Foraging in highly dynamic environments: leaf‐cutting ants adjust foraging trail networks to pioneer plant availability

Major shifts in the availability of palatable plant resources are of key relevance to the ecology of leaf‐cutting ants in human‐modified landscapes. However, our knowledge is still limited regarding the ability of these ants to adjust their foraging strategy to dynamic environments. Here, we examine a set of forest stand attributes acting as modulating forces for the spatiotemporal architecture of foraging trail networks developed by Atta cephalotes L. (Hymenoptera: Formicidae: Attini). During a 12‐month period, we mapped the foraging systems of 12 colonies located in Atlantic forest patches with differing size, regeneration age, and abundance of pioneer plants, and examined the variation in five trail system attributes (number of trails, branching points, leaf sources, linear foraging distance, and trail complexity) in response to these patch‐related variables. Both the month‐to‐month differences (depicted in annual trail maps) and the steadily accumulating number of trails, trail‐branching points, leaf sources, and linear foraging distance illustrated the dynamic nature of spatial foraging and trail complexity. Most measures of trail architecture correlated positively with the number of pioneer trees across the secondary forest patches, but no effects from patch age and size were observed (except for number of leaf sources). Trail system complexity (measured as fractal dimension; Df index) varied from 1.114 to 1.277 along the 12 months through which ant foraging was monitored, with a marginal trend to increase with the abundance of pioneer stems. Our results suggest that some leaf‐cutting ant species are able to generate highly flexible trail networks (via fine‐tuned adjustment of foraging patterns), allowing them to profit from the continuous emergence/recruitment of palatable resources.     

Adaptive foraging of leaf‐cutter ants to spatiotemporal changes in resource availability in Neotropical savannas

1. Generalist herbivores feed on a wide and diverse set of species, but fine‐scale foraging patterns may be affected by the interplay between the quality, quantity and spatial distribution of host plants. 2. The foraging patterns of a prevalent Neotropical herbivore, the leaf‐cutter ant Atta laevigata, in the Brazilian Cerrado savannas were examined in order to determine if patterns observed are in concert with central‐place foraging predictions. 3. The results showed that A. laevigata acts as a polyphagous but highly selective herbivore, with ant attacks often resulting in partial defoliation of less‐preferred species and full defoliation of preferred ones. It was found, for the first time, that there is a strong and positive relationship between the relative attack frequency on plants from preferred species and foraging distance to the nest. This suggests a balance between the quality of plant resources harvested and costs involved in their transportation. It was also observed that colonies focused their harvest on preferred species in months with low availability of young leaves. Consequently, high herbivory rate was more frequent in plants attacked far away from the nest and in dry months. 4. These assessments highlight the fact that Atta colonies may become more selective as foraging distance to the nest increases and in response to fluctuations in the availability of palatable resources throughout the year. The results also show some dissimilarities in the foraging behaviours of A. laevigata when compared with other locations, suggesting that widely distributed herbivores may modify foraging strategies across their geographic range.     

Extended phenotypes and foraging restrictions: ant nest entrances and resource ingress in leaf‐cutting ants

Several factors may restrict the acquisition of food to below the levels predicted by the optimization theory. However, how the design of structures that animals build for foraging restricts the entry of food is less known. Using scaling relationships, we determined whether the design of the entrances of leaf‐cutting ant nests restricts resource input into the colony. We measured nests and foraging parameters in 25 nests of Atta cephalotes in a tropical rain forest. Ant flux was reduced to up to 60% at nest entrances. The width of all entrances per nest increased at similar rates as nest size, but the width of nest entrances increased with the width of its associated trail at rates below those expected by isometry. The fact that entrance widths grow slower than trail widths suggests that the enlargement of entrance holes does not reach the dimensions needed to avoid delays when foraging rates are high and loads are big. The enlargement of nest entrances appears to be restricted by the digging effort required to enlarge nest tunnels and by increments in the risk of inundation, predator/parasitoid attacks and microclimate imbalances inside the nest. The design of the extended phenotypes can also restrict the ingress of food into the organisms, offering additional evidence to better understand eventual controversies between empirical data and the foraging theory. Abstract in Spanish is available with online material.     

Effects of pasture and forest microclimatic conditions on the foraging activity of leaf-cutting ants

The fragmentation and transformation of land cover modify the microclimate of ecosystems. These changes have the potential to modify the foraging activity of animals, but few studies have examined this topic. In this study, we investigated whether and how the foraging activity of the leaf-cutter ant Atta cephalotes is modified by microclimatic variations due to land cover change from forest to pasture. We characterized the microclimate of each habitat and identified alterations in foraging behavior in response to relative humidity (RH), air temperature, and surface temperature along ant foraging trails by synchronously assessing foraging activity (number of ants per 5 min including incoming laden and unladen and outgoing ants) and microclimatic variables (air temperature, RH, and maximum and minimum surface temperature along the foraging trail). There were climatic differences between habitats during the day but not throughout the night, and A. cephalotes was found to have a high tolerance for foraging under severe microclimatic changes. This species can forage at surface temperatures between 17 and 45°C, air temperatures between 20 and 36°C, and an RH between 40% and 100%. We found a positive effect of temperature on the foraging activity of A. cephalotes in the pasture, where the species displayed thermophilic behavior and the ability to forage across a wide range of temperatures and RH. These results provide a mechanism to partially explain why A. cephalotes becomes highly prolific as anthropogenic disturbances increase and why it has turned into a key player of human-modified neotropical landscapes.     

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.     

A meta‐analysis of leaf‐cutting ant nest effects on soil fertility and plant performance

1. Leaf‐cutting ants (LCAs) are considered as one of the most important agents of soil disturbances that affect vegetation patterns, but these assertions are based on isolated studies or anecdotal data. In this study, meta‐analysis techniques were used to quantitatively analyse the generality of these effects and determine some of their sources of variation. 2. The results reveal the following: (i) LCA nest sites showed higher levels of soil fertility than control sites, but the key source of these nutrients is the refuse material rather than the nest soil itself; (ii) refuse material from external piles tended to be richer in nutrient content than refuse material from internal refuse chambers; (iii) nest sites from temperate habitats showed higher cation content than those located in tropical/subtropical habitats; and (iv) nest sites showed higher plant growth than adjacent non‐nest sites (especially if plants have access to the refuse) but similar plant density and plant richness. 3. As LCAs improve nutrient availability in nest sites through the accumulation of refuse material, the location of the refuse will have a relevant role affecting vegetation. LCA species with external refuse dumps could benefit herbs, early vegetation stages and short‐living plants, whereas those with internal refuse chambers could benefit long‐living, large trees. However, the positive effect on individual plants does not extend to population and community levels. The foraging preferences of ants and the changes in microclimatic conditions around nests could act as selective ecological filters. 4. As refuse material from external piles and nest sites in temperate habitats tend to show higher fertility than refuse material from internal nest chambers and nest sites in tropical/subtropical habitats, LCA species with external refuse dumps in temperate regions could be of particular relevance for nutrient cycling and vegetation patterns.     

Forest edge orientation influences leaf‐cutting ant abundance and plant drought stress in the Brazilian Atlantic forest

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Drought stress drives intraspecific choice of food plants by Atta leaf‐cutting ants

Leaf‐cutting ants (LCA) are polyphagous and dominant herbivores throughout the Neotropics that carefully select plant individuals or plant parts to feed their symbiotic fungus. Although many species‐specific leaf traits have been identified as criteria for the choice of food plants, the factors driving intraspecific herbivory patterns in LCA are less well studied. Herein, we evaluate whether or not drought‐stressed native plants are a preferred food source using free‐living colonies of two leaf‐cutting ants, Atta sexdens L. (Hymenoptera: Formicidae: Attini), in combination with five plant species, Ocotea glomerata Nees (Lauraceae), Lecythis lurida S. A. Mori (Lecythidaceae), Miconia prasina DC (Melastomataceae), Tovomita brevistaminea Engl. (Clusiaceae), and Tapirira guianensis Aubl. (Anacardiaceae), and Atta cephalotes L., in combination with two plant species, O. glomerata and Licania tomentosa Benth. (Chrysobalanaceae). In dual‐choice bioassays, ants removed about three times more leaf area from drought‐stressed plants compared to control plants. Both leaf‐cutting ant species consistently preferred drought‐stressed plants for all species tested, except T. guianensis. The mean acceptability index – expressing the preference for one of two options on a scale of 0 to 1 – of drought‐stressed plants ranged from 0.65 to 0.86 across plant species, and the preference did not differ significantly among the tested plant species. Our results suggest that selection of drought‐stressed individuals is a general feature of food plant choice by leaf‐cutting ants irrespective of ant or plant species. As human‐modified forest assemblages across the Neotropics are increasingly prone to drought stress, the documented preference of Atta for drought‐stressed plants may have tangible ecological implications.     

Human disturbance promotes herbivory by leaf‐cutting ants in the Caatinga dry forest

Anthropogenic disturbances are known to modify plant–animal interactions such as those involving the leaf‐cutting ants, the most voracious and proliferating herbivore across human‐modified landscapes in the Neotropics. Here, we evaluate the effect of chronic anthropogenic disturbance (e.g., firewood collection, livestock grazing) and vegetation seasonality on foraging area, foliage availability in the foraging area, leaf consumption and herbivory rate of the leaf‐cutting ant Atta opaciceps in the semiarid Caatinga, a mosaic of dry forest and scrub vegetation in northeast Brazil. Contrary to our initial expectation, the foraging area was not affected by either disturbance intensity or the interaction between season and disturbance intensity. However, leaf consumption and herbivory rate were higher in more disturbed areas. We also found a strong effect of seasonality, with higher leaf consumption and herbivory rate in the dry season. Our results suggest that the foraging ecology of leaf‐cutting ants is modulated by human disturbance and seasonality as these two drivers affect the spectrum and the amount of resources available for these ants in the Caatinga. Despite the low productivity of Caatinga vegetation, the annual rates of biomass consumption by A. opaciceps are similar to those reported from other leaf‐cutting ants in rain forests and savannas. This is made possible by maintaining high foraging activity even in the peak of the dry season and taking benefit from any resource available, including low‐quality items. Such compensation highlights the adaptive capacity of LCA to persist or even proliferate in human‐modified landscapes from dry to rain forests.     

Edge‐mediated reduction of phorid parasitism on leaf‐cutting ants in a Brazilian Atlantic forest

Previous studies have shown that leaf‐cutting ant populations benefit greatly from living in or near the edges of the Brazilian Atlantic forest. One of the mechanisms responsible for this rise in population density is an edge‐mediated increase of pioneer plants, resulting in increased food availability for the ants (i.e., less bottom‐up control). Here, we hypothesized that the release from natural enemies (i.e., less top‐down control) may also contribute to the phenomenon. We investigated whether parasitism of phorid flies on leaf‐cutting ants decreases in colonies located along the forest edge vs. the interior of a large tract of Atlantic forest in northeastern Brazil. For this, we assessed abundance and rates of oviposition attack by phorids in bimonthly intervals over a period of 1 year in 10 adult colonies of Atta cephalotes (L.) (Hymenoptera: Formicidae: Myrmicinae), five at the forest edge and five in the forest interior. The number of phorids attracted by ants at edge colonies was 40% lower than that at interior colonies. The temporal variation in phorid attraction was also significant, with approximately 35% fewer flies in the dry months as compared to the rainy months. As a result of lower phorid abundance, ant workers of edge colonies suffered three times fewer oviposition attacks than those of interior colonies. There was a tendency for fewer attacks during dry months, but the difference in the temporal variation was not significant. Our findings suggest that edge creation contributes to increased leaf‐cutting ant abundance, not only via the attenuation of bottom‐up forces, but also through an environmentally triggered depression of parasitoid abundance/efficiency, possibly because of adverse environmental conditions in edge habitats.     

Parallel foraging cycles for different resources in leaf‐cutting ants: a clue to the mechanisms of rhythmic activity

1. Leaf‐cutting ants display regular diel cycles of foraging, but the regulatory mechanisms underlying these cycles are not well known. There are, however, some indications in the literature that accumulation of leaf tissue inside a nest dampens recruitment of foragers, thereby providing a negative feedback that can lead to periodic foraging. We investigated two foraging cycles occurring simultaneously in an Atta colombica colony, one involving leaf harvesting and the other exploiting an ephemeral crop of ripe fruit. 2. Leaf harvesting followed a typical diel pattern of a 10–12 h foraging bout followed by a period of inactivity, while fruit harvesting occurred continuously, but with a regular pre‐dawn dip in activity that marked a 24 h cycle. 3. Although the results of the present study are drawn from a single field colony, the difference found is consistent with a mechanism of negative feedback regulation acting in parallel on two resources that differ in their rates of distribution and processing, creating cycles of formation and depletion of material caches. 4. This hypothesis should provoke further interest from students of ant behaviour and some simple manipulative experiments that would begin to test it are outlined. Any role of resource caches in regulating foraging by Atta colonies may have similarities to the logistics of warehouse inventories in human economic activity.     

The Function of Hitchhiking Behavior in the Leaf‐cutting Ant Atta cephalotes1

In some leaf‐cutting ant species, minim workers ride on the fragments of leaves as they are carried back to the nest from the cutting site. There is convincing evidence that these “hitchhikers” can protect the leaf carriers from attack by phorid (Diptera: Phoridae) parasitoids, but we consider the possibility of other functions for the hitchhiking behavior. It has been hypothesized that the hitchhikers (1) feed on leaf sap from the edges of the cut leaves; (2) ride back to the nest to save energy; (3) get caught on the fragments as they are cut, and hitchhike because they cannot (or will not) get off; and (4) begin the process of preparing the leaf to enter the fungal gardens in the nest, perhaps by removing microbial contaminants. We observed hitchhikers of Atta cephalotes in 14 nests at the La Selva Biological Station in Costa Rica. There was no difference in the proportion of leaf carriers with hitchhikers between day and night. Because the nests we observed were largely nocturnal, more than 90 percent of the hitchhiking occurred at night. The phorid parasitoids are usually considered to be diurnal, so the preponderance of nocturnal hitchhiking suggests other functions in addition to parasitoid defense. Hitchhikers spent more time in the defensive head‐up posture during the day, but spent more time in the head‐down posture at night. The head‐down posture may indicate cleaning or other leaf preparation. The hitchhikers were never observed feeding on sap. Hitchhikers frequently got onto and off of the fragments, and so they were not “marooned.” Few hitchhikers rode all the way back to the nest and were often moving on the leaf fragment; these observations make the energy conservation hypothesis less likely, although we cannot reject it. We conclude that parasitoid defense is an important function of hitchhiking but also that there are probably other functions when parasitoids are absent. Based on available data, the most likely possibility is preparation of the leaf fragment before it enters the nest.     

Ecosystem engineering by leaf‐cutting ants: nests of Atta cephalotes drastically alter forest structure and microclimate

1. The role played by Atta species as ecosystem engineers remains poorly investigated despite previous evidence that their nests can impact plant assemblages. 2. In a large remnant of Atlantic forest, we compared forest structure at 36 Atta cephalotes nests to control sites and assessed shifts in microclimate along transects from nests up to 24 m into the forest (11 representative colonies). 3. Nests (average size: 55 m²) were virtually free of understorey vegetation with a high proportion of dead stems (up to 70%). 4. Canopy openness above colonies increased by roughly 40% compared with controls (5.3% at colony vs. 3.7% at control sites). 5. At nest centres, about 6% of the total radiation penetrated through the sparse canopy. Light levels declined exponentially, reaching a third (2%) in the unaffected forest understorey. 6. Likewise, maximum soil temperatures and daily amplitudes declined exponentially from 25 to 23 °C and 1.6 to 0.8 °C, respectively. Soil moisture increased significantly along transects, yet the effect was small and no differences were detected for air temperature and humidity. 7. We extrapolated that individual A. cephalotes nests modify the microclimate in an area of almost 200 m² on average. For the population, this amounts to 6% of the area along forest edges, where colonies are strongly aggregated, compared with only 0.6% in the forest interior. 8. Nests changed microclimate to an extent that has been reported to impact seed germination, plant growth, and survival of seedlings, conclusively demonstrating that leaf‐cutting ants act as ecosystem engineers.     

Performance and fate of tree seedlings on and around nests of the leaf‐cutting ant Atta cephalotes: Ecological filters in a fragmented forest

Habitat fragmentation is currently the most pervasive anthropogenic disturbance in tropical forests and some species of leaf‐cutting ants of the genus Atta (dominant herbivores in the neotropics) have become hyper‐abundant in forest edges where their nests directly impact up to 6% of the forest area. Yet, their impacts on the regeneration dynamics of fragmented forests remain poorly investigated. Here we examine the potential of Atta cephalotes nests to function as ecological filters impacting tree recruitment. Growth, survival and biomass partitioning of experimentally planted seedlings (six tree species) were examined at eight spatially independent A. cephalotes colonies in a large Atlantic Forest fragment. Seedling performance and fate (leaf numbers and damage) were monitored up to 27 months across three habitats (nest centre, nest edge and forest understorey). Plants at illuminated nest centres showed twice the gross leaf gain as understorey individuals. Simultaneously, seedlings of all species lost many more leaves at nests than in the forest understorey, causing a negative net leaf gain. Net leaf gain in the shaded understorey ranged from zero (Licania and Thyrsodium species) to substantial growth for Copaifera and Virola, and intermediate levels little above zero for Protium and Pouteria. Also seedling survival differed across habitats and species, being typically low in the centre and at the edge of nests where seedlings were often completely defoliated by the ants. Lastly, seedling survival increased strongly with seed size at nest edges while there was no such correlation in the forest. Our results suggest that Atta nests operate as ecological filters by creating a specific disturbance regime that differs from other disturbances in tropical forests. Apparently, Atta nests favour large‐seeded tree species with resprouting abilities and the potential to profit from a moderate, nest‐mediated increase in light availability.     

Insects and light interact to mediate vine colonization of fast growing Microberlinia bisulcata tree seedlings in gaps of an African rain forest

Vines thrive in lowland tropical forests, yet the biotic factors underlying their colonization of host tree seedlings and saplings remain surprisingly understudied. Insect herbivores presumably could influence this process, especially where disturbance has opened the canopy (i.e., gaps)—temporary areas of higher primary productivity favoring the recruitment of vines and trees and invertebrates in forests—but their impact on vine colonization has never been experimentally tested. Using data from an insect herbivore exclusion (mesh-netting cages) experiment conducted in an African rain forest (Korup, Cameroon), I logistically modeled the probability of vines colonizing seedlings of three co-dominant species (Microberlinia bisulcata vs. Tetraberlinia bifoliolata and T. korupensis) in paired shaded understory and sunny gap locations (41 blocks across 80 ha, starting n = 664 seedlings) in a 1–2-yr period (2008–2009). Vine colonization occurred almost exclusively in gaps, occurring on 16% of seedlings there. Excluding herbivores in gaps doubled colonization of the light-demanding and faster growing M. bisulcata but had negligible effects on the two shade-tolerant, slower growing and less palatable Tetraberlinia species, which together were twice as susceptible to vines under natural forest gap conditions (controls). When protected from herbivores in gaps, more light to individual seedlings strongly increased vine colonization of M. bisulcata whereas its well-lit control individuals supported significantly fewer vines. These results suggest vines preferably colonize taller seedlings, and because light-demanding tree species grow faster in height with more light, they are more prone to being colonized in gaps; however, insect herbivores can mediate this process by stunting fast growing individuals so that colonization rates becomes more similar between co-occurring slow and fast growing tree species. Further influencing this process might be associational resistance or susceptibility to herbivores linked to host species’ leaf traits conferring shade-tolerant ability as seedlings or saplings. A richer understanding of how vines differentially influence forest regeneration and species composition may come from investigating vine–tree–herbivore interactions across light gradients, ideally via long-term studies and intercontinental comparisons. Abstract in French is available with online material.     

The Multiple Impacts of Leaf‐Cutting Ants and Their Novel Ecological Role in Human‐Modified Neotropical Forests

Herbivory has been identified as a potent evolutionary force, but its ecological impacts have been frequently underestimated. Leaf‐cutting ants represent one of the most important herbivores of the Neotropics and offer an interesting opportunity to address the role played by herbivorous insects through a perspective that embraces population‐ to ecosystem‐level effects. Here we: (1) qualitatively summarize the multiple ways leaf‐cutting ants interact with food plants and their habitats and elucidate the ultimate outcome of such interactions at multiple organization levels; (2) update our understanding of leaf‐cutting ant‐promoted disturbance regimes; and (3) examine potential ecological roles by leaf‐cutting ants within the context of human‐modified landscapes to guide future research agendas. First, we find that leaf‐cutting ants show that some herbivorous insects are able to generate ecologically important disturbance regimes via non‐trophic activities. Second, impacts of leaf‐cutting ants can be observed at multiple spatio‐temporal scales and levels of biological organization. Third, ecosystem‐level effects from leaf‐cutting ants are ecosystem engineering capable not only of altering the abundance of other organisms, but also the successional trajectory of vegetation. Finally, effects of leaf‐cutting ants are context‐dependent, species‐specific, and synergistically modulated by anthropogenic interferences. Future research should examine how leaf‐cutting ants respond to deforestation and influence remaining vegetation in human‐modified landscapes. By promoting either heterogeneity or homogeneity, leaf‐cutting ants operate not only as agricultural pests but also as ecological key players.     

Canopy disturbance and gap partitioning promote the persistence of a pioneer tree population in a near‐climax temperate forest of the Qinling Mountains,China

An unresolved question of temperate forests is how pioneer tree species persist in mature forests. In order to understand the responsible mechanisms, we investigated a near‐climax mixed temperate forest dominated by Betula albosinensis in the Qinling Mountains of China. Through establishing four 50 m × 50 m plots, we examined the canopy disturbance characteristics and its effects on tree recruitments. We further test the intra‐ and interspecific effects on the recruitment of B. albosinensis. The obtained data demonstrated canopy disturbance was frequent but most small‐sized. The canopy gaps are caused mainly by adult B. albosinensis by snapping. The regeneration of coexistent tree species shows a distinct preference for gap size. B. albosinensis were clumped at the juvenile stage and small scales. B. albosinensis juveniles were positively associated with B. utilis juveniles and negatively associated with the conspecific and B. utilis large trees. In addition, B. albosinensis juveniles showed negative associations with contemporary other tree species. Our results suggested that canopy disturbance caused by canopy trees and gap partitioning among the coexistent tree species are important for the persistence of the mixed forest. As a main gapmaker, B. albosinensis appear to develop a self‐perpetuating life‐history trait and allow them to persist.