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.     

Leaf-cutting ants and avoided plants: Defences against Atta texana attack

Summary Leaf-cutting ants (Formicidae; Attini) characteristically never attack some common plant species in their habitats. These plants may be defended against the ants in several ways. In Texas, mature leaves of Sapindus saponaria (Sapindaceae) and Celtis reticulata (Ulmaceae) are unpalatable to Atta texana Buckley foragers, while mature leaves of Berberis trifoliata (Berberidaceae) are palatable to the ants, but are too tough to cut. Young Celtis leaves and and young Berberis leaves are palatable and can be cut by the ants, however. These young leaves may escape attack by remaining palatable a brief amount of time (new Celtis leaves), or by occurring patchily in space and time (new Berberis leaves).     

New role for majors in Atta leafcutter ants

Abstract.  1.  Atta (Hymenoptera: Formicidae) leafcutter ants display the most polymorphic worker caste system in ants, with different sizes specialising in different tasks. The largest workers (majors) have large, powerful mandibles and are mainly associated with colony defence.
2. Majors were observed cutting fallen fruit and this phenomenon was investigated in the field by placing mango fruit near natural Atta laevigata and Atta sexdens colonies in São Paulo State, Brazil.
3. Ants cutting the fruit were significantly heavier (mean = 49.1 mg, SD = 11.1 mg, n = 90) than the ants carrying the fruit back to the nest (mean = 20.9 mg, SD = 9.2 mg, n = 90).
4. Fruit pieces cut by majors were small (mean = 15.9 mg), approximately half the weight of leaf pieces (mean = 28.5 mg) cut and carried by media foragers. It is hypothesised that it is more difficult to cut large pieces from three-dimensional objects, like fruit, compared to two-dimensional objects, like leaves, and that majors, with their longer mandibles, can cut fruit into larger pieces than medias.
5. The study shows both a new role for Atta majors in foraging and a new example of task partitioning in the organisation of foraging.     

The effect of wilting on the selection of leaves by the leaf-cutting ant Atta laevigata

Using field assays of leaf preference, we tested the hypothesis that wilting affects the selection of leaves by the leaf-cutting ant Atta laevigata (Fr. Smith). Detached leaves were left to air-dry until noticeably wilted. The area removed by the ants from wilted leaves was significantly greater than the area removed from fresh leaves, this effect being observed in several plant species, in leaves of different age, and in assays with different ant colonies. Leaves collected from water-stressed plants were also preferred to leaves from non-stressed plants. A. laevigata was found to employ a two-stage, size-related, strategy when cutting plants. Larger workers climbed the plant stem and dropped whole leaves to the ground by severing their petioles; smaller workers cut the lamina of the dropped leaves. The ants frequently left dropped leaves on the ground, until the next foraging day or even later, when they were harvested in a wilted condition in preference to newly-dropped leaves.It is possible that during wilting some repellent substances evaporate or become less effective, thus enhancing leaf palatability. Alternatively or in addition, changes in nutrient and water content may have rendered wilted leaves more palatable to leaf-cutting ants.     

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.

     

Load size selection by foraging leaf-cutter ants (Atta cephalotes)

ABSTRACT.

• 1 Velocity of load-carrying Atta cephalotes (L.) foragers increases with increasing ant size and decreasing load size.
• 2 Foragers are selective in the sizes of loads they carry, but heavier loads would apparently increase their rate of leaf transport to the nest (mg of leaf m s^?1).
• 3 Even for very thin leaves, leaf diameter is not correlated with ant body size despite the method of cutting (rotating around a fixed point on the leaf edge).
• 4 When cutting leaves of different densities, load mass is more closely matched to ant size than is load surface area. This implies that ants choose loads based on mass rather than surface area, and thus the several possible disadvantages associated with carrying loads of large surface area (e.g. increased disturbance by wind or rain) are unlikely explanations of why ants do not select larger loads.
• 5 The relationship beween forager size and load size is made more complex by further selectivity at the level of colony recruitment: larger ants recruit to higher-density (thicker) leaf types.
• 6 Gross leaf transport rate is not maximized by foraging A.cephalotes, but net rate of energy intake cannot be assumed to follow the same pattern. If costs/time (not measured) are constant with changing load size, then the net rate of energy intake is not maximized. An alternative hypothesis is that costs/time increase with larger loads, thereby decreasing net rate of gain for larger loads.

     

Geometry explains the benefits of division of labour in a leafcutter ant

Many ant species have morphologically distinct worker sub-castes. This presumably increases colony efficiency and is thought to be optimized by natural selection. Optimality arguments are, however, often lacking in detail. In ants, the benefits of having workers in a range of sizes have rarely been explained mechanistically. In Atta leafcutter ants, large workers specialize in defence and also cut fruit. Fruit is soft and can be cut by smaller workers. Why, therefore, are large workers involved? According to the geometry hypothesis, cutting large pieces from three-dimensional objects like fruit is enhanced by longer mandibles. By contrast, long mandibles are not needed to cut leaves that are effectively two-dimensional. Our results from Atta laevigata support three predictions from the geometry hypothesis. First, larger workers cut larger fruit pieces. Second, the effect of large size is greater in cutting fruit than leaves. Third, the size of fruit pieces cut increases approximately in proportion to the cube of mandible length. Our results are a novel mechanistic example of how size variation among worker ants enhances division of labour.     

Pretarsus structure in relation to climbing ability in the ants Brachyponera sennaarensis and Daceton armigerum

We studied the external and internal pretarsus structure of the ants Brachyponera sennaarensis and Daceton armigerum in relation to their very different climbing ability. B. sennaarensis is a ground-dwelling species that is not able to climb vertical smooth walls. They have a pair of straight pretarsal claws with an average claw tip angle of 56 degrees, while the ventral tarsal surface lacks fine hairs that touch the substrate. They have no adhesive pad on the vestigial arolium, while the arolium gland is very small. D. armigerum, on the other hand, is an arboreal and thus well-climbing species with a very strong grip on the substrate. Their pretarsal claws are very hooked, with a claw tip angle around 75 degrees. They have dense arrays of fine hairs on the ventral tarsal surface, a well-developed arolium and arolium gland. These clearly different morphological characteristics are in line with the opposite climbing performance of both species.     

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.     

The ‘truck‐driver’ effect in leaf‐cutting ants: how individual load influences the walking speed of nest‐mates

The foraging behaviour of social insects is highly flexible because it depends on the interplay between individual and collective decisions. In ants that use foraging trails, high ant flow may entail traffic problems if different workers vary widely in their walking speed. Slow ants carrying extra‐large loads in the leaf‐cutting ant Atta cephalotes L. (Hymenoptera: Formicidae) are characterized as ‘highly‐laden’ ants, and their effect on delaying other laden ants is analyzed. Highly‐laden ants carry loads that are 100% larger and show a 50% greater load‐carrying capacity (i.e. load size/body size) than ‘ordinary‐laden’ ants. Field manipulations reveal that these slow ants carrying extra‐large loads can reduce the walking speed of the laden ants behind them by up to 50%. Moreover, the percentage of highly‐laden ants decreases at high ant flow. Because the delaying effect of highly‐laden ants on nest‐mates is enhanced at high traffic levels, these results suggest that load size might be adjusted to reduce the negative effect on the rate of foraging input to the colony. Several causes have been proposed to explain why leaf‐cutting ants cut and carry leaf fragments of sizes below their individual capacities. The avoidance of delay in laden nest‐mates is suggested as another novel factor related to traffic flow that also might affect load size selection The results of the presennt study illustrate how leaf‐cutting ants are able to reduce their individual carrying performance to maximize the overall colony performance.     

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.     

Plant palatability to leaf‐cutter ants (Atta laevigata) and litter decomposability in a Neotropical woodland savanna

Although leaf‐cutter ants have been recognized as the dominant herbivore in many Neotropical ecosystems, their role in nutrient cycling remains poorly understood. Here we evaluated the relationship between plant palatability to leaf‐cutter ants and litter decomposability. Our rationale was that if preference and decomposability are related, and if ant consumption changes the abundance of litter with different quality, then ant herbivory could affect litter decomposition by affecting the quality of litter entering the soil. The study was conducted in a woodland savanna (cerrado denso) area in Minas Gerais, Brazil. We compared the decomposition rate of litter produced by trees whose fresh leaves have different degrees of palatability to the leaf‐cutter ant Atta laevigata. Our experiments did not indicate the existence of a significant relationship between leaf palatability to A. laevigata and leaf‐litter decomposability. Although the litter mixture composed of highly palatable plant species showed, initially, a faster decay rate than the mixture of poorly palatable species, this difference was no longer visible after about 6 months. Results were consistent regardless of whether litter invertebrates were excluded or not from litter bags. Similarly, experiments comparing the decomposition rate of litter from pairs of related plant species also showed no association between plant palatability and decomposition. Decomposition rate of the more palatable species was faster, slower or similar to that of the less palatable species depending upon the particular pair of species being compared. We suggest that the traits that mostly influence the decomposition rate of litter produced by cerrado trees may not be the same as those that influence plant palatability to leaf‐cutter ants. Atta laevigata select leaves of different species based – at least in part – on their nitrogen content, but N content was a poor predictor of the decomposition rates of the species we studied.     

On Heels and Toes: How Ants Climb with Adhesive Pads and Tarsal Friction Hair Arrays

Ants are able to climb effortlessly on vertical and inverted smooth surfaces. When climbing, their feet touch the substrate not only with their pretarsal adhesive pads but also with dense arrays of fine hairs on the ventral side of the 3^rd and 4^th tarsal segments. To understand what role these different attachment structures play during locomotion, we analysed leg kinematics and recorded single-leg ground reaction forces in Weaver ants (Oecophylla smaragdina) climbing vertically on a smooth glass substrate. We found that the ants engaged different attachment structures depending on whether their feet were above or below their Centre of Mass (CoM). Legs above the CoM pulled and engaged the arolia (‘toes’), whereas legs below the CoM pushed with the 3^rd and 4^th tarsomeres (‘heels’) in surface contact. Legs above the CoM carried a significantly larger proportion of the body weight than legs below the CoM. Force measurements on individual ant tarsi showed that friction increased with normal load as a result of the bending and increasing side contact of the tarsal hairs. On a rough sandpaper substrate, the tarsal hairs generated higher friction forces in the pushing than in the pulling direction, whereas the reverse effect was found on the smooth substrate. When the tarsal hairs were pushed, buckling was observed for forces exceeding the shear forces found in climbing ants. Adhesion forces were small but not negligible, and higher on the smooth substrate. Our results indicate that the dense tarsal hair arrays produce friction forces when pressed against the substrate, and help the ants to push outwards during horizontal and vertical walking.     

The effects of light on foliar chemistry,growth and susceptibility of seedlings of a canopy tree to an attine ant

Summary Seedlings of Inga oerstediana Benth. (Mimosaceae) growing in three different light environments (the understory, tree-fall gaps and full sun) were tested for differences in chemistry (nutrients and tannins), wound-induced increases in tannins, growth, and susceptibility to leaf-cutter ants, Atta cephalotes (L.) (Formicidae: Attini). I hypothesized that seedlings of I. oerstediana would contain higher concentrations of tannins when growing in high light conditions and, therefore, would be less susceptible to leaf-cutter ants.Foliar concentrations of condensed tannins were much higher in plants growing in full sun compared to those growing in the understory. The concentrations of condensed tannins did not increase following damage. Despite higher concentrations of condensed tannins in sun foliage, leaf-cutter ants found these leaves more acceptable. The preference for sun leaves was consistent with higher concentrations of foliar nutrients. I suggest that the magnitude of the increase in condensed tannins was not great enough to override the benefits of increased concentrations of foliar nutrients. Finally, based on these results and those of others, I suggest that foraging by leaf-cutter ants may be an important factor determining patterns of succession in early successional habitats.     

Walking on smooth or rough ground: passive control of pretarsal attachment in ants

The hymenopteran tarsus is equipped with claws and a movable adhesive pad (arolium). Even though both organs are specialised for substrates of different roughness, they are moved by the same muscle, the claw flexor. Here we show that despite this seemingly unfavourable design, the use of arolium and claws can be adjusted according to surface roughness by mechanical control. Tendon pull experiments in ants (Oecophylla smaragdina) revealed that the claw flexor elicits rotary movements around several (pre-) tarsal joints. However, maximum angular change of claws, arolium and fifth tarsomere occurred at different pulling amplitudes, with arolium extension always being the last movement. This effect indicates that arolium use is regulated non-neuronally. Arolium unfolding can be suppressed on rough surfaces, when claw tips interlock and inhibit further contraction of the claw flexor or prevent legs from sliding towards the body. To test whether this hypothesised passive control operates in walking ants, we manipulated ants by clipping claw tips. Consistent with the proposed control mechanism, claw pruning resulted in stronger arolium extension on rough but not on smooth substrates. The control of attachment by the insect claw flexor system demonstrates how mechanical systems in the body periphery can simplify centralised, neuro-muscular feedback control.     

Euphorbia cotinifolia (Euphorbiaceae): a promising alternative for leaf cutting ant Atta cephalotes (Hymenoptera: Formicidae) control

Field observations indicate that Euphorbia cotinifolia escapes attack by leaf cutting ants, which are the largest generalist herbivores of the Neotropics. We used controlled bioassays to evaluate the effect of E. cotinifolia on the foraging of the Atta cephalotes ant. In a free-choice trial, to five colonies were offered Mangifera indica leaves with a 10% aqueous E. cotinifolia extract, leaves with distilled water and untreated leaves. The carrying time and leaf area consumed were determined over a five-hour period. The effect of E. cotinifolia on the development of the symbiotic fungus on three sets of five colonies fed the leaves of this plant were compared to the controls fed M. indica and oat flakes, and the effect of the addition of extracts on the culture medium used for the symbiotic fungus isolation was evaluated. Euphorbia leaf consumption was lower than that of the other diets; its consumption as the exclusive foraging resource significantly affected the symbiotic fungus, resulting in changes in colour and texture and an 83.57% decrease in volume that occasionally caused 100% mortality. Although the aqueous extract of E. cotinifolia is not a phagodeterrent for foraging workers, it is evident that E. cotinifolia is not a preferred resource for A. cephalotes due to the negative effect on the growth and viability of the symbiotic fungus.     

Competition between grass‐cutting Atta vollenweideri ants (Hymenoptera: Formicidae) and domestic cattle (Artiodactyla: Bovidae) in Argentine rangelands

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Distal leg structures of the Aculeata (Hymenoptera): A comparative evolutionary study of Sceliphron (Sphecidae) and Formica (Formicidae)

The distal parts of the legs of Sceliphron caementarium (Sphecidae) and Formica rufa (Formicidae) are documented and discussed with respect to phylogenetic and functional aspects. The prolegs of Hymenoptera offer an array of evolutionary novelties, mainly linked with two functional syndromes, walking efficiently on different substrates and cleaning the body surface. The protibial-probasitarsomeral cleaning device is almost always well-developed. A complex evolutionary innovation is a triple set of tarsal and pretarsal attachment devices, including tarsal plantulae, probasitarsomeral spatulate setae, and an arolium with an internal spring-like arcus, a dorsal manubrium, and a ventral planta. The probasitarsal adhesive sole and a complex arolium are almost always preserved, whereas the plantulae are often missing. Sceliphron has retained most hymenopteran ground plan features of the legs, and also Formica, even though the adhesive apparatus of Formicidae shows some modifications, likely linked to ground-oriented habits of most ants. Plantulae are always absent in extant ants, and the arolium is often reduced in size, and sometimes vestigial. The arolium contains resilin in both examined species. Additionally, resilin enriched regions are also present in the antenna cleaners of both species, although they differ in which of the involved structures is more flexible, the calcar in Sceliphron and the basitarsal comb in Formica. Functionally, the hymenopteran distal leg combines (a) interlocking mechanisms (claws, spine-like setae) and (b) adhesion mechanisms (plantulae, arolium). On rough substrate, claws and spine-like setae interlock with asperities and secure a firm grip, whereas the unfolding arolium generates adhesive contact on smooth surfaces. Differences of the folded arolium of Sceliphron and Formica probably correlate with differences in the mechanism of folding/unfolding.     

Fine structural analysis of the fibrillar adhesion apparatus in ladybird beetle

The attachment system on the ladybird beetle Harmonia axyridis is composed of a pair of pretarsal claws and adhesive pads at the tarsal segments. The claws, which are connected to the pretarsal segment, are mainly used to hold the rough substrates by their apical diverged hooks. In contrast, the adhesive pads have an adhesive function when landing on smooth surfaces. They are interspersed at the ventral adhesive pad of each tarsomere, and are composed of two kinds of hairy setae. The discoid tip seta (DtS) is located at the central region of each adhesive pad. The DtS has a spoon‐shaped endplate with a long and narrow shaft. In contrast, the pointed tip seta (PtS) is interspersed along the marginal regions of each adhesive pad, and has a hook‐shaped spine near the tip. In the present study, we found numerous fine cuticular pores beneath the setae, which seem to be related to the secretion of some adhesive fluids. It may be deduced that ladybird beetles can attach to smooth surfaces more effectively by employing adhesive fluids filling in surface crevices to overcome problems cause by their larger size endplates.     

Phylogeny of leafcutter ants in the genus Atta Fabricius (Formicidae: Attini) based on mitochondrial and nuclear DNA sequences

Leafcutting ants of the genus Atta are the most conspicuous members of the tribe Attini, the fungus-growing ants. Atta species have long attracted the attention of naturalists, and have since become a common model system for the study of complex insect societies as well as for the study of coevolutionary dynamics due to their numerous interactions with fungi and other microbes. Nevertheless, systematics and taxonomy of the 15 species in the genus Atta have proven challenging, due in part to the extreme levels of worker polymorphism these species display, leading to disagreements about the validity of as many as five different subgenera and calling into question the monophyly of the genus. Here, we use DNA sequence information from fragments of three mitochondrial genes (COI, tRNA leucine and COII) and one nuclear gene (EF1-αF1), totaling 1070 base pairs, to reconstruct the phylogenetic relationships of Atta species using maximum parsimony, maximum likelihood and Bayesian inference techniques. Our results provide support for monophyly of the genus Atta, and suggest that the genus is divided into four monophyletic groups, which correspond to four of the five previously erected Atta subgenera: Atta sensu stricto and Archeatta, each with species composition identical to earlier proposals; Neoatta and Epiatta, with major differences in species composition from earlier proposals. The current geographic ranges of these species suggest that the historical separation of South America from Central and North America has played a role in speciation within this genus.