Observation of leaf-cutting ants foraging on wild mushrooms

This study reports on the observation of an unusual behavior in leaf-cutting ants: foraging on wild mushrooms. A colony of Acromyrmex lundi in Buenos Aires (Argentina) was observed intensively harvesting basidiomes (mushroom fructifications) of wild Agrocybe fungus developing on a tree bark. Another colony maintained for a month in laboratory conditions also accepted Agrocybe mushroom and incorporated the cut bits into the fungus garden in the same way as they do with leaves. We recorded these events confident that they open a new perspective on the study of the feeding habits of leaf-cutting ants as well as on the relationship between their fungus garden and other organisms.     

Allometric scaling of foraging rate with trail dimensions in leaf-cutting ants

Leaf-cutting ants (Atta spp.) create physical pathways to support the transport of resources on which colony growth and reproduction depend. We determined the scaling relationship between the rate of resource acquisition and the size of the trail system and foraging workforce for 18 colonies of Atta colombica and Atta cephalotes. We examined conventional power-law scaling patterns, but did so in a multivariate analysis that reveals the simultaneous effects of forager number, trail length and trail width. Foraging rate (number of resource-laden ants returning to the nest per unit time) scaled at the 0.93 power of worker numbers, the -1.02 power of total trail length and the 0.65 power of trail width. These scaling exponents indicate that individual performance declines only slightly as more foragers are recruited to the workforce, but that trail length imposes a severe penalty on the foraging rate. A model of mass traffic flow predicts the allometric patterns for workforce and trail length, although the effect of trail width is unexpected and points to the importance of the little-known mechanisms that regulate a colony's investment in trail clearance. These results provide a point of comparison for the role that resource flows may play in allometric scaling patterns in other transport-dependent entities, such as human cities.     

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.     

Adaptive social immunity in leaf-cutting ants

Social insects have evolved a suite of sophisticated defences against parasites. In addition to the individual physiological immune response, social insects also express ‘social immunity’ consisting of group-level defences and behaviours that include allogrooming. Here we investigate whether the social immune response of the leaf-cutting ant Acromyrmex echinatior reacts adaptively to the virulent fungal parasite, Metarhizium anisopliae. We ‘immunized’ mini-nests of the ants by exposing them twice to the parasite and then compared their social immune response with that of naive mini-nests that had not been experimentally exposed to the parasite. Ants allogroomed individuals exposed to the parasite, doing this both for those freshly treated with the parasite, which were infectious but not yet infected, and for those treated 2 days previously, which were already infected but no longer infectious. We found that ants exposed to the parasite received more allogrooming in immunized mini-nests than in naive mini-nests. This increased the survival of the freshly treated ants, but not those that were already infected. The results thus indicate that the social immune response of this leaf-cutting ant is adaptive, with the group exhibiting a greater and more effective response to a parasite that it has previously been exposed to.     

Reliability theory and foraging by ants

Reliability theory is used to explore the consequences of ant colony's foraging techniques for the evolution of individual competence. Five fundamental strategies are outlined according to Oster & Wilson (1978) and corresponding probabilities of food being returned to the nest are derived. The strategies differ in redundancy schemes and levels of worker reliability. Colony-level selection produces workers of imperfect competence. System reliability can be very high even when the workers are inept, if the foraging strategy is complex and redundant. Individual competence of foragers in a colony depends on diet breadth, caste polymorphism, and tempo. The implications of each variable for colony survival are discussed.     

Individual foraging components of harvester ants: movement patterns and seed patch fidelity

Summary We investigated individual foraging components of the western harvester ant,Pogonomyrmex occidentalis, in the native seed background of a shrub-steppe environment. Our study identified factors affecting foraging movements and seed selection by individual ants. Some assumptions and predictions of central-place foraging theory and a correlated random walk were evaluated for individual foragers. Results showed that ant size was only weakly correlated with the seed sizes harvested; seed size was a more important constraint than a predictor of seed selection. Individual ants spent more time in localized search behavior than traveling between search areas and nests.P. occidentalis foragers encountered seeds randomly with respect to time, and handled a mean of 1.7 seeds/trip. A correlation of increased search effort with greater travel distances was consistent with central-place foraging theory but, contrary to it, search and travel effort were not associated with energetic reward.Individual ants exhibited fidelity in both search site and native seed species. Spatial analyses of foraging movements showed a highly oriented travel path while running, and an area-restricted path while searching. Searching ants moved in a manner consistent with a correlated random walk. The deterministic component of patch fidelity and the stochastic component of search may override energetic foraging decisions in individualP. occidentalis ants.     

Larval isolation and brood care in Acromyrmex leaf-cutting ants

The larvae of leaf-cutting ants are maintained within the fungus gardens of their colonies and are fed pieces of fungus by the adult workers. However, little else is known about the nature of the worker-larva interaction in these ecologically important ants. To examine whether workers can gauge the needs of individual larvae, we isolated larvae without adult workers for different lengths of time. We then placed workers with the larvae and recorded the type and frequency of the subsequent behaviours of the workers. Workers scraped the mouthparts of larvae, ingested their faecal fluid, fed them with fungal hyphae, transported them around the fungus garden and, most frequently, licked their bodies. The workers were also observed to ‘plant’ fungal hyphae on the bodies of larvae. Workers interacted more frequently with larvae that had been isolated without workers than with those that had not, but there was no effect of the length of isolation. The results suggest that the interactions are complex, involving a number of behaviours that probably serve different functions, and that workers are to some extent able to assess the individual needs of larvae. Received 8 November 2004; revised 31 March 2005; accepted 22 April 2005.     

With a little help from my friends: Individual and collaborative performance during trail clearing in leaf-cutting ants

Social organisms express collaborative behaviors, allowing them to solve problems that exceed their individual capabilities. Group coordination and environmental context are some of the factors that may determine the performance of individual and collaborative strategies. Using the trail-clearing behavior of leaf-cutting ants, we evaluated experimentally for both strategies whether the success probability and clearing time depend on problem characteristics and context. We placed obstacles of different sizes and shapes (problem characteristics), in trails with different foragers' fluxes and soil roughness (context) in 10 field nests of Atta cephalotes, and compared removal success (i.e., if ants could remove obstacles) and time of individual and collaborative strategies. Very large obstacles could only be removed collaboratively, confirming individual limitations for transporting large objects. For all obstacle shapes, collaborative removals were more successful but took longer, suggesting that coordination among individuals delays these actions. Individual strategies were faster, regardless of ant flux. However, as ant flux increased, removal success was higher for collaborative than for individual removals. Lastly, trail roughness had no effect. This work highlights one advantage of sociality, the option of collaboratively solving problems that exceed the individual abilities. In addition, it reveals the associated costs of joint actions, since they can be time-consuming presumably due to coordination problems.     

Evolutionary aspects of ant-fungus interactions in leaf-cutting ants

Leaf-cutting ants are highly successful herbivores because they are able to use a wide variety of plants as food The workers harvest and process plant material to be used as substrate for a fungus on which they feed. New hypotheses concerning the evolution of the ant-fungus relationship have now been proposed. Although the relationship between the ants and the fungus is mutualistic, if may appear that the fungus has little control over the ants. However, evidence suggests that the fungus may be exploiting the ants to provide it with substrate and antimicrobial defence. Furthermore, experimental evidence suggests that the fungus can select its substrate by controlling the foraging behaviour of the ants, by means of an ingenious chemical feedback mechanism.     

Yeasts and filamentous fungi carried by the gynes of leaf-cutting ants

Insect-associated microbes exhibit a wide range of interactions with their hosts. One example of such interactions is the insect-driven dispersal of microorganisms, which plays an essential role in the ecology of several microbes. To study dispersal of microorganisms by leaf-cutting ants (Formicidae: Attini), we applied culture-dependent methods to identify the filamentous fungi and yeasts found in two different body parts of leaf-cutting ant gynes: the exoskeleton and the infrabuccal pocket. The gynes use the latter structure to store a pellet of the ants’ symbiotic fungus during nest founding. Many filamentous fungi (n = 142) and yeasts (n = 19) were isolated from the gynes’ exoskeleton. In contrast, only seven filamentous fungi and three yeasts isolates were recovered from the infrabuccal pellets, suggesting an efficient mechanism utilized by the gynes to prevent contamination of the symbiotic fungus inoculum. The genus Cladosporium prevailed (78%) among filamentous fungi whereas Aureobasidium, Candida and Cryptococcus prevailed among yeasts associated with gynes. Interestingly, Escovopsis, a specialized fungal pathogen of the leaf-cutting ant-fungus symbiosis, was not isolated from the body parts or from infrabuccal pellets of any gynes sampled. Our results suggest that gynes of the leaf-cutter ants Atta laevigata and A. capiguara do not vertically transmit any particular species of yeasts or filamentous fungi during the foundation of a new nest. Instead, fungi found in association with gynes have a cosmopolitan distribution, suggesting they are probably acquired from the environment and passively dispersed during nest foundation. The possible role of these fungi for the attine ant–microbial symbiosis is discussed.     

Edge-induced narrowing of dietary diversity in leaf-cutting ants

Much of the ecological alteration faced by human-modified Neotropical forests can be assigned to edge effects, including the proliferation of some voracious herbivores such as leaf-cutting ants. However, the underlying mechanisms/impacts of tropical forest edge on herbivores performance and their foraging behaviour (e.g. dietary diversity) have rarely been investigated. The goal of this study was, therefore, to determine whether and how the annual diet (i.e. species richness, diversity and the relative proportion of pioneer versus non-pioneer species of plant materials) of Atta cephalotes colonies differs in the forest edge versus the interior zone of a large remnant of Atlantic forest in northeastern Brazil. Among the key results was a strong habitat effect on dietary diversity (explaining ca. 40-50% of the variation), which, in edge colonies, decreased approximately by one fourth compared to interior colonies (inverse of Simpson's index: 3.7±0.84 versus 4.99±0.95). There was a predominance of leaf fragments collected from pioneer species in the diet in both habitat (86% in edge and 80.4% in interior). Edge colonies collected proportionally more fragments from pioneer species than colonies located in the forest interior. Our results are the first to demonstrate an edge-mediated relaxation of dietary restrictions in leaf-cutting ants. These findings render robust support to previous evidence indicating the reduction of bottom-up forces as a key factor explaining both edge-induced hyper-abundance and increased herbivory of leaf-cutting ants in human-modified Neotropical landscapes.     

Genetic polymorphism in leaf-cutting ants is phenotypically plastic

Advanced societies owe their success to an efficient division of labour that, in some social insects, is based on specialized worker phenotypes. The system of caste determination in such species is therefore critical. Here, we examine in a leaf-cutting ant (Acromyrmex echinatior) how a recently discovered genetic influence on caste determination interacts with the social environment. By removing most of one phenotype (large workers; LW) from test colonies, we increased the stimulus for larvae to develop into this caste, while for control colonies we removed a representative sample of all workers so that the stimulus was unchanged. We established the relative tendencies of genotypes to develop into LW by genotyping workers before and after the manipulation. In the control colonies, genotypes were similarly represented in the large worker caste before and after worker removal. In the test colonies, however, this relationship was significantly weaker, demonstrating that the change in environmental stimuli had altered the caste propensity of at least some genotypes. The results indicate that the genetic influence on worker caste determination acts via genotypes differing in their response thresholds to environmental cues and can be conceptualized as a set of overlapping reaction norms. A plastic genetic influence on division of labour has thus evolved convergently in two distantly related polyandrous taxa, the leaf-cutting ants and the honeybees, suggesting that it may be a common, potentially adaptive, property of complex, genetically diverse societies.     

Immune defense in leaf-cutting ants: a cross-fostering approach

To ameliorate the impact of disease, social insects combine individual innate immune defenses with collective social defenses. This implies that there are different levels of selection acting on investment in immunity, each with their own trade-offs. We present the results of a cross-fostering experiment designed to address the influences of genotype and social rearing environment upon individual and social immune defenses. We used a multiply mating leaf-cutting ant, enabling us to test for patriline effects within a colony, as well as cross-colony matriline effects. The worker's father influenced both individual innate immunity (constitutive antibacterial activity) and the size of the metapleural gland, which secretes antimicrobial compounds and functions in individual and social defense, indicating multiple mating could have important consequences for both defense types. However, the primarily social defense, a Pseudonocardia bacteria that helps to control pathogens in the ants' fungus garden, showed a significant colony of origin by rearing environment interaction, whereby ants that acquired the bacteria of a foster colony obtained a less abundant cover of bacteria: one explanation for this pattern would be co-adaptation between host colonies and their vertically transmitted mutualist. These results illustrate the complexity of the selection pressures that affect the expression of multilevel immune defenses.     

Regulation and specificity of antifungal metapleural gland secretion in leaf-cutting ants

Ants have paired metapleural glands (MGs) to produce secretions for prophylactic hygiene. These exocrine glands are particularly well developed in leaf-cutting ants, but whether the ants can actively regulate MG secretion is unknown. In a set of controlled experiments using conidia of five fungi, we show that the ants adjust the amount of MG secretion to the virulence of the fungus with which they are infected. We further applied fixed volumes of MG secretion of ants challenged with constant conidia doses to agar mats of the same fungal species. This showed that inhibition halos were significantly larger for ants challenged with virulent and mild pathogens/weeds than for controls and Escovopsis-challenged ants. We conclude that the MG defence system of leaf-cutting ants has characteristics reminiscent of an additional cuticular immune system, with specific and non-specific components, of which some are constitutive and others induced.     

Evidence that the fungus cultured by leaf-cutting ants does not metabolize cellulose

Leaf‐cutting ants are a very specialized group of ants that cultivate fungus gardens in their nests, from which they obtain food. The current opinion is that the fungus cultivated by leaf‐cutting ants digests cellulose. Here we reassess the cellulose‐degrading capability of the fungus by using two complementary approaches tested in four Attini species (genera Atta and Acromyrmex): (1) ability of fungus to grow in cellulose; and (2) lignin/cellulose ratio in the refuse material dumped outside the nest, as an indicator of cellulose consumption. We found that (1) the fungus did not grow in cellulose, and (2) the lignin/cellulose ratio was much lower in the ants' refuse than in material digested by cellulose‐digesting organisms, such as brown‐rot fungus, termites, and ruminant mammals. This evidence strongly suggests the inability of the fungus to degrade cellulose. Therefore, the fungus–ant symbiosis and the ecological role of leaf‐cutting ants need to be reconsidered.     

Density-dependence and within-host competition in a semelparous parasite of leaf-cutting ants

Background  

Parasite heterogeneity and within-host competition are thought to be important factors influencing the dynamics of host-parasite relationships. Yet, while there have been many theoretical investigations of how these factors may act, empirical data is more limited. We investigated the effects of parasite density and heterogeneity on parasite virulence and fitness using four strains of the entomopathogenic fungus, Metarhizium anisopliae var. anisopliae, and its leaf-cutting ant host Acromyrmex echinatior as the model system.