ArticlePDF Available

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

Article

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

Abstract

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.
A preview of the PDF is not available
... palomastix possess large opener and closer muscles in its head that allows it to chew live wood in the bark of living trees to build its nest (Khalife et. al 2018). This is different from ant-myrmecophyte associations, whereby the myrmecophyte host possess special structures such as hollow stems for ants to nest in (Fiala et. al 1989(Fiala et. al , 1994Janzen 1966Janzen , 1969. Owing to the bark-digging nature of Rhopalomastix, they can construct a complex network of tunnels and chambers in the cork cambium layer (Yong et. al 2019) to house their brood and diaspidid partners. Ants like Camponotus (Tschinkel 2005), Acromyrmex (Verza et. al 2020) and Formica (Mikheyev and Tschinkel 2004) ...
Article
Rhopalomastix is a bark digger ant that nests in the bark of living trees. The ants share a mutualistic relationship with diaspidids (armoured scale insects), housing them in their nest tunnels in the bark of a tree. Two colonies of Rhopalomastix sp. were sampled from two cultivars of mango trees in a mango plantation in Thailand. The architecture of the nest was mapped out and the respective resident diaspidid partners collected. Rhopalomastix built two different types of tunnels, one chewed through the live wood while the other was created by covering fissures in the bark with a frass roof. Tunnels were constructed at different depths and were inter-connected to form a complex network. Ant brood and diaspidids were not evenly distributed, with most found in deeper and wider chewed tunnels. A new species of pupillarial diaspidid, Ligaspis sp. was found in both colonies - this is the second report of a pupillarial diaspidid being associated with Rhopalomastix. We discuss the trophic relationship between ants and their diaspidid partners, and the potential impact this association has on host fruit trees.
... Resource flow from plant to ant should increase with coevolutionary specialization, because plants that maintain larger resident ant colonies are better protected (Rocha & Bergallo 1992), and ants that better protect the plant reap more benefits. The lineages that have been studied conform to this expectation, with specialized myrmecophytes supplying food resources to their resident ants at higher rates than do their less specialized congeners to opportunistic ants (reviewed by Heil & McKey 2003), and specialized plant-ants providing more effective protection than do opportunistic ants (Fiala et al. 1994;Nomura et al. 2000). The cost to the plant of supporting its ants increases proportionally to investment: producing more resources entails greater costs. ...
... EFNs are produced by at least 4,000 plant species throughout the world (Weber & Keeler, 2012). Their nectar functions to attract ants (Bentley, 1977), which then repel or kill insect herbivores (Del-Claro et al., 2016;Heil, 2015;Rosumek et al., 2009), potentially reducing plant herbivory and increasing plant growth and reproductive success (Fiala, Grunsky, Maschwitz, & Linsenmair, 1994;Marazzi, Conti, Sanderson, McMahon, & Bronstein, 2012;Nascimento & Del-Claro, 2010). Extrafloral nectar can be of particular value as a food resource for ants, with important implications for the structure and composition of ant communities and for multitrophic ant-plant-herbivore interactions Dáttilo et al., 2015;Díaz-Castelazo, Chavarro-Rodríguez, & Rico-Gray, 2017;Lange, Calixto, & Del-Claro, 2017;Lange, Dáttilo, & Del-Claro, 2013). ...
Article
Full-text available
1. Most terrestrial species occur in human‐modified landscapes that are experiencing climate change. In addition to direct impacts on species, both anthropogenic disturbance and climate change can have important effects through changes in species interactions, including the disruption of ecological services provided by them. 2. Here we investigate how chronic anthropogenic disturbance (CAD) and aridity affect the effectiveness of plant protection services provided by ants to plants bearing extrafloral nectaries (EFNs). 3. The study was conducted across 13 01‐ha plots distributed along CAD and aridity gradients in Caatinga vegetation of northeastern Brazil. We focused on Pityrocarpa moniliformis, the most abundant and widely distributed EFN‐bearing tree species occurring in our study area, and we used experimental attack rates on termites as a measure of effectiveness of ant protection services. We investigated the relative roles of nectar production (volume and concentration) and ant species composition in mediating the effects of CAD and aridity on the effectiveness of protection services. 4. Attack rates by ants declined with increasing aridity but were not related to CAD. The volume of extrafloral nectar declined with increasing CAD but was not affected by aridity, whereas the concentration was not related to either CAD or aridity. The composition of attendant ant species varied with aridity but not with CAD. 5. Synthesis: Our findings suggest that CAD does not affect plant‐protection services mediated by EFNs in Brazilian Caatinga. However, ant‐protection services declined with increased aridity, and this occurred through changes in the composition of attendant ant species rather than by changes in the production of extrafloral nectar. Such a response to increasing aridity highlights the vulnerability of EFN‐bearing plants to climate change through decreased predation of herbivores.
... More broadly, many plant species form strong mutualistic associations with ants to reduce the risk of herbivory by offering them rewards such as food bodies, extra-floral nectaries, and domatia (i.e., nesting sites; Chomicki, Staedler, Schönenberger, & Renner, 2016;Fiala, Maschwitz, Pong, & Helbig, 1989;Janzen, 1966;Webber, Moog, Curtis, & Woodrow, 2007). Even facultative or opportunistic ant-plant interactions are known to reduce herbivory and deter other arthropods from plants occupied or visited frequently by ants (Bentley, 1977;Chamberlain & Holland, 2009;Fiala, Grunsky, Maschwitz, & Linsenmair, 1994;Rosumek et al., 2009;Trager et al., 2010). ...
Article
Full-text available
Competitive interactions between distantly related clades could cause complementary diversity patterns of these clades over large spatial scales. One such example might be ants and birds in the eastern Himalaya; ants are very common at low elevations but almost absent at mid‐elevations where the abundance of other arthropods and insectivorous bird diversity peaks. Here, we ask if ants at low elevations could compete with birds for arthropod prey. Specifically, we studied the impact of the Asian weaver ant (Oecophylla smaragdina), a common aggressive ant at low elevations. Diet analysis using molecular methods demonstrate extensive diet overlap between weaver ants and songbirds at both low and mid‐elevations. Trees without weaver ants have greater non‐ant arthropod abundance and leaf damage. Experimental removal of weaver ants results in an increase in the abundance of non‐ant arthropods. Notably, numbers of Coleoptera and Lepidoptera were most affected by removal experiments and were prominent components of both bird and weaver ant diets. Our results suggest that songbirds and weaver ants might potentially compete with each other for arthropod prey at low elevations, thereby contributing to lower insectivorous bird diversity at low elevations in eastern Himalaya. Competition with ants may shape vertebrate diversity patterns across broad biodiversity gradients.
... Resource flow from plant to ant should increase with coevolutionary specialization, because plants that maintain larger resident ant colonies are better protected (Rocha & Bergallo 1992), and ants that better protect the plant reap more benefits. The lineages that have been studied conform to this expectation, with specialized myrmecophytes supplying food resources to their resident ants at higher rates than do their less specialized congeners to opportunistic ants (reviewed by Heil & McKey 2003), and specialized plant-ants providing more effective protection than do opportunistic ants (Fiala et al. 1994;Nomura et al. 2000). The cost to the plant of supporting its ants increases proportionally to investment: producing more resources entails greater costs. ...
... The tree genus Macaranga Thouars (Euphorbiaceae) is widely distributed from Africa to the Pacific islands (Whitmore 2008) and has a wide spectrum of ant-plant mutualisms (e.g. Fiala et al. 1991Fiala et al. , 1994Fiala et al. , 1999. Many Macaranga species are true myrmecophytes harboring mutualistic species-specific ants of the genus Crematogaster Lund (Hymenoptera: Formicidae) that reduce the infestation of herbivores (Fiala et al. 1989;Itioka et al. 2000). ...
Article
We describe a gall midge Macarangamyia itiokai Elsayed & Tokuda gen. n., sp. n. belonging to the subtribe Schizomyiina (Diptera: Cecidomyiidae: Asphondyliini) inducing petiole galls on Macaranga bancana (Miq.) in Lambir Hills National Park, Borneo, Malaysia. The new genus is distinguishable from all known genera of Schizomyiina by the unique dorsally placed aedeagus slit, the short, membranous, protrusible ovipositor, with scattered strong setae ventrally and dorsally, and the presence of spiracles on all larval thoracic segments. It is compared and separated from its closely related Oriental genera of Schizomyiina.
Article
Full-text available
Terpenes are an important group of plant specialized metabolites (PSM) influencing, amongst other functions, defence mechanisms against pests. We used a Genome-Wide Association Study (GWAS) to identify single nucleotide polymorphism (SNP) markers and putative candidate genes for terpene traits. We tested 15,387 informative SNP markers derived from genotyping 416 Eucalyptus grandis individuals for association with three terpene traits, 1,8-cineole, γ-terpinene and p-cymene. A Multi-Locus Mixed Model (MLMM) analysis identified 21 SNP markers for 1,8-cineole on chromosomes 2, 4, 6, 7, 8, 9, 10 and 11, that individually explained 3.0% to 8.4% and jointly 42.7% of the phenotypic variation. Association analysis of γ-terpinene found 32 significant SNP markers on chromosomes 1, 2, 4, 5, 6, 9 and 11, explaining 3.4 to 15.5% and jointly 54.5% of phenotypic variation. For p-cymene 28 significant SNP markers were identified on chromosomes 1, 2, 3, 5, 6, 7, 10 and 11, explaining 3.4% to 16.1% of the phenotypic variation and jointly 46.9%. Our results show that variation underlying the three terpene traits is influenced by a few minor loci in combination with a few major effect loci, suggesting an oligogenic nature of the traits.
Article
Ants benefit myrmecophytic plants by two main activities defending them from herbivores and offering nutrients. Ants' territorial defense behavior also benefits their myrmecophytic plants; in the case of trees, this behavior includes eliminating structural parasites (epiphytes and lianas). These benefits could also occur with myrmecophytic epiphytes by decreasing the abundance of competing epiphytes. In two subunits of a tropical dry forest in the center of Mexico, we a.- recorded the diversity of ants associated with the myrmecophyte Tillandsia caput-medusae, and experimentally tested: b.- the effect of the ants associated with the myrmecophyte in the removal of its seeds and the seeds of other sympatric non-myrmecophyte species of Tillandsia; and c.- if seed remotion by ants corresponds with epiphyte load in the preferred (Bursera copallifera) and limiting phorophyte species (B. fagaroides, Ipomoea pauciflora, and Sapium macrocarpum). In five trees per species, we tied seed batches of Tillandsia caput-medusae, T. hubertiana, T. schiedeana, and T. recurvata. One seed batch was close, and the other far away from a T. caput-medusae with active ants. Between forest subunits, ant richness was similar, but diversity and evenness differed. Ants diminish seed establishment of all the Tillandsia species; this effect is stronger in the forest subunit with a large ant diversity, maybe because of ant competition. Seed remotion by ants is independent of phorophyte species identity. Although ants can provide benefits to T. caput-medusae, they also could be lowering their abundance.
Chapter
Full-text available
A study on the phylogenetics of Macroglossus sobrinus (Greater Long‐nosed Fruit Bat) from Peninsular Malaysia was done using partial cytochrome b (cyt‐b) mitochondrial DNA (mtDNA) gene. The specimens of M. sobrinus were collected from Kedah (Weng Ulu Muda Forest Reserve), Perak (Bintang Forest Reserve), Selangor (Ulu Langat), Melaka (Asahan Catchment Area), Johor (Gunung Ledang), Kelantan (Gua Musang), and Pahang (Krau Wildlife Reserve). Thirty nine cyt‐b sequences including eighteen sequences of M. sobrinus, twenty sequences of M. minimus taken from the GenBank, and a sequence of Penthetor lucasi (Lucas's Short‐nosed Fruit Bat) as an outgroup were incorporated in the analyses. Three main methods namely neighbour joining (NJ), maximum parsimony (MP), and maximum likelihood (ML) were used in the phylogenetic trees reconstruction followed by the consensus phylogenetic tree to summarize the overall findings. The four trees were reconstructed to determine the genetic relationship between M. sobrinus and M. minimus. Generally, the trees indicated genetic divergence between populations of M. sobrinus. The result was further supported by very low genetic distances based on Kimura 2‐parameter distance (1980) calculation. There was an individual of M. sobrinus (Gua Musang, Kelantan) clustered with the M. minimus individuals, thus indicating of possible misidentification. Apart from that, M. sobrinus from Kelantan gave the highest nucleotide diversity, Pi (Jukes & Cantor 1969) with 0.65%, followed by Perak (0.36%), Kedah (0.27%), Selangor (0.18%), and finally Pahang and Melaka with no nucleotide diversity. Overall, the nucleotide diversity of M. sobrinus in Peninsular Malaysia was 0.29% indicating low level of genetic diversity. However, the sample size is too small to relate the results with the phylogeography and population genetic views. Therefore, more extensive studies incorporating other mtDNA genes with higher rate of evolution such as control region gene are highly recommended in the future study.
Article
Full-text available
Vetches (Vicia spp.) were studied in the San Francisco Bay Area of California in the spring of 1978. The stipular nectaries of the vetches are visited by the Argentine ant, Iridomyrmex humilis Mayr. The nectaries were removed to exclude ants in controlled experiments to determine if these ants protect the vetches from herbivores or seed predators. Plants with excised nectaries suffered substantially greater damage to their foliage than control plants, indicating that ants protect the foliage. There was no indication that ants protect the vetches from seed predators, but fruit set was substantially lower in plants with excised nectaries. Analysis of sugar and amino acid composition of extrafloral nectar served as a basis for feeding tests with Argentine ants by using artificial nectar solutions. Ants preferred sucrose and glucose solutions over fructose. They showed no preference for any one sugar mixture over another, nor did they exhibit differential recruitment to artificial nectar solutions containing only sugars or sugars and amino acids.
Article
Insect herbivores that specialize on ant-plants must contend with a resident colony of predators that can use the insect as food or at least deter it from feeding on the plant. In Papua New Guinea, the euphorb Endospermum labios Schodde is commonly inhabited by Camponotus quadriceps F Smith ants that are easily alarmed, recruit effectively, and bite intruders on the host plant. Plants that lack Camponotus often have other resident ant species. We compared the size, herbivore load, herbivory level, frequency of plants supporting vines, and degree of ant defense on E. labios with different ant inhabitants growing intermixed in disturbed forest. A glabrous morph of this tree had distinctly larger colonies of Camponotus, was dramatically larger on average, and suffered very little herbivore damage compared to pubescent morphs even though the morphs appeared to be equally preferred by foundress ants for colony initiation and as food by uraniid caterpillars. Herbivores on E. labios escaped ant defenses by exploiting plants that lacked Camponotus colonies. We hypothesize that colony initiation was less successful in the pubescent morphs in part because of a parasitic fly that attacks foundress ants.
Article
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.
Article
Novel 2-ethyl-5-alkylpyrrolidines and their corresponding 1-pyrrolines have been identified as poison gland products from an unidentified Australian species ofMonomorium. The major alkaloids present in the venom of this ant aretrans-2-ethyl-5-undecylpyrrolidine andtrans-2-ethyl-5-(12-tridecen-1-yl)pyrrolidine. The position of the double bond in the latter was established from its dimethyl-disulfide adduct after the amine function had been protected, and the stereochemistry of the alkyl groups was determined by direct comparison with synthetic compounds. The corresponding 1-pyrrolines were also detected in varying amounts in this venom. The pyrrolidines and 1-pyrrolines possess considerable insecticidal activity when evaluated against termite workers. The alkaloidal venoms ofMonomorium appear to be an important factor contributing to the success of these small ants both as competitors and as predators.
Article
We present the results of a study of the ant and herbivore faunas found on the leaves of five species of euphorbiaceous saplings (Macaranga aleuritoides, M. punctata, M. quadriglandulosa, Mallotus philippensis, and Homalanthus novo-guineensis) during the wet season in a submontane tropical rain forest in Papua New Guinea. All of these species have foliar extrafloral nectaries. The abundance, density, and composition of the ant and herbivore communities differed among the tree species; ant densities per unit leaf area varied by a factor of ca 20; and herbivore densities varied by a factor of ca 3. The leaves of these species were visited by 6 to 13 species of ants. Ants were experimentally excluded from branches or small saplings of three tree species: Macaranga aleuritoides, M. punctata, and Homolanthus novo-guineensis. Numbers of herbivores and levels of leaf damage were found to be significantly greater on ant exclusion saplings than on ant access saplings for M. aleuritoides, but not for the other two species. Macaranga aleuritoides was visited by more ant species than the other four tree species and had the highest number of ants per leaf. The antplant associations we examined are relatively unspecialized compared with most of the ant associations with euphorbs that have been studied previously in the Indo-Malesian tropics.
Article
The hypothesis that ants (Pheidole minutula) associated with the myrmecophytic melastome Maieta guianensis defend their host-plant against herbivores was investigated in a site near Manaus, Amazonas, Brazil. M. guianensis is a small shrub that produces leaf pouches as ant domatia. Plants whose ants were experimentally removed suffered a significant increase in leaf damage compared with control plants (ants maintained). Ants patrol the young and mature leaves of Maieta with the same intensity, presumably since leaves of both ages are equally susceptible to herbivore attack. The elimination of the associated ant colony, and consequent increase in herbivory, resulted in reduced plant fitness. Fruit production was 45 times greater in plants with ants than in plants without ants 1 year after ant removal.