Studies on Neotropical Fauna and Environment 0165-0521/89/2404-0213-3.

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Vol. 24 (1989), No. 4, pp. 213-229 © Swets & Zeitlinger

Nest Architecture and Distribution of the Primitive

Stingless Bee, Mourella caerulea (Hymenoptera,
Apidae, Meliponinae): Evidence for the Origin of
Plebeia (s. lat.) on the Gondwana Continent*
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Joao M.F. CAMARGO and Dieter WITTMANN

CAMARGO, J.M.F. and WITTMANN, D. 1989: Nest Architecture and

Distribution of the Primitive Stingless Bee Mourella caerulea: Evidence for
the Origin of Plebeia (s. lat.) on the Gondwana Continent
Studies on Neotropical Fauna and Environment 24, pp. 213-229.

The stingless bee Mourella caerulea is distributed in the subtropical parts of

Brazil, Argentina and Paraguai. In the Serra do Sudeste of Rio Grande do
Sul, on the southern part of the Brazilian shield, this species is one of the most
abundant meliponine bees. Nests of M. caerulea are built in the soil and
exhibit architectural characters typical to all other genera of obligatory
ground nesting species, like Schwarziana, and the African genera Meliple-
beia, Plebeiella and Plebeina. The possibility that the similar solutions for the
construction of subterranean nests in these genera did not evolve by
convergence or parallelism is discussed. The occurence of Mourella together
with other more primitive representatives of the Plebeia group on the
southern parts of the Brazilian Shield cannot be explained by biogeographic
models proposed by some authors. Adopting an alternative model we
suggest that, during the lower Cretaceous, ancestor populations of the
Pleibeia-line inhabiting the meridional shields of Western Gondwanaland
(now southern Brazil and southern Africa), were separated by the south-
northward opening of the South Atlantic. During the Cretaceous until the lower Tertiary the remnant
populations on the southern parts of the Brazilian shield were isolated by the immense basalt flows and
subsequent volcanic Tertiary activity bordering this area. During their dispersal in the Tertiary species
of Plebeia (s. str.; post Gondwanic derived forms) may have radiated via the Patagonian shields and
their terrestrial connections to Antarctica and from there to Australia, while other Plebeia (s. str.)
species dispersed into the northern parts of South America. The monotypic genera Mourella and
Schwarziana and most of the more primitive species of Plebeia (s. str.), however, remained restricted to
their presumable subtropical centers of origin.
Joao M.F. Camargo, Departamento de Biologia (Setor de Ecologa), Faculdade de Filosofia, Ciências e
Letras de Ribeirao Preto, USP, 14.049 Riberiao Preto, SP, Brazil.
Research Associate, CNPq; Ref.: 300014/84-8/ZO/FV

D. Wittmann, Zoologisches Institut, Universität Tübingen, Auf der Morgenstelle 28, D-7400
Tübingen, FRG.

* We dedicate this paper to Prof. Jesus S. Moure on the occasion of his 75th birthday (2. Nov. 1987) and
for his 50 years of work on bees.
 214 J.M.F. CAMARGO AND D. WITTMANN

Introduction

Mourella caerulea workers were originally described by Friese (1900) as

belonging to the genus Melipona and later as Trigona cyanescens (Friese, 1911).
Schwarz (in Moure, 1946, Schwarz, 1948) erected the subgenus Mourella and
already pointed out the similarity with the genus Plebeia (s. str.). Finally, Mourella
was established as a genus by Moure (1971, cf. Camargo & Moure, 1988).
Only a very few worker specimens had been recorded in the southern Brazilian
States of Parana, Santa Catarina and Rio Grande do Sul as well from certain
regions in Paraguay, and the Province of Missiones, Northern Argentina (Ducke,
1925; Schwarz, 1948; Moure, 1951). The biology of M. caerulea remained
unknown.
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During a four year survey of the bees of Rio Grande do Sul (Witmann &
Hoffmann, 1990) the subterranean nests of Mourella caerulea were found for the
first time. Subsequently we have studied the oviposition behaviour in nests
transfered to the laboratory (Wittmann et al., 1988, 1990) and identified the
components of the pheromonal bouquet from pentane extracts of worker heads
(Wittmann et al., 1989b). These studies may provide additional data for the
interpretation of the systematic position of the monotipic genus Mourella.
Here we describe the niche and nest architecture and compare its attributes
with other subterranean nesting stingless bee species. Furthermore, we give some
remarks on the present day distribution of M. caerulea and discuss the probable
biogeographical history of the Plebeia (s. lat.).

Materials and Methods

To monitor the bee fauna of Rio Grande do Sul, the state was devided in 7 superregions covering the
main climatic, vegetational and geomorphological areas within which we sampled bees along various
transects. In the southeastern region covering the Serra do Sudeste and the western shore of the Lagoa
dos Patos, workers of Mourella caerulea were encountered in large numbers on flowering plants.
During a subsequent scanning of the area, subterranean nests of this species were found in various
localities. Four nests were excavated, partly opened and studied in situ. In search for habitat
characteristics which might influence the restricted distribution of M. caerulea, samples of soil from
the nest cavity were analyzed at the Department of Agriculture of the Federal University of Rio
Grande do Sul. Furthermore, pollen samples taken from storage pots were analyzed. The nests were
transfered in wooden boxes to the Departamento de Biologia, Universidade de Sao Paulo at Ribeirâo
Preto, for further examination of their architecture and for studies of intranidal behaviour. Two of the
nests were kept in observation boxes for more than 8 months.
For our comparative study of the nest architecture of subterraneanly nesting stingless bees, all
descriptions of nests that we are aware of were taken into account. In addition recordings of the
distribution of neotropical subterranean nesting species and illustrated descriptions of their nests
made by Camargo (unpubl.) were evaluated.
Specimens of M. caerulea workers and males were deposited at the Fundaçâo Zoobotânica do Rio
Grande do Sul, Porto Alegre, Brazil, the Zoological Institute of the University of Tübingen,
W-Germany, the Depto. de Biologia, Faculdade de Filosofia, Ciêcias e Letras, USP, Ribeirao Preto, SP,
the Smithsonian Institution, Washington, USA, and the Snow Entomological Museum, University of
Kansas, Lawrence, USA.
 NEST ARCHITECTURE OF MOURELLA CAERULEA 215

Results
The nest of Mourella caerulea

Nesting site. Four nests of Mourella caerulea were excavated in the district of
Canguçu located in the Serra do Sudeste, the southernmost part of the Brazilian
Shield. This region of 200-500 m elevation is floristically characterized as a
transition zone of the southernmost spurs of the subtropical rain forest to
bushland, consisting mainly of Myrtaceae. All nests were located in open
bushland, in two cases at the margins of small plantation, one of them adjacent to
the gallery forest of a creek. The local people reported further nests of stingless
bees to us. According to their descriptions, about 20 of them could be identified as
nest of Mourella. The popular name in the Canguçu region is "bieira" or "mirim
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do chao". In this area these bees are well known for their honey production which
reaches up to one liter per nest. Other ground nesting stingless bees, like
Schwarziana quadripunctata and Geotrigona spp., were not recorded in the region
(cf. Wittmann & Hoffmann, 1990); this indicates the possibility of vicariance.

Soil characteristics at nesting sites. The soils in the area where nests of Mourella
were found and where workers were collected are light and well drained rankers
or podsol-rankers of granitic origin (FAO nomenclature). They are of a rough
sandy texture with little clay content. These soils are characterized by poorly
developed A- and B-horizons, with displacement of organic material, Fe and Al
to lower layers, and rather abrupt transitions to the granitic C-horizon (Tab. 1).

Nests cavity. The nests of Mourella caerulea are built in light, well drained soil of
granitic origin, taking advantage of hollows between roots and other small
subterranean cavities; but there is no evidence that these bees use abandoned
nests of other social insects like termites or ants. Three of the four nests excavated
were found between 45-50 cm directly beneath the nest entrance. A younger nest,
however, which did not yet contain combs, although a queen was present, was
encountered between large roots about 80 cm below the surface and 1.5 m to the
side of the entrance hole. The ceiling and the walls of the nest cavity are hardened
and smoothed by the bees so that layers of the wall can easily be separated from
the surrounding soil. Older nests fit closely to the shape and size of the cavity,
supported by roots protruding into the nest, and by batumen lamellae and pillars
spanning the gap between the batumen layer and the cavity wall. No drainage
holes were found underneath the nest. The bottom of the nest cavity coincided in
three cases with the abrupt transition from soil horizon A to the C-horizon of

Table 1. Analysis of a podsol-ranker soil sampled from the surroundings of a Mourella caerulea nest.
CEC = cation exchange capacity at pH 7; me = milliequivalents per 100 g.

Texture Organic pH P K S Zn Cu B Mn Fe AI Ca Mg CEC

material
%clay % ppm % me/100g

28 4.3 5.6 9 114 11.8 3.3 0.5 0.1 23 0.16 0 11.3 1.7 15.2
 216 J.M.F. CAMARGO AND D. WITTMANN
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Fig. 1. Nest of Mourella cearulea. Top right: Detail of the nest entrance and part of a brood comb with
a gyne cell. To expose the internal structures of the nest, part of the batumen was removed.
Left, from top to bottom: The unlined upper part of the entrance tunnel and the lower part
(internal nest entrance tube) made from cerumen. The nest is surrounded by batumen and fixed
with pillars and lamellae to the refined walls of the nest cavity. The multilayered involucrum
surrounds the brood area. Storage pots are arranged in a ring around the lower part of the
involucrum. The bottom of the nest is partly open. The nest is constructed on top of a layer of
little eroded granitic gravel.
The entrance gallery was shortened by 1/2. Scales: A - 1 cm; B - 0.5 cm; C - 2.0 cm.
 NEST ARCHITECTURE OF MOUKELLA CAERULEA 217

advanced erosion and permeability (Fig. 1). Dumping sites for faeces and other
material like dead larvae, pupae and bees were encountered underneath the nests
as well as a rich fauna of soil organisms living on detritus.
Nest entrance. The nest entrance is an inconspicuous hole about 0.45 cm in
diameter, surrounded by a small mount of excavated material (soil and granitic
particles) less than 1.0 cm high and about 2.5 cm in diameter. Immediatelly
below the entrance, the tunnel is enlarged to 0.7-1.2 cm. Its walls between the
entrance and the top of the nest chamber are not lined; in some nests the inferior
part is slightly reinforced by cerumen. The part of the tunnel which leads from the
upper part of the nest cavity to the interior of the nest (internal entrance tube) is
made of cerumen and ends below or to the side of the brood chamber.
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Batumen layer and involucrum. The nests of M caerulea are about 15 cm high
and measure approximately 25 cm in diameter. The typical shape is a vertically
compressed sphere with the lower part being more flattened. The nest is enclosed
by a single hard and brittle, dark brown batumen layer (according to the
nomenclature of Wille and Michener, 1973) or external involucrum (nomencla-
ture of Camargo, 1974) of 1,0-1.5 mm thickness from which about 5 mm high
pillars or lamellae protrude to the unlined walls of the cavity. Young nests are of
rather irregular shape and are not surrounded by this type of batumen layer. At the
lower part of the nest the batumen layer is partly opened by horizontal slits so that
the basal layers of the involucrum and some of the storage pots are in direct
contact with the substrate. The brood chamber is surrounded by 6-7 layers of
involucrum each up to 0.5 mm thick.

Brood area. The brood combs are horizontal and comprise 10 combs with
approximately 3.000 cells in the largest nest found. Brood cells for workers and
drones are 5.64 - 5.90 mm high and 2.90 - 3.15 mm in diameter. Gyne cells
measure 6.64 - 7.22 mm in hight and 4.06 - 4.15 mm in diameter. They are
located at the margins of the combs. Brood cells are constructed synchronous-

Storage pots. The storage pots are constructed with geminate walls and arranged
in a compact ring 2 or 3 pots wide and 2 or 3 pots high. This ring surrounds the
involucrum of the lower part of the brood chamber and forms the broad basis of
the nest structure. Pollen and honey pots are of equal shape and size, measuring
2.0 - 2.5 cm in height and 1.5 cm in diameter. Pollen pots and honey pots were
found to be arranged in groups.

Behaviour, ecology and distribution of Mourella caerulea

Behaviour of bees at the nest entrance. The nest entrance is mostly guarded by a
single worker bee which is positioned slightly underneath the opening and
retreats whenever a foraging bee is leaving or entering the nest. When the nest
was excavated and opened, some of the bees left it and flew around in its close
vicinity but did not exhibit any aggressive reaction.
 218 J.M.F. CAMARGO AND D. WITTMANN

Bees returning from foraging trips apparently have difficulties to localize the
nest entrance even in the last centimeters of their approach. They may repeatedly
land close to the entrance hole and fly up again until they finally enter the nest.
Orientation flights were observed at a nest kept in the laboratory with an entrance
in a dirt filled box on the outside of the wall. The bees faced the entrance hole
while flying in half circles with an initial radius of about 15 cm. Towards the end
of the orientation flight they extended the semicircular tracks to a radius of about
2 m.

Forage plants. Analysis of pollen from storage pots of the nests found in the Serra
do Sudeste and plants on which workers M caerulea foraged in an agricultural
area in the vicinity of Porto Alegre revealed an ample spectrum of plant species
visited (Tab. 2). Among the pollen plants which comprise species flowering from
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October until January the Myrtaceae are most frequently represented: Eugenia
spp. (83.7%, Myrtaceae), Centella biflora (5.7%, Umbelliferae), Lanthoxylum
astrigerum (5.0%, Rutaceae), Cedrella sp. (1.3%, Meliaceae) and others (4.2%).
Table 2. Plant species visited by Mourella caeruka bees for pollen (P) and/or nectar collection (NP).

Amaranthaceae Gomphrena sp. (P)

Pfaffia tuberosa (NP)

Anacardiaceae Hthraea molleoides (P)

Aguifoliaceae Ilex sp. (P)

Caryophyllaceae Silène sp. (P)

Silène gallica QiP)

Convolvulaceae lpomoea cairica (NP)

Compositae Aspilia montevidensis (NP)

Baccharidastrum triplinervium (NP)
Baccharis articulata (NP)
Baccharis sp. (P)
Bidens pilosa (NP)
Chrysanthemum mycosis (NP)
Elephantopus mollis (NP)
Hypochoeris brasilknsis (NP)
Pluchea sagittalis (NP)
Senecio bonariensis (NP)
Senecio brasiliensis (NP)
Senecio oleraceus (NP)
Senecio pinnatus (NP)
Senecio selloi (NP)
Taraxacum sp. (P)
Vernonia flexuosa (NP)
Vemonia nudiflora (NP)

Cruciferae Raphanus raphanistrum (NP)

Labiata Hyptis mutabilis (NP)

Mentha sp. (NP)
Scutellaria racemosa (NP)
 NEST ARCHITECTURE OF MOURELLA CAERULEA 219

Leguminosae Acacia sp. (P)

Mimosa scabrella (P)

Linaceae Linum usitatissimus (NP)

Lythraceae Heimia myrtifolia (NP)

Malcaceae Sida rhombifoUa (NP)

Meliaceae Cedrela sp. (P)

Myrtaceae Eugenia sp. (P)

Onagraceae Ludwigia elegans (NP)

Ludwigia sp. (NP)
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Oxalidaceae Oxalis subvilbsa (NP)

Oxalis conorrhiza (NP)

Proteaceae Grevillea banksii (NP)

Ranunculaceae Clematis denticulata (NP)

Rubiaceae Borreria verticillata (NP)

Borreria sp. (NP)
Richardia brasiliensis (NP)

Rutaceae Citrus sp. (P)

Lanthoxylum astrigerum (P)

Sapindaceae AHop/ry/!««/u/És(NP)

Solanaceae Solatium sisymbriifolium (NP)

Sterculiaceae Dombeya wallichii (NP)

Umbelliferae Cente/fa fci/tora (P)

Eryngium sp. (NP)

Verbenaceae Wfet sp. (P)

Verbena montevidensis (NP)

Distribution. The following list summarizes localités where workers of Mourella

caerulea were found according to our data and those given by Ducke (1925),
Schwarz (1948) and Moure (unupl.)

Brazil: Rio Grande do Sul: Bage, Canguçu, Estéio, Sâo Leopoldo, Säo Lourenço
do Sul, Porto Alegre, Rosârio, Minas de Quamaquâ, Viamäo. Santa Catalina:
Indayal. Parana: Lapa, Castro. Paraquay: Puerto Bertoni, Villa Rica, Villa
Encarnacion. Argentina: Missiones: Posadas.

Since the first records of M caerulea at the beginning of the century only a few
data on its distribution have been compiled. They indicate, however, that this
obviously rare species is restricted to the subtropical regions of southeastern
 220 J.M.F. CAMARGO AND D. WITTMANN

South America. Furthermore, our survey of the apifauna of Rio Grande do Sul
(Wittmann and Hoffmann, 1990) strongly suggests a contagious dispersal. This
becomes even more evident by the high abundance and clumped occurrence of
nests in the granitic areas of the Serra do Sudeste. In this region Mourella and
Plebeia wittmanni are the predominant stingless bee species (Hoffmann &
Wittmann, 1987; Wittmann, 1989). The obligate subterranean nesting species of
Geotrigona and Schwarziana, the latter monotypic genus being also restricted to
the southern and southwestern parts of Brasil, were not recorded in the Serra do
Sudeste region (Wittmann and Hoffmann, 1990). However, in the surroundings of
the granitic area Mourella is a very rare element of the apifauna, whereas
Schwarziana is the more abundant subterraneously nesting species. The non-
diversification of Mourella and its geographical restriction may be associated
with its strong conservationism in respect to the habit of nesting in little developed
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soils, and its preferences for a subtropical climate and for Myrtaceae, a plant
family with a typical panaustral distribution (Michener, 1979). The geographical
exclusion between Mourella and Schwarziana may be explained by their different
preferences for nesting sites. Schwarziana preferably nests in deep soils and,
therefore, constructs a much more elaborate drainage system to control the
humidity in the nest (Camargo, 1974). To clarify the habitat characteristcs which
influence the distribution pattern of Mourella, more nests in other regions will
have to be studied. Based on the data so far available we suggest intensifying the
search for nesting sites of M. caerulea in those subtropical regions which are
characterized by poorly developed, acid podsol-ranker soils and a vegetation with
a high relative abundance of Myrtaceae.

Comparison of subterranean nesting stingless bees

The problems in establishing homologies among architectural attributes of nests
of different stingless bee species were already discussed by Michener (1961) who
considers it justified to assume homologies at least for the basic and obligatory
structures, like brood cells, brood chamber, involucrum, batumen, storage pots,
pillars and connectives and the nest entrance. Other structures which are not
present in all nests could be considered adaptive responses to the niche occupied
by a species.
In respect to the involucrum and the batumen, Michener points out to the
difficulties in establishing a logical sequence of derivations necessary to presume
homologies. In many cases it is not clear whether a structure is derived from the
involucrum or from the batumen (Wille, 1964) as both have a similar protective
function. Even for the other basic structures it seems difficult to establish series of
derivations, as many of their modifications (convergencies or reversions - Wille
and Michener, 1973) are associated with the mode of life and the species niche.
Therefore, for an evolutionary evaluation of nest architectural structures, other
attributes of the bees in question, especially morphological characters on a
generic and specific level, have to be considered.

Genera with exclusively subterranean nesting species. Despite these difficul-

ties we have to recognize the great similarity in the nest architecture of the
 NEST ARCHITECTURE OF MOURELLA CAERULEA 221

neotropical genera Mourella, Schwarziana (Camargo, 1974), Geotrigona

(Nogueira-Neto and Sakagami, 1966; Camargo, unpubl.) and Camargoia, a new
genus of the Tetragona group described by Moure (1988, Camargo, unpubl.) and
in the African genera like Melipkbeia, Plebeiella and Plebeina (Smith, 1954;
Portugal-Araujo, 1963; Pooley and Michener, 1969; Fletcher and Crewe, 1981).
All species of these genera obligatory build their nests in subterranean cavities
(Tab. 3). The following characters are typical for these nests.

1. The subterranean cavity is modified and/or refined by the bees,

2. the nests are surrounded by a batumen,
3. the involucrum around the brood chamber consists of various layers,
4. the storage pots form a ring surrounding the brood chamber between the
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batumen and the involucrum,

5. the entrance tunnel or gallery ends in the involucrum layers under or to the side
of the brood chamber,
6. brood cells are arranged in horizontal or spiral combs in the middle of the
nest,
7. the entrance tunnel between the surface and the nest cavity is either not lined
or only slightly reinforced by cerumen,
8. the nest entrance is either an inconspicuous hole or a small turret made from
soil or cerumen.
Nests of these bees are never found in inhabited colonies of other social insects
like termites and ants (Portugal-Araujo, 1963; Pooley and Michener, 1969;
Camargo, 1974; Camargo, unpubl.), except for Plebeia denoiti which facultatively

Table 3. Genera of stingless bees in which all species are obligate subterranean nesting.
(1) monotypic genera; (2) 16 species or subspecies; (3) 3 species; (4) 6 species; (5) 4
species or subspecies.

Neotropics
Mourella caeruka ( 1 ) Camargo and Wittmann (here)

Schwarziana quadripunctata ( 1 ) Camargo ( 1974)

Geotrigona mombuca (2) Nogueira-Neto & Sakagami (1966)
Geotrigona spp. Camargo (unpubl.)
Camargoia spp. (3) Camargo (unpubl.)

Africa

Melipkbeia beccarii (4) Smith (1954), Pooley and Michener (1969)

Melipkbeia tanganyikae medionigra Portugal-Araujo (1963)
Pkbeiella lendliana ( 1 ) Portugal-Araujo ( 1963)

Pkbeina denoiti (5) Smith (1954), Fletcher and Crewe (1981)

 222 J.M.F. CAMARGO AND D. WITTMANN

nests in living termite colonies (Smith, 1954). The batumen consists either of a
single layer as in Mourella, Plebeklla, Meliplebeia and Plebeina, or it is modified as
in Schwarziana where longitudinal batumen galleries reach from the top to the
bottom of the nest (Camargo, 1974). In Geotrigona and Camargoia these galleries
are constructed between the outer batumen and the walls of ß\e nest cavity
(Camargo, unpubl.). In one of the Mourella nests the upper part of the batumen
was fixed to the ceiling of the nest cavity by lamellate, gallery-like structures,
resembling those in Geotrigona. Bees of the genera Geotrigona and Camargoia
line the upper parts of the cavity walls with cerumen (Camargo, unpubl.). In
species of Plebeia (s. lat., including Mourella, Schwarziana, Plebeina, Pleibeiella
and Meliplebeia), however, these walls are apparently of unlined but compacted
soil. The position of the storage pots between the involucrum and the batumen
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and their arrangement as a compact ring surrounding the brood nest as in

Mourella, Schwarziana, Geotrigona and Camargoia, or in a more dispersed
arrangement as in Meliplebeia and Plebeklla, but not above or below the brood
nest (Portugal-Araujo, 1963), is a typical character of such nests. The nest
entrance holes are the simplest among all Meliponiae. The most simple and
inconspicuous we are aware of is the nest entrance ofMourella. Bees of the genera
Schwarziana and Camargoia construct small soil turrets which in the other genera
are made from cerumen.
One of the characters which can be interpreted as an adaptive response to the
specific nesting site is the drainage system of the nest cavity. In Plebeiella
(Portugal-Araujo, 1963), Geotrigona and Camargoia (Camargo, unpubl.) the
nests are fixed to the upper part of the cavity so that beneath about 11A of the
cavity remains unoccupied. This is also the case in nest cavities of Schwarziana,
although in some of them drainage galleries were found (Camargo, 1974;
Wittmann, unpubl.). In Meliplebeia (Portugal-Araujo, 1963) and Plebeina (Smith,
1954) the nest occupies the whole cavity and a drainage gallery is dug into the soil
underneath the nest. Both systems, free space or drainage gallery under the nest,
are common in those species nesting in sandy soils or soils with high clay content.
In Mourella the problem of draining the nest cavity seems to be resolved by the
choice of the nesting habitat: the nests are constructed in soils of little depth above
an highly permeable layer of granitic gravel on the eroding C-horizon.
The above mentioned nest characters are found only in those genera with obligate
subterranean nesting species (Tab. 3). However, this type of nest architecture is
not the only solution for subterranean nesting known in stingless bees.

Genera with some subterranean nesting species. On the other hand, there are
some other genera of stingless bees like Melipona, Trigona, Paratrigona,
Nogueirapis, Partamona and Tetragonisca which include at least a few subterra-
nean nesting species (Tab. 4). These species have apparently adopted other
architectural solutions for the underground construction of their nests. Generally
they have long external entrance tubes which are made from resin, vegetal
material and soil, except for that in Melipona quinquefasciata which is a mere soil
construction. The entrance tunnel usually ends in the upper part of the nest, except
in N. mirandula and M. quinquefasciata where it reaches into the involucrum. In
most of these species the nest is surrounded by either batumen or by involucrum
(Camargo, 1970). In N. mirandula (Wille, 1964) and in M. quinquefasciata
 NEST ARCHITECTURE OF MOURELLA CAERULEA 223

Table 4. Stingless bee species with some obligate (ob) and/or facultatively (fac) subterranean nesting
species.

Neotropics

MELIPONA (ca. 40 species)

Melipona quinquefasciata (ob) Camargo (unpubl.)

TRIGONA (s. str., ca. 30 species)

Trigona recursa (ob) Schwarz (1948), Camargo (1970), Camargo (un-
publ.)
Tfulviventris (ob) apud Schwarz (1948), Wille & Michener (1973),
Camargo (unpubl.)
T. amalthea (fac) Camargo (unpubl.)
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I hypogea (fac) Silvestri (1902), Camargo and Roubik (unpubl.)

TETRAGONA (ca. 15 species)

Tetragona dorsalis (fac) Wille & Michener (1974)

PARATRIGONA (ca. 15 species)

Paratrigona lineata (ob) apud Schwarz (1948), Camargo (unpubl.)
P. lineata nuda (ob ?) Schwarz (1948)
P. subnuda (-petropolis) (ob) apud Schwarz (1948), Fonseca et al. (1972)

NOGUEIRAPIS (3 species)
Nogueirapis mirandula (ob) Wille (1964), Wille and Michener (1973)
Nests of other species unknown.

PARTAMONA (s. str; ca. 15 species)

Partamona testacea (ob) Kerr et al. (1967), Camargo (1970, 1980), Camargo
(unpubl.)

TETRAGONISCA (3 species)
Tetragonisca buchwaldi (ob) Wille (1966), Wille and Michener (1974), Roman
(1986)
T, angustula angustula (fac) Wille and Michener (1973)

Indomalayan and Australian Region

TETRAGONULA (ca. 32 species)

Tetragonula iridipennis (fac) Michener (1961)

(Camargo, unpubl.), both structures are present. In P. testacea fine cerumen layers
surround the brood chamber and are directly connected to the cavity wall by
pillars and connectives; here a proper batumen is missing, although the cavity
walls are lined with resin. In nests of Trigona recursa and Trigona fulviventris
(Camargo, unpubl.) the brood chamber and the storage pots are surrounded by 2
or 3 layers of thick cerumen; in these cases an involucrum is missing. In none of
these nests the storage pots are arranged as a ring around the involucrum at the
lower part of the brood chamber. In R testacea and in N. mirandula the storage pots
are generally underneath the brood chamber, in T. recursa they usually surround
the whole brood chamber, in Tfulviventris they are above or at the side of it, and in
Tetragonisca buchwalbdi they are built in a chamber at the side of the brood nest
 224 J-M.F. CAMARGO AND D. WITTMANN

(Wille, 1966; Roman, 1986). In all these species the nest cavity is little refined by
the bees. Generally the nests occupy the whole cavity, except for those of M
quinquefasciata which are frequently located in large cavities amongst tree roots.
Nests of other species are built within subterranean colonies of termites or ants, as
is the case in T. recursa and P. testacea, the latter having nest aggregations within
Atta colonies (Camargo, unpubl.). Drainage tubes are only known from nests of
P. testacea, N. mirandula and of one species of the T recursa group.

Discussion

Systematic relations
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Melipona, Trigona, Paratrigona, Partamona and Nogueirapis are genera which

exhibit derived morphological characters, only Tetragonisca is conservative (cf.
Moure, 1951). These genera probably differentiated in the Guiana Shield and in
the northern parts of the Brazilian Shield. In each of these genera (Noguerapis, in
which the nest of only one species is known being probably an exception), the nest
architecture of the subterranean nesting species differs little from that of
congeneric species which nest in or on trees, in termite nests, or in other
above-ground substrates like roots of epiphytes, bird nests, cracks in rocks, etc.
For example, the nest of P. testacea only differs from congeneric species in that it
has a drainage tube. This and the fact that subterranean nesting is not obligatory
for all species of these genera may indicate that they have only in recent times
been derived from their arboreous, termitophilous or other above-ground
ancestral species.
On the other hand, Mourella and Schwarziana as well as their African vicariants
Meliplebeia, Plebeiella and Plebeina are, with respect to their morphological
characters, members of conservative groups of little diversification: Mourella,
Schwarziana and Plebeiella are monotypic, while for Meliplebeia and for Plebeina
only 6 respectively 4 specific and subspecific names are known (Moure,
1961). Bees of the African genera are found predominantly in southern latitudes
on well drained plateaus, their neotropical vicariants occur on the southern parts
of the Brazilian Shield and its surroundings.
The consistency of morphological characters (synapomorpies, see Moure,
1951, 1961) suggests that these genera (Mourella, Schwarziana, Meliplebeia,
Plebeiella and Plebeina) are phylogenetically closely interrelated. Therefore, it is
highly probable that their similar solutions for the construction of subterranean
nests did not evolve by convergence of parallelism, this is, we assume that the
obligate subterranean nesting habits and the features of their nest architecture are
symplesiomorphic characters conserved by these genera.
Accepting this point of view, Geotrigona and Camargoia would be, in terms of
their nidification habits, the most conservative genera of Tetragona (s. lat.), a
divergent phyletic group. The center of dispersal of the neotropical members of
this group is probably on the Guiana- and the northern parts of the Brazilian
Shield. The biogeography of the species of the Tetragona-line and problems of
their vicariance will be treated in a future paper.
Mourella exhibits a series of morphological characters as well as properties in
the nest architecture which suggest that it is one of the more primitive neotropical
 NEST ARCHITECTURE OF MOURELLA CAERULEA 225

species of the Plebeia group, or even a relic form. Its most related vicariants, in
terms of morphology and nesting habits, are the African genera Plebeiella,
Plebeina and Meliplebeia. How can we explain the occurence of Maurella and that
of Schwarziana, another conservative and monotypic genus, isolated in Southern
Brazil?

Biogeographical problems
Kerr and Maule (1964) assume that the Meliponinae had their center of origin in
South America from where they radiated at the beginning of the Eocene to North
America and from there via the Bering Street to Eurasia, finally arriving in the
Indo-Malayan region and in Africa at the end of the Oligocène and in Australia
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during the Miocene. Even if we consider that migration routes between South
America and North Anerica did exist, at least in the Oligocene/Miocene
(Camargo et al., 1988), this model cannot explain the presence of species
derivated from Plebeia (s. lat.) in Australia and Africa and the absence of such
forms in the Indo-Malayan region.
Wille (1979) gives reasonable arguments that the center of origin of the
Meliponinae is in Africa where they had evolved during the upper Cretaceous and
lower Tertiary. He assumes that they migrated during the Tertiary to Europe from
where they dispersed to the other continents. Here we apply the same argument as
used to reject the hypothesis of Kerr and Maule: the absence of Plebeia (s. lat.) in
the Indo-Malayan region. For the neotropical region one could still argue that
actually there do occur representatives of Plebeia (s. str.) in Central America, the
regions of the Guiana Craton and the northern parts of the Brazilian Shield which
possibly indicate that the Central American connection was used by stingless bees
as a migration route from North to South America.
This hypothesis is also supported by the recent discovery of a fossil meliponine
bee, Trigona prisca, from the upper Cretaceous (80 mya) in New Jersey, USA
(Michener and Grimaldi, 1988a, 1988b). These authors relate this species
directly to Trigona (s. str.) of the neotropical region and consider the possibility
that this phyletic line had its origin in the nearctic region from which it migrated
to South America after this continent had separated from Africa during the
Campanian (ca. 75 mya). However, this still does not explain the isolated
occurrence of conservative genera like Mourella and Schwarziana in the southern
regions of Brazil. Furthermore, it does not explain the absence of those
neotropical groups in Central America which represent phyletic lines related but
not derived from Trigona (s. str.) like Duckeola, Trichotrigona and Camargoia and
others which are related to Plebeia (s. lat.) like Friesella, Schwarziana and
Parapartamona (the latter being restricted to the Andean region) and groups like
Leurotrigona and Celetrigona whose taxonomic position is still not established. It
is of little probability that these groups, which are well differentiated, are of more
recent origin than Trigona (s. str.) which already represent a derived line within the
Meliponinae. Therefore, if they had emigrated from the nearctic region, they
should be represented in the Central American bee fauna.
Michener and Grimaldi (1988b) argument that: "the Trigona-species now in
Mesoamerica may not represent a northward extension from South America;
instead they could be remnants of a formerly wide tropical nearctic distribution".
 226 NEST ARCHITECTURE OF MOVRELLA CAERULEA

However, to our view the actual distribution and the taxonomic relationships
between the species of Trigona (s. str.) do not corroborate this hypothesis: Of the
actual ca. 30 species of Trigona (s. str.) only 9 reach Central America and only
T. corvina and T. nigerrima represent a certain exception, as they are distributed
from Southern Mexico to Colombia (T. nigerrima to Ecuador). But even these
species are part of a group (T. hyalinata, T.Branneri, T. spinipes and T. amazonensis
which has an sample distribution in South America. Of the other Trigona (s. str.)
about 16 species are restricted to the Guiana Craton and the northern parts of the
Brazilian Shield. It is possible that T.prisca represents an extinct form related to
the Eurasian fauna and not directly to Trigona (s. str.) of the neotropical region
(like Kelnermelia, a fossil stingless bee from the upper Eocene of the baltic amber;
Moure and Camargo, 1979). Furthermore, one has to consider that the
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distribution of groups related to Trigona (s. str.) is typically pantropical. There are
at least 13 supra specific lines in the Indo-Malayan region of which at least 2
groups reach to New Guinea and one, Tetragonula, reaches to the north-east of
Australia. In Africa only one genus, the highly differenciated Dactylurina, occurs.
In the Neotropics at least 11 groups are found (Moure, 1951, 1961) which
principally occupy the Guiana Craton and the northern parts of Brazil, while only
a few species reach further south.
The distribution of Trigona (s. lat.), however, does not explain the distribution
pattern of Plebeia (s. lat.) which is a group of panaustral dispersion. Of its 4
neotropical genera, 3 (Mourella, Schwarziana and Friesella) occur exclusively in
south-southeastern Brazil. In Africa 3 genera occur (Pleibeiella, Pkbeina and
Meliplebeia) and one genus (Austroplebeia) in northeastern Australia and New
Guinea.
The possibility that some of the forms included in the Plebeia line are products
of convergence and not part of a direct ancestral group cannot totally be
neglected. On the other hand, it is little probable that notable series of similarities
in the external morphology of workers, like those found between Austroplebeia
and Plebeia (s. str.) (Moure, 1961), are mere casual products but are true
synapomorphies indicating very close phyletic relations.

Is Mourella a bridging element between African and Neotropical Plebeia (s.

lat)?
Moure (1951) and Michener in an eaerlier paper (1979) suggested that the
Meliponinae had their early center of origin on the Gondwana Continent and
considered continental drift as the intrinsic mechanism for the disjunct recent
dispersal of stingless bees.
Adopting their ideas to our hypothesis, we have to date back the origin of the
Plebeia line at least to the lower Cretaceous. According to recent dating, the
ancient Gondwana Continent at that time started to break up at its western part
into present day Africa and 3 major cratons (or shields) which later formed South
America. This breakage began and continued in a south-north direction by the
separation of the Patagonian Shields and subsequently the Brazilian and Guyana
Shields from Africa as the South Atlantic developed by sea floor spreading
110-130 mya (Tarling, 1981; Zeil, 1986). During the early stages of the
fracturing, the southern part of the Brazilian Shield with the present regions of Rio
 J.M.F. CAMARGO AND D. WITTMANN 227

Grande do Sul, Santa Catarina and Parana were separated from Namibia and
Angola in Africa while the northern part of the Brazilian Shield and the Guyana
Shield maintained their connection with Africa until 100 mya.
Thus, during an early stage of continental drift, ancestral populations of the
Plebeia line on the southern part of the Brazilian Shield may have been separated
from those in Africa.
The separation of the continents was accompanied by the formation of basaltic
masses which flowed out of tectonic fractures on both sides of the expanding gap.
From 150 untill 118 mya, huge basaltic areas at the southern fracture lines of both
continents were formed. In Southern Brazil up to 13 basaltic layers covered the
major areas of present-day Rio Grande do Sul, Santa Catarina and Parana as well
as parts of Paraguay, Uruguay and northeastern Argentina (Beurlen, 1970; Zeil,
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1986). The repeated basalt flows must have interrupted the development of deep
soils and of a closed vegetation cover on each of the layers, thus inhibiting or
intercepting attempts of radiation, especially of ground nesting species. Subse-
quently large parts of these regions were covered by lava and vulcanic ashes. The
vulcanic activity ceased only in the early Tertiary, about 42 mya (Petrini and
Fulfaro, 1983).
As a consequence of these geological events populations of species of the
Plebeia line on the southern part of the Brazilian Shield must have been restricted,
at least during the early stages after their separation from Africa, to the cristalline
elevations of the Serra do Sudeste in Rio Grande do Sul and its continuation in the
Serra do Mar of Santa Catarina and Parana as well as to the carboniferous and
permian areas of the Serra Gérai. Therefore, we consider these regions the most
important refuges in southeastern Brazil during the Cretaceous and early
Tertiary.
Accepting this hypothesis as a more probable one for the distribution and
vicariance of Plebeia (s. lat.) one must also recognize that Plebeia (s. str.) is a
derived post-Gondwana form which differentiated on the southern parts of the
Brazilian Shield. Early forms of Plebeia (s. str.) may have abandoned the
subterranean nesting habit of their ancestors and occupied new niches, thus
successfully radiating during the lower Tertiary into northern Brazil and via the
Patagonian Shields and their terrestrial connections to Antarctica, finally
reaching Australia. This route of dispersal would explain the absence of derived
forms of Plebeia (s. lat.) in the Indo-Malayan region.
Further indication that Plebeia (s. str. - and probably also Friesella) are genera
which probably evolved on the southern parts of the Brazilian Shield comes from
the fact that the major number of the more primitive species of this genus are still
depending on nesting habitats typical for the Brazilian Craton (Wittmann,
1989).
 228 NEST ARCHITECTURE OF MOURELLA CAERULEA

Acknowledgements
We thank M. Hoffmann for providing the list of forage plants, M. Ramalho for the pollen analysis, R.
Radtke for his assistance in the field and D. de Jong for Englisch corrections. Furthermore, we thank
CD. Michener for suggestions and critics. D.W. thanks J.W. Thome for the invitation to work at the
Fundaçâo Zoobotânica do Rio Grande do Sul, and the Alexander von Humboldt-Foundation for
financial support by a Feodor - Lynen - Scholarship. Funding for J.M.F.C. came from FAPESP, Proj. Nr.
85/2842-7. This study was carried out in a cooperation program between the PUC-University, Porto
Alegre, and the University of Tübingen. The generous help of Joaozinho Diaz and other local people at
the study sites is gratefully acknowledged.

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