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Nest architecture development of grass-cutting ants

ABSTRACT

Atta bisphaerica is a species of grass-cutting ants commonly found in the Cerrado biome. The Brazilian Cerrado (savanna) biome covers 2 million km representing 23% of the area of the country. It is an ancient biome with rich biodiversity, estimated at 160,000 species of plants, fungi and animals. However, little is known about their nest architecture development. This study investigated the architecture of fourteen A. bisphaerica nests from Botucatu, São Paulo, Brazil. Molds were made of the nests by filling them with cement to allow better visualization of internal structures such as chambers and tunnels. After excavation, the depth and dimensions (length, width, and height) of the chambers were measured. As expected, there was a lateral development in the nests and increase in the number of chambers over time. Results showed that in nests with an estimated age of 14 months, the average depth was 1.6 ± 0.4 m; for those with 18 months it was 2.2 ± 0.7 m and at 28 months it was 2.5 ± 0.7 m. The number of chambers varied from 4 to 7 in 28-month nests, 2 to 4 in 18-month nests, and from 2 to 3 in 14-month nests. With respect to the dimensions of the internal tunnels, there were variations in their average width, increasing with time. The fungus chambers were located beneath the largest mound of loose soil. This study contributes to a better understanding of the so far unknown nest architecture development of A. bisphaerica grass-cutting ants.

Keywords:
Grass-cutting ants; Nest; Social insects

Introduction

The nests of leaf-cutting ants consist of an externally visible part, a mound of loose soil, which is characterized by having a large number of holes that lead to the internal part, with the latter being made up of tunnels of various diameters and shapes, which allow the traffic of the ants and interconnect holes with chambers. The tunnels that reach the surface of the loose soil of the nest open through holes that are the exits of the landfill tunnels, along which the ants transport the soil removed from their excavations. The foraging tunnels, along which workers cut leaves, open to the outside of the nest in holes (Gonçalves, 1964Gonçalves, C.R., 1964. As formigas cortadeiras. Boletim Campo 20, 7-23.) usually located outside the limits of the loose soil area at variable distances from the latter.

The mound of loose soil of Atta nests is one of the most relevant aspects, since it is a characteristic initially observed in the field for identification of species, as small or large variations may occur depending on the species. According to Mariconi (1970)Mariconi, F.A.M., 1970. As saúvas. Ceres, São Paulo, pp. 167., in a general way, Atta sexdens, Atta laevigata, Atta bisphaerica and Atta cephalotes nests present a soil mound only. On the other hand, Atta capiguara also shows a certain number of secondary areas.

Although most species present a single mound, there are variations in the form of soil deposition by the ants and in the choice of the site to build these nests. The A. sexdens and A. cephalotes species build their nests preferably in shady places, and land deposition occurs irregularly, through the formation of small mounds of soil, with the shape of small volcanoes located around the holes above the mound of loose soil. In A. laevigata, deposition occurs in a regular way, being concentrated and convex, and nests are constructed in both sunny and shady places (Pereira-da-Silva, 1975Pereira-Da-Silva, V., 1975. Contribuição ao estudo das populações de Atta sexdens rubropilosa Forel e Atta laevigata Fr. Smith no Estado de são Paulo (Hym: Formicidae). Stud. Entomol. 18, 201-250.; Moreira et al., 2004aMoreira, A.A., Forti, L.C., Andrade, A.P.P., Boaretto, M.A.C., Lopes, J.F.S., 2004. Nest Architecture of Atta laevigata (F. Smith, 1858) (Hymenoptera: Formicidae). Stud. Neotrop. Fauna Environ. 39, 109-116.).

Normally, the loose soils are on the cluster of chambers. According to Eidmann (1932)Eidmann, H., 1932. Beitrage zur kenntnis der biologie, insbesondere des nestbaves der Blattschneiderameise Atta sexdens L.. Z. Morphol. Oekol. Ziere 25, 154-183., Autuori (1942)Autuori, M., 1942. Contribuição para o conhecimento da saúva (Atta spp.) (Hymenoptera:Formicidae): III – Escavação de um sauveiro (Atta sexdens rubropilosa Forel, 1908). Arq. Inst. Biol. 13, 136-148., Jacoby (1950)Jacoby, M., 1950. A arquitetura do ninho. In: Jacoby, M. (Ed.), A. saúva: uma inteligência nociva. , 2nd ed. Serviço de Informação Agrícola 3, Rio de Janeiro, pp. 21–31., Mariconi and Paiva Castro (1960)Mariconi, F.A.M., Paiva Castro, U., 1960. Notas sobre a saúva e o sauveiro. Biológico 26, 97-108., Paiva Castro et al. (1961)Paiva Castro, U., Zamith, A.P.L., Mariconi, F.A.M., 1961. Contribuição para o conhecimento da “saúva de vidro” Atta laevigata Fred. Smith, 1958. An. An. Esc. Super. Agric. 18, 313-325, “Luiz de Queiroz”., Amante (1967)Amante, E., 1967. Saúva tira boi da pastagem. Coopercotia 23 (207), 38-40., Gonçalves (1967)Gonçalves, C.R., 1967. As formigas cortadeiras. Boletim Campo 22, 3-13., Pereira-da-Silva (1975)Pereira-Da-Silva, V., 1975. Contribuição ao estudo das populações de Atta sexdens rubropilosa Forel e Atta laevigata Fr. Smith no Estado de são Paulo (Hym: Formicidae). Stud. Entomol. 18, 201-250., Jonkman (1980aJonkman, J.C.M., 1980. The external and internal structure and growth of nests of the leaf-cutting ant Atta vollenweideri Forel, 1893 (Hym: Formicidae): Part I. Sonderdr. Aus. Bd. 89, 158-173.,b)Jonkman, J.C.M., 1980. The external and internal structure and growth of nests of the leaf cutting ant Atta vollenweideri Forel, 1893 (Hym: Formicidae): Part II. Sonderdr. Aus. Bd. 89, 217-246., Pretto (1996)Pretto, D.R., Dissertação (Mestrado em Agronomia/Proteção de Plantas) 1996. Arquitetura dos túneis de forrageamento e do ninho de Atta sexdens rubropilosa Forel, 1908(Hymenoptera – Formicidae), dispersão de substrato e dinâmica do inseticida na colônia. Faculdade de Ciências Agronômicas, Universidade Estadual Paulista, Botucatu, 110 pp. and Moreira et al. (2004aMoreira, A.A., Forti, L.C., Andrade, A.P.P., Boaretto, M.A.C., Lopes, J.F.S., 2004. Nest Architecture of Atta laevigata (F. Smith, 1858) (Hymenoptera: Formicidae). Stud. Neotrop. Fauna Environ. 39, 109-116.,b)Moreira, A.A., Forti, L.C., Boaretto, M.A.C., Andrade, A.P.P., Lopes, J.F.S., Ramos, V.M., 2004. External and internal structure of Atta bisphaerica Forel (Hymenoptera: Formicidae). J. Appl. Entomol. 128, 204-211., A. bisphaerica, A. sexdens, A. laevigata and Atta vollenweideri ants build their chambers in the underground, in the projection of loose soil. Therefore, the loose soil is the ant colony's core, while, according to Amante (1967)Amante, E., 1967. Saúva tira boi da pastagem. Coopercotia 23 (207), 38-40. and Forti (1985)Forti, L.C., 1985. Ecologia da saúva Atta capiguara Gonçalves, 1944 (Hymenoptera, Formicidae) em pastagem. Tese (Doutorado em Ciências) – Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de são Paulo, Piracicaba, 234 pp., the A. capiguara species constructs its nest in a different way – the apparent core does not coincide with the real one, and huge garbage chambers can be found under the apparent core.

Chambers vary in shape, location and dimensions, depending on the species and in some cases of the role. Studies on A. vollenweideri carried out by Bonetto (1959)Bonetto, A., 1959. Las Hormigas “Cortadoras” De La Provincia De Santa Fé (Generos: Atta Y Acromyrmex). Dir. Gen. de Rec. Nat. 2, 17-26., Carvalho (1976)Carvalho, S., 1976. Atta (Neoatta) vollenweideri Forel, 1893, no Brasil: ocorrência, aspectos externos e internos do sauveiro. Tese (Livre Docência) – Centro de Ciências Rurais, Universidade Federal de Santa Maria, Santa Maria, 39 pp. and Jonkman (1980b)Jonkman, J.C.M., 1980. The external and internal structure and growth of nests of the leaf cutting ant Atta vollenweideri Forel, 1893 (Hym: Formicidae): Part II. Sonderdr. Aus. Bd. 89, 217-246. indicated that living chambers had an oval shape with a flat bottom and that garbage chambers had a conical shape. For A. sexdens, Jacoby (1950)Jacoby, M., 1950. A arquitetura do ninho. In: Jacoby, M. (Ed.), A. saúva: uma inteligência nociva. , 2nd ed. Serviço de Informação Agrícola 3, Rio de Janeiro, pp. 21–31. concluded that the chamber structure is simple, varying from a spherical enclosure or an ellipsoid one with closed dome, while Gonçalves (1964)Gonçalves, C.R., 1964. As formigas cortadeiras. Boletim Campo 20, 7-23. found spherical chambers with a flat bottom.

The chambers of A. sexdens nests studied by Gonçalves (1964)Gonçalves, C.R., 1964. As formigas cortadeiras. Boletim Campo 20, 7-23. presented diameter between 20 and 40 cm, while Pretto (1996)Pretto, D.R., Dissertação (Mestrado em Agronomia/Proteção de Plantas) 1996. Arquitetura dos túneis de forrageamento e do ninho de Atta sexdens rubropilosa Forel, 1908(Hymenoptera – Formicidae), dispersão de substrato e dinâmica do inseticida na colônia. Faculdade de Ciências Agronômicas, Universidade Estadual Paulista, Botucatu, 110 pp. found chambers with an average height of 18.31 cm, width of 24.25 cm and length of 24.24 cm. For A. capiguara, Mariconi et al. (1961)Mariconi, F.A.M., Zamith, A.R.L., Paiva Castro, U., 1961. Contribuição para o conhecimento da “saúva parda” Atta capiguara Gonçalves, 1944. An. Esc. Super. Agric. 18, 301-312, “Luiz de Queiroz”, Univ. São Paulo. found small or medium chambers measuring approximately 21 cm in height by 27 cm, 15 cm and 17 cm in width, and 17 cm and 16 cm in length.

The chambers of A. laevigata, in Paiva Castro et al. (1961)Paiva Castro, U., Zamith, A.P.L., Mariconi, F.A.M., 1961. Contribuição para o conhecimento da “saúva de vidro” Atta laevigata Fred. Smith, 1958. An. An. Esc. Super. Agric. 18, 313-325, “Luiz de Queiroz”., were mostly located between 0.50 and 1.80 m deep, while Pereira-da-Silva (1975)Pereira-Da-Silva, V., 1975. Contribuição ao estudo das populações de Atta sexdens rubropilosa Forel e Atta laevigata Fr. Smith no Estado de são Paulo (Hym: Formicidae). Stud. Entomol. 18, 201-250. found them on the surface (including in the loose soil area) up to 6 m deep, and Moreira et al. (2004a)Moreira, A.A., Forti, L.C., Andrade, A.P.P., Boaretto, M.A.C., Lopes, J.F.S., 2004. Nest Architecture of Atta laevigata (F. Smith, 1858) (Hymenoptera: Formicidae). Stud. Neotrop. Fauna Environ. 39, 109-116. up to 7 m deep. Thus, depending probably on loose soil area, soil type, species studied and the colony's microclimatic needs, depth may vary.

As for depth of location of the chambers, Bonetto (1959)Bonetto, A., 1959. Las Hormigas “Cortadoras” De La Provincia De Santa Fé (Generos: Atta Y Acromyrmex). Dir. Gen. de Rec. Nat. 2, 17-26. found chambers from 0.70 to 3.0 m, concentrated in the center of the nest of A. vollenweideri. In studies on A. capiguara, Mariconi et al. (1961)Mariconi, F.A.M., Zamith, A.R.L., Paiva Castro, U., 1961. Contribuição para o conhecimento da “saúva parda” Atta capiguara Gonçalves, 1944. An. Esc. Super. Agric. 18, 301-312, “Luiz de Queiroz”, Univ. São Paulo. observed that the chambers were concentrated between 1.0 and 1.60 m deep. In A. sexdens, Gonçalves (1964)Gonçalves, C.R., 1964. As formigas cortadeiras. Boletim Campo 20, 7-23. found a larger number of them in the center of the anthill and between 1 and 2 m deep, while Pretto (1996)Pretto, D.R., Dissertação (Mestrado em Agronomia/Proteção de Plantas) 1996. Arquitetura dos túneis de forrageamento e do ninho de Atta sexdens rubropilosa Forel, 1908(Hymenoptera – Formicidae), dispersão de substrato e dinâmica do inseticida na colônia. Faculdade de Ciências Agronômicas, Universidade Estadual Paulista, Botucatu, 110 pp. found only 22% up to 1 m, with the others being below this.

In studies on nest architecture of A. cephalotes, Stahel and Geijskes (1939)Stahel, G., Geijskes, D.C., 1939. Über den Bau der Nester von Atta cephalotes L. und Atta sexdens L. (Hym: Formicidae). Rev. Entomol. 10, 27-78. found a total of 373 chambers, of which 344 contained fungus. For A. sexdens, a total of 1027 chambers were found by Autuori (1942)Autuori, M., 1942. Contribuição para o conhecimento da saúva (Atta spp.) (Hymenoptera:Formicidae): III – Escavação de um sauveiro (Atta sexdens rubropilosa Forel, 1908). Arq. Inst. Biol. 13, 136-148., which generated a density of 8.52 chambers m−3, while Pretto (1996)Pretto, D.R., Dissertação (Mestrado em Agronomia/Proteção de Plantas) 1996. Arquitetura dos túneis de forrageamento e do ninho de Atta sexdens rubropilosa Forel, 1908(Hymenoptera – Formicidae), dispersão de substrato e dinâmica do inseticida na colônia. Faculdade de Ciências Agronômicas, Universidade Estadual Paulista, Botucatu, 110 pp. obtained densities of 1.75; 2.43, 2.66 and 4.17 chambers m−3 for the four nests studied.

The mentioned studies were carried out in adult nests, but little is known about the growth of the colony and, consequently, of the nest. The present study described nest architecture development in three periods: estimated ages of 14, 18 and 28 months of A. bisphaerica grass-cutting ants.

Material and methods

Studied area

The study was conducted at Santana Farm (20º50'46" S; 48º26'2" W), located near UNESP's Lageado Experimental Farm, Botucatu, São Paulo, Brazil, in a Cerrado fragment.

Age of nests

Two thousand founder queens were observed immediately after the nuptial flight on 4 October 2008 at the Lageado Experimental Farm, FCA/UNESP, Botucatu, Brazil, after, they started to dig their nests, we marked individually all nests with wood white stake. After that, fourteen nests were excavated for architecture study.

Studied nests

Fourteen nests were used in this study – with approximately 14 months (4 nests), eighteen months (5 nests) and twenty-eight months (5 nests) after nest foundation.

The size of the nests was confirmed by mapping two or three active entrance holes near the nests. The holes were mapped using plastic straw baits of different colors and cut types (totaling 48 types of baits).

The straws were cut into 3–4 mm pieces and immersed in a solution of concentrated orange juice containing sugar (forming a syrup). The straw fragments were removed with sieves and transferred to trays where a mixture of citrus pulp and sugarcane leaf powder was added. The pieces were carefully moved inside these trays so the mixture impregnated well on the straws and was highly attractive to the ants. The straws were dried for 24 h at room temperature. After this period, the baits were stored in plastic bags identified with numbers by color and type of straw to facilitate handling in the field.

In the field, the plastic straw baits were placed in the active holes near the nests. The number corresponding to each type of bait was marked on the stake. After 24 h, the mound of loose soil to which each straw was returned by the ants was identified and the type and color found, which indicate which entrance holes belong to each nest, were recorded.

Internal architecture

The nests were molded using a mixture of 5 kg of cement in 10 L of water, which was poured into all open holes above the soil mound of the nest and into the holes spread on the soil surface (foraging holes) as described by Moreira et al. (2004aMoreira, A.A., Forti, L.C., Andrade, A.P.P., Boaretto, M.A.C., Lopes, J.F.S., 2004. Nest Architecture of Atta laevigata (F. Smith, 1858) (Hymenoptera: Formicidae). Stud. Neotrop. Fauna Environ. 39, 109-116.,b)Moreira, A.A., Forti, L.C., Boaretto, M.A.C., Andrade, A.P.P., Lopes, J.F.S., Ramos, V.M., 2004. External and internal structure of Atta bisphaerica Forel (Hymenoptera: Formicidae). J. Appl. Entomol. 128, 204-211.. The water-cement mixture was poured into the holes using aluminum funnels. Excavation started 7 days after application of the cement.

Prior to excavation, the external area of the nest was determined by the traditional method, which consists of measuring the greatest width and greatest length of the area comprising all mounds of loose soil. Two nylon strings were then stretched over the nest area, forming two orthogonal axes (x; y), whose center corresponded to the center of the nest area. These axes were used to identify the chambers and tunnels.

The areas of the nests filled with cement were excavated using small manual tools to avoid their destruction. A 0.70-m wide and 1-m deep ditch was opened around the nest area and excavation was performed from the outside to the inside. The ditch was deepened until complete appearance of the chambers, which were numbered for subsequent measurement. After excavation, the chambers and tunnels were measured and photographed. The following parameters were obtained: dimension (width, height, and length), depth from the soil surface, and position on the orthogonal axes (x, y). The mean, standard deviation and range of the measurements were calculated for statistical analysis. The variables studied were compared between nests at the 3 different ages, by means of ANOVA, at 5% of significance.

Results and discussion

As expected, there was a lateral development in the nests and increase in the number of chambers over time (ANOVA, F2;13 = 16.96, p < 0.001), that is, the colony growing as a function of time. However, A. bisphaerica nests of different ages did not present major changes in depth (ANOVA, F2;13 = 1.35, p = 0.2973).

Morphologically, the chambers of A. bisphaerica nests studied were located in the projection of the loose soil mound, as already reported by Amante (1967)Amante, E., 1967. Saúva tira boi da pastagem. Coopercotia 23 (207), 38-40. and Moreira et al. (2004b)Moreira, A.A., Forti, L.C., Boaretto, M.A.C., Andrade, A.P.P., Lopes, J.F.S., Ramos, V.M., 2004. External and internal structure of Atta bisphaerica Forel (Hymenoptera: Formicidae). J. Appl. Entomol. 128, 204-211.. Other Atta species also construct their chambers in the projection of loose soil mound, including: A. sexdens (Eidmann, 1932Eidmann, H., 1932. Beitrage zur kenntnis der biologie, insbesondere des nestbaves der Blattschneiderameise Atta sexdens L.. Z. Morphol. Oekol. Ziere 25, 154-183.; Autuori, 1942Autuori, M., 1942. Contribuição para o conhecimento da saúva (Atta spp.) (Hymenoptera:Formicidae): III – Escavação de um sauveiro (Atta sexdens rubropilosa Forel, 1908). Arq. Inst. Biol. 13, 136-148.; Jacoby, 1950Jacoby, M., 1950. A arquitetura do ninho. In: Jacoby, M. (Ed.), A. saúva: uma inteligência nociva. , 2nd ed. Serviço de Informação Agrícola 3, Rio de Janeiro, pp. 21–31.; Amante, 1967Amante, E., 1967. Saúva tira boi da pastagem. Coopercotia 23 (207), 38-40.; Gonçalves, 1967Gonçalves, C.R., 1967. As formigas cortadeiras. Boletim Campo 22, 3-13.; Pretto, 1996Pretto, D.R., Dissertação (Mestrado em Agronomia/Proteção de Plantas) 1996. Arquitetura dos túneis de forrageamento e do ninho de Atta sexdens rubropilosa Forel, 1908(Hymenoptera – Formicidae), dispersão de substrato e dinâmica do inseticida na colônia. Faculdade de Ciências Agronômicas, Universidade Estadual Paulista, Botucatu, 110 pp.), A. vollenweideri (Jonkman, 1980bJonkman, J.C.M., 1980. The external and internal structure and growth of nests of the leaf cutting ant Atta vollenweideri Forel, 1893 (Hym: Formicidae): Part II. Sonderdr. Aus. Bd. 89, 217-246.) and A. laevigata (Mariconi and Paiva Castro, 1960Mariconi, F.A.M., Paiva Castro, U., 1960. Notas sobre a saúva e o sauveiro. Biológico 26, 97-108.; Paiva Castro et al., 1961Paiva Castro, U., Zamith, A.P.L., Mariconi, F.A.M., 1961. Contribuição para o conhecimento da “saúva de vidro” Atta laevigata Fred. Smith, 1958. An. An. Esc. Super. Agric. 18, 313-325, “Luiz de Queiroz”.; Pereira-da-Silva, 1975Pereira-Da-Silva, V., 1975. Contribuição ao estudo das populações de Atta sexdens rubropilosa Forel e Atta laevigata Fr. Smith no Estado de são Paulo (Hym: Formicidae). Stud. Entomol. 18, 201-250.; Moreira et al., 2004aMoreira, A.A., Forti, L.C., Andrade, A.P.P., Boaretto, M.A.C., Lopes, J.F.S., 2004. Nest Architecture of Atta laevigata (F. Smith, 1858) (Hymenoptera: Formicidae). Stud. Neotrop. Fauna Environ. 39, 109-116.). However, in colonies of A. capiguara, fungus chambers are located outside the apparent core, distanced and distributed laterally below ground level, and garbage chambers are located below this core (Amante, 1967Amante, E., 1967. Saúva tira boi da pastagem. Coopercotia 23 (207), 38-40.; Forti et al., 2017Forti, L.C., Protti, A.P.P., Camargo, R.S., Caldato, N., Moreira, A., 2017. Discovering the giant nest architecture of grass-cutting ants, Atta capiguara (Hymenoptera, Formicidae). Insects 8, 39.).

The determination of the place of highest concentration of fungus chambers has been a relevant factor in the application of measures for Atta control, because when the limits of loose soil area coincides with the area of highest concentration of chambers in the nest, control is much easier (Moreira et al., 2004aMoreira, A.A., Forti, L.C., Andrade, A.P.P., Boaretto, M.A.C., Lopes, J.F.S., 2004. Nest Architecture of Atta laevigata (F. Smith, 1858) (Hymenoptera: Formicidae). Stud. Neotrop. Fauna Environ. 39, 109-116.).

About the internal structure of the nests, it was observed that among nests of different ages there was no great variation in depth (Fig. 1, Table 1); however, a lateral growth was observed (Fig. 1), as already reported by Moreira et al. (2004b)Moreira, A.A., Forti, L.C., Boaretto, M.A.C., Andrade, A.P.P., Lopes, J.F.S., Ramos, V.M., 2004. External and internal structure of Atta bisphaerica Forel (Hymenoptera: Formicidae). J. Appl. Entomol. 128, 204-211. in mature nests.

Fig. 1
Details of the internal architecture of Atta bisphaerica nests, with approximate age of 14 months (A), 18 months (B) and 28 months (C). Botucatu, SP, 2014.
Table 1
Number of chambers and total depth of the nests and respective data on mean, mode and standard deviation (S*), maximum and minimum number of chambers by estimated age of Atta bisphaerica nests, Botucatu, SP, 2014.

In nests with an estimated age of 14 months, the average depth was 1.6 ± 0.4 m, ranging from 1.2 to 2.1 m, while for those with 18 months, it was 2.2 ± 0.7 m and ranged from 1.4 to 2.9 m. For 18-month nests, the average depth was 2.5 ± 0.7, ranging from 1.3 to 2.9 m (Table 1). As observed in A. bisphaerica, chambers containing fungus garden with freshly incorporated plant fragments are found near the soil surface. This fact suggests an adaptation of the species to withstand variations in temperature and soil humidity, since it usually builds its nests in open areas with plenty of sunlight; even deep soils chambers are not located at great depths. It therefore seems that nest depth is not limited by the ground water table (Moreira et al., 2004bMoreira, A.A., Forti, L.C., Boaretto, M.A.C., Andrade, A.P.P., Lopes, J.F.S., Ramos, V.M., 2004. External and internal structure of Atta bisphaerica Forel (Hymenoptera: Formicidae). J. Appl. Entomol. 128, 204-211.). On the other hand, due to the complexity of the nests, ants choose the best location within the nest in terms of temperature and humidity gradients to rear eggs, larvae and pupae, as well as for the symbiotic fungus and all biota involved (Moreira et al., 2004bMoreira, A.A., Forti, L.C., Boaretto, M.A.C., Andrade, A.P.P., Lopes, J.F.S., Ramos, V.M., 2004. External and internal structure of Atta bisphaerica Forel (Hymenoptera: Formicidae). J. Appl. Entomol. 128, 204-211.).

The nests of A. bisphaerica studied presented chambers of varied forms (Fig. 2), as already observed by Moreira et al. (2004b)Moreira, A.A., Forti, L.C., Boaretto, M.A.C., Andrade, A.P.P., Lopes, J.F.S., Ramos, V.M., 2004. External and internal structure of Atta bisphaerica Forel (Hymenoptera: Formicidae). J. Appl. Entomol. 128, 204-211., Pereira-da-Silva (1975)Pereira-Da-Silva, V., 1975. Contribuição ao estudo das populações de Atta sexdens rubropilosa Forel e Atta laevigata Fr. Smith no Estado de são Paulo (Hym: Formicidae). Stud. Entomol. 18, 201-250., and Moreira et al. (2004a)Moreira, A.A., Forti, L.C., Andrade, A.P.P., Boaretto, M.A.C., Lopes, J.F.S., 2004. Nest Architecture of Atta laevigata (F. Smith, 1858) (Hymenoptera: Formicidae). Stud. Neotrop. Fauna Environ. 39, 109-116. for A. laevigata. It was observed, however, that the spherical shape was predominant for the species studied, as concluded by Moreira et al. (2004b)Moreira, A.A., Forti, L.C., Boaretto, M.A.C., Andrade, A.P.P., Lopes, J.F.S., Ramos, V.M., 2004. External and internal structure of Atta bisphaerica Forel (Hymenoptera: Formicidae). J. Appl. Entomol. 128, 204-211. for the same species, and Moreira et al. (2004a)Moreira, A.A., Forti, L.C., Andrade, A.P.P., Boaretto, M.A.C., Lopes, J.F.S., 2004. Nest Architecture of Atta laevigata (F. Smith, 1858) (Hymenoptera: Formicidae). Stud. Neotrop. Fauna Environ. 39, 109-116. for A. laevigata.

Fig. 2
Detail of the fungal chamber of Atta bisphaerica in different forms (A and B). Botucatu, SP, 2014.

The number of chambers varied from 4 to 7 in 28-month nests, from 2 to 4 in 18-month ones and from 2 to 3 in 14-month nests (Table 1, Fig. 1).

The width, height, and length dimensions of the chambers (Table 2) were variable, showing some differences between nests, already observed by Jonkman (1980b)Jonkman, J.C.M., 1980. The external and internal structure and growth of nests of the leaf cutting ant Atta vollenweideri Forel, 1893 (Hym: Formicidae): Part II. Sonderdr. Aus. Bd. 89, 217-246. when analyzing the average height of A. vollenweideri chambers, attributing this difference to colony age, and by Moreira et al. (2004aMoreira, A.A., Forti, L.C., Andrade, A.P.P., Boaretto, M.A.C., Lopes, J.F.S., 2004. Nest Architecture of Atta laevigata (F. Smith, 1858) (Hymenoptera: Formicidae). Stud. Neotrop. Fauna Environ. 39, 109-116.,b)Moreira, A.A., Forti, L.C., Boaretto, M.A.C., Andrade, A.P.P., Lopes, J.F.S., Ramos, V.M., 2004. External and internal structure of Atta bisphaerica Forel (Hymenoptera: Formicidae). J. Appl. Entomol. 128, 204-211., who observed variations in chamber dimensions between A. laevigata and A. bisphaerica nests. Variations in the dimensions of chambers of the same species may derive from the nest's need to increase fungus cultivation, due to colony growth.

Table 2
Mode, mean, standard deviation (S*), and maximum and minimum values of dimensions (width, height and length) of Atta bisphaerica nest chambers, Botucatu, SP, 2014.

When compared to the dimensions of A. bisphaerica nest chambers studied, variations were found as to average width, height and length. For nests from I to IV, with an approximate age of 14 months, the average width ranged from 7.3 ± 1.5 to 14 ± 1.4 cm; the average height was 8.3 ± 0.6 to 14 ± 1.4 cm, and the average length was 9.3 ± 1.5 to 14.5 ± 2.1 cm. For nests V to IX, with approximate age of 18 months, the average width ranged from 9.0 ± 2.6 to 12.7 ± 2.1 cm, the average height was 9.3 ± 2.1 to 11.5 ± 5.8 cm, and the average length was 11.7 ± 4 to 14.0 ± 1.7 cm. As for nests X to XIV, with an approximate age of 28 months, the average width ranged from 7.5 ± 3.1 to 13.3 ± 4.2 cm, with average height of 9.0 ± 3.9 to 15. 4 ± 4.4 cm and average length of 9.5 ± 4.8 to 15.4 ± 4.8 cm (Table 2). However, there was no significant difference in chamber width (ANOVA, F 2;13 = 0.24, p = 0.7870), height (ANOVA, F 2;13 = 0.93, p = 0.5772) and length (ANOVA, F2;13 = 0.96, p = 0.5881) between the 3 ages studied.

The first chambers of A. bisphaerica were located at small depths (between 13 and 20 cm); possibly, this species does not need very stable conditions of temperature and humidity, since these nests occur in open areas with a lot of insolation and in soils that retain little water. In species that nest in shady areas, such as A. sexdens, temperature ranges from 21 to 29 ºC and humidity is sometimes around 50% (Eidmann, 1932Eidmann, H., 1932. Beitrage zur kenntnis der biologie, insbesondere des nestbaves der Blattschneiderameise Atta sexdens L.. Z. Morphol. Oekol. Ziere 25, 154-183.).

Concerning internal tunnel dimensions, variations were found in average width and height. For nests I to IV, with approximate age of 14 months, the average width ranged from 1.5 ± 0.2 to 1.9 ± 0.6 cm and the average height was 1.4 ± 0.2 to 1.6 ± 0.3 cm. For nests V to IX, with an approximate age of 18 months, the average width varied from 1.6 ± 0.8 to 2.8 ± 1.9 cm and the average height was 1.3 ± 0.2 to 2.6 ± 0.9 cm. As for nests X to XIV, with an approximate age of 28 months, the average width ranged from 3.4 ± 1.7 to 2 ± 0.6 cm and the average height was 1.8 ± 0.3 to 2.6 ± 1.6 cm (Table 3). Significant difference was found as to the width (ANOVA, F2;13 = 13.40, p < 0.05) of the tunnels between the different ages studied. The same was not observed for the height of the tunnels (ANOVA, F2;13 = 0.2143, p = 0.8117). Probably, this difference found in the width of the tunnels occurred with the growth of the colony and, consequently, of the flow of workers inside the nest.

Table 3
Mode, mean, standard deviation (S*), and maximum and minimum values of the dimensions (width and height) of the internal tunnels of Atta bisphaerica nests. Botucatu, SP, 2014.

The measures found by Paiva Castro et al. (1961)Paiva Castro, U., Zamith, A.P.L., Mariconi, F.A.M., 1961. Contribuição para o conhecimento da “saúva de vidro” Atta laevigata Fred. Smith, 1958. An. An. Esc. Super. Agric. 18, 313-325, “Luiz de Queiroz”. for internal tunnels in A. laevigata were 3.5 cm wide and 2.8 cm high. Perhaps, the difference in the width of the tunnels between the different species is due to the greater or lesser flow of workers inside them, which are widened with the growth of the nest. In studies on Atta nests by the process of cement molding, Jacoby (1938Jacoby, M., 1938. Resumos dos estudos de formigueiros por meio da moldagem com cimento. Bol. Min. Agric. 27, 21-31., 1950)Jacoby, M., 1950. A arquitetura do ninho. In: Jacoby, M. (Ed.), A. saúva: uma inteligência nociva. , 2nd ed. Serviço de Informação Agrícola 3, Rio de Janeiro, pp. 21–31. detected the existence of several types of tunnels with different purposes. In addition to narrow tunnels that served as communication between larger tunnels, circular tunnels, more or less perpendicular, with 3–4 cm in diameter, were found, as well as elliptical tunnels, usually horizontal, with a diameter of 10–12 cm.

There are some reports on tunnels inside A. sexdens nests in Stahel and Geijskes (1939)Stahel, G., Geijskes, D.C., 1939. Über den Bau der Nester von Atta cephalotes L. und Atta sexdens L. (Hym: Formicidae). Rev. Entomol. 10, 27-78., which found the presence of tunnels descending toward the water table, having a role in the supply of water to the colony. The study also observed the movement of small puffs of smoke injected into holes above the nest, showing the existence of a primitive ventilation system in intact nests. Access to the chambers, as per observations by Bonetto (1959)Bonetto, A., 1959. Las Hormigas “Cortadoras” De La Provincia De Santa Fé (Generos: Atta Y Acromyrmex). Dir. Gen. de Rec. Nat. 2, 17-26., for A. vollenweideri, is possible through tubular galleries of diameter varying between 5 and 8 cm.

Supply tunnels of A. laevigata studied by Moreira et al. (2004a)Moreira, A.A., Forti, L.C., Andrade, A.P.P., Boaretto, M.A.C., Lopes, J.F.S., 2004. Nest Architecture of Atta laevigata (F. Smith, 1858) (Hymenoptera: Formicidae). Stud. Neotrop. Fauna Environ. 39, 109-116., molded with cement in some portions, also had an elliptical section, with average width of 14.12 cm and average height of 2 cm. Maximum and minimum widths and heights were 24 and 3 cm and 9.5 and 1 cm, respectively, with the supply holes interconnected. They reached a single tunnel that went to the area with the highest concentration of chambers, with average depth of 55 cm from ground level, maximum of 73 cm and minimum of 27 cm. It was observed that, as the tunnel approached the royal core of the nest, the depth increased, and the nest sometimes reached a depth greater than 1.20 m, a fact observed by Pretto (1996)Pretto, D.R., Dissertação (Mestrado em Agronomia/Proteção de Plantas) 1996. Arquitetura dos túneis de forrageamento e do ninho de Atta sexdens rubropilosa Forel, 1908(Hymenoptera – Formicidae), dispersão de substrato e dinâmica do inseticida na colônia. Faculdade de Ciências Agronômicas, Universidade Estadual Paulista, Botucatu, 110 pp. for tunnels of A. sexdens.

Main remarks

The nests of A. bisphaerica of different ages did not show great changes in depth, probably due to a stability in the temperature and humidity of the soil, propitious for the good development of the colony.

A lateral development in the nests and an increase in the number of chambers over time were found, probably due to the growth of the colony (population and fungus garden) as a whole.

The width of the tunnels increased over time, probably due to the higher flow of workers.

Acknowledgements

LCF was the recipient of a fellowship granted by the National Council for Scientific and Technological Development [Conselho Nacional de Desenvolvimento Científico e Tecnológico] (Grant 301718/2013-0).

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Publication Dates

  • Publication in this collection
    Jan-Mar 2018

History

  • Received
    27 June 2017
  • Accepted
    18 Oct 2017
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