Interplays between Atta ants (Formicidae: Attini), soils and environmental properties in the Brazilian Neotropics: a preliminary assessment

ABSTRACT

Leaf-cutting ants are the most important herbivore in the neotropics, represent active agents of pedobioturbation, and are regarded as ecosystem engineers. These ants have a wide variety of ecological functions, such as pollination, seed dispersal, and tree-growing control. Despite this importance, little is known on their distribution in relation to possible soil and environmental conditions that affect Atta ants occurrence. This study aimed to spatialize the main occurrences of Atta species in the Brazilian territory and evaluate the main environmental conditions driving ants species in the Brazilian tropical landscapes, at a preliminary basis. We compiled data of occurrence for 12 Atta species from Global Biodiversity Information Facility (GBIF) databases, and scientific literature (up to 2019) for each Atta species. To each point, we obtained the respective geoenvironmental data as soil properties, biome, geology, vegetation land use, and climate variables. From these data, possible zonalities of occurrence of 9/10 Atta species were discussed. We applied the principal components analysis (PCA) and Canonical Correspondence Analysis (CCA) to identify the environmental gradient and investigate the possible interplay between variables and species. Soil, vegetation, and land use attributes are the main drivers on the distribution of Atta at local scale where their evolutionary physiological and foraging adaptations allow them to nest and maintain the fungi culture. At broader scales, climatic attributes are key drivers of Atta distribution across Brazil, and also influence pedogenic processes. Our study demonstrates that species of Atta ants are not randomly dispersed in Brazil and are strongly associated with complex and diverse Brazilian landscapes. We remark that further studies on the distribution of leaf-cutting ants of the Atta genus in Brazil, as well as their evolutionary phylogenetics, are needed, based on larger database.

saúva ants; geographical distribution; climate conditions; leaf-cutting ants

INTRODUCTION

Brazil is a continental country that presents a large variability of vegetation, soils and climate, with an economy based largely on agriculture and primary environmental resources. Widely distributed across the Brazilian territory, leaf-cutting ants of the genus Atta (Formicidae: Attini) have a complex ecological interplay and a significant economic impact on agriculture. Despite representing the largest populations of herbivores in the neotropics, the genus Atta sp. are also primarily responsible for soil turbation and nutrients cycling, along with termites, far surpassing other soil animals, such as worms (Whitford and Eldridge, 2013). Leaf-cutting ants represent active agents of pedobioturbation, and are considered ecosystems engineers (Lavelle et al., 2016).

Leaf-cutting ants have a wide variety of ecological functions such as pollination, seed dispersal and tree-growing control, contributing to the stability of many forest/savanna ecosystems, besides their active role in the flow of energy and matter, in soil aeration, and nutrients cycling (Moutinho et al., 2003; Peternelli et al., 2004; Leal et al., 2014). Despite representing benefits for the soils, leaf-cutting ants, in practically all phases of forest development and cultivation, are considered pests, as they directly affect productivity (Fowler et al., 1989; MAPA, 2016), so much that a greater effort to control agricultural pests in Brazil is focused on leaf-cutting ants (Fowler et al., 1989; Zanetti et al., 2002).

The Attine tribe, dates to 65 million years before present (BP), and stands out for having leaf-cutting ants (Schultz and Brady, 2008; Branstetter et al., 2017). The two genera of leaf-cutting ants within this tribe, the genus Atta, popularly known as saúvas, and the genus Acromyrmex, known as quenquéns ants (Fowler et al., 1989), are both neotropical. The saúvas showed a great irradiation between 15BP and 5BP, and are now widely distributed in the neotropics of South America, comprising 15 different species in Brazil alone (Fowler, 1995; Bacci et al., 2009). The key aspect related Atta ants is their position as a dominant herbivore in the neotropics, consuming hundreds of kilograms of plant material per year (Mikheyev et al., 2008). In foraging areas, a single colony can consume up to 50 % of the leaves available (Costa et al., 2018; Swanson et al., 2019). Despite being considered herbivores, they do not eat indigest plant material, but rather use it to maintain a mandatory symbiotic association with fungi. Ants provide food and protection to the fungus, while the fungus is the main food supply of the colony (Mueller et al., 2005; Mehdiabadi et al., 2012).

Plant material used for the fungi cultivation is chosen by a combination of high nutrition value and low toxicity (Nichols-Orians, 1991; Mundim et al., 2009). Therefore, leaf-cutting ants preferentially cut fresh, young leaves with high levels of nitrogen, zinc, calcium, and copper (Berish, 1986; Mundim et al., 2009) and low levels of tannins, saponins, and phenolic compounds (Nichols-Orians, 1991; Folgarait et al., 1996). When carried into the nests, all this material promotes a nutritional increase and accumulation of organic matter in the soil, which benefits the access of plant roots to these nutrients within the nests and even in the surrounding areas (Sternberg et al., 2007).

There are variations among ants both in the choice of the place to build their nests, as well in the way the soil is deposited (Pereira-Da-Silva, 1975; Moreira et al., 2004a). Due to the complexity of the nests, the ants choose the best locations, with adequate conditions of temperature and humidity to create the eggs, the young stages of the ant, and the symbiont fungus (Moreira et al., 2004b; Camargo and Forti, 2015). As ant colonies grow, tunnels and chambers expand radially (Alvarado et al., 1981; Moreira et al., 2004a; Jonkman, 2009) to maintain favorable conditions. Seasonal variations on microclimatic conditions in the colony can also alter the depth of the nest, although the spatial arrangement and design of the ant nests are generally species-specific (Moreira et al., 2004a,b).

Several factors and environmental conditions can influence the geographical distribution and richness of Atta ants, such as soil, vegetation, rainfall, temperature, and land-use history (Fowler et al., 1989; Swanson et al., 2019). The relationship with the climate, for example, is quite complex and not completely understood as well as the relationships between ants diversity and environmental aspects (Jenkins et al., 2011). Although temperate cool temperatures are a limiting factor, ants survive in a wide thermal and moisture spectrum due to an extensive and complex network of galleries, both horizontally and vertically depending on seasonal conditions, existing a continuous excavation process. Hence these networks can regulate the internal environment in terms of moisture, temperature, and gases concentration (CO₂, CH₄, N₂O, water vapor) (Swanson et al., 2019).

Few studies attempted to understand how the edaphoclimatic factors and land use, together, affect the distribution of Atta species. In this context, we aimed to spatialize the main occurrences of Atta species in the Brazilian territory and evaluate the main environmental conditions driving Atta ants in the Brazilian tropical landscapes. This preliminary study provides the first discussion on the interplay between the spatial distribution of Atta and key environmental variables.

MATERIALS AND METHODS

Study area

Brazil is a large territory in the neotropical zone of South America, with a complex geoenvironmental variability. According to Köppen-Geiger climate classification system (Peel et al., 2007), Brazil comprehends nine basic climate types: Tropical Rainforest (Af), Tropical Monsoon (Am), Tropical Savannah (Aw), Arid Steppe Hot (BSh), Arid Desert Hot (BWh), Temperature dry winter with warm summer (Cwb), Temperature dry winter with hot summer (Cwa), Temperature without a dry season and warm summer (Cfb) and Temperature dry summer with hot summer (Csa). In geological terms, Brazil has extensive exhumed Precambrian basement rocks, both igneous and metamorphic hate Precambrian to Paleozoic metasedimentary rocks, young Mesozoic to Cenozoic, sedimentary cover (Campos et al., 1974; Hasui et al., 2012) across the continental and coastal areas.

Brazilian soils encompass thirteen classes according to the Brazilian Soil Classification System (Santos et al., 2018) and eighteen according to Soil Survey Staff (2014), ranging from Acrisols, Cambisols, Chernozems, Podzols, Gleysols, Solonchaks, Ferrasols, Luvisols, Fluvisols, Lepptsols, Arenosols, Regosols, Nitisols, Histosols, Planosols, Solonetz, Plinthosols, and Vertisols. Brazil has six main biomes, represented by the Amazon Forest, Atlantic Forest, Dry Caatinga, Savanna (Cerrado), Pantanal, and Pampa (IBGE, 2004a). Agricultural areas are a growing part of land-use types, since colonial times, with widespread deforestation of large areas of the Atlantic Forest biome (Dean, 1997), and fire remains a form of pasture to this day (Arroyo-Kalin, 2012). Alarming deforestation rates have been increasing in the last three decades, replacing rainforest and Cerrado by pasture land, agriculture, and urban areas (Rezende et al., 2018; Turubanova et al., 2018; Zaiatz et al., 2018).

Environmental data and spatial distribution

Registers of Atta in Brazil were obtained by the Global Biodiversity Information Facility (GBIF) databases, and scientific literature (Della-Lucia, 2011; GBIF, 2020). Twelve Atta species were identified, represented by Atta cephalotes, A. laevigata, A. goiana, A. opaciceps, A. robusta, A. silvai, A. bisphaerica, A. capiguara, A. vollenweideri, A. sexdens piriventris, A. sexdens rubropilosa, and A. sexdens sexdens. We chose not to use the very limited distribution of A. goiana and A. silvai due to scale compatibility and doubtful occurrence. For each Atta point in the territory, we extracted the respective geoenvironmental data. These data were biomes (IBGE, 2004a), climate (IBGE, 2002), and soils (Embrapa, 2011) on 1:5.000.000 spatial scale. Soil classes were adapted from the Brazilian Soil Classification System (Santos et al., 2018) to WRB (Soil Survey Staff, 2014). We also used the geology and vegetation land use map (IBGE, 2004b) at 1:1.000.000 scale (Campos et al., 1974). Soil properties, as total organic carbon (TOC), pH, sand, clay, Cation Exchange Capacity (CEC) were obtained by the inverse distance weighting (IDW) method from the soil database of Geoprocessing Laboratory (Labgeo) at Federal University of Viçosa. Climate attributes were annual average rainfall (AARainf), average rainfall wetter trimester (ARainWt), average rainfall driest trimester (ARainDt), annual amplitude temperature (AAmpT), annual average temperature (AATemp), average temperature wetter trimester (ATempWt) and average temperature driest trimester (ATempDt) obtained from the WorldClim (Hijmans et al., 2005). From these data, possible zonalities of occurrence of each Atta species were identified.

Statistical analyses

The A. vollenweideri data was considered in zone aspects as sufficient and excluded in all further statistical analysis. The selected 9 Atta species that present sufficient points and information about habitat and occurrence were submitted to statistical methods and zone mapping. The possible relations between Atta species occurrence with environmental variables were carried out using R Environment (R CoreTeam, 2020). Considering all 473 points that showed all the variables under study, obtained in the previous processing steps. To better describe the occurrence of the Atta’s species in relation to the different environmental features, we performed a relative proportion bar plotting. For all variables, we tested the normal distribution with the Shapiro-Wilk test, evaluated the Q-Q plot, and assessed homogeneity of variances by Lavene’s test (p<0.05) using the “car” package (Fox and Weisberg, 2019). We used the Kruskal-Wallis’ test followed by a post hoc Dunn’s test (p<0.05) with the ‘Dunn.test’ package to compare the environmental properties (non-normally distributed data) represented by the CEC, TOC, pH, clay, sand, AATemp and AARainf, AAmpT, ATempWt and ATempDt, and ARainWt and ARainDt.

All variables were summarized with principal components analysis (PCA) to identify the environmental gradient (Qian et al., 2014; Villa et al., 2018). We also calculated Pearson correlations among all variables and the PCA ordination axes. The PCA was performed using the ‘FactoMineR’ package (Lê et al., 2008). To investigate a possible relationship between variables and species, a Canonical Correspondence Analysis (CCA) was used. For predictor selection, we assessed collinearity between selected predictor variables using Pearson correlation analysis; when two variables were strongly correlated (r≥0.7) the most ecologically relevant predictors were selected (discarded variables were Average Annual Temperature and Average Annual Rainfall) for subsequent analyses for CCA. The environmental data were submitted to a multicollinearity test, to check the inflation factor of the variation (VIF <5). This analysis tests if the coefficients of variation are influenced by other explanatory variables, creating instability in the model (Borcard et al., 2011). Canonical Correspondence Analysis examines the similarity or dissimilarity in species composition (occurrence register point) along the environmental gradient. The significance of each variable in determining species compositional change was assessed by applying Monte Carlo randomizations (999 randomizations). The CCAs were performed using the ordiplot function of the “vegan” package (Oksanen et al., 2019).

RESULTS

Spatial distribution of the Atta species

The A. laevigata and A. sexdens are the two species with the largest distribution across the Brazilian territory. A. laevigata occupies 7.002.950 km², which represents 78.1 % of Brazil, while A. sexdens extends over 6.926.983 km² (77.2 %). Both A. laevigata and A. sexdens species occur throughout the Amazon, Cerrado, and Atlantic Forest biome domains (Figure 2e). The A. sexdens has three main subdivisions, the A. sexdens sexdens (4.621.580 km²; 51.5 %), in the Amazon and coastal Atlantic Forest biomes, whereas the A. sexdens rubropilosa (1.671.270 km²; 18.6 %) is located in central Brazil in Cerrado and parts of the highlands of Atlantic Forest; A. sexdens piriventris (634.133 km²; 7.1 %) is preferentially located along the borders of Pampa and southern Atlantic Forest. A. vollenweideri (263.401 km²; 2.9 %) partially share the same area with A. sexdens piriventris, at the extreme south of Brazil (Figure 1), under temperate/subtropical climate.

Figure 2
The proportion of Atta points occurrence and respective variables of the soils (a), rocks (b), land-use (d), base saturation (c) and biome (e).

Figure 1
The genus Atta (Formicidae: Attini) spatial distribution at Brazilian territory.

Atta cephalotes (3.916.930 km²; 43.7 %) shares an extensive forest area with A. laevigata and A. sexdens sexdens, covering the Amazon and the coastal Atlantic Forest biomes associated with tropical hot and wet conditions. On the other hand, A. opaciceps occupies 755.154 km² (8.4 %), with most occurrences in the Brazilian semi-arid zone (Caatinga biome). At the highlands of southern and southeastern regions A. bisphaerica (193.760 km²; 2.2 %) and A. capiguara (269.781 km²; 3.2 %), occur under special environmental conditions of the Atlantic Forest domain. Finally, A. robusta has the most restricted occurrence, representing 87.912 km² (1.0 %) of the coastal and sandy Restinga ranging from São Paulo to Pará (Figure 1).

All nine Atta species have registers in Ferrasols and Acrisols, which represent the most expressive soil classes in Brazilian territory. Cambisols are also common and only A. cephalotes and A. opaciceps have no records on this soil class (Figure 2a). Podzols are closely related to A. robusta along the coastline, followed by the A. laevigata, A. sexdens sexdens, and A. cephalotes in the Amazonian domain. Arenosols are also dominated by A. robusta, followed by A. opaciceps and A. sexdens rubropilosa. Nitisols have registers of A. capiguara, A. sexdens piriventris, A. sexdens rubropilosa, and A. laevigata. Planosols present a larger number of registers of A. opaciceps, with much less association with the following species: A. robusta, A. laevigata, A. sexdens sexdens, A. sexdens piriventris, and A. bisphaerica (Figure 2a). Most Atta ants are associated with low base saturation and dystrophy, except for A. opaciceps that occur mainly on eutrophic soils (Figure 2c).

All the nine Atta species have registers on ancient granite-gneiss basement rocks and sedimentary covers. Igneous rock of volcanic type revealed the presence of A. sexdens piriventris and A. capiguara preferably, and these two species appear to be absent from metamorphic or sedimentary rocks. The Quaternary sedimentary sequences are concentrated at the coastline with a close relationship with the presence of A. robusta, A. sexdens sexdens, A. opaciceps, A. laevigata, and A. cephalotes (Figure 2b).

Nine of ten Atta species are found on the Atlantic Forest, with A. robusta exclusively related to coastal Restinga vegetation. Five species are found in Cerrado (A. bisphaerica, A. capiguara, A. laevigata, A. sexdens rubropilosa, and A. sexdens sexdens), three in the Amazonian region (A. cephalotes, A. laevigata, and the A. sexdens sexdens), two in grassy Pampa (A. sexdens piriventris and A. vollenweideri) and only one specie in Caatinga - A. opaciceps - with a small extension in the ecotonal zone with the Atlantic Forest (Figures 1 and 2e).

Most Atta species are found in lands under agricultural and livestock land use (A. capiguara, A. sexdens piriventris, and A. bisphaerica) or natural vegetation (A. cephalotes, A. laevigata, and A. sexdens sexdens). A. robusta and A. sexdens piriventris have not been recorded in urban areas (Figure 2d).

Atta - environment interplays

To unveil the main relationships between leaf-cutting and Atta ants and environmental variables, we discuss the PCA results. Firstly, the PCA of soil properties explained 71.5 % of the variance in the edaphic aspects (Figure 3). The PCA1 explained 48.5 %, with a positive correlation with clay (R = 0.88, p<0.001), TOC (R = 0.71, p<0.001) and CEC (R = 0.40, p<0.001), and inversely, negative with sand (R = - 0.90, p<0.001) and pH (R = - 0.42, p<0.001). The PCA2 explained 23 % and was positively correlated with CEC (R = 0.71, p<0.001) and pH (R = 0.70, p<0.001), and negatively correlated with sand (R = - 0.22, p<0.001) and TOC (R = - 0.32, p<0.001).

Figure 3
Principal Component Analysis (PCA) of relations between the Atta species points and soil properties. The soil variables are Total Organic Carbon (TOC), cation exchangeable capacity (CEC), pH, sand, and clay. Pearson correlation of each vector is indicated in cos2.

The PCA of climate attributes explained 73.2 % of the variance and the temperature regime attributes were more important than rainfall attributes (Figure 4). The PCA1 explained 47.4 % and was positively correlated with AATemp (R = 0.87, p<0.001), ATempDt (R = 0.90, p<0.001), ATempWt (R = 0.86, p<0.001), ARainWt (R = 0.41, p<0.001), and negatively with AAmpT (R = - 0.71, p<0.001). The PCA2 explained 25.8 % and was positively correlated with AARainf (R = 0.97, p<0.001), ARainWt (R = 0.78, p<0.001), ARainDt (R = 0.36, p<0.001) and AAmpT (R = 0.33, p<0.001).

Figure 4
Principal Component Analysis (PCA) of relations between the Atta species points and climatic aspects. The variables are annual average rainfall (AARainf), average rainfall wetter trimester (ARainWt), average rainfall driest trimester (ARainDt), annual amplitude temperature (AAmpT), annual average temperature (AATemp), average temperature wetter trimester (ATempWt), and average temperature driest trimester (ATempDt). Pearson correlation of each vector is indicated in cos2.

The CCA of soil properties explained 76.7 % (CCA1, 53.3 %; CCA2, 23.4 %) of Atta species variances according to pedology (Figure 5a). The CCA separated Atta species along pedological gradients, on which A. opaciceps, A. sexdens sexdens, and A. capiguara were positively associated with high pH and sand content, while A. sexdens piriventris, A. sexdens rubropilosa, and A. bisphaerica were linked to clay and organic carbon contents. A. cephalotes has positively associated with CEC whereas A. robusta was inversely correlated with this variable.

Figure 5
Canonical correspondence analysis (CCA) of soil and climate properties associated with different Atta species occurrence. In A, the soil aspects of Total Organic Carbon (TOC), cation exchangeable capacity (CEC), pH, sand, and clay. In B, the climate attributes of annual average rainfall (AARainf), average rainfall wetter trimester (ARainWt), average rainfall driest trimester (ARainDt), annual amplitude temperature (AAmpT), annual average temperature (AATemp), average temperature wetter trimester (ATempWt), and average temperature driest trimester (ATempDt).

The CCA of climate attributes explained 77 % (CCA1, 46.4 %; CCA2, 30.6 %) of Atta species variances according to climatology (Figure 5b). The CCA divided Atta species with temperature and rainfall regimes. A. opaciceps, A. sexdens sexdens, A. cephalotes, A. robusta, and A. laevigata were positively associated with higher temperatures; while A. capiguara, A. sexdens rubropilosa, and A. bisphaerica were linked to high rainfall and thermal amplitude, and A. sexdens piriventris associated with high pluviosity in the driest trimester and thermal amplitude, and A. opaciceps with hot, dry climates.

DISCUSSION

All nine Atta species showed records nutrients-poor dystrophic soils and ancient weathered granite-gneiss and sedimentary terrains, which represent most of the Brazilian geology, with Precambrian shields and Paleozoic platform covers (Hasui et al., 2012). A. opaciceps and A. sexdens piriventris are the two species with a high occurrence in nutrient-rich eutrophic soils, whereas A. capiguara has a close occurrence in eutric Nitisols associated with basalts rocks of the Paraná Basin (Hasui et al., 2012).

The close association between Atta and dystrophic soils may be attributed to the acid conditions required for fungus culture, where more fertile soils can increase the competition of soil microbiota (Bento et al., 1991; Moutinho et al., 2003; Siciliano et al., 2014), leading to lower fungi richness (Sun et al., 2016). There are differences between Atta species in their ability to control invasive microorganisms that can damage the colony’s fungal culture (Vieira et al., 2015) and acid, weathered soils may promote lesser invasion risk. In addition, nutrient-poor dystrophic soils, such as Ferrasols (Latossolos), have a friable microaggregate structure that favors the establishment of new colonies (Ker, 1997; Schoereder and Silva, 2008), resulting in a positive feedback.

Soil structure is considered very important in driving spatial distribution and nesting of leaf-cutters ants (Costa-Milanez et al., 2017). In soils with high clay content, ants roll or “pelletize” soil particles into 1‐ to 3‐mm‐sized aggregates used building blocks in the construction of wind turrets over vent openings in nests of A. vollenweideri, for instance (Swanson et al., 2019). A. cephalotes also uses pellets in their nests and A. sexdens sub-species create a drier, less dense, more porous mound with pelletized soils that enhance evaporation in nests depths ranging from 0.50 to 2.00 m (Swanson et al., 2019) (Figure 6). Note that the deeper chamber of A. sexdens sub-species, at 1.90 m depth, (Figure 6c) display cominuted fragments of plastic brought to the nest by the indiscrimate cutting behaviour of Atta sexdens sub-species. The microaggreegates are clearly visible in the old, abandoned chambers (Figures 6a and 6b.) Poor soils raises their importance in ecosystem functions.

Figure 6
The progressive infilling of a nest chamber with microaggregates (100-300 micrometers in diameter) of Oxisol (Latossolo) within a gneiss saprolite from Viçosa, MG.

Leaf-cutter ants remove 1-2 tons of fresh plant material annually that is rapidly decomposed in the nest by symbiotic fungi, promoting changes in physical, chemical and biological conditions, and also affecting the availability of nutritional resources and habitats for other organisms such as plants (Swanson et al., 2019). The fine root biomass is higher within leaf-cutting ant nests, with higher densities around and within external and internal litter chambers, evidencing its important role as an enhancer of nutritional quality in poor soils (Swanson et al., 2019).

Results showed the overlapping of three different species in Amazon, but with different correlations with soil attributes. A. laevigata do not have any preference, whereas A. cephalotes is correlated with soils with high TOC, CEC, and A. sexdens sexdens is more positively correlated with sand contents and pH. A. cephalotes is closely related to old, mature native forest environments, being an indicator of their conservation status. A. laevigata prefers disturbed habitats, in secondary regenerating process, and A. sexdens sexdens, the most flexible of all species, can be found in both environments (Fowler et al., 1989; Vasconcelos and Cherrett, 1995; Forti et al., 2020).

Overlapping of A. sexdens rubropilosa, A. capiguara, and A. bisphaerica does not imply competition. A. sexdens rubropilosa and A. bisphaerica have a positive correlation with TOC and clay content in soils, while A. capiguara have an opposite correlation, also reported by Forti et al. (2020). A. s. rubropilosa prefers dicots, while A. capiguara and A. bisphaerica prefer monocots (Fowler et al., 1989; Cabral, 2015; Pereira et al., 2016), and these species are more associated, respectively, with pasture and sugarcane areas. This can indicate that replacing natural vegetation and large monoculture monocotyledonous plantations may be an important factor in disseminating and increasing population density of these species (Forti et al., 2020).

Atta sexdens rubropilosa predominates in Ferrasols, generally of clayey texture, with organic-rich and microbiota-rich surface horizons (Vieira et al., 2015). The nests of this species are built up to approximately 0.15 m depth (Vieira et al., 2015). These shallow nests afford greater production of antibiotic compounds inside metapleural glands, which help control the invading microbiota (Vieira et al., 2015). These physiological traits favored during the evolution allowed the of A. sexdens rubropilosa nesting in the Brazilian highlands, with widespread distribution in southeastern Brazil (Cabral, 2015; Vieira et al., 2015).

In southern Brazil, just two species occur A. sexdens piriventris and A. vollenweideri. Although both species can be found in the same region, A. sexdens piriventris occur in Araucária Forest and Pampa. This species is associated with clayey soils, and can be found in Grasslands below 1000 m, and associated or not with Araucária (Giesel et al., 2013, 2020). The A. vollenweideri occurs mainly in the southern grasslands of lowland Pampa, preference foraging monocots, whereas A. sexdens piriventris prefers dicots (Fowler et al., 1989; Cosarinsky and Roces, 2007). A. vollenweideri have a low density of secretory cells, build their nests at greater depths – down to 0.368 m - in deeper clayey horizons, and with less microbial biomass due to the need to protect their colonies during flooding periods (Vieira et al., 2015). These physiological characteristics evolved to nesting in open, grassy, soil environments (Cabral, 2015; Vieira et al., 2015).

Atta robusta is restricted to coastal sandy areas with incipient pedological development, on the Quaternary fluvio-marine sediments where Restinga vegetation grows (Fowler, 1995; Cabral, 2015). It also has a strong association with sandy Restinga soils, being replaced by A. sexdens rubropilosa in places of clayey soils or disturbed by anthropic action (Fowler, 1995). The Restinga soils are commonly nutrient-poor (Scarano, 2002). The predominant soils in this pedoenvironments are Spodosols and Quartzarenic Neosols (Rossi and Mattos, 2002; Gomes et al., 2007). The occurrence of this species is related to greater temperature/rainfalls variations and low altitudes (Dáttilo et al., 2012).

A. robusta is found preferentially associated with native vegetation of Restinga thickets foraging Clusia fluminensis Planch. & Triana, a dominant species in Restingas (Fowler, 1995). The varying foraging habits of A. robusta, from the exotic species Terminalia catappa L. to the mangrove species (Rhizophora mangle L.), indicate that soils are more important for their presence than the plant species used for the cultivation of fungi. The widespread urbanization of coastal environments, including Restingas, poses a risk of extinction to A. robusta given its small geographical distribution and threats to its natural habitat (Fowler, 1995).

In the semi-arid Caatinga, an environment of severe conditions for many species, generalist species, such as A. laevigata, A. sexdens sexdens, and A. sexdens rubropilosa occur, but with a greater importance of the only “endemic” species of the genus, A. opaciceps (Fowler et al., 1989; Ulysséa and Brandão, 2013; Siqueira et al., 2017). Our results illustrate a greater association of A. opaciceps with the core semiarid area, with hotter and drier climates (Figure 5b) (Siqueira et al., 2018), whereas the other species are present in the transitional ecotones with the adjacent biomes. In addition to this occurrence in central Caatinga, A. opaciceps is well-adapted to anthropogenic landscapes (Knoechelmann et al., 2020), with a preference for open, shrubby vegetation, where Atta may contribute to maintaining this spatial pattern of vegetation, as postulated by Knoechelmann et al. (2020).

Atta ants are a key component of the biopedological system responsible for numerous nutritional, chemical, and structural changes in soils. Soils affected by nests tend to have greater microbial activity and production of hyphae and roots (Leite et al., 2018; Fernandez-Bou et al., 2019). The organic matter inputs in deep horizons and the disposal of residues, both in the garbage chambers of the colonies and at the surface outside the nests, enhances soil nutrition as well as nutrient cycling (Farji-Brener and Silva, 1995; Leite et al., 2018; Santos et al., 2019).

In addition to nutritional improvement, they increase soil aeration and infiltration by creating macropores, breaking seed dormancy, and consequently improving local physical conditions for subsequent colonization by plants during ecological succession (Sternberg et al., 2007; Giesel et al., 2013; Leite et al., 2018). In semiarid regions, A. opaciceps pedological activities may be even more important for the ecosystem’s resilience, since in the mounds nests act as collectors of the water flow in the short rainy season, directing nutrients and humidity to local points that can be instrumental in recruiting and maintaining new plants (Leite et al., 2018).

As our results indicate, Atta species are well adapted to disturbed landscapes revealing that Atta is a genus resilient to environmental disturbances (Diehl et al., 2017; Segat et al., 2017). These species were associated with young forests (Vasconcelos and Cherrett, 1995; Segat et al., 2017), forest edges (Silva et al., 2018), road edges (Forti et al., 2020), grazing sites (Leite et al., 2018) and open habitats (Dalle Laste et al., 2019; Swanson et al., 2019). This indicates that the wide dispersion of the Atta genus may have been favored by increased degradation of biomes (Siqueira et al., 2017).

The wide range of A. laevigata in open areas and disturbed habitats (Vasconcelos and Cherrett, 1995; Leite et al., 2018; Forti et al., 2020) may be related to the high abundance of pioneer species with high-nutrient contents in leaves, combined with a lower concentration of secondary chemical compounds that inhibit predation (Vasconcelos and Cherrett, 1995). Also, A. laevigata forages in both monocotyledons and dicots and this may explain its wide distribution in Brazil (Fowler et al., 1989; Vasconcelos and Cherrett, 1995; Vieira-Neto and Vasconcelos, 2010; Siqueira et al., 2017).

Given their ecological characteristics, some species may have an important role as a pedological agent counteracting the anthropogenic impacts. Agricultural activities cause soil compaction, lower infiltration, and greater runoff, consequences that are compensated or buffered by Atta’s pedobioturbation activity (Lavelle et al., 2016; Leite et al., 2018). The bioturbation performed by Atta ants acts in the structural arrangement of soils from construction to the maintenance of nests, galleries, chambers, and tunnels, bringing material from the deepest horizons to the surface, mixing organo-mineral aggregates, and creating new layers (Lavelle et al., 2016; Leite et al., 2018). Hence, A. robusta in Restinga can be an agent that affects podzolization processes, contributing to the formation of the spodic Bh horizon, for example.

This study supports further studies focused on the evolution of the genus Atta. This genus appeared approximately 8 to 13 million years ago, suggesting that irradiations, mainly across neotropical South America, are rather recent (Schultz and Brady, 2008; Bacci et al., 2009). It should be the case of the subgenus Neoatta, composed of the species A. sexdens sexdens, A. sexdens piriventris, A. sexdens rubropilosa and A. robusta, the most derived compared with the basal subgroups of the genus (Schultz and Brady, 2008; Bacci et al., 2009). Even these more differentiated species have different preferences regarding the clade of fungus used as food (Mueller et al., 2018). This adaptive irradiation is supposedly linked to the different environments/soils that Atta experienced during the successful advance throughout the Brazilian land surface, resulting in most species closely related to certain environmental conditions, as previously showed and discussed.

Also, further studies on the occurrence of the genus Atta and its environmental interplays, mainly in inland areas, such as the western Amazon and the Pantanal biome, are urgently needed to enhance our understanding of the role of Atta in anthropogenic, agropastoral landscapes.

CONCLUSIONS

Key species of Atta leaf-cutting ants in the neotropics are not randomly dispersed in the Brazilian landscape but have a close relationship with the complex environmental heterogeneity of the Brazilian neotropical zone. Latitudinal altitudinal climate gradients, soils, vegetation, geology, and anthropic landscapes - urbanization, agriculture, and livestock - are all interwoven with the spatial land distribution of the leafcutter Atta ants.

At a large scale, the spatial distribution of Atta was most correlated with a climatic gradient. At local scales, soil properties appear to be more determinant. The Atta species that occurs on most of the Brazilian land surface are the generalists A. sexdens and A. laevigata, while other species are most restricted to special environmental conditions, such as A. robusta at the sandy coastal plains, and A. opaciceps, concentrated in the semiarid Northeastern region.

ACKNOWLEDGEMENTS

We acknowledge the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil, for concession the scholarship of the authors and supporting by Geoprocessing Laboratory (LabGeo), from the Soil Department of the Federal University of Viçosa, who contributed with some preliminary data and analysis.

REFERENCES

• Alvarado A, Berish CW, Peralta F. Leaf‐cutter ant (Atta cephalotes) influence on the morphology of andepts in Costa Rica. Soil Sci Soc Am J. 1981;45:790-4. https://doi.org/10.2136/sssaj1981.03615995004500040023x
  » https://doi.org/10.2136/sssaj1981.03615995004500040023x
• Arroyo-Kalin M. Slash-burn-and-churn: Landscape history and crop cultivation in pre-Columbian Amazonia. Quat Int. 2012;249:4-18. https://doi.org/10.1016/j.quaint.2011.08.004
  » https://doi.org/10.1016/j.quaint.2011.08.004
• Bacci M, Solomon SE, Mueller UG, Martins VG, Carvalho AOR, Vieira LGE, Silva-Pinhati ACO. Phylogeny of leafcutter ants in the genus Atta fabricius (Formicidae: Attini) based on mitochondrial and nuclear DNA sequences. Mol Phylogenet Evol. 2009;51:427-37. https://doi.org/10.1016/j.ympev.2008.11.005
  » https://doi.org/10.1016/j.ympev.2008.11.005
• Bento JMS, Della Lucia TMC, Muchovej RMC, Vilela EF. Influence of soil chemical composition and microbial population on the establishment of incipient nests of Atta laevigata (Hymenoptera: Formicidae) under laboratory conditions. An Soc Entomol Bras. 1991;20:307-17.
• Berish CW. Leaf-cutting ants (Atta cephalotes) select nitrogen-rich forage. Am Midl Nat. 1986;115:268-76. https://doi.org/10.2307/2425863
  » https://doi.org/10.2307/2425863
• Borcard D, Gillet F, Legendre P. Numerical ecology with R. 2nd ed. New York: Springer; 2011.
• Branstetter MG, Ješovnik A, Sosa-Calvo J, Lloyd MW, Faircloth BC, Brady SG, Schultz TR. Dry habitats were crucibles of domestication in the evolution of agriculture in ants. Proc R Soc B Biol Sci. 2017;284:20170095. https://doi.org/10.1098/rspb.2017.0095
  » https://doi.org/10.1098/rspb.2017.0095
• Cabral DC. Into the bowels of tropical earth: leaf-cutting ants and the colonial making of agrarian Brazil. J Hist Geogr. 2015;50:92-105. https://doi.org/10.1016/j.jhg.2015.06.014
  » https://doi.org/10.1016/j.jhg.2015.06.014
• Campos CWM, Ponte FC, Miura K. Geology of the Brazilian continental margin. In: Burk CA, Drake CL, editors. The geology of continental margins. Berlin, Heidelberg: Springer; 1974. p. 447-61. https://doi.org/10.1007/978-3-662-01141-6_32
  » https://doi.org/10.1007/978-3-662-01141-6_32
• Cosarinsky MI, Roces F. Neighbor leaf-cutting ants and mound-building termites: Comparative nest micromorphology. Geoderma. 2007;141:224-34. https://doi.org/10.1016/j.geoderma.2007.06.006
  » https://doi.org/10.1016/j.geoderma.2007.06.006
• Costa AN, Bruna EM, Vasconcelos HL. Do an ecosystem engineer and environmental gradient act independently or in concert to shape juvenile plant communities? Tests with the leaf-cutter ant Atta laevigata in a Neotropical savanna. PeerJ. 2018;6:e5612. https://doi.org/10.7717/peerj.5612
  » https://doi.org/10.7717/peerj.5612
• Costa-Milanez CB, Majer JD, Castro PTA, Ribeiro SP. Influence of soil granulometry on average body size in soil ant assemblages: Implications for bioindication. Perspect Ecol Conserv. 2017;15:102-8. https://doi.org/10.1016/j.pecon.2017.03.007
  » https://doi.org/10.1016/j.pecon.2017.03.007
• Dalle Laste KC, Durigan G, Andersen AN. Biodiversity responses to land-use and restoration in a global biodiversity hotspot: Ant communities in Brazilian Cerrado. Austral Ecol. 2019;44:313-26. https://doi.org/10.1111/aec.12676
  » https://doi.org/10.1111/aec.12676
• Dáttilo W, Falcão JCF, Teixeira MC. Predictive model of distribution of Atta robusta Borgmeier 1939 (Hymenoptera: Formicidae): subsidies for conservation of a Brazilian leaf-cutting ant endangered species. Stud Neotrop Fauna Environ. 2012;47:193-201. https://doi.org/10.1080/01650521.2012.700791
  » https://doi.org/10.1080/01650521.2012.700791
• Dean W. A ferro e fogo: A história e a devastação da Mata Atlântica brasileira. São Paulo, SP: Companhia das Letras; 1997.
• Della-Lucia TMC. Formigas cortadeiras da bioecologia ao manejo. Viçosa, MG: Editora UFV; 2011.
• Diehl E, Diehl-Fleig E, Albuquerque EZ. Occurrence of Attini (Formicidae) in two geomorphological provinces of Rio Grande do Sul, Brazil. Braz J Agric. 2017;92:66-74. https://doi.org/10.37856/bja.v92i1.3303
  » https://doi.org/10.37856/bja.v92i1.3303
• Empresa Brasileira de Pesquisa Agropecuária - Embrapa. Mapa de Solos do Brasil. Escala 1:5.000.000. Rio de janeiro: Embrapa Solos; 2011.
• Farji Brener A, Silva J. Leaf-cutting ants and forest groves in a tropical parkland savanna of Venezuela: Facilitated succession? J Trop Ecol. 1995;11:651-69. https://doi.org/10.1017/S0266467400009202
  » https://doi.org/10.1017/S0266467400009202
• Fernandez-Bou AS, Dierick D, Swanson AC, Allen MF, Alvarado AGF, Artavia-León A, Carrasquillo-Quintana O, Lachman DA, Oberbauer S, Pinto-Tomás AA, Rodríguez-Reyes Y, Rundel P, Schwendenmann L, Zelikova TJ, Harmon TC. The role of the ecosystem engineer, the leaf-cutter ant Atta cephalotes, on soil CO₂ dynamics in a wet tropical rainforest. J Geophys Res Biogeosci. 2019;124:260-73. https://doi.org/10.1029/2018JG004723
  » https://doi.org/10.1029/2018JG004723
• Folgarait PJ, Dyer LA, Marquis RJ, Braker HE. Leaf-cutting ant preferences for five native tropical plantation tree species growing under different light conditions. Entomol Exp Appl. 1996;80:521-30. https://doi.org/10.1111/j.1570-7458.1996.tb00968.x
  » https://doi.org/10.1111/j.1570-7458.1996.tb00968.x
• Forti LC, Rando JS, Camargo RS, Moreira AA, Castellani MA, Leite SA, Sousa KKA, Caldato N. Occurrence of leaf-cutting and grass-cutting ants of the Genus Atta (Hymenoptera: Formicidae) in geographic regions of Brazil. Sociobiology. 2020;67:514-25. https://doi.org/10.13102/sociobiology.v67i4.5741
  » https://doi.org/10.13102/sociobiology.v67i4.5741
• Fowler HG. The population status of the endangered Brazilian endemic leaf-cutting ant Atta robusta (Hymenoptera: Formicidae). Biol Conserv. 1995;74:147-50. https://doi.org/10.1016/0006-3207(95)00009-S
  » https://doi.org/10.1016/0006-3207(95)00009-S
• Fowler HG, Pagani MI, Silva OA, Forti LC, Silva VP, De Vasconcelos HL. A pest is a pest is a pest? The dilemma of neotropical leaf-cutting ants: Keystone taxa of natural ecosystems. Environ Manage. 1989;13:671-5. https://doi.org/10.1007/BF01868306
  » https://doi.org/10.1007/BF01868306
• Fox J, Weisberg S. An {R} companion to applied regression. 3rd ed. Thousand Oaks: Sage; 2019. Available from: https://socialsciences.mcmaster.ca/jfox/Books/Companion/
  » https://socialsciences.mcmaster.ca/jfox/Books/Companion/
• Global Biodiversity Information Facility - GBIF. Free and open access to biodiversity data [internet]. Denmark: GBIF; 2020 [cited 2020 Aug 20]. Available from: www.gbif.org
  » www.gbif.org
• Giesel A, Boff MIC, Boff P. Seasonal activity and foraging preferences of the leaf-cutting ant Atta sexdens piriventris (Santschi) (Hymenoptera: Formicidae). Neotrop Entomol. 2013;42:552-7. https://doi.org/10.1007/s13744-013-0160-2
  » https://doi.org/10.1007/s13744-013-0160-2
• Giesel A, Boff P, Boff MIC, Fernandes P. Ocorrência de formigas cortadeiras em campos de altitude no sul do Brasil. Res Soc Dev. 2020;9:e839986365. https://doi.org/10.33448/rsd-v9i8.6365
  » https://doi.org/10.33448/rsd-v9i8.6365
• Gomes FH, Vidal-Torrado P, Macías F, Gherardi B, Perez JLO. Solos sob vegetação de Restinga na Ilha do Cardoso (SP). I - Caracterização e classificação. Rev Bras Cienc Solo. 2007;31:1563-80. https://doi.org/10.1590/S0100-06832007000600033
  » https://doi.org/10.1590/S0100-06832007000600033
• Hasui Y, Carneiro CDR, Almeida FFM, Bartorelli A. Geologia do Brasil. São Paulo, SP: Beca-BALL Edições Ltda; 2012.
• Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol. 2005;25:1965-78. https://doi.org/10.1002/joc.1276
  » https://doi.org/10.1002/joc.1276
• Instituto Brasileiro de Geografia e Estatística - IBGE. Mapa de Biomas do Brasil. Escala 1:5.000.000. Rio de Janeiro: IBGE; 2004a.
• Instituto Brasileiro de Geografia e Estatística - IBGE. Mapa de Vegetação do Brasil. Escala 1:1.000.000. Rio de Janeiro: IBGE; 2004b.
• Instituto Brasileiro de Geografia e Estatística - IBGE. Mapa de Clima do Brasil. Escala 1:5.000.000. Rio de Janeiro: IBGE; 2002.
• Jenkins CN, Sanders NJ, Andersen AN, Arnan X, Brühl CA, Cerda X, Ellison AM, Fisher BL, Fitzpatrick MC, Gotelli NJ, Gove AD, Guénard B, Lattke JE, Lessard J-P, McGlynn TP, Menke SB, Parr CL, Philpott SM, Vasconcelos HL, Weiser MD, Dunn RR. Global diversity in light of climate change: the case of ants. Divers Distrib. 2011;17:652-62. https://doi.org/10.1111/j.1472-4642.2011.00770.x
  » https://doi.org/10.1111/j.1472-4642.2011.00770.x
• Jonkman JCM. Biology and ecology of the leaf cutting ant Atta vollenweideri Forel, 1893. Zeitschrift Für Angew Entomol. 2009;81:140-8. https://doi.org/10.1111/j.1439-0418.1976.tb04221.x
  » https://doi.org/10.1111/j.1439-0418.1976.tb04221.x
• Ker JC. Latossolos do Brasil: Uma revisão. Geonomos. 1997;5:17-40. https://doi.org/10.18285/geonomos.v5i1.187
  » https://doi.org/10.18285/geonomos.v5i1.187
• Knoechelmann CM, Oliveira FMP, Siqueira FFS, Wirth R, Tabarelli M, Leal IR. Leaf‐cutting ants negatively impact the regeneration of the Caatinga dry forest across abandoned pastures. Biotropica. 2020;52:686-96. https://doi.org/10.1111/btp.12782
  » https://doi.org/10.1111/btp.12782
• Lavelle P, Spain A, Blouin M, Brown G, Decaëns T, Grimaldi M, Jiménez JJ, McKey D, Mathieu J, Velasquez E, Zangerlé A. Ecosystem engineers in a self-organized soil: A review of concepts and future. 2016;181:91-109. https://doi.org/10.1097/SS.0000000000000155
  » https://doi.org/10.1097/SS.0000000000000155
• Lê S, Josse J, Husson F. FactoMineR : An R package for multivariate analysis. J Stat Softw. 2008;25:1-18. https://doi.org/10.18637/jss.v025.i01
  » https://doi.org/10.18637/jss.v025.i01
• Leal IR, Wirth R, Tabarelli M. The multiple impacts of leaf-cutting ants and their novel ecological role in human-modified neotropical forests. Biotropica. 2014;46:516-28. https://doi.org/10.1111/btp.12126
  » https://doi.org/10.1111/btp.12126
• Leite PAM, Carvalho MC, Wilcox BP. Good ant, bad ant? Soil engineering by ants in the Brazilian Caatinga differs by species. Geoderma. 2018;323:65-73. https://doi.org/10.1016/j.geoderma.2018.02.040
  » https://doi.org/10.1016/j.geoderma.2018.02.040
• Mehdiabadi NJ, Mueller UG, Brady SG, Himler AG, Schultz TR. Symbiont fidelity and the origin of species in fungus-growing ants. Nat Commun. 2012;3:840. https://doi.org/10.1038/ncomms1844
  » https://doi.org/10.1038/ncomms1844
• Mikheyev AS, Vo T, Mueller UG. Phylogeography of post-Pleistocene population expansion in a fungus-gardening ant and its microbial mutualists. Mol Ecol. 2008;17:4480-8. https://doi.org/10.1111/j.1365-294X.2008.03940.x
  » https://doi.org/10.1111/j.1365-294X.2008.03940.x
• Ministério da Agricultura Pecuária e Abastecimento - MAPA. Revisão, análise e discussão sobre a viabilidade do uso das alternativas ao pfos, seus sais e PFOSF, no controle das formigas cortadeiras Atta e Acromyrmex dentro de uma abordagem de manejo integrado de manejo integrado de pragas. Brasília-DF: Mapa; 2016.
• Moreira AA, Forti LC, Andrade AP, Boaretto MA, Lopes J. Nest architecture of Atta laevigata (F. Smith, 1858) (Hymenoptera: Formicidae). Stud Neotrop Fauna Environ. 2004a;39:109-6. https://doi.org/10.1080/01650520412331333756
  » https://doi.org/10.1080/01650520412331333756
• Moreira AA, Forti LC, Boaretto MAC, Andrade APP, Lopes JFS, Ramos VM. External and internal structure of Atta bisphaerica Forel (Hymenoptera: Formicidae) nests. J Appl Entomol. 2004b;128:204-1. https://doi.org/10.1111/j.1439-0418.2004.00839.x
  » https://doi.org/10.1111/j.1439-0418.2004.00839.x
• Moutinho P, Nepstad DC, Davidson EA. Influence of leaf-cutting ant nests on secondary forest growth and soil properties in Amazonia. Ecology. 2003;84:1265-76. https://doi.org/10.1890/0012-9658(2003)084[1265:IOLANO]2.0.CO;2
  » https://doi.org/10.1890/0012-9658(2003)084[1265:IOLANO]2.0.CO;2
• Mueller UG, Gerardo NM, Aanen DK, Six DL, Schultz TR. The evolution of agriculture in insects. Annu Rev Ecol Evol Syst. 2005;36:563-95. https://doi.org/10.1146/annurev.ecolsys.36.102003.152626
  » https://doi.org/10.1146/annurev.ecolsys.36.102003.152626
• Mueller UG, Kardish MR, Ishak HD, Wright AM, Solomon SE, Bruschi SM, Carlson AL, Bacci JR M. Phylogenetic patterns of ant-fungus associations indicate that farming strategies, not only a superior fungal cultivar, explain the ecological success of leafcutter ants. Mol Ecol. 2018;27:2414-34. https://doi.org/10.1111/mec.14588
  » https://doi.org/10.1111/mec.14588
• Mundim FM, Costa AN, Vasconcelos HL. Leaf nutrient content and host plant selection by leaf-cutter ants, Atta laevigata, in a Neotropical savanna. Entomol Exp Appl. 2009;130:47-54. https://doi.org/10.1111/j.1570-7458.2008.00789.x
  » https://doi.org/10.1111/j.1570-7458.2008.00789.x
• Nichols-Orians C. Condensed tannins, attine ants, and the performance of a symbiotic fungus. J Chem Ecol. 1991;17:1177-95. https://doi.org/10.1007/BF01402942
  » https://doi.org/10.1007/BF01402942
• Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P. Vegan: community ecology package. R package version 2.5-6. Vienna: R Development Core Team; 2019.
• Peel MC, Finlayson BL, McMahon TA. Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci. 2007;11:1633-44. https://doi.org/10.5194/hess-11-1633-2007
  » https://doi.org/10.5194/hess-11-1633-2007
• Pereira-Da-Silva V. Contribuição ao estudo das populações de Atta sexdens rubropilosa Forel e Atta laevigata Fr. Smith no Estado de São Paulo (Hym: Formicidae). Stud Entomol. 1975:201-50.
• Pereira JS, Costa RR, Nagamoto NS, Forti LC, Pagnocca FC, Rodrigues A. Comparative analysis of fungal communities in colonies of two leaf-cutting ant species with different substratum preferences. Fungal Ecol. 2016;21:68-75. https://doi.org/10.1016/j.funeco.2016.03.004
  » https://doi.org/10.1016/j.funeco.2016.03.004
• Peternelli EFO, Della Lucia TMC, Martins SV. Espécies de formigas que interagem com as sementes de Mabea fistulifera Mart. (Euphorbiaceae). Rev Árvore. 2004;28:733-8. https://doi.org/10.1590/S0100-67622004000500013
  » https://doi.org/10.1590/S0100-67622004000500013
• Qian H, Hao Z, Zhang J. Phylogenetic structure and phylogenetic diversity of angiosperm assemblages in forests along an elevational gradient in Changbaishan, China. J Plant Ecol. 2014;7:154-65. https://doi.org/10.1093/jpe/rtt072
  » https://doi.org/10.1093/jpe/rtt072
• R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria; 2020. Available from: http://www.R-project.org/
  » http://www.R-project.org/
• Rezende CL, Scarano FR, Assad ED, Joly CA, Metzger JP, Strassburg BBN, Tabarelli M, Fonseca GA, Mittermeier RA. From hotspot to hopespot: An opportunity for the Brazilian Atlantic Forest. Perspect Ecol Conserv. 2018;16:208-14. https://doi.org/10.1016/j.pecon.2018.10.002
  » https://doi.org/10.1016/j.pecon.2018.10.002
• Rossi M, Mattos IFA. Solos de mangue do estado de São Paulo: caracterização química e física. Revista do Departamento de Geografia. 2002;15:101-13. https://doi.org/10.7154/RDG.2002.0015.0010
  » https://doi.org/10.7154/RDG.2002.0015.0010
• Santos HG, Jacomine PKT, Anjos LHC, Oliveira VA, Lumbreras JF, Coelho MR, Almeida JA, Araújo Filho JC, Oliveira JB, Cunha TJF. Sistema brasileiro de classificação de solos. 5. ed. rev. ampl. Brasília, DF: Embrapa; 2018.
• Santos RS, Mecenas HHB, Sousa-Souto L. Nest refuse of Atta opaciceps (Hymenoptera: Formicidae) increases plant biomass and diversity during the regrowth of herbaceous species. Appl Soil Ecol. 2019;133:160-5. https://doi.org/10.1016/j.apsoil.2018.10.002
  » https://doi.org/10.1016/j.apsoil.2018.10.002
• Scarano FR. Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic Rainforest. Ann Bot. 2002;90:517-24. https://doi.org/10.1093/aob/mcf189
  » https://doi.org/10.1093/aob/mcf189
• Schoereder JH, DaSilva WL. Leaf-cutting ants (Hymenoptera: Formicidae) and soil classes: Preference, survival and nest density. Sociobiology. 2008;52:403-15.
• Schultz TR, Brady SG. Major evolutionary transitions in ant agriculture. Proc Natl Acad Sci. 2008;105:5435-40. doi:10/1073/pnas.0711024105
  » https://doi.org/10/1073/pnas.0711024105
• Segat JC, Vasconcellos RLF, Silva DP, Baretta D, Cardoso EJBN. Ants as indicators of soil quality in an on-going recovery of riparian forests. For Ecol Manage. 2017;404:338-43. https://doi.org/10.1016/j.foreco.2017.07.038
  » https://doi.org/10.1016/j.foreco.2017.07.038
• Siciliano SD, Palmer AS, Winsley T, Lamb E, Bissett A, Brown MV, van Dorst J, Ji M, Ferrari BC, Grogan P, Chu H, Snape I. Soil fertility is associated with fungal and bacterial richness, whereas pH is associated with community composition in polar soil microbial communities. Soil Biol Biochem. 2014;78:10-20. https://doi.org/10.1016/j.soilbio.2014.07.005
  » https://doi.org/10.1016/j.soilbio.2014.07.005
• Camargo RS, Forti LC. What is the stimulus for the excavation of fungus chamber in leaf-cutting ants? Acta Ethol. 2015;18:31-5. https://doi.org/10.1007/s10211-014-0181-9
  » https://doi.org/10.1007/s10211-014-0181-9
• Silva JLG, Silva ILH, Ribeiro-Neto JD, Wirth R, Leal IR. Forest edge orientation influences leaf-cutting ant abundance and plant drought stress in the Brazilian Atlantic forest. Agric For Entomol. 2018;20:358-65. https://doi.org/10.1111/afe.12268
  » https://doi.org/10.1111/afe.12268
• Siqueira FFS, Ribeiro-Neto JD, Tabarelli M, Andersen AN, Wirth R, Leal IR. Human disturbance promotes herbivory by leaf-cutting ants in the Caatinga dry forest. Biotropica. 2018;50:779-88. https://doi.org/10.1111/btp.12599
  » https://doi.org/10.1111/btp.12599
• Siqueira FFS, Ribeiro-Neto JD, Tabarelli M, Andersen AN, Wirth R, Leal IR. Leaf-cutting ant populations profit from human disturbances in tropical dry forest in Brazil. J Trop Ecol. 2017;33:337-44. https://doi.org/10.1017/S0266467417000311
  » https://doi.org/10.1017/S0266467417000311
• Soil Survey Staff. Keys to soil taxonomy. 12th ed. Washington, DC: United States Department of Agriculture, Natural Resources Conservation Service; 2014.
• Sternberg LSL, Pinzon MC, Moreira MZ, Moutinho P, Rojas EI, Herre EA. Plants use macronutrients accumulated in leaf-cutting ant nests. Proc R Soc B Biol Sci. 2007;274:315-21. https://doi.org/10.1098/rspb.2006.3746
  » https://doi.org/10.1098/rspb.2006.3746
• Sun R, Dsouza M, Gilbert JA, Guo X, Wang D, Guo Z, Ni Y, Chu H. Fungal community composition in soils subjected to long-term chemical fertilization is most influenced by the type of organic matter. Environ Microbiol. 2016;18:5137-50. https://doi.org/10.1111/1462-2920.13512
  » https://doi.org/10.1111/1462-2920.13512
• Swanson AC, Schwendenmann L, Allen MF, Aronson EL, Artavia‐León A, Dierick D, Fernandez‐Bou AS, Harmon TC, Murillo‐Cruz C, Oberbauer SF, Pinto‐Tomás AA, Rundel PW, Zelikova TJ. Welcome to the Atta world: A framework for understanding the effects of leaf‐cutter ants on ecosystem functions. Funct Ecol. 2019;33:1386-99. https://doi.org/10.1111/1365-2435.13319
  » https://doi.org/10.1111/1365-2435.13319
• Turubanova S, Potapov PV, Tyukavina A, Hansen MC. Ongoing primary forest loss in Brazil, Democratic Republic of the Congo, and Indonesia. Environ Res Lett. 2018;13:074028. https://doi.org/10.1088/1748-9326/aacd1c
  » https://doi.org/10.1088/1748-9326/aacd1c
• Ulysséa MA, Brandão CRF. Ant species (Hymenoptera, Formicidae) from the seasonally dry tropical forest of northeastern Brazil: a compilation from field surveys in Bahia and literature records. Rev Bras Entomol. 2013;57:217-24. https://doi.org/10.1590/S0085-56262013005000002
  » https://doi.org/10.1590/S0085-56262013005000002
• Vasconcelos HL, Cherrett JM. Changes in leaf‐cutting ant populations (Formicidae: Attini) after the clearing of mature forest in Brazilian Amazonia. Stud Neotrop Fauna Environ. 1995;30:107-13. https://doi.org/10.1080/01650529509360947
  » https://doi.org/10.1080/01650529509360947
• Vieira-Neto EHM, Vasconcelos HL. Developmental changes in factors limiting colony survival and growth of the leaf-cutter ant Atta laevigata. Ecography. 2010;33:538-44. https://doi.org/10.1111/j.1600-0587.2009.05875.x
  » https://doi.org/10.1111/j.1600-0587.2009.05875.x
• Vieira AS, Camargo-Mathias MI, Roces F. Comparative morpho-physiology of the metapleural glands of two Atta leaf-cutting ant queens nesting in clayish and organic soils. Arthropod Struct Dev. 2015;44:444-54. https://doi.org/10.1016/j.asd.2015.06.005
  » https://doi.org/10.1016/j.asd.2015.06.005
• Villa PM, Martins SV, de Oliveira Neto SN, Rodrigues AC, Martorano LG, Monsanto LD, Cancio NM, Gastauer M. Intensification of shifting cultivation reduces forest resilience in the northern Amazon. For Ecol Manage. 2018;430:312-20. https://doi.org/10.1016/j.foreco.2018.08.014
  » https://doi.org/10.1016/j.foreco.2018.08.014
• Whitford WG, Eldridge DJ. Effects of ants and termites on soil and geomorphological processes. Treatise on Geomorphology. 2013;12:281-92. https://doi.org/10.1016/B978-0-12-374739-6.00335-3
  » https://doi.org/10.1016/B978-0-12-374739-6.00335-3
• Zaiatz APSR, Zolin CA, Vendrusculo LG, Lopes TR, Paulino J. Agricultural land use and cover change in the Cerrado/Amazon ecotone: A case study of the upper Teles Pires River basin. Acta Amaz. 2018;48:168-77. https://doi.org/10.1590/1809-4392201701930
  » https://doi.org/10.1590/1809-4392201701930
• Zanetti R, Carvalho GA, Silva AS, Santos A, Godoy MS. Manejo integrado de formigas cortadeiras. Lavras, MG: Editora UFLA; 2002.

• SUPPLEMENTARY DATA
  Supplementary data to this article can be found online at https://www.rbcsjournal.org/wp-content/uploads/articles_xml/1806-9657-rbcs-45-e0210073/1806-9657-rbcs-45-e0210073-suppl01.pdf

Edited by

Editors: José Miguel Reichert and Adriana Giongo.

Data availability

https://minio.scielo.br/documentstore/1806-9657/qcJ9L3sCH8mBXpqKjL5ntqt/e13b7f35b4d3033e93f0f0a143727968167bc86c.pdf

Publication Dates

• Publication in this collection
  17 Dec 2021
• Date of issue
  2021

History

• Received
  30 June 2021
• Accepted
  04 Oct 2021