Epiphyll deterrence to the leafcutter ant Atta cephalotes

Summary Epiphyll growth on leaves of the grapefruit Citrus paradisi and the understory cyclanth Cyclanthus bipartitus repelled the fungus-growing, leafcutter ant Atta cephalotes from harvesting leaves of these tropical plants. Experimental removal of epiphylls from leaves resulted in 2–3 times more herbivore damage by leafcutter ants as compared to matched leaves with epiphylls. Because of the protection from herbivore damage, host plants may derive a partial fitness benefit from association with epiphylls.     

Traffic dynamics of the leaf-cutting ant, Atta cephalotes

Colonies of Atta cephalotes (Myrmicinae: Formicidae) construct cleared paths between their nest and the vegetation sources at which they harvest leaf tissue. Here, we employ ideas from traffic engineering to study streams of laden and unladen ants on these paths. The relationship between average traffic speed and the concentration of workers on the road surface follows a relationship similar to what is expected by analogy to fluid dynamics. Although the traffic is composed of eusocial organisms with a common interest in group success, the coarse-grained behavior of Atta traffic displays little more coordination than a moving fluid. The relationship between speed and concentration implies that maximum flow rates (which are likely to be closely tied to colony-level rates of resource acquisition) occur at a relatively high concentration that keeps individual speeds well below their "free flow" maximum. We predict that this optimal concentration will characterize peak traffic throughout a trail network, and we propose a simple behavioral mechanism that would allow trails to be cleared to the correct width to provide the optimal concentration. Collisions (including encounters for antennation) are common in leaf-cutting ant traffic because traffic is not segregated into unidirectional streams. Nonetheless, we find a counterintuitive suggestion that flow rates (with concentration differences statistically removed) are higher when traffic is near a 50:50 mix of outbound and returning ants than when it contains majority flows in a single direction. Mixed-direction traffic may help disperse laden ants with reduced agility, thereby preventing inhomogeneities in the traffic stream that could clog the trail.     

Load-size determination in the leaf-cutting ant, Atta cephalotes

I examined load-size determination by a highly polymorphic leaf-cuttingant, Atta cephalotes, cutting leaves of artificial trees (branchesplaced in the top of plastic tubes). I compared load size forants cutting thin leaves (starfruit, Averrhoa carambola) andthick leaves (grapefruit, Citrus parodist). At each source,larger ants cut larger fragments. Distance from the nest hadno effect on load size. The mass of fragments cut by an antof a given size was significantly greater when cutting grapefruitleaves. The leaf area cut, however, showed no significant differencebetween the two leaf types. Leaf area increased approximatelyin proportion to ant body mass to the 0.6 power. As a resultof their method of load-size determination, ants of a givensize cut heavier loads when cutting the thicker leaves. Thisdifference, however, was counteracted at the colony level byrecruitment of larger ants, which cut smaller area fragmentsrelative to their body mass, to cut at thicker leaf sources.     

In vitro evaluation of Trichoderma and Gliocladium antagonism against the symbiotic fungus of the leaf-cutting ant Atta cephalotes

The antagonistic activity of Trichoderma and Gliocladium isolates against Attamyces sp., a symbiotic fungus of the leaf-cutting ant Atta cephalotes, was investigated. A. cephalotes cultures this fungus as the primary food source. Most of the Trichodema and Gliocladium isolates tested in vitro (82.6%) inhibited the Attamyces sp. mycelial growth, which was probably due to their colonization ability and competition for nutrients, both of them known mechanisms of some species of these genera. T. lignorum strain T-26 was the strongest inhibitor achieving a colonization of 23%. Microscopical observations indicate that the inhibitory effect was caused by an interaction that took place in close contact with the host hypha, causing wall deformation that led to the collapse of the turgor pressure. This revised version was published online in June 2006 with corrections to the Cover Date.     

Metagenomic and metaproteomic insights into bacterial communities in leaf-cutter ant fungus gardens

Herbivores gain access to nutrients stored in plant biomass largely by harnessing the metabolic activities of microbes. Leaf-cutter ants of the genus Atta are a hallmark example; these dominant neotropical herbivores cultivate symbiotic fungus gardens on large quantities of fresh plant forage. As the external digestive system of the ants, fungus gardens facilitate the production and sustenance of millions of workers. Using metagenomic and metaproteomic techniques, we characterize the bacterial diversity and physiological potential of fungus gardens from two species of Atta. Our analysis of over 1.2 Gbp of community metagenomic sequence and three 16S pyrotag libraries reveals that in addition to harboring the dominant fungal crop, these ecosystems contain abundant populations of Enterobacteriaceae, including the genera Enterobacter, Pantoea, Klebsiella, Citrobacter and Escherichia. We show that these bacterial communities possess genes associated with lignocellulose degradation and diverse biosynthetic pathways, suggesting that they play a role in nutrient cycling by converting the nitrogen-poor forage of the ants into B-vitamins, amino acids and other cellular components. Our metaproteomic analysis confirms that bacterial glycosyl hydrolases and proteins with putative biosynthetic functions are produced in both field-collected and laboratory-reared colonies. These results are consistent with the hypothesis that fungus gardens are specialized fungus–bacteria communities that convert plant material into energy for their ant hosts. Together with recent investigations into the microbial symbionts of vertebrates, our work underscores the importance of microbial communities in the ecology and evolution of herbivorous metazoans.     

The role of fungus in the diet of the leaf-cutting ant Atta cephalotes (L.)

Abstract. 1. The workers and queen of the leaf-cutting ant Atta cephalotes fed on the juice of swollen hyphae (staphylae) produced by their cultivated fungus, but neither obtained sufficient energy from this source for their respiratory needs. The number of staphylae eaten by workers increased with worker size but was not enough to satisfy their energy requirements.
2. Larvae fed on whole staphylae and staphylae previously chewed by workers, and obtained sufficient energy from this source for respiration and growth. No evidence of feeding on fungus hyphae or of trophallaxis between worker and larvae was found. Larvae preferred staphylae to hyphae when fed them artificially and they gained more weight on the former.
3. Worker ants imbibed plant sap during the preparation of plant material for the fungus garden and the uptake of carbohydrate during this process was sufficient to supply their energy needs for approximately 24 h.
4. Staphylae were richer in lipid and carbohydrate, and poorer in protein than ant fungal hyphae.
5. The number of staphylae produced by the fungus gardens of two small nests was comparable with the observed consumption rate but would provide only about 4% of the nest's respiratory requirements.
6. In the light of these findings, a revised view of the role of the fungus in the diet of the ant is discussed.     

Corrigendum: Shear adhesive performance of leaf-cutting ant workers (Atta cephalotes)

In our previous article, Shear adhesive performance of leaf-cutting ant workers (Atta cephalotes), a technical error occurred when calculating shear adhesive performance divided by tarsal pad area of worker ants carrying leaves (Stark, A. Y., Davis, H. R., & Harrison, W. K. (2019). Biotropica, 51(4), 572–580). Shear adhesive performance of worker ants carrying leaves was mistakenly divided by the tarsal pad area of workers riding on leaves. This has slightly changed our results. After correcting for this error, there is now no statistically significant difference in shear adhesive performance divided by tarsal pad area of worker ants riding on leaves and those carrying leaves. Shear adhesive performance of these groups remains statistically different than soldiers, and our original results (shear adhesive performance of all three groups differ from one another) are consistent with the reported trend in the original article using true pad area for each individual (rather than estimated). We list below the pages and figures in the original article that this correction applies to. All authors agree with this change, apologize for their error, and appreciate the opportunity granted by the editors and publisher to make this correction. Our original conclusion, that there is variation in shear adhesive performance per unit area among worker roles of Atta cephalotes, is still supported by these corrected results.     

Ontogenetic changes in forager polymorphism and foraging ecology in the leaf-cutting ant Atta cephalotes

In the leaf-cutting ant Atta cephalotes (L.) small colonies produce a relatively narrow size-range of small workers, whereas large colonies produce a much wider size-range of workers. In this study, I compared the foraging of four small A. cephalotes colonies (fewer than 5000 workers) with published data on foraging of large colonies to examine how colony size and worker size-range may be related to foraging ecology in leaf-cutting ants. I found that the foraging ecology of small A. cephalotes colonies is very different from that of large colonies. In small colonies, a relatively narrow size-range of foragers (1.4–6.7 mg, mean 3.3 mg) cut primarily herbs (ferns, grasses, and other small herbaceous plants) located within 7 m of the nest. In contrast, in large colonies, a broader size-range of workers (1.4–30 mg, mean 7.3 mg) participate in foraging, generally harvesting from trees 20–80 m from the nest, with larger workers cutting on trees with thicker and tougher leaves. Small colonies' dependence on small herbaceous plants near the nest may have a profound impact on distribution of A. cephalotes. A. cephalotes colonies are rarely found in primary forest, where the low occurrence of small herbaceous plants in the understory may preclude the establishment of young colonies.     

Forager polymorphism, size-matching, and load delivery in the leaf-cutting ant, Atta cephalotes

Abstract.

• 1 This study examined the importance of forager polymorphism and division of labour among foragers of different size for the economics of load delivery in a leaf-cutting ant, Atta cephalotes (L.). I collected A.cephalotes foragers coming down trees carrying leaf fragments to evaluate the degree of match between forager mass and the density (mass per unit area) of leaves being cut, and to quantify how this match affects whether the mass of leaf fragments cut by the ants are within the range which maximizes the rate and efficiency of load delivery.
• 2 Foragers ranged 23-fold in mass (1.4–32.1 mg). On average, larger workers cut at denser leaf sources. Leaf fragment area increased with ant mass, but relative area (fragment area/ant mass) decreased with ant mass. The density of a leaf type had little or no effect on the area cut by ants of a given size. As a result, ants of a given mass cut heavier fragments from the denser leaves. The effect of leaf density, however, was partly counteracted at the colony level by recruitment of larger ants, which cut smaller area fragments relative to their body mass, to cut at denser leaf sources.
• 3 Despite a fairly high variance in the relationship between ant mass and fragment mass, overall 87% of the laden ants (74–100% for different trees) carried leaf fragments in the 1.5–6 times body mass range. Earlier studies indicate that loads in this range yield the highest biomass transport rate and transport efficiency. Thus, the variance falls within bounds such that it has little effect on load transport efficiency. Having a broad range in optimal load mass may be considered an adaptation to the expected variability in load masses.
• 4 If there were no correlation between ant mass and leaf density, mismatches between ant mass and load mass would be more common than observed. Thus, size-matching of larger workers to cut denser leaves increases the rate and ergonomic efficiency of load delivery.

     

The Larix kaempferi genome reveals new insights into wood properties

Here, through single-molecule real-time sequencing,we present a high-quality genome sequence of the Japanese larch(Larix kaempferi), a conifer species with great value for wood production and ecological afforestation. The assembled genome is 10.97 Gb in size, harboring 45,828 protein-coding genes. Of the genome, 66.8% consists of repeat sequences, of which long terminal repeat retrotransposons are dominant and make up 69.86%. We find that tandem duplications have been responsible for the expansi...     

Synthetic amides toxic to the leaf-cutting ant Atta sexdens rubropilosa L. and its symbiotic fungus

• 1 Nine synthetic amides similar to natural N‐piperidine‐3‐(4,5‐methylenedioxyphenyl)‐2‐(E)‐propenamide and N‐pyrrolidine‐3‐(4,5‐methylenedyoxiphenyl)‐2‐(E)‐propenamide were synthesized and identified by their spectroscopic data.
• 2 The toxicity of these synthetic amides to the Atta sexdens rubropilosa workers and the antifungal activity against Leucoagaricus gongylophorus, the symbiotic fungus of the leaf‐cutting ants, were determined.
• 3 Workers ants that were fed daily on an artificial diet to which these compounds were added had a higher mortality rate than the controls for N‐pyrrolidine‐3‐(3′,4′‐methylenedioxyphenyl)‐2‐(E)‐propenamide and N‐benzyl‐3‐(3′,4′‐methylenedioxyphenyl)‐2‐(E)‐propenamide at a concentration of 100 µg/mL.
• 4 The completely inhibition (100%) of the fungal growth was observed with N‐piperidine‐3‐(3′,4′‐methylenedioxyphenyl)‐2‐(E)‐propenamide and N,N‐diethyl‐3‐(3′,4′‐methylenedioxyphenyl)‐2‐(E)‐propenamide at concentrations of 50 and 100 µg/mL and N‐pirrolidine‐3‐(3′,4′‐methylenedioxyphenyl)‐2‐(E)‐propenamide at a concentration of 100 µg/mL.
• 5 The possibility of controlling these insects in the future using synthetic piperamides that can simultaneously target both organisms is discussed.

     

Shear adhesive performance of leaf‐cutting ant workers (Atta cephalotes)

Wingless arboreal ants must resist the force of gravity while traversing substrates in their environment. For leaf‐cutting ants like Atta cephalotes, foraging may also include a ca. 30 m vertical descent while carrying a load 1–6 times their body mass. We hypothesized that heavier and larger ants would carry heavier and larger loads and that adhesive performance would positively correlate with load mass. We found no relationship between ant mass, body length, head width, or adhesive performance, and the load size an ant carried. In addition to workers carrying vegetative loads (most often leaves), workers in an active foraging trail also include smaller workers riding on the leaves carried by larger workers, and large major workers, providing protection from aerial and ground attacks (Soldiers), respectively. Despite varying functional roles, all foraging ants require secure attachment to the substrate. We measured shear adhesive performance of each foraging role and found that Soldiers produced the highest shear adhesive forces. However, when controlling for tarsal pad area, we found that ants carrying loads have higher shear adhesive performance per unit area than those riding on leaves, and that Soldiers have the lowest shear adhesive performance per unit area. This suggests that while leaf choice does not appear to be dictated by size, mass, or shear adhesive performance of individual ants, overall, ants who carry leaves adhere more strongly given their pad size than those who do not. Abstract in Spanish is available with online material.     

Some factors affecting the site and pattern of leaf-cutting activity in the ant Atta cephalotes L.

An account is given of some aspects of the leaf-cutting behaviour of the ant Atta cephalotes L. Chemical and physical factors that determine the site of cutting are described, and the significance of these in the pattern of plant attack is discussed.     

The draft genome of Actinia tenebrosa reveals insights into toxin evolution

Sea anemones have a wide array of toxic compounds (peptide toxins found in their venom) which have potential uses as therapeutics. To date, the majority of studies characterizing toxins in sea anemones have been restricted to species from the superfamily, Actinioidea. No highly complete draft genomes are currently available for this superfamily, however, highlighting our limited understanding of the genes encoding toxins in this important group. Here we have sequenced, assembled, and annotated a draft genome for Actinia tenebrosa. The genome is estimated to be approximately 255 megabases, with 31,556 protein‐coding genes. Quality metrics revealed that this draft genome matches the quality and completeness of other model cnidarian genomes, including Nematostella, Hydra, and Acropora. Phylogenomic analyses revealed strong conservation of the Cnidaria and Hexacorallia core‐gene set. However, we found that lineage‐specific gene families have undergone significant expansion events compared with shared gene families. Enrichment analysis performed for both gene ontologies, and protein domains revealed that genes encoding toxins contribute to a significant proportion of the lineage‐specific genes and gene families. The results make clear that the draft genome of A. tenebrosa will provide insight into the evolution of toxins and lineage‐specific genes, and provide an important resource for the discovery of novel biological compounds.     

Leaf density and a trade-off between load-size selection and recruitment behavior in the ant Atta cephalotes

This study considers the interplay between individual load-size selection and recruitment behavior in the leaf-cutting ant Atta cephalotes. Foraging workers anchor themselves on the leaf edge by their hind legs and pivot around them while cutting arcs from leaves. Since workers not only cut leaves but also lay chemical trails to recruit nestmates, we investigated whether there is conflict of motivation affecting the workers' decision either to quickly inform nestmates about a newly discovered food source, or instead to cut full-load leaf fragments, which could delay recruitment. Workers were presented with leaves of privet of three different grades of toughness (measured as leaf density=mass/area) as sources of different quality, and load-size selection and recruitment behavior by harvesting-satiated and harvesting-deprived workers were measured. The following results were obtained. (1) Leaf density affected individual load-size selection: both harvesting-satiated and harvesting-deprived workers were found to cut smaller leaf fragments from the denser leaves. (2) Harvesting-deprived workers cut smaller fragments than harvesting-satiated workers, and therefore saved cutting time. The fragments cut were smaller only during the initial phases of the recruitment process, when information about the discovery needed to be transferred. (3) Harvesting-deprived workers showed higher recruitment rates than harvesting-satiated workers. A considerable number of ants were observed to return to the nest unladen. During the initial phases, the ratio of laden/unladen workers was lower than that for harvesting-satiated workers, and increased with the development of the tograging process. (4) Scout workers confronted with familiar leaves ran back to the nest laying chemical trails without even contacting the leaves. They relied on olfactory cues to start recruiting nestmates, and leaf density played no role in their decisions. (5) When confronted with unfamiliar leaves, on the other hand, they assessed leaf quality by probing bites at the leaf edge, although no actual cuts occurred. In this situation, the resulting recruitment rates depended on physical leaf traits, being higher for the tenderer leaves. (6) Workers foraging on unfamiliar leaves cut smaller fragments than workers cutting familiar leaves, and most of them displayed trail-laying behavior when returning to the nest. The results support the hypothesis of a trade-off between time spent collecting and that invested to recruit nestmates. During the initial phases of exploitation of a newly discovered food source, workers reduced their individual carrying performance in order to return earlier to the colony for further recruitment.     

Rain shadow effects predict population differences in thermal tolerance of leaf-cutting ant workers (Atta cephalotes)

Tests of hypotheses for the evolution of thermal physiology often rely on mean temperatures, but mounting evidence suggests geographic variation in temperature extremes is also an important predictor of species’ thermal tolerances. Although the tropics are less thermally variable than higher latitude regions, rain shadows on the leeward sides of mountains can experience greater diel and seasonal variation in temperature than windward sites. Rain shadows provide opportunities to test predictions about the relationships of extreme temperatures with thermal physiology while controlling for latitude. We tested the hypothesis that populations of leaf-cutting ants (Atta cephalotes) in leeward, montane, and windward sites in Costa Rica would differ in upper thermal tolerances (CT_max) of workers. As predicted from rain shadow effects via extreme high temperatures, the leeward rain shadow site yielded the highest mean CT_max (rain shadow site 42.1 ± 0.3°C, Montane site 38.2 ± 0.5°C, and windward site 38.2 ± 0.3°C). This suggests that high-temperature extremes in tropical rain shadow forests can select for higher thermal tolerances. CT_max increased with worker body size within sites, but CT_max increased with body size more gradually at the two lowland sites, as predicted if local high temperatures selected more strongly on the most thermally vulnerable society members (small workers). This suggests that warmer lowland climates selected for colonies with less variation in heat tolerance than cooler high elevation climates.