Rev. Écol. (Terre Vie), vol. 69, 2014.

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Note brève

spatial distribution of nests of PaRaTRigona subnuda Moure, 1947 (apidae, Meliponini)

denise M. d. s. Mouga1

RésuMé.— distribution spatiale des nids de paratrigona subnuda Moure, 1947 (apidae, Meloponini).— Le modèle de nidification d’une espèce est une de ses caractéristiques fondamentales. Afin d’appuyer les connaissances sur la construction des nids souterrains que l’espèce d’abeille sans aiguillon Paratrigona subnuda occupe, un échantillonage de colonies vivant en milieu naturel a été entrepris et leur rassemblement a été calculé. La dispersion vérifiée montre un dessin de petits groupes qui se répètent à certaines distances et l’indice de dispersion au voisin le plus proche indique une agrégation, dans un modèle semblable à celui en chambres des nids des fourmis du genre atta. La proximité des nids implique un chevauchement des zones d’activité d’individus provenant de colonies voisines.

The building of meliponine nests follows a standard pattern: it involves the monopoli-zation of some convenient space, followed by its modification (with substances secreted and collected) for insulation and the preparation of internal areas for activities (brood, food storage, waste disposal, defense, etc.) (Nogueira-Neto, 1997). Stingless bee nests can be aerial (built or installed on hard substrates) or in the ground, in a pre-existing cavity such as a tree or stem, an ant, bird or termite nest or in a hole in the ground (Michener, 1974).

Paratrigona subnuda Moure, 1947 (Meliponini) is relatively abundant in Brazil (Bahia, Minas Gerais, Rio de Janeiro, Sao Paulo, Paraná, Santa Catarina, Rio Grande do Sul). The colonies forage on many plants, with a large pollen spectrum (Mouga, 1984). The species is endemic to the Atlantic forest (Por, 1992; Pedro & Camargo, 1999).

Combined evidence on P. subnuda colonies suggest that this species occupies abandoned nests of ants. However, there are no reports confirming this hypothesis. This study is aimed to ascertain what the pattern of nest distribution of P. subnuda is and also to verify if this reflects ant colony distribution.

1 Departamento de Ciências Biológicas, Universidade da Região de Joinville - UNIVILLE, Rua Paulo Malschitzki 10, Campus Universitário, Joinville-SC, Brazil, CEP 89219-71, e-mail: dmouga@terra.com.br.

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METHODOLOGY

sTUDY AREA

The study was performed at the Plant Vivarium of the University of São Paulo (USP), in São Paulo, Brazil (46º 43’ 38’’ W and 23º 33’ 44’’ S). The study area covers 143 900 m2. Altitude ranges between 735 and 775 m. Soil is mostly clay, acidic, poor in nutrients and with high levels of aluminum (Gomes, 1992). The climate is temperate warm and humid (Aragaki & Mantovani, 1998). The average annual rainfall is 1207 mm, temperature 19.2°C (14°C in the winter and 23°C in the summer) and relative humidity 80 % (Walter, 1986). Primary vegetation on the campus of USP includes representatives of the dense rain forest on the Serra do Mar and of the semideciduous forest (sensu Veloso et al., 1991) in São Paulo State (Pirani & Cortopassi-Laurino, 1994). Currently, this area has dense vegetation, although not pristine, because a large portion is covered by secondary forest, in various stages of regeneration (Dislich et al., 2001).

METHOD

The nests were discovered by walking in the entire area of the Vivarium and looking for the bee traffic, representing the presence of the nests. The underground nests of P. subnuda exhibit a cerumen entrance of approximately 6 mm in diameter and 1.5-2 cm in length, protruding from the ground (Fig. 1). Since the bees are tiny and the entrances inconspicuous, perhaps not all nests were found. When found, the nests were recorded/ plotted, establishing the nest density of P. subnuda in the study area. Afterwards, in order to determine nest aggregation patterns, distances between the nests were measured (Clark & Evans, 1954). To assess aggregation indices, we employed Clark & Evans’ test (1954), which provides an R index, ranging from 0 (zero) (maximum aggregation) to 1 (one) (random distribution) and a maximum value of 2.1491 (perfect uniformity). Because distances are measured from point to point, most of them are distances within the cluster (including reflexive or reciprocal ones). The denser are the clusters, the shorter are distances and the smaller is the measure of the index. This study was carried out from January to July 1981 and all nests of P. subnuda Moure, 1947, present in the study area, were searched for and when found, their locations were marked on a map.

Figure 1.— Nest entrance of Paratrigona subnuda Moure, 1947 (Illustration by Helena Ignowski).

results

A total of 34 nest entrances were found and indicated on the map (Fig. 2). The density was 2.36 nests/ha. For each nest, the distance to its nearest neighbour was measured (Tab. I). Applying Clark & Evans’ (1954) test, the dispersion index R was found to be 0.65, indicating aggregation rather than a random distribution (p < 0.001). This distribution pattern is also illustrated in Fig. 3.

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Figure 2.— Nests distribution of Paratrigona subnuda in the USP Plants Vivarium (scale 1:2000).

Figure 3.— Number of nests of Paratrigona subnuda (in ordinate), found per range of distance in meters (in abscissa).

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table idistances, in meters, between paratrigona subnuda nests

nest number nearest nest Distance between these nests1 2 79.02 3 4.123 4 1.954 3 1.955 3 53.46 5 58.67 8 43.98 32 4.89 29 39.410 11 3.7511 10 3.7512 11 12.413 14 1.814 13 1.816 18´ 2517 16 3318 18´ 42.518´ 13 2219 19´ 0.8219´ 19 0.8220 19´ 29.121 21´ 221´ 21 222 24 1723 24 1.924 23 1.925 21 7.726 20 3327 28 13.328 27 13.329 9 39.430 29 68.431 6 53.832 8 4.8

disCussion

The entrance tunnel, from turrid to the actual nest, leans at a certain depth, being oblique, with 1-2 m length and the nests are at 0.25-1 m depth (Imperatriz-Fonseca et al., 1972). Wor-kers of P. subnuda do not dig the ground to build the nest (although they have the ability to remove earth that could block the entrance) nor use clay for its preparation as this, when added, is always covered with wax. However, during our excavations, loose soil, red and granular, i.e., similar to the one crafted by ants, was found below the nest and partly around it. In one occasion, there were even ants on the grainy ground. Besides the possibility of P. subnuda sharing space with active ant species, the nests deployment design clearly refer to the building system in chambers from ant nests of the genus atta (leaf-cutting ants) which were abundant in the study area. Similarly, cultivation practices may affect the density of atta rugosus colo-nies. In the abandoned nests of this leaf-cutter ant, nests of Tetragonisca angulata were found

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(Fowler, 1979). Imperatriz-Fonseca et al. (1972) noted that the cavities where the colonies of P. subnuda were located seemed to be connected with other cavities, through passages that already Schwarz (1948) had noticed, naming the dark space below the bee nest as a link between the chambers of the leaf-cutting ant colony. Although Kerr (1951) has assigned the natural clusters of colonies as achievement easiness for construction and food, P. subnuda nest grouping is, in view of the aggregation index, a reflection of the ants’ chambers construction pattern (Fig. 4).

There are at least 28 species of leaf-cutter ants in Brazil. They share a common pattern of chambers and channels in their nests (Diehl-Fleig, 1995). A nest of atta, when mature, can occupy an area of more than 600 m2, be deep (up to 8 m), but young nests occupy of course a smaller area (Della Lucia et al., 1993). Only few incipient nests will ever become mature. Nests are composed of intercommunicating chambers with connecting tunnels (Wilson, 1971). Once the colony dies, chambers of the nest may remain suitable and accessible for a long period (Pereira, 1998).

The density of atta nests in the Vivarium was not measured. As fumigation is not permit-ted in the institution, the possibility of occupation of killed atta nests by P. subnuda does not apply. The nests of P. subnuda are situated at 1-2 m below the surface (Imperatriz-Fonseca et al., 1972) what could correspond to the location of abandoned ant chambers of young nests (Grandeza et al., 1999). Moreover, the surface area of the clusters of found bee nests conform, approximately, to a surface area of clusters of chambers of atta ant nests (Zanuncio, 1973). All these elements corroborate the hypothesis that P. subnuda occupy naturally abandoned nests of atta.

Figure 4.— Nests disposition of Paratrigona subnuda in the forest (Illustration by Helena Ignowski).

ACKNOWLEDGEMENTS

The author is obliged to CNPq for funding this study and to the Director of the Vivarium of USP for authorizing the work. Vera Lucia Imperatriz-Fonseca is thanked for her guidance. All who helped (in particular three anonymous referees) in the execution of this study are also thanked.

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