in defendable area and associated herbivore pressure. These relationships were investigated in the symbiotic mutualism between Cordia alliodora trees and Azteca pittieri ants in a Mexican tropical dry forest. As ant colonies grew, worker production remained constant relative to ant-colony size. As trees grew, leaf production increased relative to tree size. Moreover, larger trees hosted lower densities of ants, suggesting that ant-colony growth did not keep pace with tree growth. On leaves with ants experimentally excluded, herbivory per unit leaf area increased exponentially with tree size, indicating that larger trees experienced higher herbivore pressure per leaf area than smaller trees. Even with ant defense, herbivory increased with tree size. Therefore, although larger trees had larger ant colonies, ant density was lower in larger trees, and the ant colonies did not provide sufficient defense to compensate for the higher herbivore pressure in larger trees. These results suggest that in this system the tree can decrease herbivory by promoting ant-colony growth, i.e., sustaining space and food investment in ants, as long as the tree continues to grow.     

Non-ant antiherbivore defenses before plant-ant colonization in Macaranga myrmecophytes

We examined changes in the intensity of non-ant defenses of three myrmecophytic Macaranga species before and after the initiation of symbiosis with ants in a Bornean dipterocarp forest. The intensities of non-ant defenses at different growth stages of each Macaranga species were estimated by measuring the survival rate of larvae of the common cutworm, Spodoptera litura, when the larvae were fed on fresh leaves from seedlings (saplings) at three growth stages of each Macaranga species. In all species, the intensity of the non-ant defenses when seedlings had not yet received symbiont foundress queens was significantly higher than that after ant defense was well established. These results support the hypothesis that myrmecophytic Macaranga may defend themselves sufficiently via non-ant defenses before beginning symbiosis with ants and that the intensity of non-ant defenses may decrease as the symbiont colony size increases. We suggest that, where the status of myrmecophytism changes as plant–ant colonies grow, the decrease in the intensity of non-ant defenses which we detected after the establishment of ant colonies might generate an optimal allocation of metabolic cost to ant and non-ant defenses under resource limitations. We also measured leaf toughness, which is considered to be one of the most important agents of non-ant defenses against herbivorous insects, at different plant stages to assess its contribution to the change in the intensity of non-ant defenses after ant colonization. However, we found no evidence that changes in leaf toughness have a significant effect on the change in balance of the two antiherbivory mechanisms. Received: February 2, 2001 / Accepted: August 21, 2001     

Reciprocally beneficial interactions between introduced plants and ants are induced by the presence of a third introduced species

Interspecific interactions play an important role in the success of introduced species. For example, the ‘enemy release’ hypothesis posits that introduced species become invasive because they escape top–down regulation by natural enemies while the ‘invasional meltdown’ hypothesis posits that invasions may be facilitated by synergistic interactions between introduced species. Here, we explore how facilitation and enemy release interact to moderate the potential effect of a large category of positive interactions – protection mutualisms. We use the interactions between an introduced plant (Japanese knotweed Fallopia japonica), an introduced herbivore (Japanese beetle Popillia japonica), an introduced ant (European red ant Myrmica rubra), and native ants and herbivores in riparian zones of the northeastern United States as a model system. Japanese knotweed produces sugary extrafloral nectar that is attractive to ants, and we show that both sugar reward production and ant attendance increase when plants experience a level of leaf damage that is typical in the plants’ native range. Using manipulative experiments at six sites, we demonstrate low levels of ant patrolling, little effect of ants on herbivory rates, and low herbivore pressure during midsummer. Herbivory rates and the capacity of ants to protect plants (as evidenced by effects of ant exclusion) increased significantly when plants were exposed to introduced Japanese beetles that attack plants in the late summer. Beetles were also associated with greater on‐plant foraging by ants, and among‐plant differences in ant‐foraging were correlated with the magnitude of damage inflicted on plants by the beetles. Last, we found that sites occupied by introduced M. rubra ants almost invariably included Japanese knotweed. Thus, underlying variation in the spatiotemporal distribution of the introduced herbivore influences the provision of benefits to the introduced plant and to the introduced ant. More specifically, the presence of the introduced herbivore converts an otherwise weak interaction between two introduced species into a reciprocally beneficial mutualism. Because the prospects for facilitation are linked to the prospects for enemy release in protection mutualisms, species introductions can have complex effects on existing species interactions, between both native and introduced species.     

Domatia as most important adaptations in the evolution of myrmecophytes in the paleotropical tree genusMacaranga (Euphorbiaceae)

The paleotropical tree genusMacaranga (Euphorbiaceae) comprises all stages of interaction with ants, from facultative associations to obligate myrmecophytes. In SE.-Asia food availability does not seem to be the limiting factor for the development of a close relationship since all species provide food for ants in form of extrafloral nectar and/or food bodies. Only myrmecophyticMacaranga species offer nesting space for ants (domatia) inside internodes which become hollow due to degeneration of the pith. Non-myrmecophytic species have a solid stem with a compact and wet pith and many resin ducts. The stem interior of some transitional species remains solid, but the soft pith can be excavated. The role of different ant-attracting attributes for the development of obligate ant-plant interactions is discussed. In the genusMacaranga, the provision of nesting space seems to be the most important factor for the evolution of obligate myrmecophytism.