Leaf-cutting Ant Species Research Articles

A Macroglomerulus in the Antennal Lobe of Leaf-cutting Ant Workers and its Possible Functional Significance

Ants have a well-developed olfactory system, and pheromone communication is essential for regulating social life within their colonies. We compared the organization of primary olfactory centers (antennal lobes, ALs) in the brain of two closely related species of leaf-cutting ants (Atta vollenweideri, Atta sexdens). Both species express a striking size polymorphism associated with polyethism. We discovered that the ALs of large workers contain a substantially enlarged glomerulus (macroglomerulus, MG) at the entrance of the antennal nerve. This is the first description of an MG in non-sexual individuals of an insect. The location of the MG is laterally reversed in the two species, and workers of different size express a disproportional allometry of glomerular volumes. While ALs of large workers contain an MG, glomeruli in small workers are all similar in size. We further compared electroantennogram (EAG) responses to two common trail pheromone components of leaf-cutting ants: 4-methylpyrrol-2-carboxylate and 2-ethyl-3,6-dimethylpyrazine. At high concentrations the ratio of the EAG signals to 2-ethyl-3,6-dimethylpyrazine versus 4-methylpyrrol-2-carboxylate was significantly smaller in A. vollenweideri compared with the ratio of EAG signals to the same two components in A. sexdens. The differences in EAG signals and the species specific MG location in large workers provide correlative evidence that the MG may be involved in the detection of the trail pheromone.

Low variation in ribosomal DNA and internal transcribed spacers of the symbiotic fungi of leaf-cutting ants (Attini: Formicidae).

Leaf-cutting ants of the genera Atta and Acromyrmex (tribe Attini) are symbiotic with basidiomycete fungi of the genus Leucoagaricus (tribe Leucocoprineae), which they cultivate on vegetable matter inside their nests. We determined the variation of the 28S, 18S, and 5.8S ribosomal DNA (rDNA) gene loci and the rapidly evolving internal transcribed spacers 1 and 2 (ITS1 and ITS2) of 15 sympatric and allopatric fungi associated with colonies of 11 species of leafcutter ants living up to 2,600 km apart in Brazil. We found that the fungal rDNA and ITS sequences from different species of ants were identical (or nearly identical) to each other, whereas 10 GenBank Leucoagaricus species showed higher ITS variation. Our findings suggest that Atta and Acromyrmex leafcutters living in geographic sites that are very distant from each other cultivate a single fungal species made up of closely related lineages of Leucoagaricus gongylophorus. We discuss the strikingly high similarity in the ITS1 and ITS2 regions of the Atta and Acromyrmex symbiotic L. gongylophorus studied by us, in contrast to the lower similarity displayed by their non-symbiotic counterparts. We suggest that the similarity of our L. gongylophorus isolates is an indication of the recent association of the fungus with these ants, and propose that both the intense lateral transmission of fungal material within leafcutter nests and the selection of more adapted fungal strains are involved in the homogenization of the symbiotic fungal stock.

Combate sistemático de formigas-cortadeiras com iscas granuladas, em eucaliptais com cultivo mínimo

Avaliou-se a eficiência do combate sistemático de formigas-cortadeiras em áreas de reforma de eucalipto com cultivo mínimo, na Celulose Nipo-Brasileira S.A., em Belo Oriente, Minas Gerais, de setembro a dezembro de 1996. Os tratamentos consistiram na aplicação de uma isca granulada com sulfluramida (0,3%) de forma sistemática, a granel ou com microporta-iscas, na dosagem de 5 g a cada 6 m² e 10 g a cada 12 m², respectivamente. A mortalidade das colônias de formigas-cortadeiras foi avaliada 30 dias após a aplicação da isca. Foram encontradas até 396,3, 285,2, 59,3, 55,6, 29,6 e 14,8 colônias de Mycocepurus goeldii, Sericomyrmex sp., Acromyrmex subterraneus molestans, Atta spp., Acromyrmex balzani e Acromyrmex niger (Hymenoptera: Formicidae) por hectare, respectivamente. A eficiência da isca granulada no combate sistemático variou com o método empregado e com a espécie de formiga-cortadeira. A maior eficiência foi obtida para A. subterraneus molestans, com 69,2% de suas colônias mortas com a isca aplicada a granel e 62,5% com microporta-iscas, o que indica que a distribuição entre dois pontos com isca nos plantios de eucalipto foi maior que a área de forrageamento das formigas-cortadeiras encontradas e, ou, que a dosagem aplicada por ponto foi insuficiente.

Random Amplified Polymorphic DNA Markers Reveal Genetic Variation in the Symbiotic Fungus of Leaf-Cutting Ants

RAPD markers were used to examine the degree of genetic variation within the putatively asexual basidiomycete fungus (Lepiotaceae: provisionally named Leucoagaricus gongylophorus) associated with the leaf-cutting ant species Atta cephalotes. We analyzed fungal isolates from ant nests in two geographically distant sites, two isolates from Panama and five isolates from Trinidad. Ten decamer primers were used to amplify total DNA from these seven fungal isolates, and RAPD banding patterns were compared. Genetic similarity among isolates was determined by pair-wise comparisons of the shared number of DNA bands on an agarose gel. There was considerable genetic variation among isolates of the symbiotic fungus even within sites. Pairs of fungal isolates from the two different sites shared an average of only 36% of the bands in their RAPD profiles, while pairs from the within sites shared an average of 72% of the bands. RAPD markers may be useful for further investigation of the genetic structure of the fungal symbiont within species of leaf-cutting ants.

Cloning and sequencing of wsp encoding gene fragments reveals a diversity of co-infecting Wolbachia strains in Acromyrmex leafcutter ants

By sequencing part of the wsp gene of a series of clones, we detected an unusually high diversity of nine Wolbachia strains in queens of three species of leafcutter ants. Up to four strains co-occurred in a single ant. Most strains occurred in two clusters ( InvA and InvB), but the social parasite Acromyrmex insinuator hosted two additional infections. The multiple Wolbachia strains may influence the expression of reproductive conflicts in leafcutter ants, but the expected turnover of infections may make the cumulative effects on host ant reproduction complex. The additional Wolbachia infections of the social parasite A. insinuator were almost certainly acquired by horizontal transmission, but may have facilitated reproductive isolation from its closely related host.

Wolbachia in leafcutter ants: a widespread symbiont that may induce male killing or incompatible matings

Abstract Wolbachia is a maternally inherited bacterium that manipulates host reproduction by inducing cytoplasmic incompatibility (CI), parthenogenesis or male killing (MK). Here, we report on a screening of seven leafcutter ant species of the genera Atta and Acromyrmex. Using Wolbachia-specific polymerase chain reaction (PCR) primers we show that all species are infected, usually by double A + B strain infections. For Acromyrmex echinatior and A. octospinosus, a screening across all castes shows that gynes (prospective queens) have higher infection rates than workers and males. The low infection rate of workers suggests that workers lose their infection during development. This we interpret as adaptive, because a heritable symbiont does not benefit from being present in sterile workers. Both CI and MK could potentially account for the low infection rate of males. Formal theoretical models show greater support for the MK scenario in the free living species A. echinatior and A. octospinosus but indicate that Wolbachia in the social parasite A. insinuator may cause CI, supporting a scenario of sympatric speciation of the social parasite. We conclude that Wolbachia represents a previously unrecognized source of reproductive conflict in leafcutter ant colonies.

Waste management in leaf-cutting ants

Hygienic behaviour is an important aspect of social organisation because living in aggregations facilitates the spread of disease. Leaf-cutting ants face the additional problem of an obligatory dependency on a fungus, which itself is also susceptible to parasites. In this study we provide evidence for the importance of effective waste management in colonies of several Panamanian species of Atta and Acromyrmex leaf-cutting ants, differing in colony size and typical mode of waste accumulation (external or internal dumps). We show that: (1) waste is dangerous for the ants, which die at a higher rate in the presence of waste; (2) waste is dangerous for the mutualistic fungus because waste in field colonies is infected with the specialised fungal parasite Escovopsis; (3) the ants allocate considerable effort to active management of waste in order to reduce these dangers. This management follows a “conveyer belt” model according to which increasingly dangerous tasks are performed by older workers, who are less valuable to their colony. Our approach is kaleidoscopic, as different species of leafcutting ants are unequally suitable for direct observation and experimental manipulation, and suggests that more in depth studies of waste management in attine ants would be highly rewarding.

Multiple mating and facultative polygyny in the Panamanian leafcutter ant Acromyrmex echinatior

Queen mating frequency of the facultatively polygynous ant Acromyrmex echinatior was investigated by analysing genetic variation at an (AG)n repeat microsatellite locus in workers and sexuals of 20 colonies from a single Panamanian population. Thirteen colonies were found to be monogynous, 5 colonies contained multiple queens, whereas the queen number of 2 colonies remained unresolved. Microsatellite genotypes indicated that 12 out of 13 queens were inseminated by multiple males (polyandry). The mean queen mating frequency was 2.53 and the mean genetically effective paternity frequency was 2.23. These values range among the highest found in ants, and the results are in keeping with the high mating frequencies reported for other species of leafcutter ants. Consistent skew in the proportional representation of different patrilines within colonies was found, and this remained constant in two consecutive samples of offspring. Dissections showed that all examined queens from multiple-queen colonies were mated egg-layers. The mean relatedness value among nestmate workers in polygynous colonies was lower than that for monogynous colonies. No diploid males were detected in a sample of 70 genotyped males. Worker production of males was detected in one queenless colony. We discuss our findings in relation to known patterns of multiple maternity and paternity in other eusocial Hymenoptera.

Levantamento de Attini (Hymenoptera, Formicidae) em povoamento de Eucalyptus na região de Paraopeba, Minas Gerais, Brasil

This Work was conducted in Eucalyptus stands at the Itapoa farm of the Mannesmann Fi-El Florestal Ltda. in Paraopeba, MG. The species of fungus growing-ants and leaf-cutting ants found in regrowth areas and in harvesting phase plantings were: Acromyrmex balzani Emery, 1890; Acromyrmex laticeps nigrosetosus Forel 1908; Acromyrmex subterraneus subterraneus Forel, 1893; Atta laevigala (F. Smith, 1858); Alta sexdens rubropilosa Forel, 1908; Mycocepurus goeldii Forel, 1893; Sericomyrmex sp.; Trachymyrmex fuscus Emery, 1894 and three morphospecies of Trachymyrmex Forel, 1893. Taxa belonging to the genus Atta Fabricius, 1804 represented 39.14 and 41.22% of the total number of nests found in the regrowth area and in the harvesting phase plantings, respectively. For Acromyrmex Mayr, 1865 these values were 14.34 and 13.16%; for Trachymyrmex, 40.59 and 30.89%; for Mycocepurus Forel, 1893, 5.34 and 12.50% and Sericomyrmex Mayr, 1865, 0.59 and 2.23% in the regrowth area and in the harvesting phase plantations, respectively.

Foraging activity of two species of leaf-cutting ants (Atta) in a primary forest of the Central Amazon

The foraging activity of the leaf-cutting antsAtta sexdens andA. cephalotes was studied observing two colonies of each species in a primary forest of the Central Amazon. These two ant species utilize chemically and visually marked trunk trails, and it was show that foraging is centered on these trails. The number of new foraging sites was inversely reated to the distance from existing trails. As a consequence, the area effectively exploited by the studied colonies was only 15 to 23% of their respective foraging ranges. Both species attacked large trees (stem diameter >20 cm) in a proportion higher to the available one and this preference seems to be related with quality of the harvested material and with the “area restricted search” strategy employed by these ants. Although these ants were able to exploit a wide range of plant species, harvest activity was concentrated on only a few. New leaves was the main item foraged byA. cephalotes whereasA. sexdens did not show a pattern of plant part preference.A. sexdens also presented a higher temporal variation in foraging rates, and this variation was partiallly related to the type of plant part harvested. It is suggested that the more generalistic behaviour presented byA. sexdens is one of the factors that contributes to its diverse habitat distribution as compared toA. cephalotes.

Habitat selection by the queens of the leaf-cutting ant Atta sexdens L. in Brazil

The founding of a new nest is the most crucial period in the life of an ant colony (Wilson 1971). Mechanisms that enhance colony survivorship during this phase are thus of great value. Of special importance is the search for a suitable habitat by the foundress queen, since established colonies of most ant species are unable to migrate over long distances (Wilson & Hunt 1966). That ant queens select the habitat in which they will found a new colony has been demonstrated for several temperate zone species (Brian 1952, Brian et al. 1966, Pontin 1960, Wilson & Hunt 1966) and for the Neotropical leaf-cutting ants Atta cephalotes L. and Acromyrmex octospinosus Reich (Cherrett 1968). In this paper, evidence that such a mechanism is operating among the foundress queens of another leaf-cutting ant species, Atta sexdens L., is presented. Furthermore, it is shown that, once in the preferred habitat, they search for the best microhabitat. Field work was done at 'Fazenda Dimona', a ranch located about 70 km north of Manaus, Brazil (600 4' W, 20 19 S). In this ranch two forest fragments of 1 ha, one of 10 ha and one of 100 ha were created during late 1984 to meet the requirements of the Minimum Critical Size of Ecosystem Project (a collaborative binational research project between the Instituto Nacional de Pesquisas da Amazonia and the World Wildlife Fund-US). A fifth fragment about 100 m wide and bordering a local stream, but not related to the MCSE Project, was created at the same time. Brachiaria grass was planted in the cleared area, but no efforts were made to maintain the pasture free of weed species. One year later, at the beginning of the study, stands of secondary vegetation 1-2 m tall, mainly Laetia procera (Poepp.) Eichl., Solanum rugosum Dun. and species of Cecropia, were present throughout the pasture. The vegetation of the fragments was a primary, terra-firme forest (as defined by Guillaumet 1987).

The respiratory metabolism of the castes of two leaf cutting ants, Atta laevigata (F. Smith, 1858) and Atta sexdens rubropilosa forel, 1908

1. 1. The respiration of the different castes of two species of leaf-cutting ants, Atta laevigata and Atta sexdens rubropilosa was measured in both workers and sexed forms. 2. 2. The respiratory rates (μl O 2/mg(live)/hr) were, in A. laevigata, 0.644 (gardeners), 0.594 (cutters), 0.354 (soldiers), 0.233 (males) and 0.085 (females); in A. s. rubropilosa, 0.803 (gardeners), 0.748 (cutters), 0.510 (soldiers), 0.375 (males) and 0.274 (females), significantly higher than A. laevigata. 3. 3. All castes considered, the b-values of the equation relating oxygen consumption and weight in A. laevigata (0.53) were significantly different from that in A. s. rubropilosa (0.73).

Plant Selection and Foraging Patterns in Two Species of Leaf‐Cutting Ants (Atta)

Three colonies each of two species of leaf—cutting ants (Atta colombica Guer. and Atta cephalotes L.) were studied for 1 yr in the Guanacaste Province of Costa Rica to determine the following: (1) Do colonies of Atta cut leaves from a limited number of species (i.e., are they selective)? (2) What determines which plant species are attacked? (3) Do leaf—cutters optimize foraging in terms of energy expended by attacking palatable plants closest to the nest or do they distribute their efforts more or less evenly throughout their foraging territory? Several line of evidence support the hypothesis that A. cephalotes and A. colombica are selective in terms of plant material attacked. The ants sampled a large majority of the plant species present, but concentrated their foraging on a restricted subset of species. The mature leaves of only 31.4% and 22.0% of the species present were readily acceptable to A. colombica and A. cephalotes, respectively. The new leaves of another 12—16 plant species were acceptable. Different colonies of the same Atta species consistently attacked the same plant species if they were available, cut leaves from the same species at similar rates, and even attacked the same species of plants at the same time of year. The amount of material cut from host plant species was not correlated with host plant abundance in four of the six colonies studied, and was even slightly negatively correlated in two of these four. An analysis of plant distance from the nest versus amount harvested shows that palatable plant species close to the nest have a greater probability of being visited by the ants, but do not necessarily suffer more defoliation than other such plants within 50—60 m of the nest. Amount harvested decreases greatly for plants farther than 60—80 m from the nest. Thus colonies of Atta do not normally concentrate their efforts on plants closest to the nest, but foraging cannot be described as evenly distributed either. The factor responsible for selectivity in colonies of Atta is probably the internal chemistry of the material selected. An Atta colony must provide the fungus garden when a proper balance of nutrients and moisture without overlapping it with secondary compounds from the plants selected. The ants' attempt to solve this problem may explain some of the complexities of leaf—cutter foraging behavior.

The Effects of Seasonality on Foraging in Two Species of Leaf-Cutting Ants (Atta) in Guanacaste Province, Costa Rica

The foraging behavior of three colonies each of two species of leaf-cutting ants (Atta colombica and Atta cephalotes) was studied for a year in the seasonal evergreen forest of Guanacaste Province, Costa Rica. Foraging was predominantly nocturnal during the season and diurnal during the season, probably induced by seasonal changes in rain patterns, insolation, and vegetative cover. Largest quantities of vegetation were harvested at the beginning of the and seasons, in correlation with peaks in the number of plant species producing new leaves or flowering. Colonies harvested new leaves or flowers (especially during the season) as they became available. Though large amounts of mature leaves were available to them throughout the year, during the season the ants cut the mature leaves of a limited number of host plant species. It is proposed that Atta ants select new leaves, flower parts, and mature leaves of certain plant species because of their suitability for the growth of their fungus gardens and therefore the colony. ALTHOUGH THE EFFECTS OF SEASONALITY on temperate-zone biological communities are well known, the consequences of seasonal weather patterns on plants and animals in the tropics have only begun to be documented. Unlike temperate areas, variation in temperature is minimal. Seasonality is primarily manifested by distribution patterns of rainfall, and is expressed in terms of dry and rainy seasons. So-called rain forests usually have short seasons which appear to require little adjustment by organisms. In other areas the season is severe and lasts up to six months. To survive, plants and animals have evolved life-histories which enable them to avoid or even take advantage of the season (Fleming, Hooper, and Wilson 1972; Janzen 1967, 1970, 1973; Janzen and Schoener 1968; Wolf 1970). The season is a particular challenge to colonies of leaf-cutting ants (species of Atta). Leaf-cutters feed upon a fungus which they culture in their nest using leaves and other vegetative matter which they cut as a substrate for the fungus. Since most trees drop their leaves during the season, and herbaceous plants become inactive or die, the amount of potential harvest decreases greatly. As humidity drops and direct insolation increases, not only do conditions for foraging become unfavorable, but it becomes difficult to maintain the proper microclimate within the nest for growth of the fungus. Finally, species of Atta in the Guanacaste Province of Costa Rica mature reproductives during the season which are very large and make substantial demands on the fungus gardens. Mating flights occur at the start of the season (Rockwood 1972, 1973). The season may not be the only difficult season for leaf-cutters. During periods of heavy or continuous rainfall, foraging may be impossible or very difficult for several days. A number of workers are lost during each rainstorm (Rockwood, unpublished field observations; Weber 1972), and whole colonies may be lost during floods (Rockwood 1973). Since previous studies on leaf-cutter foraging have usually been of short duration (Cherrett 1968; Lugo et al. 1973), the effects of seasonality have been only briefly discussed in the literature (Weber 1972; Moser 1963, 1967; Lewis et al. 1974a, 1974b). This paper presents the results of a year's study and examines the effects of seasonality on the foraging of two species of leaf-cutting ants (A. colomnbica Guer. and A. cephalotes L.) in the highly seasonal Guanacaste Province of Costa Rica.

Laboratory investigations of the trail-following responses of four species of leaf-cutting ants with notes on the specificity of a trail pheromone ofAtta texana (Buckley)

Interspecific trail following activity of poison sac contents from four species of leaf-cutting ants was investigated. With only one exception, all the species tested followed trails made from each others poison sac contents. However when the ants were given a choice of following one of two separate trails, clear differences were shown in the poison sac contents of the three species tested. The responses of 24 species of ants and one species of termite to anAtta texana (Buckley) trail pheromone were tested.