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.     

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

To examine interspecific variation in the intensity of ant defense among three sympatric species of obligate myrme‐cophytes of Macaranga (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 was M. winkleri, M. trachyphylla, and M. 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 on Macaranga. 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 three Macaranga species 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 among Macaranga species to understand the herbivore community on Macaranga plants and the mechanisms that promote the coexistence of multiple Macaranga myrmecophytes.     

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     

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.     

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.     

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.     

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.     

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.     

Correlation between the leaf turnover rate and anti-herbivore defence strategy (balance between ant and non-ant defences) amongst ten species of <Emphasis Type="Italic">Macaranga</Emphasis> (Euphorbiaceae)

We measured variation in the intensities of ant and non-ant anti-herbivore defences amongst ten Macaranga species in Sarawak, Malaysia. Intensities of non-ant defences were estimated by measuring effects of fresh leaves (provided as food) of these Macaranga species on survival of common cutworm larvae [Spodoptera litura (Fabricius), Lepidoptera: Noctuidae]. Intensities of ant defences were estimated by measuring ant aggressiveness in the presence of artificial damage inflicted on plants. As part of our examination of non-ant defences, we measured leaf toughness (punch strength, by penetrometry), and the contents of total phenols and condensed tannin. We demonstrated interspecific variation in intensities of both ant and non-ant defences amongst ten Macaranga species and showed that the rank order of ant defence intensity was negatively correlated with the intensity of non-ant defence. We also found that the balance between ant and non-ant defence intensity was correlated with the rates of leaf turnover and shoot growth. Species investing more in ant defence tended to have higher leaf turnover rates. Macaranga species that occur preferentially in shadier microhabitats had lower leaf turnover rates, suggesting that non-ant defences are more cost-effective in more shade-tolerant species. Our results also suggest that the total intensity of non-ant defences is positively correlated with both leaf toughness and total phenol content.     

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.     

Pruning of host plant neighbours as defence against enemy ant invasions: <Emphasis Type="Italic">Crematogaster </Emphasis>ant partners of <Emphasis Type="Italic">Macaranga</Emphasis> protected by "wax barriers" prune less than their congeners

Many ant partners of tropical ant-plants prune the leaves and shoot tips of other plants growing around their hosts. According to the hypothesis proposed by Davidson et al. (Ecology 69:801-808), this specialized behaviour not only protects the host plants against overgrowth, but it also conveys a direct benefit to the ant colony as it removes contact points to the neighbouring vegetation where invasions of enemy ants could occur. Here we test this hypothesis by comparing pruning intensity in five closely related Crematogaster (subgenus Decacrema) plant-ant species (and one species of Technomyrmex) that differ in their exposure to competition by other ants. Pruning intensity was quantified by measuring the area loss of paper tape pieces wrapped around the stems of Macaranga host plants. All Crematogaster (Decacrema) ants tested but not Technomyrmex sp. pruned, but the intensity of the behaviour varied strongly between and within species. Pruning was significantly weaker in the three tested Crematogaster species inhabiting Macaranga host plants with a slippery, waxy stem surface, which functions as a mechanical barrier protecting the specific ant partners against generalist competitors. Pruning was generally stronger on more densely ant-populated trees. Even though the number of ants per twig length was lower in associations of ants with glaucous Macaranga hosts, only part of the variation of pruning activity could be explained by "ant density". When corrected for ant density, "wax-running" Crematogaster (Decacrema) ants still pruned more weakly than their congeners inhabiting non-glaucous Macaranga hosts. Pruning is obviously most important when an ant-plant is potentially accessible to intruders, but less necessary when the ant colony is isolated by a protective wax barrier. Our results support the hypothesis that "selfish" defence against invasions is the major selective pressure that has led to the development and maintenance of pruning behaviour in weakly competitive plant-ants.     

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.     

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.     

Thorn‐dwelling ants provide antiherbivore defence for camelthorn trees,Vachellia erioloba,in Namibia

Ants are widely employed by plants as an antiherbivore defence. A single host plant can associate with multiple, symbiotic ant species, although usually only a single ant species at a time. Different plant‐ant species may vary in the degree to which they defend their host plant. In Kenya, ant–acacia interactions are well studied, but less is known about systems elsewhere in Africa. A southern African species, Vachellia erioloba, is occupied by thorn‐dwelling ants from three different genera. Unusually, multiple colonies of all these ants simultaneously and stably inhabit trees. We investigated if the ants on V. erioloba (i) deter insect herbivores; (ii) differ in their effectiveness depending on the identity of the herbivore; and (iii) protect the tree against an important herbivore, the larvae of the lepidopteran Gonometa postica. We show that experimental exclusion of ants leads to greater levels of herbivory on trees. The ants inhabiting V. erioloba are an effective deterrent against hemipteran and coleopteran, but not lepidopteran herbivores. Defensive services do not vary among ant species, but only Crematogaster ants exhibit aggression towards G. postica. This highlights the potential of the V. erioloba–ant mutualism for studying ant–plant interactions that involve multiple, simultaneously resident thorn‐dwelling ant species.     

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.     

Host‐plant dissections reveal contrasting distributions of Crematogaster ants and their symbionts in two myrmecophytic Macaranga species

1. Ant–plant mutualisms are among the most widespread and ecologically important insect–plant interactions in the tropics. The multitrophic mutualism involving Macaranga plants (Euphorbiaceae) and Crematogaster ants (Formicidae) is the most diverse in Southeast Asia. This interaction also includes trophobiotic scale insects (Coccidae) and nematodes inhabiting ant refuse piles. 2. Here two myrmecophytic systems were compared, Macaranga trachyphylla with Crematogaster captiosa (Mt + Cc) and Macaranga beccariana with Crematogaster decamera (Mb + Cd), using a fine‐scale dissection of the stems. For the two plant species, for each internode, both contents (ants, coccids, refuse piles) and structure (internode height, numbers of open and occluded ant holes) were recorded. 3. There were significant patterns in the vertical distribution of ant colonies and their symbionts in the plant stems. Most coccids were kept in the highest sections of both systems, although Mb + Cd hosted a broader range of coccid species than Mt + Cc. Three nematode species were recorded, but with a rather low specificity to plant or ant species. Furthermore, the fine‐scale distribution showed aggregation of closed holes with ant brood and separation of nematode‐infested refuse piles from eggs. 4. The results of this study indicate that ants manipulate spatial colony structure via distribution of brood, holes and the symbionts. It is suggested that ants optimise the location of refuse piles and occluded holes via spatial heterogeneity in their distribution among internodes. This paper discusses the protective role of occluded holes and demonstrates some general interactions with other symbiotic fauna.     

DEVELOPMENTAL ANATOMY AND ULTRASTRUCTURE OF THE ANT-FOOD BODIES (BECCARIIAN BODIES) OF MACARANGA TRILOBA AND M. HYPOLEUCA (EUPHORBIACEAE)

Macaranga is a common secondary growth tree of S.E. Asia. Nine species possess hollow stems which harbor an ant colony, and also produce food bodies which are eaten by the ants. In return, the ants protect the plant from herbivore damage. The multicellular food bodies of M. triloba (Bl.) Muell. Arg. are developed on the underside of down-turned clasping stipules, while in M. hypoleuca (Reichb. f. and Zoll.) Muell. Arg. they are produced on the abaxial surface of young leaves. Food body cells of both species are very rich in lipid, contain large starch grains, and possess an electron-dense hyaloplasm. It is proposed to name the Macaranga ant-food bodies Beccariian bodies in honor of the Italian botanist Odoardo Beccari who explored S.E. Asia in the late 1800s.     

Aggressiveness of ants attracted to the extrafloral nectary‐bearing plant,Mallotus japonicus,and temporal fluctuations in their abundance

Many plants that bear extrafloral nectaries (EFNs) attract various ant species that can exclude herbivores. The aggressiveness of the attracted ants and their temporal activity patterns are important factors that can affect the efficiency of herbivore exclusion from the plant. However, the characteristics of this mutualistic relationship between EFN‐bearing plants and ants have not been sufficiently elucidated. We investigated the aggressiveness of six ant species against the common armyworm, Spodoptera litura Fabr., and temporal fluctuations in the abundance of four aggressive ant species on an EFN‐bearing plant, Mallotus japonicus (L.f.) Müll. Arg. Workers of Crematogaster teranishii Santschi, Pheidole noda Smith, Pristomyrmex punctatus Smith and Formica japonica Motschoulsky were observed to be highly aggressive. In contrast, workers of Camponotus vitiosus Smith showed low aggressiveness. Paratrechina flavipes Smith workers did not attack the herbivore. The activity patterns of the four aggressive ant species greatly differed. Crematogaster teranishii and Ph. noda workers were constantly active throughout the day and night. In contrast, F. japonica was diurnal. Pristomyrmex punctatus was principally nocturnal. Formica japonica workers foraged solitarily, whereas workers of the other three species foraged in a group or recruited nestmates. Our results suggest that the efficacy of the indirect defense in M. japonicus depends principally on the attracted ant species.     

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.