Spatial distribution of nests of Paratrigona subnuda Moure, 1947 (Apidae, Meliponini)
Rev. Écol. (Terre Vie), vol. 69, 2014.
– 345 –
spatial distribution of nests of Paratrigona subnuda Moure, 1947
Denise M. D. S. Mouga
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: firstname.lastname@example.org.
– 346 –
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).
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
Figure 1.— Nest entrance of Paratrigona subnuda Moure, 1947 (Illustration by Helena Ignowski).
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.
– 347 –
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).
– 348 –
Distances, in meters, between Paratrigona subnuda nests
Nest number Nearest nest Distance between these nests
1 2 79.0
2 3 4.12
3 4 1.95
4 3 1.95
5 3 53.4
6 5 58.6
7 8 43.9
8 32 4.8
9 29 39.4
10 11 3.75
11 10 3.75
12 11 12.4
13 14 1.8
14 13 1.8
16 18´ 25
17 16 33
18 18´ 42.5
18´ 13 22
19 19´ 0.82
19´ 19 0.82
20 19´ 29.1
21 21´ 2
21´ 21 2
22 24 17
23 24 1.9
24 23 1.9
25 21 7.7
26 20 33
27 28 13.3
28 27 13.3
29 9 39.4
30 29 68.4
31 6 53.8
32 8 4.8
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
– 349 –
(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
Figure 4.— Nests disposition of Paratrigona subnuda in the forest (Illustration by Helena Ignowski).
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.
Aragaki, S. & Mantovani, W. (1998).— Caracterização do clima e da vegetação de remanescente florestal no Pla-
nalto Paulistano (SP). Annal. du IV Simpósio de Ecossistemas Brasileiros (S. Watanabe, coord.). Acad.Ciênc.
Est. S. P., 2: 25-36.
Clark, P.J. & Evans, F.C. (1954).— Distance to nearest neighbor as a measure of spatial relationships in populations.
Ecology, 35: 445-453.
Della Lucia, T.M.C. & Moreira, D.D.O. (1993).— Caracterização dos ninhos. Pp 32-42 in: T.M.C. Della Lucia (ed.).
As formigas cortadeiras. Imprensa Universitária, Viçosa, Brazil.
– 350 –
Diehl-Fleig, E. (1995).— Formigas: organização social e biologia comportamental. Universidade do Vale do Rio dos
Sinos, São Leopoldo, Brazil.
Dislich, R., Cersósimo, L. & Mantovani, W. (2001).— Análise da estrutura de fragmentos florestais no Planalto
Paulistano – SP. Rev. Bra. Bot., 24: 321-332.
Fowler, h.g. (1979).— Responses by a stingless bee to a subtropical environment. Rev. Biol. Trop., 27: 111-118.
Gomes, E.P.C. (1992).— Fitossociologia do componente arbóreo de um trecho de mata em São Paulo, SP. MSc Thesis.
University of São Paulo, São Paulo, Brazil.
Grandeza, L.A.O., Moraes, J.C. & Zanetti, R. (1999).— Estimativa do crescimento externo de ninhos de Atta sex-
dens rubropilosa Forel e Atta laevigata (F. Smith) (Hymenoptera: Formicidae) em áreas de reflorestamento
com eucalipto. Am. Soc. Entom. Brasil, 28: 59-64.
Imperatriz-Fonseca, V.L., Ferreira de Souza, S.C. & Nogueira Neto, P. (1972).— Subterranean nest structure
of a stingless bee (Paratrigona subnuda Moure) (Meliponinae, Apidae, Hymenoptera). Ciência e Cultura,
Kerr, W.E. (1951).— Bases para o estudo da genética de poplações do Hymenoptera em geral e dos Apinae sociais em
particular. An. Esc. Sup. Agric. Luiz de Queiróz, 8: 219-354.
Michener, C.D. (1974).— The social behavior of the bees: a comparative study. Belknap Harvard University Press,
Mouga, D.M.D.S. (1984).— Coleta de pólen e nectar de Paratrigona subnuda (Hymenoptera, Apidae, Meliponinae).
36a Annual Reunion of SBPC. São Paulo. Anais.
Nogueira-Neto, P. (1997).— Vida e criação de abelhas indígenas sem ferrão. Editora Nogueirapis, São Paulo.
Pedro, S.R.M. & Camargo, J.M.F. (1999).— Apoidea apiformes. Pp 193-211 in: C.R.F. Brandão & E.M. Cancello
(eds.). Biodiversidade do Estado de São Paulo. Invertebrados Terrestres. Vol. 5. Fapesp, São Paulo.
Pereira, R. C. (1998).— Espécies de formigas cortadeiras em plantações de eucalipto: relação com fatores ambientais
e consumo foliar. MSc Thesis. Federal University of Viçosa, Brazil.
Pirani, J.R. & Cortopassi-Laurino, M. (1994).— Flores e abelhas em São Paulo. EDUSP/ FAPESP, São Paulo.
Por, F.D. (1992).— Sooretama, the Atlantic rain forest of Brazil. SBP Academic Publishing, The Hague.
Schwarz, H.F. (1948).— Stingless bee (Meliponidae) of the Western Hemisphere. Bull. Am. Mus. Nat. Hist., 90: 1-546.
Veloso, H.P., Rangel Filho, A.L.R. & Lima, J.C.A. (1991).— Classificação da vegetação brasileira adaptada a um
sistema universal. IBGE, Rio de Janeiro.
Walter, H. (1986).— Vegetação e zonas climáticas. EPU, São Paulo.
Wilson, E.O. (1971).— The insect societies. Belknap Press, Cambridge, MA.
Zanuncio, J.C. (1973).— Entomologia florestal. UFV, Viçosa.