Size and lipid content of nonmyrmecochorous diaspores: Effects on the interaction with litter-foraging ants in the Atlantic rain forest of Brazil

Ants are often attracted to diaspores not adapted for dispersal by ants. These diaspores may occasionally benefit from this interaction. We selected six nonmyrmecochorous plant species (Virola oleifera, Eugenia stictosepala, Cabralea canjerana, Citharexylum myrianthum, Alchornea glandulosa and Hyeronima alchorneoides) whose diaspores differ in size and lipid content, and investigated how these features affect the outcome of ant-diaspore interactions on the floor of a lowland Atlantic forest of Southeast Brazil. A total of 23 ant species were seen interacting with diaspores on the forest floor. Ants were generally rapid at discovering and cleaning the diaspore pulp or aril. Recruitment rate and ant attendance were higher for lipid-rich diaspores than for lipid-poor ones. Removal rate and displacement distance were higher for small diaspores. The large ponerine ant Pachycondyla striata, one of the most frequent attendants to lipid-rich arillate diaspores, transported the latter into their nests and discarded clean intact seeds on refuse piles outside the nest. Germination tests with cleaned and uncleaned diaspores revealed that the removal of pulp or aril may increase germination success in Virola oleifera, Cabralea canjerana, Citharexylum myrianthum and Alchornea glandulosa. Gas chromatography analyses revealed a close similarity in the fatty acid composition of the arils of the lipid-rich diaspores and the elaiosome of a typical myrmecochorous seed (Ricinus communis), corroborating the suggestion that some arils and elaiosomes are chemically similar. Although ant-derived benefits to diaspores - secondary dispersal and/or increased germination - varied among the six plant species studied, the results enhanced the role of ant-diaspore interactions in the post-dispersal fates of nonmyrmecochorous seeds in tropical forests. The size and the lipid-content of the diaspores were shown to be major determinants of the outcome of such interactions.

Ant-tended hemiptera in Amazonian myrmecophytes: Patterns of abundance and implications for mutualism function (Hymenoptera: Formicidae)

We assessed how the abundance of ant-tended Hemiptera associated with two Amazonian myrmecophytes, Tococa bullifera and Maieta guianensis, varied as a function of resident ant species. We collected five species or morpho-species of adult hemiptera in the domatia of M. guianensis, with four of these species also found in Tococa bullifera. Maieta guianensis plants inhabited by Crematogaster laevis had over four-fold more hemiptera in them than plants inhabited by Pheidole minutula. In contrast, the density of hemiptera in Tococa bullifera domatia was independent of the species of ant resident. For each of the two ant species inhabiting Maieta guianensis, there was a positive and significant relationship between the abundance of hemiptera and workers inhabiting a plant. This relationship was also significant and positive for the Tococa bullifera plants inhabited by C. laevis. However, there was no relationship between Azteca worker and hemipteran density, although there was a trend towards a positive relationship. Our results indicate that hemipteran abundance can vary significantly between different myrmecophyte species, but that the nature of this relationship is mediated by the identity of the ant associate. Because hemipterans are herbivores, the costs and benefits of different ant partners to the host plant may vary in ways that are often overlooked.

Cost limitation through constrained oviposition site in a plant-pollinator/seed predator mutualism

Mutualism often involves reciprocal exploitation due to individual selection for increased benefits even at the expense of the partner. Therefore, stability and outcomes of such interactions crucially depend on cost limitation mechanisms. In the plant, pollinator /seed predator interaction between Silene latifolia (Caryophyllaceae) and Hadena bicruris (Lepidoptera: Noctuidae), moths generate pollination benefits as adults but impose seed predation costs as larvae. We examined whether floral morphology limits over-exploitation by constraining oviposition site. Oviposition site varies naturally inside vs. outside the corolla tube, but neither its determinants nor its effect on the interaction have been investigated. In a common garden with plants originating from eight populations, corolla tube length predicted oviposition site, but not egg presence or pollination efficiency, suggesting that long corolla tubes constrain the moth to lay eggs on petals. Egg position was also predicted by the combined effect of corolla tube and moth ovipositor lengths, with shorter ovipositor than corolla tube resulting in higher probability for eggs outside. Egg position on a given plant was repeatable over different exposure nights. When egg position was experimentally manipulated, eggs placed on the petal resulted in significantly fewer successful fruit attacks compared with eggs placed inside the corolla tube, suggesting differences in egg/larval mortality. Egg position also differently affected larval mass, fruit mass and fruit development. Our results indicate that constraining oviposition site through a long corolla tube reduces seed predation costs suffered by the plant without negatively affecting pollination efficiency and, hence may act to limit over-exploitation. However, the net effects of corolla tube depth variation on this interaction may fluctuate with extrinsic factors affecting egg mortality, and with patterns of gene flow affecting trait matching between the interacting species. The intermediate fitness costs incurred by both plant and insect associated with the different egg positions may reduce selective pressures for this interaction to evolve towards antagonism, favouring instead a mutualistic outcome. While a role for oviposition site variation in cost limitation is a novel finding in this system, it may apply more generally also to other mutualisms involving pollinating seed predators.

The curious case of the camelthorn: competition, coexistence and nest-site limitation in a multispecies mutualism

Myrmecophyte plants house ants in domatia in exchange for protection from herbivores. Ant-myrmecophyte mutualisms exhibit two general patterns due to competition between ants for plant occupancy: i) domatia nest-sites are a limiting resource and ii) each individual plant hosts one ant species at a time. However, individual camelthorn trees (Vachellia erioloba) typically host two to four ant species simultaneously, often coexisting in adjacent domatia on the same branch. Such fine-grain spatial coexistence brings into question the conventional wisdom on ant-myrmecophyte mutualisms. Camelthorn ants appear not to be nest-site limited, despite low abundance of suitable domatia, and have random distributions of nest-sites within and across trees. These patterns suggest a lack of competition between ants for domatia and contrast strongly with other ant-myrmecophyte systems. Comparison of this unusual case with others suggests that spatial scale is crucial to coexistence or competitive exclusion involving multiple ant species. Furthermore, coexistence may be facilitated when co-occurring ant species diverge strongly on at least one niche axis. Our conclusions provide recommendations for future ant-myrmecophyte research, particularly in utilising multispecies systems to further our understanding of mutualism biology.

A trophic cascade induced by predatory ants in a fig-fig wasp mutualism

Summary 1. A trophic cascade occurs when predators directly decrease the densities, or change the behaviour, of herbivores and thus indirectly increase plant productivity. The predator–herbivore– plant context is well known, but some predators attack species beneficial to plants (e.g. pollinators) and/or enemies of herbivores (e.g. parasites), and their role in the dynamics of mutualisms remains largely unexplored. 2. We surveyed the predatory ant species and studied predation by the dominant ant species, the weaver ant Oecophylla smaragdina, associated with the fig tree Ficus racemosa in southwest China. We then tested the effects of weaver ants on the oviposition behaviour of pollinating and non-pollinating fig wasps in an ant-exclusion experiment. The effects of weaver ants on fig wasp community structure and fig seed production were then compared between trees with and without O. smaragdina. 3. Oecophylla smaragdina captured more non-pollinating wasps (Platyneura mayri) than pollinators as the insects arrived to lay eggs. When ants were excluded, more non-pollinators laid eggs into figs and fewer pollinators entered figs. Furthermore, trees with O. smaragdina produced more pollinator offspring and fewer non-pollinator offspring, shifting the community structure significantly. In addition, F. racemosa produced significantly more seeds on trees inhabited by weaver ants. 4. Oecophylla smaragdina predation reverses the dominance of the two commonest wasp species at the egg-laying stage and favours the pollinators. This behavioural pattern is mirrored by wasp offspring production, with pollinators’ offspring dominating figs produced by trees inhabited by weaver ants, and offspring of the non-pollinator P. mayri most abundant in figs on trees inhabited by other ants. 5. Overall, our results suggest that predation by weaver ants limits the success of the non-pollinating P. mayri and therefore indirectly benefits the mutualism by increasing the reproductive success of both the pollinators and the plant. Predation is thus a key functional factor that can shape the community structure of a pollinator-plant mutualistic system. Key-words: competitive release, fig wasp, mutualism, predation, predator-exclusion experiment, trophic cascade

Metabolism of plant polysaccharides by Leucoagaricus gongylophorus, the symbiotic fungus of the leaf-cutting ant Atta sexdens L.

Atta sexdens L, ante feed on the Fungus they cultivate on cut leaves inside their nests. The fungus, Leucoagaricus gongylophorus, metabolizes plant polysaccharides, such as xylan, starch, pectin, and cellulose, mediating assimilation of these compounds lay the ants, This metabolic integration may be an important part of the ant-fungus symbiosis, and it involves primarily xylan and starch, both of which support rapid fungal growth. Cellulose seems to be less important for symbiont nutrition, since it is poorly degraded and assimilated by the fungus. Pectin is rapidly degraded but slowly assimilated by L. gongylophorus, and its degradation may occur so that the fungus can more easily access other polysaccharides in the leaves.

Planting of fungus onto hibernating workers of the fungus-growing ant Mycetosoritis clorindae (Attini, Formicidae)

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Interspecific variation in the defensive responses of obligate plant-ants: experimental tests and consequences for herbivory

The aggressive behavior of ants that protect plants from herbivores in exchange for rewards such as shelter or food is thought to be an important form of biotic defense against herbivory, particularly in tropical systems. To date, however, no one has compared the defensive responses of different ant taxa associated with the same plant species, and attempted to relate these differences to longer-term efficacy of ant defense. We used experimental cues associated with herbivory-physical damage and extracts of chemical volatiles from leaf tissue-to compare the aggressive responses of two ant species obligately associated with the Amazonian myrmecophyte Tococa bullifera (Melastomataceae). We also conducted a colony removal experiment to quantify the level of resistance from herbivores provided to plants by each ant species. Our experiments demonstrate that some cues eliciting a strong response from one ant species elicited no response by the other. For cues that do elicit responses, the magnitude of these responses can vary interspecifically. These patterns were consistent with the level of resistance provided from herbivores to plants. The colony removal experiment showed that both ant species defend plants from herbivores: however, herbivory was higher on plants colonized by the less aggressive ant species. Our results add to the growing body of literature indicating defensive ant responses are stimulated by cues associated with herbivory. However, they also suggest the local and regional variation in the composition of potential partner taxa could influence the ecology and evolution of defensive mutualisms in ways that have previously remained unexplored.

Plant glandular trichomes mediate protective mutualism in a spider-plant system

1. Although several species of Peucetia (Oxyopidae) live strictly in association with plants bearing glandular trichomes worldwide, to date little is known about whether these associations are mutualistic.2. In this study we manipulated the presence of Peucetia flava on the glandular plant Rhynchanthera dichotoma in the rainy and post-rain season, to test the strength of its effects on leaf, bud, and flower damage and plant reproductive output. In addition, we ran independent field experiments to examine whether these sticky structures improve spider fidelity to plants.3. Peucetia suppressed some species of foliar phytophages, but not others. Although spiders have reduced levels of leaf herbivory, this phenomenon was temporally conditional, i.e. occurred only in the post-rain but not in the rainy season. Floral herbivory was also reduced in the presence of spiders, but these predators did not affect plant fitness components.4. Plants that had their glandular trichomes removed retained fewer insects than those bearing such structures. Spiders remained longer on plants with glandular trichomes than on plants in which these structures had been removed. Isotopic analyses showed that spiders that fed on live and dead labelled flies adhered to the glandular hairs in similar proportions.5. Spiders incurred no costs to the plants, but can potentially increase individual plant fitness by reducing damage to reproductive tissues. Temporal conditionality probably occurred because plant productivity exceeded herbivore consumption, thus dampening top-down effects. Specialisation to live on glandular plants may have favoured scavenging behaviour in Peucetia, possibly an adaptation to periods of food scarcity.

The role of multiple partners in a digestive mutualism with a protocarnivorous plant

Background and aimsThe protocarnivorous plant Paepalanthus bromelioides (Eriocaulaceae) is similar to bromeliads in that this plant has a rosette-like structure that allows rainwater to accumulate in leaf axils (i.e. phytotelmata). Although the rosettes of P. bromelioides are commonly inhabited by predators (e.g. spiders), their roots are wrapped by a cylindrical termite mound that grows beneath the rosette. In this study it is predicted that these plants can derive nutrients from recycling processes carried out by termites and from predation events that take place inside the rosette. It is also predicted that bacteria living in phytotelmata can accelerate nutrient cycling derived from predators.MethodsThe predictions were tested by surveying plants and animals, and also by performing field experiments in rocky fields from Serra do Cipó, Brazil, using natural abundance and enriched isotopes of 15N. Laboratory bioassays were also conducted to test proteolytic activities of bacteria from P. bromelioides rosettes.Key ResultsAnalyses of 15N in natural nitrogen abundances showed that the isotopic signature of P. bromelioides is similar to that of carnivorous plants and higher than that of non-carnivorous plants in the study area. Linear mixing models showed that predatory activities on the rosettes (i.e. spider faeces and prey carcass) resulted in overall nitrogen contributions of 26·5 % (a top-down flux). Although nitrogen flux was not detected from termites to plants via decomposition of labelled cardboard, the data on 15N in natural nitrogen abundance indicated that 67 % of nitrogen from P. bromelioides is derived from termites (a bottom-up flux). Bacteria did not affect nutrient cycling or nitrogen uptake from prey carcasses and spider faeces.ConclusionsThe results suggest that P. bromelioides derive nitrogen from associated predators and termites, despite differences in nitrogen cycling velocities, which seem to have been higher in nitrogen derived from predators (leaves) than from termites (roots). This is the first study that demonstrates partitioning effects from multiple partners in a digestion-based mutualism. Despite most of the nitrogen being absorbed through their roots (via termites), P. bromelioides has all the attributes necessary to be considered as a carnivorous plant in the context of digestive mutualism. © 2012 The Author. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.

A metabolic pathway assembled by enzyme selection may support herbivory of leaf-cutter ants on plant starch

Mutualistic associations shape the evolution in different organism groups. The association between the leaf-cutter ant Atta sexdens and the basidiomycete fungus Leucoagaricus gongylophorus has enabled them to degrade starch from plant material generating glucose, which is a major food source for both mutualists. Starch degradation is promoted by enzymes contained in the fecal fluid that ants deposit on the fungus culture in cut leaves inside the nests. To understand the dynamics of starch degradation in ant nests, we purified and characterized starch degrading enzymes from the ant fecal fluid and from laboratory cultures of L. gongylophorus and found that the ants intestine positively selects fungal α-amylase and a maltase likely produced by the ants, as a negative selection is imposed to fungal maltase and ant α-amylases. Selected enzymes are more resistant to catabolic repression by glucose and proposed to structure a metabolic pathway in which the fungal α-amylase initiates starch catalysis to generate byproducts which are sequentially degraded by the maltase to produce glucose. The pathway is responsible for effective degradation of starch and proposed to represent a major evolutionary innovation enabling efficient starch assimilation from plant material by leaf-cutters. © 2013 Elsevier Ltd.

Leaf-cutter ant fungus gardens are biphasic mixed microbial bioreactors that convert plant biomass to polyols with biotechnological applications

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Mutualism from the inside: coordinated development of plant and insect in an active pollinating fig wasp

Recent studies on the obligate interaction between fig trees and their pollinating agaonid wasps have focused on population aspects and wasp-seed exploitation at the level of the inflorescence. Detailed studies on larval and gall development are required to more fully understand how resources are exploited and adaptations fine-tuned by each partner in nursery pollination mutualisms. We studied the larval development of the active pollinating fig wasp, Pegoscapus sp., and the galling process of individual flowers within the figs of its monoecious host, Ficus citrifolia, in Brazil. The pollinator development is strongly dependent on flower pollination. Figs entered by pollen-free wasps were in general more likely to abort. Retained, unpollinated figs had both higher larval mortality and a lower number of wasps. Pegoscapus sp. larvae are adapted to plant development, with two contrasting larval feeding strategies proceeding alongside gall development. The first two larval stages behave as ovary parasites. Later larval stages feed on hypertrophied endosperm. This indicates that a successful galling process relies on endosperm, and also reveals why pollination would be a prerequisite for the production of high-quality galls for this Pegoscapus species.

Effect of leaf-cutting ant nests on plant growth in an oligotrophic Amazon rain forest

This study examined whether high nutrient concentrations associated with leaf-cutting ant nests influence plant growth and plant water relations in Amazon rain forests. Three nests of Atta cephalotes were selected along with 31 Amaioua guianensis and Protium sp. trees that were grouped into trees near and distant (>10 m) from nests. A 15N leaf-labelling experiment confirmed that trees located near nests accessed nutrients from nests. Trees near nests exhibited higher relative growth rates (based on stem diameter increases) on average compared with trees further away; however this was significant for A. guianensis (near nest 0.224 y−1 and far from nest 0.036 y−1) but not so for Protium sp. (0.146 y−1 and 0.114 y−1 respectively). Water relations were similarly species-specific; for A. guianensis, near-nest individuals showed significantly higher sap flow rates (16 vs. 5 cm h−1), higher predawn/midday water potentials (−0.66 vs. −0.98 MPa) and lower foliar δ13C than trees further away indicating greater water uptake in proximity to the nests while the Protium sp. showed no significant difference except for carbon isotopes. This study thus shows that plant response to high nutrient concentrations in an oligotrophic ecosystem varies with species. Lower seedling abundance and species richness on nests as compared with further away suggests that while adult plants access subterranean nutrient pools, the nest surfaces themselves do not encourage plant establishment and growth.

Ant abundance and occurrence along the plant diversity gradient in the Jena Experiment (Main Experiment, year 2006)

This data set contains measurements of ant abundance (number of individuals observed at the baits) and ant occurrence (binary data) measured in the Main Experiment plots of a large grassland biodiversity experiment (the Jena Experiment; see further details below). Ants were sampled in 80 plots of the Main Experiment using baited traps in July 2006. In each plot two petri dishes were set on the ground, one received ~10g of Tuna the other ~10g of sugar (Sucrose). After 30min the occurrence (presence = 1 / absence = 0) and abundance (number) of ants at the two baits was recorded. Given is, per plot, the sum of ants attracted to the two different baits. In the Main Experiment, 82 grassland plots of 20 x 20 m were established from a pool of 60 species belonging to four functional groups (grasses, legumes, tall and small herbs). In May 2002, varying numbers of plant species from this species pool were sown in the plots to create a gradient of plant species richness (1, 2, 4, 8, 16 and 60 species) and functional richness (1, 2, 3, or 4 functional groups). Plots were maintained by bi-annual weeding and mowing.