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Natural History and Ecological Correlates of Fungus-Growing Ants (Formicidae: Attini) in the Neotropical Cerrado Savanna

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Natural History and Ecological Correlates of Fungus-Growing Ants (Formicidae: Attini) in the Neotropical Cerrado Savanna ECOLOGY AND POPULATION BIOLOGY Natural History and Ecological Correlates of Fungus-Growing Ants (Formicidae: Attini) in the Neotropical Cerrado Savanna 1,2 3 4 INARA R. LEAL, PAULO S. D. SILVA, AND PAULO S. OLIVEIRA Ann. Entomol. Soc. Am. 104(5): 901Ð908 (2011); DOI: 10.1603/AN11067 ABSTRACT Fungus-growing ants (Formicidae: Attini) comprise a diverse and ecologically impor- tant group in Neotropical habitats. Compared with leaf-cutters, however, relatively little is known about the biology of less conspicuous attine species. Here, we compare nest siZe and structure, colony siZe and demographic composition, and worker siZe and polymorphism among the genera Cypho- myrmex , Mycetarotes , Mycocepurus , Myrmicocrypta , Sericomyrmex , and Trachymyrmex . In total, 25 ant colonies (one species per genus) were investigated at one site in the BraZilian savanna. Results indicate a consistent variation in nest siZe and structural complexity (architecture), colony and worker siZe, and a tendency to polymorphism among the studied genera. In addition, nest mound volume was found to be a good predictor of both worker number and volume of the fungus garden. Based on morpho- metric analyses, Sericomyrmex and Trachymyrmex together formed a distinct group from the other genera. The transition from the ancestral agricultural system toward the derived leaf-cutting habit also is followed by remarkable changes in nest siZe and architecture, colony siZe, and worker siZe and polymorphism. Our results support other recent studies that consider Sericomyrmex and Trachy- myrmex as possessing transitional habits, distinct both from species that cultivate fungus by using mostly nonplant items (insect feces and corpses) as well as from typical leaf-cutters Atta and Acromyrmex . This is the Þrst study to detect correlations of nest traits with worker number and siZe of fungus garden in the less conspicuous attines. Results highlight the importance of combining data on natural history and morphometry to understand the evolutionary history of fungus-growing ants. KEY WORDS attine ants, colony siZe, demographic attributes, nest architecture, worker morphom- etry The ant tribe Attini (Myrmicinae) includes 15 genera myrmex and Sericomyrmex ) that collect mostly fallen and Ͼ230 species occurring in the tropical and sub- leaßets, fruit, and ßowers, as well as the typical leaf- tropical Americas (Mehdiabadi and SchultZ 2010). cutters that collect fresh leaves from shrubs and trees These ants are known as fungus growers because they (genera Atta and Acromyrmex ) (see SchultZ and maintain an obligate mutualism with fungi cultured Brady 2008, Mehdiabadi and SchultZ 2010). inside their nests, and which is the only food source for Leaf-cutting ants are very well known due to their the larvae and an important resource for the adult ants remarkable effects on vegetation as herbivores. For as well (Weber 1972). A wide variety of material can example, they can 1) remove up to 15% of the standing be used as substrate for fungus culturing (Ho ¨lldobler leaf crop (Wirth et al. 2003, Urbas et al. 2007) and up and Wilson 1990, Rico-Gray and Oliveira 2007), and to 50% of the plant species in their foraging territory this variation can be used to categoriZe the Attini into each year (Vasconcelos and Fowler 1990); 2) reduce two groups based on their agricultural habits. The the vegetation cover by up to 18% and increase light so-called lower attines include species that collect availability within foraging areas (Wirth et al. 2003); mainly ßowers, fruits, insect corpses, and feces fallen and 3) secondarily disperse seeds of forest and sa- in the vicinity of their nests (Leal and Oliveira 2000, vanna plants (Leal and Oliveira 1998, Silva et al. 2007, Mehdiabadi and SchultZ 2010). The higher attines Christianini and Oliveira 2009). Moreover, leaf-cut- include nonleaf-cutting species (genera Trachy- ters are considered important ecosystem engineers because their huge nests can signiÞcantly alter soil 1 Programa de Po ´s-Graduac¸a˜o em Ecologia, Universidade Estadual attributes (Sternberg et al. 2007) and light regimes de Campinas, C.P. 6109, 13083-862 Campinas SP, BraZil. (Farji-Brener and Illes 2000), which in turn may in- 2 Current afÞliation: Departamento de Botaˆnica, Universidade Fed- eral de Pernambuco, 50670-901, Recife, PE, BraZil. ßuence forest structure, composition, and dynamics 3 Laborato ´rio de Biossistema´tica Animal, Universidade Estadual do (Corre ˆa et al. 2010), even after 15 yr of colony death Sudoeste da Bahia (UESB), BR 415, Km 03, s/n Њ, 45700-000 Itapetinga or nest abandonment (Bieber et al. 2010). BA, BraZil. Although nonleaf-cutters comprise a diverse and 4 Corresponding author: Departamento de Biologia Animal, Uni- versidade Estadual de Campinas, C.P. 6109, 13083-862 Campinas SP, abundant group of fungus-growing ants, only more BraZil (e-mail: [email protected]). recently the general biology of these less conspicuous 0013-8746/11/0901Ð0908$04.00/0 ᭧ 2011 Entomological Society of America 902 A NNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 104, no. 5 attine species have been investigated in greater detail and occasional forest strips along streams known as (Ferna´ndeZ-Marõ´n et al. 2004, Pitts-Singer and Espelie gallery forests (Oliveira-Filho and Ratter 2002). The 2007, Adams and Longino 2007, Diehl-Fleig and Diehl climate in the study region is characteriZed by a coldÐ 2007, Klingenberg and Branda˜o 2009, Solomon et al. dry season occurring from April to September and a 2011). Lack of Þeld data are probably due to their small warmÐrainy season from October to March. The max- colonies and the small siZe and discrete habit of for- imum monthly rainfall is 235 mm in December and the agers, which make them less noticeable in nature mean temperature reaches a minimum of 8.7 ЊC in July (Weber 1972, Ho ¨lldobler and Wilson 2011). Perhaps and a maximum of 30.4 ЊC in February (De Vuono et most importantly, because nonleaf-cutters use mostly al. 1986). The reserve presents ßoodplain soils and fallen plant material and feces as substrate for fungus- yellow-red latosols with medium texture to clay, and culturing, their impact on vegetation and economic altitude varies from 585 to 635 m (Mantovani 1983). importance as crop pests is irrelevant compared with Five trails (totaling 7 km) were selected in the leaf-cutting Atta and Acromyrmex (Vander Meer et al. cerrado sensu stricto (i.e., dense scrub of shrubs and 1990, Wirth et al. 2003, and references therein). trees) as well as in the transition between cerrado and Several biological traits such as colony siZe, nest gallery forest (Oliveira-Filho and Ratter 2002). Baits structure, worker siZe, and polymorphism may inßu- made of fruits (orange) and dry oats were used to ence the foraging ecology of nonleaf-cutting attines attract attine ants and locate their nests. External and and their relationship with co-occurring plant and internal nest traits and demographic data were re- animal species (Ho ¨lldobler and Wilson 1990; Leal and corded for 25 ant colonies during March and April Oliveira 1998, 2000). In addition, studying these traits 1995 (end of warmÐrainy season). We excavated at may clarify understand the appearance of some rele- least three colonies of the most abundant species in vant evolutionary steps within the Attini, such as the each genus as follows: Cyphomyrmex gr. rimosus sp. 2, gradual increase in colony siZe, nest siZe and com- Mycetarotes parallelus (Emery), Sericomyrmex sp., plexity, worker siZe and polymorphism, and the use of Trachymyrmex sp. 4 (three colonies each), Myrmico- fresh material, especially leaves (Ho ¨lldobler and Wil- crypta sp. (Þve colonies), and Mycocepurus goeldi son 1990, 2011). Indeed, Leal and Oliveira (2000) Forel (eight colonies). Except for Mycetarotes colo- documented that the substrate used for fungus-cul- nies, which were collected in gallery forest, all other turing by nonleaf-cutting attines varies from mainly ants were collected in cerrado sensu stricto. The ma- insect feces and corpses in genera such as Cypho- terial collected as fungal substrate by these colonies myrmex, Mycetarotes, and Mycocepurus, to mostly has previously been described by Leal and Oliveira fallen soft leaßets in Sericomyrmex and Trachymyrmex (2000), and included leaves, ßowers, fruit, seeds, (also see SchultZ and Brady 2008, Mehdiabadi and wood, mosses, lichens, insect feces, and corpses (also SchultZ 2010). Although the types of fungal substrate see Ferna´ndeZ-Marõ´n et al. 2004; SchultZ and Brady used by different genera suggest a trend in agricultural 2008; Mehdiabadi and SchultZ 2010; Ho ¨lldobler and habits, other biological features of the Attini remain Wilson 1990, 2011, and references therein). Species poorly documented. names and morphospecies designations used here fol- In the current study, we compare several biological low Leal and Oliveira (2000); hereafter, they will be traits of six genera of nonleaf-cutting Attini ( Cypho- referred to by their generic names only. Ant voucher myrmex, Mycetarotes, Mycocepurus, Myrmicocrypta, specimens are deposited in the Museu de Zoologia da Sericomyrmex, and Trachymyrmex ) in the cerrado sa- Universidade de Sa˜o Paulo (MZUSP). vanna of BraZil. We used the most abundant species in Nest siZe was evaluated based on the volume of the each genus to assess nest siZe (volume of nest mound) mound (i.e., width, length and height of soil deposition and structure (chamber depth and volume), siZe of around the main nest entrance), number of chambers, fungus garden, and colony siZe and demography as well as the depth and volume of each chamber. Each (number of immatures, workers, queens, and alates). nest excavation began by digging a circle around the In addition, we investigated whether the external main nest entrance, so as to form a cylinder (1 m in structure of the nests is a good predictor of worker diameter; 50 cm in depth) that included the whole number and volume of the fungus garden.
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