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Journal of Insect Biodiversity 5(10): 1-9, 2017 http://www.insectbiodiversity.org
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RESEARCH ARTICLE
Nesting sites characteristics of stingless bees (Hymenoptera:
Apidae) in Central Sulawesi, Indonesia
Nelky Suriawanto1 Tri Atmowidi1* Sih Kahono2
1Department of Biology, Faculty of Mathematics and Natural Sciences, Bogor Agricultural University,
Dramaga Campus, Bogor 16680, Indonesia. 2Zoology Division, Research Center for Biology-LIPI, Bogor
16911, Indonesia. *Corresponding author e-mail: atmowidi@gmail.com
Abstract: Stingless bees (Hymenoptera: Apidae) is eusocial insects that live together in a
colony. This research was aimed to study the nesting site characteristics of stingless bees in
the settlement areas at Central Sulawesi, Indonesia. The nesting sites were observed by
purposive sampling method from July 2015 to January 2016. Four species belong to genus
Tetragonula were found, namely T. fuscobalteata, T. biroi, T. sapiens, and T. laeviceps. Two
spesies, T. biroi and T. sapiens are the new record in Sulawesi island. The highest abundance
of stingless bees colony was T. fuscobalteata (92.26%), followed by T. biroi (4.17%), T.
sapiens (2.98%), and T. laeviceps (0.59%). Nesting sites of T. fuscobalteata were found in
the stone, brick wall, wooden wall, bamboo, and iron cavities, T. biroi in the wooden wall,
stone, and brick wall cavities, T. sapiens in stone cavities, while T. laeviceps in wooden
walls.
Key words: Nesting sites, Stingless bees, Tetragonula, Settlement area, Central Sulawesi.
Introduction
The diversity of stingless bees vary among different ecosystems. The most diverse
commonly is found in the natural forest and gradually reduce in secondary forest, utilized
forest, and settlement area, respectively (Boontop et al. 2008; Salim et al. 2012; Kelly et al.
2014; Syafrizal et al. 2014; Rahman et al. 2015). Generally, lowland ecosystem has more
diverse of stingless bees than highland ecosystem (Sakagami & Inoue 1989; Salim et al.
2012). In the settlement areas, nests of stingless bees usually are found in the part of
buildings and houses, i.e., roof and wooden wall cavities.
Nesting sites of stingless bees Suriawanto et al.
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The nesting sites, nest structure, and characteristics of nest entrance are characters can
be used for identification of stingless bees species. The nest entrance of stingless bees varied
in shape, length, and colour (Syafrizal et al. 2014; Kelly et al. 2014). For examples, nest
entrance of Heterotrigona itama is funnel shape, whereas, in Geniotrigona thoracica is round
mount-like shape (Kelly et al. 2014). The common structure of stingless bees nests consists
of entrance tunnels, brood cells, food storages (honey and pollen cells), cerumen and batumen
layers (Sakagami et al. 1983; Starr & Sakagami 1987; Michener 2007; Boongird 2011;
Erniwati 2013).
Sulawesi island has a high degree of endemicism of plants and animals. Honey bee,
Apis nigrocincta is endemic species in Sulawesi (Hadisoesilo 2001; Engel 2012). The other
endemic of stingless bee species in Sulawesi is Geniotrigona incisa that found in Central
Sulawesi forest in the altitude more than 900 m above sea level (Sakagami & Inoue 1989).
Central Sulawesi has different land use, such as plantation, agriculture, secondary forest,
primary forest, and settlement areas that favorable for nesting and foraging sites of stingless
bees. Until now, bee keeping of stingless bees in Sulawesi is very limited. People prefer to
keep honey bee, Apis cerana for honey production rather than stingless bees. The nesting
sites of stingless bees in the settlement areas in Central Sulawesi were described in this study.
Material and methods
Study Sites
The study was conducted from July 2015 to January 2016 in Watumaeta, Lore Utara Sub-
distric, Poso Regency (01o23'57,1" S, 120o19'30,0" E; 1.200 m asl), Pakuli, Gumbasa Sub-
distric, Sigi Regency (01o13'51,0" S, 119o56'43,2" E; 130 m asl), and Purwosari, Torue Sub-
distric, Parigi Moutong Regency (00o58'31,0" S, 120o19'04,8" E; 10 m asl). Observations of
stingless bees were conducted in settlement areas in Watumaeta village (about 20.000 ha),
Pakuli village (about 502 ha) and Purwosari village (about 94 ha), respectively.
Observation of Stingless Bee Nesting Sites
Observations of stingless bee nesting sites were carried out in 90 days, consist of 30 days in
Watumaeta (July 2015), 30 days in Pakuli (August 2015), and 30 days in Purwosari
(September 2015) using purposive sampling method (Tongco 2007). The nest characters
observed were location of nesting sites, nest-entrance measurements (length, diameter, height
from ground surface), shapes (funnel, mount-like, or round-ringed), colour (brown, black, or
light brown), and rigidity (soft or hard) (Kelly et al. 2014).
Collection, Preservation, and Identification of Stingless Bee specimens
Collection of workers stingless bee of each colony were conducted by using sweep net. The
specimens collected (10 individuals of each colony) were put into a bottle with 90% ethanol.
Stingless bee specimens were preserved in the laboratory of Entomology, Zoology Division,
Research Center for Biology, Indonesian Institute of Sciences (LIPI), Bogor, Indonesia. The
stingless bee specimens were identified based on Sakagami (1978), Sakagami & Inoue
(1987), Dollin et al. (1997), Sakagami et al. (1990), and Smith (2012). All specimens were
also verified with specimen collections of the Museum Zoologicum Bogoriense (MZB),
Bogor, Indonesia.
Data Analysis
Statistical analysis of one-way ANOVA and Tukey’s test were used to compare the diameter,
length, and height of the nest entrance from the ground surface among three species of
Journal of Insect Biodiversity 5(10): 1-9, 2017 http://www.insectbiodiversity.org
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Tetragonula. All the analysis used software Paleontological Statistics (PAST) ver. 1.89
(Hammer et al., 2009).
Results
Species and Nesting Sites of Stingless Bees
A total of 168 colonies which belong to four species of stingless bees were found in
this study. Three, ninety three, and seventy two colonies were found in Watumaeta, Pakuli,
and Purwosari, respectively. Four species of stingless bee were identified, namely
Tetragonula fuscobalteata, T. laeviceps, T. biroi, and T. sapiens. Two stingless bee species
were recorded in each vilage. Tetragonula fuscobalteata and T. sapiens were found in Pakuli,
T. laeviceps and T. biroi were found in Watumaeta, while T. fuscobalteata and T. biroi were
collected in Purwosari.
The workers of each bee species have varied morphological characteristics (Fig 1).
Tetragonula fuscobalteata has 3.47-3.54 mm body length, blackish-brown of body color,
mesoscutum with six longitudinal hair bands, each band separated by five conspicuous
glabrous areas (Fig. 1A). Tetragonula laeviceps has 3.40-3.43 mm body length, black body
color, metasoma with brown color, first and second tergum are pale, while fourth and fifth
tergum are dark. Mesoscutum is hairy, vertex is blackish and not banded, and anterior hind
tibia is hairy (Fig. 1B). Workers of T. biroi had 4.00 - 4,17 mm body length, body color
predominantly black, abdomen is brownish, clypeus and tegula are dark, mesoscutum and
mesoscutellum with black hairs, malar space clearly separate the mandible and eyes (Fig.
1C). Workers of T. sapiens had 3.69-3.80 mm body length, black body color, metasoma is
brown, first and second tergum are blackish-brown, and blackish in the apical. Mesoscutum
consisted of glabrous areas and anterior hind tibia with dark to blackish-brown hairs, while in
the posterior is brownish-yellow (Fig. 1D).
The highest number of colonies found was T. fuscobalteata (155 colonies), followed
by T. biroi (7 colonies), T. sapiens (5 colonies), and T. laeviceps (1 colony). The nesting sites
of Tetragonula were found in the parts of the houses, such as stone, brick, wooden, bamboo,
and iron cavities. The highest number of T. fuscobalteata colonies was found in wooden wall
(74 colonies), followed by stone cavity (40 colonies), brick wall (31 colonies), bamboo (6
colonies), and iron cavity (4 colonies). The nesting sites of T. biroi were found in the wooden
wall (3 colonies), stone cavity (2 colonies), and brick wall (2 colonies). While, nesting sites
of T. sapiens were found in stone cavity (5 colonies) and nesting site of T. laeviceps was
found in wooden wall (1 colony) (Table 1).
Characteristics of nest entrance
Characteristics of nest entrance are properties that can be used to identify species of
stingless bees. In average, the diameter and length of nest entrance are 1.86 + 1.40 cm and
2.23 + 2.52 cm in T. biroi, 2.18 + 1.27 cm and 1.88 + 0.95 cm in T. sapiens, and 1.24 + 0.49
cm and 3.70 + 3.88 cm in T. fuscobalteata. The diameter and the height of nest entrance of T.
sapiens and T. fuscobalteata were significanly different (p=0.002 and p= 0.009), but the
length of nest entrance among three species of Tetragonula was not significanly different
(p>0.05) (Table 2). Unfortunately, there was no data available of the diameter and length of
nest entrance of T. laeviceps, because the entrance was accidentally destroyed. The highest
position of nest entrance from the ground surface occured in T. laeviceps (321.00 cm),
Nesting sites of stingless bees Suriawanto et al.
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Figure 1. Worker adults of Tetragonula species. A, Tetragonula fuscobalteata; B, T. laeviceps; C,
T. biroi; D, T. sapiens.
Tabel 1. Number of colony of stingless bees found in different nesting sites in Central Sulawesi
Species
Number of colony found (colony)
Brick wall
Stone
cavity
Bamboo
Iron cavity
Wooden
wall
Total
Percentage (%)
Tetragonula biroi
2
2
0
0
3
7
4.17
Tetragonula fuscobalteata
31
40
6
4
74
155
92.26
Tetragonula sapiens
0
5
0
0
0
5
2.98
Tetragonula laeviceps
0
0
0
0
1
1
0.59
Total
33
47
6
4
78
168
100
followed by T. fuscobalteata (116.90 + 67.54 cm), T. biroi (56.64 + 38.08 cm), and T.
sapiens (1.88 + 4.71 cm) (Table 2).
The shape, color, and rigidity of nest entrance varied in each species of Tetragonula.
Characteristics of nest entrance of T. biroi are a funnel shape, mount-like, and round-ringed,
color are black and light-brown, and soft rigidity. Nest entrance of T. sapiens is characterized
by mount-like shape, round-ringed, black in color, and soft rigidity. Funnel shape, black and
light-brown in color, and soft rigidity are characters of nest entrance of T. fuscobalteata,
while, brown in color and hard rigidity are characters of nest entrance of T. laeviceps (Table
2).
Journal of Insect Biodiversity 5(10): 1-9, 2017 http://www.insectbiodiversity.org
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Table 2. Size of nest entrance: diameter, length, and height of the entrance from the ground surface of
four species of Tetragonula.
Species
Diameter (cm)
Length (cm)
Height from ground surface
(cm)
Shape
Color
Rigi
dity
Mean
Range
St.dev
Mea
n
Range
St.dev
Mean
Range
St.dev
T. biroi (n=7)
1.86ab
0.1-3.6
1.40
2.23a
0.1-7.0
2.52
56.64a
b
20-130
38.08
F, R,
M
Bl,
Lb
S
T. sapiens (n=5)
2.18a
0.9-4.2
1.27
1.88a
0.5-3.0
0.95
23.8a
18-31
4.71
M, R
Bl
S
T. fuscobalteata (n=156)
1.24b
0.1-3.6
0.49
3.7a
0.1-25
3.88
116.9b
0.95-300
67.54
F
Br,
Lb
S
T. laeviceps (n=1)
na
na
na
na
na
na
321
na
na
na
Br
H
Note: St.dev= standart deviation, F=funnel (tube-like), M=mount-like, R=round-ringed, Br=brown, Bl=black, Lb=light
brown, S=soft, H=hard, na=data not available. Different letter(s) in the same column indicated significant difference
among means based Tukey’s test.
Figure 2. Nest entrance of Tetragonula species. A, T. fuscobalteata; B, T. laeviceps; C, T. biroi; D,
T. sapiens.
Nesting sites of stingless bees Suriawanto et al.
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Discussions
All species stingless bees found in this study belong to the genus Tetragonula. The
genus is small body size (Sakagami 1978; Smith 2012) and distributed in wide range in the
world. Genus Tetragonula has been reported in the Asia continental and Sri Lanka (Sakagami
1978), Indian subcontinent (Rasmussen 2013), Southeast Asia (Sakagami & Inoue 1985),
Thailand (Schwarz 1939; Sakagami et al. 1985; Michener & Boongird 2004; Klakasikorn et
al. 2005; Boontop et al. 2008; Boongird 2011), Vietnam (Chinh et al. 2005), Peninsular
Malaysia (Rasmussen & Michener 2010; Salim et al. 2012), Philippines (Starr & Sakagami
1987), and Indonesia (Erniwati 2013). In Indonesia, genus Tetragonula has been reported in
Sumatra (Sakagami et al. 1990), Samarinda-East Kalimantan (Syafrizal et al. 2014), Sulawesi
(Schwarz 1939), Maluku and Irian Jaya (Dollin et al. 1997).
Four species, T. fuscobalteata, T. laeviceps, T. biroi and T. sapiens were collected in
the study and the most abundant colony was T. fuscobalteata, followed by T. biroi, T.
sapiens, and T. laeviceps. Previous study showed that in Sulawesi islands were reported three
species of stingless bee, namely T. fuscobalteata (Schwarz 1939), Geniotrigona insica as
endemic species in Sulawesi (Sakagami & Inoue 1989), and T. laeviceps (Erniwati 2013).
Tetragonula biroi had been reported in the Philippines (Oceanic Islands) and New Guinea
(Starr & Sakagami 1987; Dollin et al. 1997). While, T. sapiens had been reported in
Indonesia (Maluku), Philippines, New Guinea, and Australia (Dollin et al. 1997; Rasmussen
2008; Smith 2012). Both species, T. biroi and T. sapiens found in this study were the new
record from Sulawesi islands. The common species found in Sulawesi is T. fuscobalteata.
The species was distributed in the Southeast Asia (Thailand, Cambodia, peninsular Malaysia,
Borneo, Sumatra, Sulawesi, Palau Island, Caroline Island, and Philippines (Palawan and
Oceanic Islands) (Rasmussen 2008; Smith 2012).
In Sulawesi, nest of Tetragonula commonly were found in the part of the houses, such
as wooden wall, brick, and stone cavities. Nesting sites of Tetragonula in the settlement areas
had been reported, such as T. laeviceps, T. minangkabau (Sakagami et al. 1983; Erniwati
2013), T. fuscobalteata, and T. sapiens (Starr & Sakagami 1987). Nest of Tetragonula also
were found in forest areas, such as dry dipterocarp forest, upper mixed deciduous forest,
lower mixed deciduous forest, and dry evergreen forest in Thailand (Boontop et al. 2008),
dipterocarp reserve forest in Peninsular Malaysia (Salim et al. 2012), and Lempake Education
Forest in east Kalimantan (Syafrizal et al. 2014). Their nests also are adaptable in open
forests and grasslands (Inoue et al. 1984). These species often built their nest in the hollow
trunk as well as on termite and ants nests (Michener 1974; Sakagami 1982). Results showed
that nests of T. fuscobalteata were highest in the wooden wall (74 colonies) than in the stone
cavity, brick wall, bamboo, and iron cavity. While, all nests of T. sapiens found (5 colonies)
in stone cavity and one colony of T. laeviceps was found in wooden wall. The nesting sites of
T. biroi were found in the wooden wall, stone cavities, and brick walls. In the Philippines,
Starr & Sakagami (1987) reported 26 colonies of T. fuscobalteta and 7 colonies of T. sapiens
nest in bamboo cavities. As reported by Sakagami et al. (1983), nests of T. laeviceps can be
found in some parts of houses and the nests also were found in hollow of tree with diameter
30-50 cm (Chinh et al. 2005; Kelly et al. 2014). In Karnataka, India, T. iridipennis build its
nest around the manmade structures, such as residential, educational areas, and road sides
parks that made by different substratum (brick walls, rock crevices, pillars, metallic sheath,
and water pipes) (Pavithra et al. 2013).
The shape, color and rigidity of nest entrance of Tetragonula varied between species
(Fig. 2). Nest entrance properties of stingless bees related to many factors, such as age of
nest, microclimate, predators, parasites, and symbionts (Roubik 2006). The size of nest
Journal of Insect Biodiversity 5(10): 1-9, 2017 http://www.insectbiodiversity.org
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entrance of stingles bees also varied (Kelly et al. 2014). Starr & Sakagami (1987) stated that
the nest entrance of T. sapiens and T. fuscobalteata are tube-like with many variations of
texture, diameter, and length. Variation of nest entrances related to defense and foraging
activities of stingless bees (Biesmeijer et al. 2005).
Acknowledgements
We are grateful to Chief of Watumaeta, Pakuli, and Purwosari villages for giving us
to conduct the study and Rizka, Iwan, and Rendy as field assistants. Thanks to all staffs at
the Laboratory of Animal Biosystematics and Ecology, Department of Biology, Faculty of
Mathematics and Natural Sciences, Bogor Agricultural University and the researchers and
staffs at the Laboratory of Entomology, Zoology Division, Research Center for Biology
(LIPI) for giving assistance in identification of stingless bee specimens. Special thanks to Dr.
Clause Rasmussen and Anne E. Dollin, PhD for valuable references.
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Correspondence: Tri Atmowidi, e-mail: atmowidi@gmail.com
Received: 05.04.2017 Accepted: 05.06.2017 Published: 13.06.2017
Cite paper: Suriawanto N., Atmowidi T. & Kahono S. 2017. Nesting sites characteristics of stingless bees
(Hymenoptera: Apidae) in Central Sulawesi, Indonesia. Journal of Insect Biodiversity 5(10): 1–9.
http://dx.doi.org/10.12976/jib/2017.5.10 http://www.insectbiodiversity.org
