Azteca Ants Research Articles

Specialist fig-consuming lepidopterans can inflict costs to plant reproductive success that are mitigated by ant bodyguards

Insect herbivores can inflict substantial costs on plant reproductive success. Seed herbivory impacts directly by reducing the number of seeds and therefore the dispersal and reproductive potential of the plant. Fig trees, Ficus, provide keystone resources for tropical forests. The pollinating fig wasps develop inside figs, so consumption of unripe figs results in trees not only losing seeds but also their pollen dispersers. Selection to defend figs should therefore be strong. Seed herbivory is understudied in tropical forests and most data has been collected from fallen fruits. Here we use canopy sampling to identify fig-consuming larvae in central Panama and quantify both their consequences for the fig trees’ reproductive success and the defensive value that ants provide against these larvae. Field surveys of 46 crops from nine fig species revealed that larvae could destroy up to 80% of figs on a tree. From seven Ficus species we barcoded (using COI) 51 individual fig consuming larvae (mainly Lepidoptera) that grouped into seven molecular operational taxonomic units. Lepidopteran larvae formed two feeding strategies, either stationary within a fig or tunneling between figs. Within the context of our study, stationary larvae were specialists whereas tunneling larvae were either specialists or generalists found on different Ficus species. Trees with ants had significantly fewer figs consumed by larvae (9% ± 17% (mean ± SD) for trees with azteca ants and 16% ± 24% for trees with other ants) than did trees without ants (51% ± 27%). Our results corroborate earlier findings that hosting ants can be an effective defensive mechanism for trees against seed herbivores or other antagonistic insects. Our study contributes to a wider body of research around the networks of insects associated with figs that highlights the importance of a multitrophic approach for understanding mutualism stability and persistence in the face of antagonism.

Bacterial diversity in arboreal ant nesting spaces is linked to colony developmental stage

The omnipresence of ants is commonly attributed to their eusocial organization and division of labor, however, bacteria in their nests may facilitate their success. Like many other arboreal ants living in plant-provided cavities, Azteca ants form dark-colored “patches” in their nesting space inside Cecropia host plants. These patches are inhabited by bacteria, fungi and nematodes and appear to be essential for ant colony development. Yet, detailed knowledge of the microbial community composition and its consistency throughout the life cycle of ant colonies was lacking. Amplicon sequencing of the microbial 16S rRNA genes in patches from established ant colonies reveals a highly diverse, ant species-specific bacterial community and little variation within an individual ant colony, with Burkholderiales, Rhizobiales and Chitinophagales being most abundant. In contrast, bacterial communities of early ant colony stages show low alpha diversity and no ant species-specific community composition. We suggest a substrate-caused bottleneck after vertical transmission of the bacterial patch community from mother to daughter colonies. The subsequent ecological succession is driven by environmental parameters and influenced by ant behavior. Our study provides key information for future investigations determining the functions of these bacteria, which is essential to understand the ubiquity of such patches among arboreal ants.

Nutrient Supplementation to Arboreal Ants: Effects on Trophic Position, Thermal Tolerance, Community Structure and the Interaction with the Host-Tree

Carbohydrates and proteins are essential to maintain the basic functions of animals. Over the course of one year we conducted a factorial experiment to determine the influence of carbohydrate (sucrose) and protein supplementation on the thermal tolerance, trophic position, overall abundance, species richness and composition, and on the strength of the protective effects of arboreal ants on their host tree (Caryocar brasiliense). Using Azteca ants as a model we found evidence of dietary and thermal plasticity among arboreal ants as colonies supplied with protein increased their trophic level relative to colonies that received no protein. Colonies that received sucrose increased their thermal tolerance on average by 1.5 °C over a six-month period, whereas those that did not receive sucrose did not change their thermal tolerance. Overall ant abundance was lower in control trees than in those that received any nutrient addition treatment. Species richness was also lower in control trees, but those receiving sucrose presented more species than those receiving only protein. There was greater similarity in species composition between the trees that received sucrose than between these and those receiving only protein or just water as control. Trees whose ant colonies received sucrose presented lower levels of leaf damage than those that did not. Overall, these results indicate that food resources can modulate the population and community ecology of arboreal ants as well as their interaction with the host trees. Interestingly, although arboreal ants are thought to be N-limited, it was the supplementation of sucrose—not protein—that elicited most of the responses.

Brakemyia, a New Neotropical Jackal Fly Genus of Milichiidae (Insecta: Diptera) Associated with Carton Ant Nest.

Brakemyia metallica gen. et sp. nov. (Diptera, Milichiidae) is described and illustrated based on male and female specimens reared from carton nests of the ant Azteca aff. chartifex Forel (Formicidae: Dolichoderinae). The new genus is widely distributed in the Brazilian Amazon, and it can be readily distinguished from the other Neotropical genera by the broadened lunule, which extends well posterior of the antennae, and the hypandrial complex parallel to epandrium.

Host-tree selection by the ant garden-initiating arboreal ponerine Neoponera goeldii.

Host-tree selection by the ant garden-initiating arboreal ponerine Neoponera goeldii.

Coryanthes macrantha (Orchidaceae: Stanhopeinae) and their floral and extrafloral secretory structures: an anatomical and phytochemical approach.

Coryanthes is one of the most fascinating genera of Stanhopeinae (Orchidaceae) because of its complex pollination mechanism and the peculiar structures of its flowers. Although Coryanthes macrantha is widely studied, investigation of the secretory structures and floral biology is important to understand the mechanisms and ecology of pollination, which deserve attention despite the difficulties of collecting fertile material in nature. We conducted a morpho-anatomical analysis of the floral and extrafloral secretory structures of C. macrantha to better understand the secretory structures, contribute to the knowledge of its floral biology and/or pollination processes and understand the ecological function of these structures. The analysis revealed that C. macrantha has epidermal osmophores with unicellular papillae that were foraged by male Eulaema bees, floral nectaries in the sepals and extrafloral nectaries in the bracts. In both the floral and extrafloral nectaries, the nectar is exuded by the stomata. Azteca ants foraged the bract and sepal nectaries in pre-anthesis and post-anthesis. We also described the secretory epidermis of pleuridia, and the mode of secretion of osmophores and nectaries and found that they attract specific foraging agents.

A new species of Neoscutops Malloch (Diptera: Periscelididae) reared from an ant nest.

A new species of Neoscutops Malloch (Diptera: Periscelididae), Neosctups rungae sp. nov., is described from the Brazilian Amazon based on three specimens (2 males and 1 female) reared from carton nests of the ant Azteca aff. chartifex Forel (Formicidae: Dolichoderinae). The new species belongs to the rotundipennis species-group, which is now composed of five valid species. The new species can be readily diagnosed by the following combination of characters: face fully dark brown and surstylus with a basal rounded projection on inner margin.

Azteca ants repair damage to their Cecropia host plants

Some Azteca ants are well-known symbionts that defend their Cecropia host plants against herbivory, although there is considerable variability in behavior among colonies, conditions, and species. In exchange, ants receive food, and also shelter within the plants’ internodes. Here we demonstrate that ants repair damage to the host plant when their brood is directly threatened. Using comminuted plant fibers and an unidentified binding liquid (probably plant sap) ants generally began patching holes in the tree trunk immediately, and significantly reduced the size of the hole 2.5 hours after it was created, and they generally completed the repairs within 24 hours.

Comparative phylogeography of an ant-plant mutualism: An encounter in the Andes

Evolutionary processes in ant-plant mutualisms are mediated by intrinsic features of the association and by change through time in abiotic components of the system (e.g. geography and climate). Incorporating both biotic and abiotic components and the phylogenies of the taxa involved is central to understanding their respective roles in mutualism evolution. We used a comparative phylogeographic approach to assess the effects of the Andean uplift on the mutualism between Azteca ants and an ant plant, Tococa guianensis , and to ask whether plant and ant diversification were promoted by geography or by the association. We used a combination of nuclear and organellar sequence data to resolve relationships between populations of ants and plants at sites spanning the northern Andes Cordillera in Colombia. To test for phylogenetic and chronological congruence between taxa and major uplift events, we used fossil calibrations and estimated the timing of diversification. We found phylogeographic structure in both Azteca and T. guianensis that coincides spatially and temporally with peaks of activity during the Andean uplift. However, lineage divergence occurs earlier in Azteca than in T. guianensis . We suggest that the Andean uplift had a greater impact on lineage diversification than did the mutualism. • The evolution of Azteca-Tococa guianensis mutualism is consistent with ecological fitting and not with co-diversification. • The effect of the Andean uplift differs between ant and plant lineages; Azteca diversified earlier than Tococa guianensis . • Geographic structure of Azteca and Tococa populations is trans-Andean and consistent with vicariance. • The Northern Andes cordillera is porous barrier to gene flow between populations located near low heights (<1600 masl).

Multiple effects of mutualistic ants improve the performance of a neotropical ant-plant: A long-term study with the Cecropia-Azteca system

Comprehension of the benefits involved in mutualisms is crucial to disentangle the role of interactions in the structure and functioning of populations, communities and ecosystems. In ant-plant mutualisms, benefits provided by plants to ants are immediately recognizable, but reverse benefits are less obvious, conditional and accumulate over longer time spans. Here we tested the hypothesis that the ant Azteca muelleri simultaneously provides multiple benefits to its host plant (Cecropia glaziovii), ultimately increasing plant performance. We planted seedlings and experimentally prevented ant colonization for half of them. Over 4.5 years we quantified the effects of ant presence or absence on plant growth, herbivory levels, fungal infection, fertilization via ant debris and changes in defense strategies. Ant colonization increased plant height by 125% compared to ant-free plants. Such an improvement in plant performance can be explained because plants with ants faced less herbivory, lower prevalence of pathogenic fungi, invested less in foliar trichomes and had more foliar nitrogen. We thus confirmed that ant mutualists provide cumulative benefits including nutritional benefits, effective defense and lower investment into other defenses – which result in increased plant growth. We highlight the importance of long-term experiments that simultaneously evaluate a multiplicity of potential ant effects to better understand their relative contribution to the performance of the mutualistic partner.

Insights Into the Ecological Role of Pseudomonas spp. in an Ant-plant Symbiosis.

In the myrmecophytic mutualistic relationship between Azteca ants and Cecropia plants both species receive protection and exchange nutrients. The presence of microorganisms in this symbiotic system has been reported, and the symbiotic role of some fungi involved in the myrmecophytic interactions has been described. In this work we focus on bacteria within this mutualism, conducting isolations and screening for antimicrobial activities, genome sequencing, and biochemical characterization. We show that Pantoea, Rhizobium, Methylobacterium, Streptomyces and Pseudomonas are the most common cultivable genera of bacteria. Interestingly, Pseudomonas spp. isolates showed potent activity against 83% of the pathogens tested in our antimicrobial activity assays, including a phytopathogenic fungus isolated from Cecropia samples. Given the predicted nitrogen limitations associated with the fungal patches within this myrmecophyte, we performed nitrogen fixation analyses on the bacterial isolates within the Proteobacteria and show the potential for nitrogen fixation in Pseudomonas strains. The genome of one Pseudomonas strain was sequenced and analyzed. The gene cluster involved in the biosynthesis of cyclic lipodepsipeptides (CLPs) was identified, and we found mutations that may be related to the loss of function in the dual epimerization/condensation domains. The compound was isolated, and its structure was determined, corresponding to the antifungal viscosinamide. Our findings of diazotrophy and production of viscosinamide in multiple Pseudomonas isolates suggests that this bacterial genus may play an important role in the Cecropia-Azteca symbiosis.

Defensive Strategies of a Noctuid Caterpillar in a Myrmecophytic Plant: are Dyops Larvae Immune to Azteca Ants?

Immature stages of insects are generally susceptive to their natural enemies, but many species developed defensive and evasive mechanisms to circumvent predation. Gregarious larvae of the noctuid moth Dyops cf. cuprescens feed on leaves of young Cecropia pachystachya shrubs colonized by Azteca ants. Ants avoid contact with larval clusters, retreating to the nest when larvae are moving near the stems. Provoked encounters revealed that Dyops caterpillars present several specialized behaviors to avoid and overcome ant attacks, such as fleeing to under leaf, jumping off the leaf, curling and wriggling vigorously the anterior portion of the body, spitting droplets of oral fluids, or killing ants by pouncing them. These mechanisms allow the caterpillars to overcome ant attacks and consume leaves of ant-colonized plants. By feeding on a heavily protected plant, larvae can enjoy not only a competitor-free plant, but possibly also the enemy-free space created by the aggressive ants.

An uneasy alliance: a nesting association between aggressive ants and equally fierce social wasps.

Although the Neotropical territorially dominant arboreal ant Azteca chartifex Forel is very aggressive towards any intruder, its populous colonies tolerate the close presence of the fierce polistine wasp Polybia rejecta (F.). In French Guiana, 83.33% of the 48 P. rejecta nests recorded were found side by side with those of A. chartifex. This nesting association results in mutual protection from predators (i.e., the wasps protected from army ants; the ants protected from birds). We conducted field studies, laboratory-based behavioral experiments and chemical analyses to elucidate the mechanisms allowing the persistence of this association. Due to differences in the cuticular profiles of the two species, we eliminated the possibility of chemical mimicry. Also, analyses of the carton nests did not reveal traces of marking on the envelopes. Because ant forager flows were not perturbed by extracts from the wasps' Dufour's and venom glands, we rejected any hypothetical action of repulsive chemicals. Nevertheless, we noted that the wasps "scraped" the surface of the upper part of their nest envelope using their mandibles, likely removing the ants' scent trails, and an experiment showed that ant foragers were perturbed by the removal of their scent trails. This leads us to use the term "erasure hypothesis." Thus, this nesting association persists thanks to a relative tolerance by the ants towards wasp presence and the behavior of the wasps that allows them to "contain" their associated ants through the elimination of their scent trails, direct attacks, "wing-buzzing" behavior and ejecting the ants.

Anatomical analyses of floral and extrafloral secreting structures indicate the presence of nectaries and colleters in Stanhopea grandiflora Lindl.

Anatomical studies involving secreting structures in Stanhopeinae have described lipid-producing structures, the osmophores, these structures have been linked to pollinator attraction. Stanhopea, which belongs to the subtribe Stanhopeinae, has Neotropical distribution and is exclusively pollinated by male Euglossini bees, which are attracted to the aromatic compounds exuded by osmophores—a secreting structure that produces volatile lipids. However, due to the structural diversity found in this genus and the lack of data on which foragers visit these flowers, our aim is to elucidate floral anatomical aspects of the Stanhopeinae group, focusing on the secreting structures of Stanhopea grandiflora Lindl., an orchid that occurs in the Amazon region. Analyses were performed under bright-field microscopy and scanning electron microscopy. Osmophores, nectaries, idioblasts and glandular trichomes were the secreting structures observed in Stanhopea grandiflora. The osmophores are responsible for attracting and offering rewards the male Euglossini bees, which are their exclusive pollinators, while the nectaries offering nectar to the foragers Dolichoderus and Azteca ants which in turn offer protection against herbivores. Nectariferous stomata and glandular trichomes role similar to those of colleters are described in the first record of the subtribe Stanhopeinae.

Ant and spider species as surrogates for functional community composition of epiphyte-associated invertebrates in a tropical moist forest

Epiphytes represent up to 50% of all plant species in rainforests, where they host a substantial amount of invertebrate biomass. Efficient surrogates for epiphyte invertebrate communities could reduce the cost of biomonitoring surveys while preventing destructive sampling of the plants. Here, we focus on the invertebrate communities associated to tank bromeliads. We ask whether the presence of particular ant and/or spider taxa (easily surveyed taxa) that use these plants as nesting and/or foraging habitats predicts functional trait combinations of aquatic invertebrate communities hosted by the plants. Functional community composition of invertebrates was predicted both by bromeliad habitat features and the presence of certain ant and spider species. The ant Azteca serica preferred wider bromeliad rosettes that trap large amount of detritus, indicating interstitial-like food webs dominated by deposit feeders that burrow in fine particulate organic matter. Leucauge sp. spiders preferred narrower bromeliad rosettes bearing smaller detrital loads, thereby indicating a dominance of pelagic filter-feeding and predatory invertebrates in the water-filled leaf axils. Both Neoponera villosa ants and Eriophora sp. spiders preferred rosettes at intermediate size bearing moderate amounts of detritus, indicating a benthic food web dominated by leaf shredders and gathering collectors. Owing to the animal diversity and biomass supported by rainforest epiphytes, our approach would deserve to be further tested on a range of epiphytes involved in tight interactions with invertebrates. In this context, surrogate species could serve both as indicators of functional diversity, and as early-warning indicators of network disassembly.

Detection, ultrastucture and phylogeny of Sclerorhabditis neotropicalis (Nematoda: Rhabditidae) nematodes associated with the Azteca ant-Cecropia tree symbiosis

The nematode involved in ant-plant symbioses have been poorly studied, and originated an area of research that is now receiving increasing attention. One example is Sclerorhabditis neotropicalis, that inhabit the nests of Azteca ants in Cecropia trees. The goal of the present study is to increase our knowledge about these organisms and their possible symbiotic relationship with the ants and their host plant. The samples were collected during 2011-2013 in different locations in Costa Rica: Parque Nacional Carara (Puntarenas province), San Pedro de Montes de Oca and Highway 27 (San Jose) and La Selva Biological Station (Sarapiquí, Heredia). We examined 576 internodes from 23 plants, comprising four species of Cecropia (including one non-myrmecophyte) and five Azteca species. S. neotropicalis was found in all but one of the Azteca/Cecropia combinations examined. Queen and worker ants were placed in water in order to dislodge nematodes and the results were largely positive, suggesting that alate queens carry S. neotropicalis between trees and that workers carry them between internodes. In addition to transport, preliminary observations suggest that the ants provide masses of scraped parenchyma (possibly fertilized with feces) as a substrate for bacteria upon which the nematodes presumably feed. We also found S. neotropicalis associated with Azteca in another myrmecophyte, Cordia alliodora, suggesting that this ant/nematode association is not restricted to Cecropia. SEM photographs of S. neotropicalis were provided to supplement the original description of this species, and molecular phylogenetic analyses employing three different markers suggest that Sclerorhabditis forms a well-supported clade of bacteria-feeding nematodes associated with Azteca. Indirect evidence suggests that this is a mutualistic association, but the benefits to the ants remain unknown.

High intermediary mutualist density provides consistent biological control in a tripartite mutualism

Understanding the ecology of mutualisms becomes a particularly important task when considering agroecosystems, as many ecosystem services are associated with mutualistic interactions. Here we report on experiments associated with an indirect pest control mutualism between the arboreal nesting ant Azteca sericeasur and coffee. This system is particularly interesting because the indirect Azteca-Coffea mutualism emerges from an Azteca-scale insect mutualism that takes place on the coffee plant. We describe this interaction structure as a mutualism-dependent mutualism and ask whether the density of intermediary mutualist (scale insects, Coccus) that benefits Azteca also influences the benefits provided to coffee plants. We found that indeed Azteca’s benefit to Coffea is consistent when Coccus density is high. Furthermore, we also found that at low Coccus density Azteca only benefits Coffea in the beginning of the rainy season, and this effect is likely due to the fact that Coccus produces less sugars with higher precipitation. We suggest a framework for thinking about context-dependency in agroecosystem mutualisms that may provide a more mechanistic way to tease apart the prevalent context-dependent results in ecological literature. Finally, we address some past recommendations as it pertains to the management of the Azteca-Coffea-Coccus complex in coffee agroecosystems.

Nest building by a neotropical social wasp using Cecropia trichomes as main construction material (Hymenoptera, Vespidae, Polistinae)

Nest architecture is such a splendid product of social wasp behavior, there being a large diversity of nest types in the Neotropical fauna. Charterginus is a small wasp genus with six species recorded from Honduras through South America, and one species C. fulvus is notable for normally making nests with a very peculiar star shape. Few behavioral traits of this genus have been described, an exception being a record of cleptobiosis between Charterginus species and Azteca ants on Cecropia trees in Amazonia and Central America. Here we describe behavioral traits of C. fulvus related to the construction process of the nest envelope and the materials used, discussing the apparent dependency of this wasp species on resources provided by Cecropia trees. Experimental induction of reconstruction of the envelope resulted in a different oval regular shape, without the characteristic hollow points. Evidence is also presented of the use by this wasp of lichen components to make the white spots typically seen on nests.

Recurrent breakdowns of mutualisms with ants in the neotropical ant-plant genus Cecropia (Urticaceae)

Mutualisms could be evolutionarily unstable, with changes in partner abundances or in the spatial context of interactions potentially promoting their dissolution. We test this prediction using the defense mutualisms between species of the Neotropical genus Cecropia and Azteca ants. A new, multigene phylogeny with representatives of all five genera of Cecropieae (most of them from the Neotropics) and half of the 61 species of Cecropia shows the West African endemic Musanga (2spp.) as sister to Cecropia, implying dispersal from the Neotropics to Africa, with a molecular clock suggesting that this occurred about 23Mya. Cecropia, a genus of neotropical pioneer trees, started diversifying ca. 8Mya. We infer a single origin of specialized symbiosis with Azteca within Cecropia, eight complete losses of this symbiosis, and a potential partner shift involving the replacement of Azteca by Neoponera luteola ants. Niche space modeling based on geo-referenced occurrences of over 9000 collections representing 58 of the 61 species of Cecropia, together with several comparative analyses, implies that mutualism loss is concentrated at high altitudes and on Caribbean islands, with the surprisingly frequent breakdowns potentially facilitated by low species-specificity of interacting Cecropia and Azteca mutualists.

Rediscovery and reclassification of the dipteran taxon Nothomicrodon Wheeler, an exclusive endoparasitoid of gyne ant larvae

The myrmecophile larva of the dipteran taxon Nothomicrodon Wheeler is rediscovered, almost a century after its original description and unique report. The systematic position of this dipteran has remained enigmatic due to the absence of reared imagos to confirm indentity. We also failed to rear imagos, but we scrutinized entire nests of the Brazilian arboreal dolichoderine ant Azteca chartifex which, combined with morphological and molecular studies, enabled us to establish beyond doubt that Nothomicrodon belongs to the Phoridae (Insecta: Diptera), not the Syrphidae where it was first placed, and that the species we studied is an endoparasitoid of the larvae of A. chartifex, exclusively attacking sexual female (gyne) larvae. Northomicrodon parasitism can exert high fitness costs to a host colony. Our discovery adds one more case to the growing number of phorid taxa known to parasitize ant larvae and suggests that many others remain to be discovered. Our findings and literature review confirm that the Phoridae is the only taxon known that parasitizes both adults and the immature stages of different castes of ants, thus threatening ants on all fronts.