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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.
... reticulatus (Dunn) F.P.Metcalf. The description of leaf micromorphological features follows Fiala et al. (1994) and Živa et al. (2012), and based on seven specimens collected in the field, including the holotype and the two paratypes. ...
Mallotus bullatus M.T.An & J.H.Yu, sp. nov. (Euphorbiaceae), a species new to science discovered in Guizhou, China, is described and illustrated here, and its phylogenetic position among other Mallotus species is presented. Morphological, micro-morphological, and molecular evidence is presented as attestation of its novelty. The new species morphologically resembles M. philippensis var. reticulatus and M. philippensis var. philippensis, but it clearly differs by having bullate leaf surfaces (vs. not bullate), leaf margins entire or nearly so (vs. entire or nearly so in M. philippensis var. philippensis and coarsely serrate in M. philippensis var. reticulatus), leaf margins sometimes bearing red glands (vs. red glands absent), 5 sepals in staminate flowers (vs. 3–4 in M. philippensis var. philippensis and 4 in M. philippensis var. reticulatus), fruits with spines (vs. spines absent in M. philippensis var. philippensis and present in M. philippensis var. reticulatus), and abaxial leaf epidermal scattered and clustered vein hairs 0.1–0.8 mm long (vs. 0.04–0.28 mm long in M. philippensis var. philippensis and 0.05–0.1 mm long in M. philippensis var. reticulatus). Molecular phylogenetic analysis (BS = 100% / BS = 96%, PP = 1 / PP = 1) provides strong evidence supporting M. bullatus as a new species within the genus Mallotus and supports its placement in M. sect. Philippinenses as sister to M. philippensis.
... The interaction between ants and myrmecophytes is often obligate and involves a few ant species associated with each plant species, while EFN plants sustain a facultative interaction with ants, meaning non-specialization between both parties (Bl€ uthgen et al., 2007;Fiala et al., 1999). This gradient between facultative and obligatory interactions can, therefore, impact the results of the protection mutualism (Fiala et al., 1994). ...
Extrafloral nectaried plants and myrmecophytes offer resources to ants that engage in protective mutualisms. The role of different ant species in herbivore deterrence has long been analyzed by using insect baits, and ants are regarded as effective plant guards if they attack the insects. Here, by performing a literature review, we conducted a comparative investigation on which ants display aggression toward experimental prey, which ants are better plant guards, and which plants (extrafloral nectaried plants or myrmecophytes) are better defended by ants. Data revealed that studies evaluating ant aggression toward insect baits have been performed on 37 extrafloral nectaried plant species and 19 myrmecophytes, and have involved over 30 genera of ants. Extrafloral nectaried plants and myrmecophytes rely on specific ant fauna to defend them from herbivores. In extrafloral nectaried plants, Camponotus and Crematogaster were regarded as the best plant protectors, as they attacked insects in nearly all plants. In myrmecophytes, Azteca, Pheidole, and Pseudomyrmex were the most important insect attackers. Myrmecophytes were better protected by ants, as all insects were attacked; in extrafloral nectaried plants, some ants failed to attack the insects. Plants are patrolled by several different ants, but there is a core of ants that excel in protection, and this varies according to plant type (extrafloral nectaried plants and myrmecophytes). With this knowledge, it may be possible to label different ants as effective plant guards, to anticipate their effects on plant performance, and even to understand their potential role as biological control agents.
... Three Macaranga species, M. hosei, M. rufescens, and M. beccariana, are host plants of the bug species examined in this study. They are obligate myrmecophytic species that have hollow stems and peltate leaves with long petioles (Fiala et al. 1994, Itioka 2005. Macaranga hosei and M. rufescens are closely related (Davies 2001) and are mainly associated with Crematogaster borneensis and C. linsenmairi, whereas M. beccariana is associated with C. decamera (Fiala et al. 1999, Feldhaar et al. 2016). ...
Myrmecophytes have mutualistic relationships with symbiotic ants. Although myrmecophytic Macaranga (Malpighiales: Euphorbiaceae) species are well protected by aggressive Crematogaster (Hymenoptera: Formicidae) ants, some bug species occur on the myrmecophytes. To clarify the associations of these bugs with the plants and the ants, we studied the food habits of 3 bug species, Pilophorus lambirensis Nakatani et Komatsu, 2013 (Hemiptera: Miridae: Phylinae), Phylinae sp. 1, and Arbela sp. 1 (Hemiptera: Nabidae). We conducted field observations in a Bornean rainforest. First, we located these bugs and studied their behavioral responses to the ants on Macaranga species; we then conducted stable isotope analyses. All bugs avoided direct contact with ants, but they occurred only on trees with active ants. Pilophorus lambirensis and Phylinae sp. 1 were most commonly observed on the apical parts of host trees, whereas Arbela sp. 1 was mainly in areas distant from the apical parts where ants were sparse. The stable isotope ratios indicated that Phylinae sp. 1 fed on food bodies, which are nutrient-rich spherical bodies produced by Macaranga trees on the apical parts for ants. Although the main diet of the other 2 species remains unclear, nitrogen isotopic signatures demonstrated that P. lambirensis is herbivorous, whereas Arbela sp. 1 is carnivorous. However, the distant location from ants and its isotopic signatures indicated that Arbela sp. 1 rarely fed on the ants. At least 2 mirid bug species might obtain enemy-free space in addition to the food provided by the myrmecophytes.
... While non-myrmecophytic Macaranga species opportunistically attract ants by offering them food bodies and/or extrafloral nectar, obligate myrmecophytes form tighter associations by providing both food and nesting spaces to their ant partners (Fiala et al., 1989). The ants in return protect their host plants against herbivory, competition from encroaching vines (Fiala et al., 1989(Fiala et al., , 1994, and fungal pathogens (Heil et al., 1999). These obligate myrmecophytes are confined to three taxonomic sections-Pachystemon, Pruinosae, and Winklerianae (Davies, 2001;Davies et al., 2001;Whitmore et al., 2008)-and are only found in the ever-wet rainforests of Sundaland with Borneo being a diversity hotspot (reviewed in Fiala, 1999;Blattner et al., 2001). ...
The Southeast Asian region of Sundaland is among the world’s major biodiversity hotspots. The region’s biodiversity coupled with its complex and dynamic geographic and climatic histories makes it an ideal region to study the various factors that determine the diversification and distribution patterns of tropical biota. Here we investigate the biogeographic patterns in the partly myrmecophytic Macaranga section Pruinosae to reveal some of the factors that play a role in determining the distribution of biota in Sundaland. We used single nucleotide polymorphisms (SNP) data derived from GBS, a next generation sequencing technique, in maximum likelihood and cluster analyses to determine phylogenetic relationships and population structures within this taxonomic section. Bayesian inference based on secondary calibration points and ancestral area reconstruction analyses were performed to infer spatial–temporal origins of the major lineages in the section. The results from these analyses were further substantiated using nuclear microsatellite data obtained from a broader sample set of two widely distributed species within the section: Macaranga gigantea and Macaranga pruinosa. Phylogenetic and cluster analyses reveal four well-defined, discrete species groups within section Pruinosae, all of which but one originated in Borneo with the crown node dated at 3.58 mya. Biogeographic patterns within the species reveal a biogeographic barrier between east and west Sundaland besides bringing to light the role played by various geological factors, especially the Crocker Range, on Borneo. Patterns also reveal a biogeographic barrier between the Bangka/Belitung islands and Sumatra for ant-free, swamp-adapted species. This study provides evidence that geographic barriers, edaphic conditions, and ecological adaptations are tightly linked and that their mutual interaction determines the diversification and distribution of species.
... Aggressive plant-ants can defend plant tissue, reducing biomass loss to herbivores (Calixto et al., 2018;Rosumek et al., 2009), and many woody plants have traits that reward ant mutualists (e.g., nearly a third of woody plants in a Panamanian forest, Schupp & Feener, 1991). Plants traits that attract and benefit ant mutualists divert resources from growth or reproduction (e.g., Fagundes et al., 2017;Fiala et al., 1994;Gibert et al., 2019;Marting et al., 2018;Mayer et al., 2014;Stanton & Palmer, 2011). Nevertheless, ant-plants can dominate habitat patches or even across landscapes , ostensibly because ant defense yields a net preservation of key resources by the plant. ...
Cooperative interactions may frequently be reinforced by “partner fidelity feedback,” in which high‐ or low‐quality partners drive positive feedbacks with high or low benefits for the host, respectively. Benefits of plant–animal mutualisms for plants have been quantified almost universally in terms of growth or reproduction, but these are only two of many sinks to which a host‐plant allocates its resources. By investigating how partners to host‐plants impact two fundamental plant resources, carbon and water, we can better characterize plant–partner fidelity and understand how plant–partner mutualisms may be modulated by resource dynamics. In Laikipia, Kenya, four ant species compete for Acacia drepanolobium host‐plants. These ants differ in multiple traits, from nectar consumption to host‐plant protection. Using a 5‐year ant removal experiment, we compared carbon fixation, leaf water status, and stem non‐structural carbohydrate concentrations for adult ant–plants with and without ant partners. Removal treatments showed that the ants differentially mediate tree carbon and/or water resources. All three ant species known to be aggressive against herbivores were linked to benefits for host‐plant resources, but only the two species that defend but do not prune the host, Crematogaster mimosae and Tetraponera penzigi, increased tree carbon fixation. Of these two species, only the nectivore C. mimosae increased tree simple sugars. Crematogaster nigriceps, which defends the tree but also castrates flowers and prunes meristems, was linked only to lower tree water stress approximated by pre‐dawn leaf water potential. In contrast to those defensive ants, Crematogaster sjostedti, a poor defender that displaces other ants, was linked to lower tree carbon fixation. Comparing the effects of the four ant species across control trees suggests that differential ant occupancy drives substantial differences in carbon and water supply among host trees. Our results highlight that ant partners can positively or negatively impact carbon and/or water relations for their host‐plant, and we discuss the likelihood that carbon‐ and water‐related partner fidelity feedback loops occur across ant–plant mutualisms.
... 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) ...
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.
Mallotus bullata M.T.An & J.H. Yu sp. Nov. (Euphorbiaceae), a species new to science discovered in Guizhou, China, is described and illustrated here, along with its phylogenetic position among other Mallotus species. Morphological, micro-morphological, and molecular evidence is presented as attestation of its novelty. The new species morphologically resembles M. philippensis var. reticulatus and M. philippensis , but it clearly differs by having leaf surface bullate, absence of coarse serrations on leaf margins, lateral veins reticulate near margins, sepals in male flowers 5, polygamous flowers, pollen grains 3 apertures with have obvious protrusions in the apertures, abaxial leaf epidermal microhairs 1-8 mm long. Molecular phylogenetic analysis (BS = 100% / BS = 96%, PP = 1 / PP = 1) provides strong evidence supporting M. bullata as a new species within the genus Mallotus .
Ant-plant symbioses are complex between-species interactions found only in the tropical environment. Typically, in such symbioses, plants provide housing structures and food to their ant symbionts. In return, the ants protect their plants' host against herbivore attack and additional nutrients to help with plants' growth. These win-win interactions range from facultative to obligate mutualism. This proposal aims to test the three main mechanisms: (1) by-product benefits, (2) partner fidelity feedback and (3) partner choice in stabilising the ant-plant mutualism. Understanding the mechanisms are crucial as they form the foundation of the ant-plant distribution and growth, in other words - the health of the myrmecophyte (ants-loving) trees in the forest ecosystem. Hence, ant-plant symbioses are an ideal model system for investigating the effects of anthropogenic changes, such as deforestation and climate change on the outcome of ant-plant mutualistic interactions. This project attempts to identify the mechanisms regulating the mutualistic interactions and, in particular, identify the context in which such mutualistic interactions evolved and adapt to the changing environment. We hypothesise that there will be a higher diversity of obligate mutualistic ant-plant interactions in the undisturbed environment compared to degraded habitat. Furthermore, we expect there are different complexity of symbioses, involving multiple partners (ants-hemipteran insects-bacteria-fungi-plants) that deepen our understanding of how such symbioses can be stabilised. Finally, the deforestation combined with climate change in Southeast Asia will have a detrimental effect on ant-plant symbioses, causing breakdown of mutualistic partners and invasion of cheater ant species that do not confer a protective advantage to their plants' host.
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.
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.
The Euphorbiaceae is a large and diverse plant family, widespread in both the Old and New World tropics (Webster 1967), many members of which have extrafloral nectaries (Elias 1983) or other adaptations that encourage ant visitation. Most studies to date on interactions between ants and Old World members of this family have been conducted on myrmecophytic species, such as Macaranga triloba, which provide specialized food bodies and hollow stem domatia for one or a few species of ants (Ridley 191 O; Tho 1978; Rickson 1980; Maschwitz et al. 1984; Fiala et al. 1989, Chapter 18, this volume) and very little experimental work has been done on nonmyrmecophytic associations in which plants provide food bodies and/or extrafloral nectar for ants, but not nest sites (Whalen and Mackay 1988; Fiala et al. 1989).
Schemske (1983) stressed that plants providing ‘limited’ resources for ants, such as extrafloral nectar, generally have a higher diversity of ant associates than those providing ‘major’ resources, such as nest sites and diverse foods. Since extrafloral nectar comprises only a part of the nutritional requirements of an ant colony, ant-guard systems mediated solely by the supply of nectar are usually very generalized (Schemske 1983; Beattie 1985).
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.
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.
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.
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.