Apidologie * INRA, DIB and Springer-Verlag, France, 2012 DOI: 10.1007/s13592-012-0152-y
Original article
Trap-nests for stingless bees (Hymenoptera, Meliponini) Ricardo Caliari OLIVEIRA1 , Cristiano MENEZES2,3 , Ademilson Espencer Egea SOARES4 , Vera Lúcia Imperatriz FONSECA5 1
Erasmus Mundus Master Programme in Evolutionary Biology, Ludwig-Maximilians-Universität München, Germany and Rijksuniversiteit Groningen, The Netherlands 2 Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, São Paulo, SP, Brazil 3 Embrapa Amazônia Oriental, Belém, PA, Brazil 4 Departamento de Genética da Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, São Paulo, SP, Brazil 5 Universidade Federal Rural do Semiárido, Mossoró, RN, Brazil Received 8 April 2012 – Revised 27 May 2012 – Accepted 5 June 2012
Abstract – Most stingless bee species build their nests inside tree hollows. In this paper, we present trap-nest containers which simulate nesting cavities so as to attract swarms of stingless bees. Although regularly used by stingless bee beekeepers in Brazil, this technique to obtain new colonies has not yet been systematically studied. We used two different types of trap-nests (plastic and cardboard) of four different sizes (0.5, 1.0, 2.0, and 3.0 L) containing propolis extract and wax. Over a period of 2 years, 61 swarms of nine different stingless bee species were attracted to the trap-nests. Most swarms chose the largest container (3 L); swarms were collected mostly in springtime (October–December). The plastic containers were more successfully occupied than others by stingless bee swarms. Trap-nests are a viable tool for stingless beekeepers, researchers and conservation biologists to obtain and study stingless bee colonies. stingless bees / trap-nest / swarming / Meliponini
1. INTRODUCTION The majority of stingless bee species (Hymenoptera, Meliponini) build their nests inside preexisting hollows, usually in tree trunks, branches or ground cavities (Roubik 1983, 2006; Nogueira-Neto 1997; Eltz et al. 2003). Few species can build their own cavity inside termite nests (Camargo and Pedro 2003), and some can build exposed nests on walls or tree branches (Roubik 2006, Rasmussen and Camargo 2008). Nest architecture, entrance shape and population size are very diverse and usually characteristic Corresponding author: R.C. Oliveira, ricardo.oliveira@evobio.eu Manuscript editor: James Nieh
for each species (Roubik 2006; Rasmussen and Camargo 2008). In highly eusocial bees (honey bees and stingless bees), the foundation of new colonies occurs through swarming. Unlike honeybees, the swarming process in stingless bees is gradual and occurs in rather small numbers. During the swarm process in stingless bees, workers from the mother nest choose a new cavity and start to prepare it by cleaning and bringing nest material from the mother nest. They build the colony entrance (which is usually species specific) and food pots, and some workers start to forage while others remain visiting the mother nest. When the new nest is ready, more workers fly together with a virgin queen, which will perform the nuptial
R.C. Oliveira et al.
flight soon after arriving at the new nest. The contact between mother and daughter nest can last from few days to several months, according to resources availability and the stingless bee species (Nogueira-Neto 1954; Juliani 1967; Terada 1972; Wille and Orozco 1975; Inoue et al. 1984; Engels and Imperatriz-Fonseca 1990; van Veen and Sommeijer 2000). It has been predicted that many stingless bee species need to swarm only once in 20 years to maintain their populations (Slaa 2006). Factors like the colony capacity to generate virgin queens and workers for the swarm are very important in the swarming process (Michener 1974). Although the swarming process has been described several times, many aspects remain unknown; for example, how and why do they choose the new nesting site. Stingless bee beekeepers have observed that stingless bees tend to establish new nests in old hives which were previously occupied by other colonies. Based on these observations, they started to lay out empty containers containing propolis and wax around their meliponaries, in order to attract the swarms to these “traps”. Many beekeepers report success in obtaining new colonies in this manner. Such “trap-nests” can be made from different materials (such as wood, plywood, cardboard or plastic) and are often baited with substances attractive to bees such as propolis, honey and/or wax. The use of trap-nests is the only legal method of collecting stingless bee colonies in the field in Brazil (CONAMA 2004). Moreover, collecting wild nests is costly in terms of both time and labor. Although some people are successful in collecting established colonies from trees without apparent loss (Colleto-Silva 2005), this technique is not ideal as it may result in the death of the tree and has high rates of colony loss due to damage to the colony during transfer to a hive. Although the use of trap-nests by stingless bee beekeepers is becoming more common, this technique has only been studied a few times before, mainly looking to see whether the trapnests were occupied or not by stingless bees (Inoue et al. 1993; Malkowski et al. 2006; Alvarenga 2008). Understanding how the trap-nests work is
an important step to improving success rates and making this technique a viable tool for beekeeping, research and conservation of stingless bees. The objectives of this study were to verify the effectiveness of the use of trap-nests for stingless bees in terms of: (1) which stingless bee species are attracted to trap-nests; (2) the ideal volume for each species; (3) the best season to attract swarms; (4) whether one material is preferable to another; and (5) what limitations, if any, this technique suffers from. We also discuss the possibility of using trap-nests in stingless bee conservation efforts.
2. MATERIALS AND METHODS 2.1. Trap-nests Plastic bottles and cardboard boxes with four different volumes were used to build the trap-nests (0.5, 1.0, 2.0, and 3.0 L). These two materials were chosen because they are relatively easy to obtain and cheap (compared to wooden boxes, for example), facilitating the use of hundreds of them and decreasing the possibility of robbery. Each trap-nest consists of a set of four different volumes, made either of plastic or cardboard (Figure 1). A solution of propolis was made by diluting batumen and cerumen of different stingless bee species (Melipona quadrifasciata, Tetragonisca angustula, Frieseomellita varia, and Scaptotrigona sp.) in alcohol. This solution was then sprayed inside the containers. A PVC elbow (20 mm) coated in Apis mellifera wax and propolis solution was inserted in the middle section of the container to act as an entrance tube. Plastic containers were black to prevent light shining through the walls, and the cardboard trap-nests were wrapped with black plastic bags to protect them from rain. Every 6 months, more propolis solution was spread at the entrance and the damaged trap-nests were refurbished.
2.2. Study site and experimental setup The study was carried at University of São Paulo (USP), Ribeirão Preto campus (21°09′50″S, 47°51′ 30″W) and at Aretuzina Farm in São Simão (21°26′ 18″S, 47° 34′45″W), about 40 km from the campus. These areas show a relative high density of stingless bee nests, as meliponaries stocked with several species are kept in both of them. The sites are “green
Trap-nests for stingless bees (Hymenoptera, Meliponini)
a
b
Figure 1. Trap-nests installed on tree trunks: a plastic trap-nest, b cardboard trap-nest. islands” surrounded by urban areas or agricultural fields. Currently, there are 21 stingless bee species among native and introduced at Ribeirão Preto campus and approximately 10 more are kept in hives in the scientific meliponary (Freitas 2001; Oliveira, unpublished data). The trap-nests were installed on tree trunks ca. 1.5 m in height. Their positions at each site was randomly chosen. The study was carried out from April 2007 to April 2009. In the first year, we used only plastic trapnests (200 groups of plastic trap-nests at Ribeirão Preto campus and 100 groups at Aretuzina Farm). In the second year, cardboard trap-nests were added at both study sites (200 groups of cardboard trap-nests at Ribeirão Preto campus and 100 groups at Aretuzina Farm). Nests on the Ribeirão Preto campus were inspected every 15 days, so as to obtain a better overview about seasonality of swarming behavior, while trap-nests at Aretuzina Farm were inspected every 3 months. An experiment to test the attractiveness of trap-nests was also carried out after the study period. In this experiment, trap-nests made from Styrofoam were also used. Twenty groups of 3-L containers made of plastic, cardboard and Styrofoam were made. The cardboard and the Styrofoam trap-nests were wrapped with a black bag to avoid influence of color on nest choice by swarms. The groups were installed at the same height (about 2.0 m) at the Ribeirão Preto campus between August and December 2009.
2.3. Statistical analysis As most of the collected data was categorical, e.g., species, volume, and season, we used Chi-square
analyses with Monte Carlo permutation tests (10,000 random permutations) to evaluate whether the observed frequencies were different from random. A Pearson test was used to measure the correlation between the average monthly temperature and the number of swarms to the trap-nests. Statistical analysis was carried out using R 2.11.1 (R Development Core Team 2010).
3. RESULTS 3.1. Species attractiveness In the 2 years of experiments, 61 stingless bee swarms of nine different species were attracted to the trap-nests (10.2 % of trap-nests occupation rate): Tetragonisca angustula (n=38); Tetragona clavipes (n=6); Scaptotrigona bipunctata (n=6); Frieseomelitta varia (n=3); Frieseomelitta silvestrii (n=1); Friesella schrottkyi (n=1); Nannotrigona testaceicornis (n=2); Plebeia remota (n=1); and Plebeia droryana (n=3). On Aretuzina farm , six swarms of Melipona quadrifasciata were attracted to the trap-nests but none of them successfully settled. One of these swarms was observed from the beginning of the swarming process. During the first 2 days, the bees built the entrance, brought building materials and food from the mother source, and built food pots and involucrum. On the third day, we observed very low activity and a few dead bees being thrown
R.C. Oliveira et al.
from the trap-nest. We opened the container and most bees were dead inside the plastic container because of excessive moisture. There were 245 workers and one virgin queen, including a few worker bees which were still alive. This is the first time that the number of bees involved in a stingless bee swarm has been estimated. Although we may have lost a few workers, we counted almost all of them, because bees that entered the container were not able to leave it, dying inside the trap-nest. When only the plastic trap-nests were used (April 2007 to April 2008), 48 stingless bee swarms were attracted (38 at the Ribeirão Preto campus and 10 at Aretuzina farm). During this first year, 24 other swarms were attracted to old empty hives in Aretuzina farm. The empty hives were previously used by stingless bees and were spread at the studied area by the farm owner. In the second year (April 2008 to April 2009), when cardboard trap-nests were used, 12 swarms were attracted at the Ribeirão Preto campus and only 1 at Aretuzina farm (no swarms in empty hives were observed). Some stingless bee species were attracted only to plastic trap-nests (Table I), others were only attracted to cardboard trap-nests (Table II) and only T. angustula was attracted to both materials, but we cannot take conclusions about material preferences from this experiment because of low sample size to most species in the different areas. Table I. Number of stingless bee swarms attracted to the plastic trap-nest during the first year each area. Species
Plastic
S. bipunctata T. clavipes F. varia F. silvestrii T. angustula P. droryana Total
6 RP 6 RP 3 RP 1 RP 22 RP; 7 SS 3 SS 48
RP Ribeirão Preto campus, SS Aretuzina farm, São Simão
Table II. Number of stingless bee swarms attracted to the cardboard trap-nests during the second year for each area. Species
Cardboard
T. angustula N. testaceicornis F. schrottkyi P. remota Total
9 RP 1 RP; 1 SS 1 RP 1 RP 13
RP Ribeirão Preto campus, SS Aretuzina farm, São Simão
3.2. Container volume It is possible to observe that some stingless bee species were attracted to small volumes (F. silvestrii and N. testaceicornis), others to larger volumes (S. bipunctata, T. clavipes, F. varia, F.schrottkyi and P. remota) while a few apparently showed no preference (T. angustula and P. droryana). Also, seven out of the nine species were observed occupying the large trap-nests (2 and 3 L), while only two were found only in the smaller volumes (0.5 and 1 L) (Table III). Therefore, stingless bees generally preferred to move into larger trap-nests (χ 2 = 20.11 P<0.0005, n=61). 3.3. Seasonality In the Ribeirão Preto campus, where regular observations were made, the monthly frequency of swarms was distributed non-randomly during the first experimental year (χ 2 = 35.26; P < 0,0005; n = 38) and most of swarming attempts occurred from December to April. These 2 months accounted for 40 % of the swarms, with 20 % in each month (Figure 2). It was possible to observe a trend in the swarming process towards the spring season (ending of dry and beginning of wet season) in the Ribeirão Preto campus in both years (n=18), although not significant (χ2 =7.12; P>0.05; n=50). There was a significant difference in the swarms frequency during the different seasons in the first year (χ2 =10.42; P<0.05; n=38) but not in the second, likely due to the
Trap-nests for stingless bees (Hymenoptera, Meliponini)
Table III. Number of stingless bee swarms moving into trap-nests for each species, container volume and material. Species
Volume 0.5 L
S. bipunctata T. clavipes T. angustula F. varia F. silvestrii N. testaceicornis F. schrottkyi P. droryana P. remota Total
1P
Total 1.0 L
2.0 L
3.0 L
13 P; 2 C
2P 3P 7 P; 2 C
4 3 8 3
P P P; 5 C P
1P 1 P; 1 C 1P
1P
2
19
14
1C 1P 1C 26
6 6 38 3 1 2 1 3 1 61
P Plastic trap-nests, C cardboard trap-nests
overall low number of swarms (Ď&#x2021;2 = 3.33; P>0.05; n=12) (Figure 3). During the first year, there was a significant correlation (rs =0.8; P<0.005) between monthly average temperature and number of swarms. Again, no significant pattern emerged in the second year (rs =â&#x20AC;&#x201C;0.39; P>0.005). For T. angustula (the most abundant stingless bee species occupying the trap-nests in the
experiments), swarming does not occur randomly throughout the year. Most swarming attempts occurred during months that correspond to the ending of the dry and beginning of the wet season (spring and summer) in the southern hemisphere (n=25), with only six swarming events occurring on the dry season (autumn and winter) (Ď&#x2021;2 =13.25; P<0.005; n=31). For T. clavipes, the more favorable season is autumn
Figure 2. Number of installed swarms on plastic trap-nests (bars) from April 2007 to March 2008 for each month, with average temperature (black line).
R.C. Oliveira et al.
Figure 3. Number of installed swarms on cardboard trap-nests (bars) from April 2008 to March 2009 for each month, with average temperature (black line).
(χ2 =18; P<0.005; n=6), and for S. bipunctata we found no annual pattern for swarming behavior (χ2 =3.33; P>0.05; n=6). There were not enough data for other species to allow further analysis. 3.4. Material attractiveness Plastic trap-nests showed to be the most attractive for stingless bees since eight swarms were attracted to them, as compared to one swarm to Styrofoam and none to cardboard trap-nests (χ2 =12.67; P<0.005). Eight of those swarms were T. angustula and one F. varia. 3.5. Limitations of trap-nests Some factors, such as direct sunlight, excessive moisture inside the containers, and use by other animals, might have influenced the success rate of swarm attraction to the trap-nests. Spiders and ants were the most common competitors for the nesting sites occupying 19 % of plastic trap-nests and 5 % of cardboard trap-nests. Trap-nests were also occasionally occupied used by a social wasp (Polybia occidentalis, Hymenoptera, Vespidae) (Table IV). Nests occupied by other animals
were never occupied by stingless bees. However, there was one exception: a F. schrottkyi colony shared a trap-nest with a Camponotus sp. ant colony.
4. DISCUSSION Different trap-nests methodologies have been successfully used to attract stingless bee swarms. Inoue et al. (1993) used bamboo and wooden boxes of ca. 2 L as trap-nests and succeeded in attracting one stingless bee species (Trigona (Tetragonula) minangkabau) out of 24 which swarmed in the area, resulting in 6 % of the traps being occupied. In a different study site in Ribeirão Preto, 11.46 % of the trap-nests were occupied: 3 by Scaptotrigona sp. and 8 by T. angustula using plastic trap-nests identical to the ones used in this experiment (Alvarenga 2008). In southern Brazil, (Malkowski et al. 2006) obtained 22 % occupation (30 colonies) by T. angustula using a similar method, and Witter et al. (2007) related that Plebeia nigriceps used a wooden trap-nest. Trap-nests are efficient in a range of different areas and stingless bee species. In this study, we showed that at least nine different stingless bee species
Trap-nests for stingless bees (Hymenoptera, Meliponini)
Table IV. Trap-nests occupied by animals other than stingless bees. Occupant
n
Total percentage
Spiders Ants Wasps Spiders and ants Wasps and ants Total
20 C; 12 P 27 C; 21 P 4C 3 C; 5 P 2C 94
8 12 1 2 0.5 23.5
P Plastic trap-nests, C cardboard trap-nests
colonized trap-nests and give some hints about preferential season, volume and material. Nine out of 21 species found on the University campus were attracted to the trapnests. Four of them build their nests at 1 m height on average (F. schrottkyi, N. testaceicornis, S. bipunctata and T. angustula), two at about 3 m (F. varia and T. clavipes) and for the other two there are no data (F. silvestrii and P. remota) (Freitas 2001). The other species build their nests between 2 and 10 m high, which may have influenced the diversity of species attracted to trap-nests since they were installed at approximately 1.5 m high. Another factor that may influence the attractiveness of trap-nests to particular species is the nesting habits of the species. Out of 19 species sampled by Freitas (2001) at RiberĂŁo Preto campus, 5 build their nests in the ground, on walls, trees or inside termite nests (Trigona fuscipenis, Trigona hyalinata, Trigona spinipes, Partamona helleri and Scaura latitarsis) (Wille and Michener 1973; Michener 1974; Freitas 2001). These species will most likely not be attracted to trap-nests. Natural stingless bee nest sizes vary widely amongst different species. Nests of some species are smaller than 0.5 L, while others can be over 300 L (Inoue et al. 1993). It has been observed that stingless bee species are limited by a minimum volume and diameter cavities but not by a maximum (Hubbell and Johnson 1977; Eltz et al. 2003). Honey bees also prefer nesting sites with larger volumes (Seeley and Buhrman 2001). In this study, we also observed a trend where the
stingless bees settled in the larger volumes. In general, larger volumes can be considered more efficient, as they attract a larger number of swarms and species. Trap-nests of 2 and 3 L attracted 40 swarms of seven different species, as compared to 21 swarms of four different species for 0.5- and 1L trap-nests. Species with small body size usually build small nests (Hubbell and Johnson 1977), such as F.schrottkyi, P. droryana and T. angustula, which occupied both small and large volume trapnests. On the other hand, species with large body size would generally build large nests (Hubbell and Johnson 1977): S. bipunctata and F. varia only occupied large trap-nests (2.0 and 3.0 L). Although N. testaceicornis and F. silvestrii were only found in the small volume trap-nests, based on our data, we predict that they would also be able to settle in a larger volume trap-nest. Swarming in social bees usually occurs during the reproductive seasons, which are periods with favorable environmental conditions, i.e. food availability and temperature (Winston 1991). Resources availability is an important factor in colony reproduction because during this process about 30 % of mother colony will move to the daughter colony, producing 20â&#x20AC;&#x201C;50 % more brood cells and about double the amounts of pollen and honey pots (Inoue et al. 1984; van Veen and Sommeijer 2000). Slaa (2006) observed that the foundation of new stingless bee colonies was more frequently during the dry season in the lowland dry tropics. In our study, there was a trend towards swarming events occuring in the end of dry season (spring) (18 out of 50), and in the first year, the average temperature and the number of swarms in the trap-nests were positively correlated, showing that there was an increase in the number of swarms during the warmer seasons, i.e. spring and summer. Therefore, we recommend placing trap-nests in early spring. During the second year, lower swarming rates were observed both at RibeirĂŁo Preto campus and Aretuzina farm, not only into the trap-nests but also into the old wooden hives, to which no swarming was observed. This difference between the first year and the second year of experiment may have been influenced by many factors such as weather conditions and nesting site availability (Inoue et al. 1993; Roubik and Wolda 2001).
R.C. Oliveira et al.
Also, it has been shown that most colonies are not able to reproduce in two consecutive years (Slaa 2006). This suggests to us that the colonies were suffering from a lack in nesting site availability before the first year of experiments and, once the first trap-nests were settled, this demand was fulfilled and prevented swarming in the next year. Moreover, the different materials used to build the trap-nests may have had an influence on the total number of swarming in the trap-nests. In the material attractiveness experiment, we observed that plastic trap-nests were more attractive to stingless bee swarms (n=8) than cardboard (n=0) or Styrofoam (n=1). However, the lower swarming rates were generally observed during the second year of experiments and not only in the cardboard trap-nests. Trap-nests were also occupied by other animals such as ants, spiders, and wasps. In Sumatra, Indonesia, ants occupied 50 % of the trap-nests (Inoue et al. 1993). Ants were also the major competitors for nesting sites in our study (12 %), showing that these animals compete for the nesting sites with stingless bees. In only one instance, a colony swarmed into an occupied trap-nest. On that occasion, F. schrottkyi built its nest in a nest occupied by an ant species (Camponotus spp.). Nannotrigona testaceicornis is known to build nests associated with Camponotus species (Camargo and Pedro 2008), but this type of association has never been described before for F. schrottkyi. Most stingless bees build their nests in trees (Roubik 1983, 2006; Nogueira-Neto 1997; Eltz et al. 2003). Deforestation is therefore a serious threat to the conservation of stingless bee populations. It has been shown that nonfragmented habitats are required to maintain stingless bee communities (Brosi et al. 2008). From 1988 to 2010, deforestation in the Amazon rainforest proceeded on average at 16,773 km2/year (INPE 2011) and the Atlantic rainforest has already lost ca. 90 % of its natural vegetation in about 200 years of exploitation (Ribeiro et al. 2009). Stingless bees appear to suffer from lack of suitable nesting sites, and deforestation exacerbates this problem. However, experimental addition of nesting sites can
cause an increase in solitary bees (SteffanDewenter and Schiele 2008) as well as stingless bee populations (Inoue et al. 1984). These studies were corroborated by our results showing that the trap-nest can be a useful tool to help in the conservation of natural stingless bee populations in the future.
ACKNOWLEDGEMENTS This work was financed by the São Paulo Research Foundation (FAPESP - 04/15801-0) and National Council for Scientific and Technological Development (CNPq - 112818/2007-2 for RCO). We are thankful to Ayrton Neto, Denise Alves and Tomer Czaczkes for the suggestions on the manuscript, Rafael Silva and Ayrton Neto for helping in the field work. We thank also to Klaus Hartfelder, James Nieh and the anonymous referees. Finally, we would like to thank Dr. Paulo Nogueira Neto, in particular, for allowing us to work in the Aretuzina farm and for all his suggestions. and we would like to dedicate this paper to him for the occasion of his ninetieth anniversary. Nids-pièges pour abeilles sans aiguillon (Hymenoptera, Meliponini) Abeille sans aiguillon / piègeage / essaimage / Meliponini
Fallennester für Stachellose Bienen (Hymenoptera, Meliponini) Stachellose Bienen / Fallennest / Schwärmen / Meliponini
REFERENCES Alvarenga, P.E.F., (2008) Levantamento da fauna de abelhas (Hymenoptera, Apidae, Meliponina) na mata Santa Tereza, estação ecológica de Ribeirão Preto-SP, e limitantes da densidade de seus ninhos. Master thesis, FFCLRP-USP. Brosi, B.J., Daily, G.C., Shih, T.M., Oviedo, F., Duran, G. (2008) The effects of forest fragmentation on bee communities in tropical countryside. J. Appl. Ecol. 45, 773–783 Camargo, J.M.F., Pedro, S.R.M. (2003) Neotropical Meliponini: The genus Partamona Schwarz, 1939 (Hymenoptera, Apidae, Apinae) - bionomy and biogeography. Rev. Bras. Entomol. 47, 311–372
Trap-nests for stingless bees (Hymenoptera, Meliponini)
Camargo, J.M.F., Pedro, S. R. M., (2008) Meliponini Lepeletier, 1836. In Moure, J. S., Urban, D. & Melo, G. A. R. (Orgs), Catalogue of Bees (Hymenoptera, Apoidea), in the Neotropical Region – [online] http://www. moure.cria.org.br/catalogue. Accessed on 26/10/2011.
Nogueira-Neto, P. (1954) Notas bionômicas sobre Meliponíneos III- Sobre a enxameagem (Hymenoptera- Apoidea). Arq Mus Nac 42, 419–452
Colleto-Silva, A. (2005) Captura de enxames de abelhas sem ferrão (Hymenoptera, Apidae, Meliponinae) sem destruição de árvores. Acta Amaz 35(3), 383– 388
Rasmussen, C., Camargo, J.M.F. (2008) A molecular phylogeny and the evolution of nest architecture and behavior in Trigona s.s. (Hymenoptera: Apidae: Meliponini). Apidologie 39, 102–118
Conama, (2004) ResoluçãoConama nº 346, de 16 de agosto de 2004 Publicada no DOU no 158, de 17 de agosto de 2004, Seção 1, página 70, Gestão de espécies – Fauna, [online] www.areaseg.com/conama/ 2004/346-2004.pdf, Accessed on 08/07/2010.
R Development Core Team (2010) R: A language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria, ISBN 3900051-07-0, URL http://www.R-project.org.
Eltz, T., Bruhl, C.A., Imiyabir, Z., Linsenmair, K.E. (2003) Nesting and nest trees of stingless bees (Apidae: Meliponini) in lowland dipterocarp forests in Sabah, Malaysia, with implications for forest management. For. Ecol. Manag. 172, 301– 313 Engels, W. and Imperatriz-Fonseca, V. L., (1990) Caste development, reproductive strategies and control of fertility in honeybees and in stingless bees, In: Engels, W. (ed.), Social Insects, an evolutionary approach to caste reproduction. Springer, pp. 167–230. Freitas, G. S., (2001) Levantamento de ninhos de meliponíneos (Hymenoptera, Apidae) em área urbana: Campus da USP, Ribeirão Preto/SP. Master thesis. FFCLRP, USP. Ribeirão Preto, SP. Hubbell, S.P., Johnson, L.K. (1977) Competition and nest spacing in a tropical stingless bee community. Ecology 58, 949–963 Inoue, T., Sakagami, S.F., Salmah, S., Yamane, S. (1984) The process of colony multiplication in the Sumatran stingless bee Trigona (Tetragonula) laeviceps. Biotropica 16, 100–111 Inoue, T., Nakamura, K., Salmah, S., Abbas, I. (1993) Population-dynamics of animals in unpredictably-changing tropical environments. J. Biosci 18, 425–455 INPE - Instituto Nacional de Pesquisas Espaciais (2011) Monitoramento da floresta amazônica brasileira por satélite: 1988-2010. INPE, São José dos Campos, Brasil. [online] http://www.obt.inpe.br/prodes/ prodes_1988_2010.htm, Accessed on 25/10/2011 Juliani, L. (1967) A descrição do ninho e alguns dados biológicos sobre a abelha Plebeia julianii Moure, 1962 (Hymenoptera: Apoidea). Rev. Bras. Entomol 12, 31–58 Malkowski, S.R., Faraj, B.H., Schwartz-Filho, D.L., (2006) Eficiência de garrafas-iscas na captura de enxames de Tetragonisca angustula (Latreille, 1811) (Hymenoptera, Apidae), Anais do 16º. Congresso Brasileiro de Apicultura e 2º Congresso Brasileiro de Meliponicultura, Aracaju, SE, CD Rom. Michener, C.D. (1974) The social behavior of the bees. A comparative study. Harvard University Press, Cambridge.
Nogueira-Neto, P., (1997) Vida e criação de abelhas indígenas sem ferrão, Nogueirapis.
Ribeiro, M.C., Metzger, J.P., Martensen, A.C., Ponzoni, F.J., Hirota, M.M. (2009) The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biol. Conserv. 142, 1141–1153 Roubik, D.W. (1983) Nest and colony characteristics of stingless bees from Panama (Hymenoptera, Apidae). J. Kans .Entomol. Soc. 56, 327–355 Roubik, D.W. (2006) Stingless bee nesting biology. Apidologie 37, 124–143 Roubik, D.W., Wolda, H. (2001) Do competing honey bees matter? Dynamics and abundance of native bees before and after honey bee invasion. Popul. Ecol. 43, 53–62 Seeley, T.D., Buhrman, S.C. (2001) Nest-site selection in honey bees: how well do swarms implement the “best-of-N” decision rule? Behav. Ecol. Sociobiol. 49, 416–427 Slaa, E.J. (2006) Population dynamics of a stingless bee community in the seasonal dry lowlands of Costa Rica. Insectes Soc. 53, 70–79 Steffan-Dewenter, I., Schiele, S. (2008) Do resources or natural enemies drive bee population dynamics in fragmented habitats? Ecology 89, 1375–1387 Terada, Y., (1972) Enxameagem em Frieseomelitta varia Lepeletier (Hymenoptera: Apidae), In: Homenagem à W. E. Kerr. Rio Claro, SP. Brasil, pp. 293–299. van Veen, J.W., Sommeijer, M.J. (2000) Colony reproduction in Tetragonisca angustula (Apidae, Meliponini). Insectes Soc 47, 70–75 Wille, A., Michener, C.D., (1973) The nest architecture of stingless bees with special reference to those of Costa Rica (Hymenoptera, Apidae), Rev. Biol. Trop., San José, Supl. 1. pp. 278. Wille, A., Orozco, E. (1975) Observations on the founding of a new colony by Trigona cupira (Hymenoptera: Apidae) in Costa Rica. Rev Biol Trop 22, 253–287 Winston, M.L. (1991) The biology of the honey bee. Harvard University Press, Cambridge. Witter, S., Blochtein, B., Andrade, F., Wolff, L.F., Imperatriz-Fonseca, V.L. (2007) Meliponiculture in Rio Grande do Sul: contribution to the biology and conservation of Plebeia nigriceps (Friese, 1901) (Apidae, Meliponini). Biosci. J. 23, 134–140