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Trap-nests for stingless (, Meliponini) Ricardo Oliveira, Cristiano Menezes, Ademilson Soares, Vera Fonseca

To cite this version:

Ricardo Oliveira, Cristiano Menezes, Ademilson Soares, Vera Fonseca. Trap-nests for stingless bees (Hymenoptera, Meliponini). Apidologie, Springer Verlag, 2012, 44 (1), pp.29-37. ￿10.1007/s13592- 012-0152-y￿. ￿hal-01201269￿

HAL Id: hal-01201269 https://hal.archives-ouvertes.fr/hal-01201269 Submitted on 17 Sep 2015

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie (2013) 44:29–37 Original article * INRA, DIB and Springer-Verlag, France, 2012 DOI: 10.1007/s13592-012-0152-y

Trap-nests for stingless bees (Hymenoptera, Meliponini)

1 2,3 Ricardo Caliari OLIVEIRA , Cristiano MENEZES , 4 5 Ademilson Espencer Egea SOARES , Vera Lúcia Imperatriz FONSECA

1Erasmus Mundus Master Programme in Evolutionary Biology, Ludwig-Maximilians-Universität München, Germany and Rijksuniversiteit Groningen, The Netherlands 2Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, São Paulo, SP, 3Embrapa Amazônia Oriental, Belém, PA, Brazil 4Departamento de Genética da Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, São Paulo, SP, Brazil 5Universidade Federal Rural do Semiárido, Mossoró, RN, Brazil

Received 8 April 2012 – Revised 27 May 2012 – Accepted 5 June 2012

Abstract – Most stingless 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 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 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 for each species (Roubik 2006; Rasmussen and Camargo 2008). The majority of stingless bee species (Hyme- In highly eusocial bees ( bees and noptera, Meliponini) build their nests inside pre- stingless bees), the foundation of new colonies existing hollows, usually in tree trunks, branches occurs through swarming. Unlike honeybees, or ground cavities (Roubik 1983, 2006; the swarming process in stingless bees is Nogueira-Neto 1997;Eltzetal.2003). Few gradual and occurs in rather small numbers. species can build their own cavity inside During the swarm process in stingless bees, nests (Camargo and Pedro 2003), and some can workers from the mother nest choose a new build exposed nests on walls or tree branches cavity and start to prepare it by cleaning and (Roubik 2006, Rasmussen and Camargo 2008). bringing nest material from the mother nest. Nest architecture, entrance shape and population They build the colony entrance (which is size are very diverse and usually characteristic usually species specific) and food pots, and some workers start to forage while others Corresponding author: R.C. Oliveira, remain visiting the mother nest. When the new [email protected] nest is ready, more workers fly together with a Manuscript editor: James Nieh virgin queen, which will perform the nuptial 30 R.C. Oliveira et al. flight soon after arriving at the new nest. The an important step to improving success rates and contact between mother and daughter nest can making this technique a viable tool for beekeep- last from few days to several months, according ing, research and conservation of stingless bees. to resources availability and the stingless bee The objectives of this study were to verify the species (Nogueira-Neto 1954;Juliani1967; effectiveness of the use of trap-nests for stingless Terada 1972; Wille and Orozco 1975; Inoue et bees in terms of: (1) which stingless bee species al. 1984; Engels and Imperatriz-Fonseca 1990; are attracted to trap-nests; (2) the ideal volume for van Veen and Sommeijer 2000). It has been each species; (3) the best season to attract predicted that many stingless bee species need swarms; (4) whether one material is preferable to swarm only once in 20 years to maintain their to another; and (5) what limitations, if any, this populations (Slaa 2006). Factors like the colony technique suffers from. We also discuss the capacity to generate virgin queens and workers possibility of using trap-nests in stingless bee for the swarm are very important in the conservation efforts. swarming process (Michener 1974). Although the swarming process has been described several times, many aspects remain unknown; 2. MATERIALS AND METHODS for example, how and why do they choose the new nesting site. 2.1. Trap-nests Stingless bee beekeepers have observed that stingless bees tend to establish new nests in old Plastic bottles and cardboard boxes with four different hives which were previously occupied by other volumes were used to build the trap-nests (0.5, 1.0, 2.0, colonies. Based on these observations, they and 3.0 L). These two materials were chosen because started to lay out empty containers containing they are relatively easy to obtain and cheap (compared to propolis and wax around their meliponaries, in wooden boxes, for example), facilitating the use of order to attract the swarms to these “traps”. hundreds of them and decreasing the possibility of Many beekeepers report success in obtaining robbery. Each trap-nest consists of a set of four different new colonies in this manner. Such “trap-nests” volumes, made either of plastic or cardboard (Figure 1). A solution of propolis was made by diluting batumen can be made from different materials (such as and cerumen of different stingless bee species (Meli- wood, plywood, cardboard or plastic) and are pona quadrifasciata, angustula, Frieseo- often baited with substances attractive to bees mellita varia,andScaptotrigona sp.) in alcohol. This such as propolis, honey and/or wax. solution was then sprayed inside the containers. A PVC The use of trap-nests is the only legal method elbow (20 mm) coated in Apis mellifera wax and of collecting stingless bee colonies in the field in propolis solution was inserted in the middle section of Brazil (CONAMA 2004). Moreover, collecting the container to act as an entrance tube. Plastic wild nests is costly in terms of both time and containers were black to prevent light shining through labor. Although some people are successful in the walls, and the cardboard trap-nests were wrapped collecting established colonies from trees without with black plastic bags to protect them from rain. Every apparent loss (Colleto-Silva 2005), this technique 6 months, more propolis solution was spread at the entrance and the damaged trap-nests were refurbished. is not ideal as it may result in the death of the tree and has high rates of colony loss due to 2.2. Study site and experimental setup damage to the colony during transfer to a hive. Although the use of trap-nests by stingless bee The study was carried at University of São Paulo beekeepers is becoming more common, this (USP), Ribeirão Preto campus (21°09′50″S, 47°51′ technique has only been studied a few times 30″W) and at Aretuzina Farm in São Simão (21°26′ before, mainly looking to see whether the trap- 18″S, 47° 34′45″W), about 40 km from the campus. nests were occupied or not by stingless bees (Inoue These areas show a relative high density of stingless et al. 1993; Malkowski et al. 2006; Alvarenga bee nests, as meliponaries stocked with several 2008). Understanding how the trap-nests work is species are kept in both of them. The sites are “green Trap-nests for stingless bees (Hymenoptera, Meliponini) 31

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 analyses with Monte Carlo permutation tests (10,000 fields. Currently, there are 21 stingless bee species random permutations) to evaluate whether the ob- among native and introduced at Ribeirão Preto served frequencies were different from random. A campus and approximately 10 more are kept in hives Pearson test was used to measure the correlation in the scientific meliponary (Freitas 2001; Oliveira, between the average monthly temperature and the unpublished data). number of swarms to the trap-nests. Statistical The trap-nests were installed on tree trunks ca. 1.5 m analysis was carried out using R 2.11.1 (R Develop- in height. Their positions at each site was randomly ment Core Team 2010). chosen. The study was carried out from April 2007 to April 2009. In the first year, we used only plastic trap- nests (200 groups of plastic trap-nests at Ribeirão Preto 3. RESULTS 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 3.1. Species attractiveness campus and 100 groups at Aretuzina Farm). Nests on the Ribeirão Preto campus were inspected every 15 days, so In the 2 years of experiments, 61 stingless bee as to obtain a better overview about seasonality of swarms of nine different species were attracted to swarming behavior, while trap-nests at Aretuzina Farm the trap-nests (10.2 % of trap-nests occupation were inspected every 3 months. rate): (n=38); An experiment to test the attractiveness of trap-nests clavipes (n=6); bipunctata (n=6); was also carried out after the study period. In this varia (n=3); Frieseomelitta silves- experiment, trap-nests made from Styrofoam were also trii (n=1); Friesella schrottkyi (n=1); Nannotri- used. Twenty groups of 3-L containers made of plastic, gona testaceicornis (n=2); remota (n=1); cardboard and Styrofoam were made. The cardboard and (n=3). On Aretuzina farm , and the Styrofoam trap-nests were wrapped with a black bag to avoid influence of color on nest choice by six swarms of quadrifasciata were swarms. The groups were installed at the same height attracted to the trap-nests but none of them (about 2.0 m) at the Ribeirão Preto campus between successfully settled. One of these swarms was August and December 2009. observed from the beginning of the swarming process. During the first 2 days, the bees built the 2.3. Statistical analysis entrance, brought building materials and food from the mother source, and built food pots and As most of the collected data was categorical, e.g., involucrum. On the third day, we observed very species, volume, and season, we used Chi-square low activity and a few dead bees being thrown 32 R.C. Oliveira et al. from the trap-nest. We opened the container and Table II. Number of stingless bee swarms attracted to most bees were dead inside the plastic container the cardboard trap-nests during the second year for because of excessive moisture. There were 245 each area. workers and one virgin queen, including a few worker bees which were still alive. This is the first Species Cardboard time that the number of bees involved in a T. angustula 9RP stingless bee swarm has been estimated. Although N. testaceicornis 1 RP; 1 SS we may have lost a few workers, we counted F. schrottkyi 1RP almost all of them, because bees that entered the container were not able to leave it, dying inside P. remota 1RP the trap-nest. Total 13 When only the plastic trap-nests were used RP Ribeirão Preto campus, SS Aretuzina farm, São Simão (April 2007 to April 2008), 48 stingless bee swarms were attracted (38 at the Ribeirão 3.2. Container volume Preto campus and 10 at Aretuzina farm). During this first year, 24 other swarms were It is possible to observe that some stingless attracted to old empty hives in Aretuzina bee species were attracted to small volumes (F. farm. The empty hives were previously used silvestrii and N. testaceicornis), others to larger by stingless bees and were spread at the volumes (S. bipunctata, T. clavipes, F. varia, studied area by the farm owner. In the F.schrottkyi and P. remota) while a few appar- second year (April 2008 to April 2009), ently showed no preference (T. angustula and P. when cardboard trap-nests were used, 12 droryana). Also, seven out of the nine species swarms were attracted at the Ribeirão Preto were observed occupying the large trap-nests (2 campus and only 1 at Aretuzina farm (no and 3 L), while only two were found only in the swarms in empty hives were observed). smaller volumes (0.5 and 1 L) (Table III). Some stingless bee species were attracted Therefore, stingless bees generally preferred to only to plastic trap-nests (Table I), others move into larger trap-nests (χ2 =20.11 were only attracted to cardboard trap-nests P<0.0005, n=61). (Table II) and only T. angustula was attracted to both materials, but we cannot take conclu- 3.3. Seasonality sions about material preferences from this experiment because of low sample size to most In the Ribeirão Preto campus, where regular species in the different areas. observations were made, the monthly frequency of swarms was distributed non-randomly during χ2 Table I. Number of stingless bee swarms attracted to the first experimental year ( =35.26; the plastic trap-nest during the first year each area. P<0,0005; n=38) and most of swarming attempts occurred from December to April. Species Plastic These 2 months accounted for 40 % of the swarms, with 20 % in each month (Figure 2). It S. bipunctata 6RP was possible to observe a trend in the swarming T. clavipes 6RP process towards the spring season (ending of F. varia 3RP dry and beginning of wet season) in the F. silvestrii 1RP Ribeirão Preto campus in both years (n=18), 2 T. angustula 22 RP; 7 SS although not significant (χ =7.12; P>0.05; P. droryana 3SS n=50). There was a significant difference in Total 48 the swarms frequency during the different seasons in the first year (χ2=10.42; P<0.05; RP Ribeirão Preto campus, SS Aretuzina farm, São Simão n=38) but not in the second, likely due to the Trap-nests for stingless bees (Hymenoptera, Meliponini) 33

Table III. Number of stingless bee swarms moving into trap-nests for each species, container volume and material.

Species Volume Total

0.5 L 1.0 L 2.0 L 3.0 L

S. bipunctata 2P 4P 6 T. clavipes 3P 3P 6 T. angustula 1 P 13 P; 2 C 7 P; 2 C 8 P; 5 C 38 F. varia 3P 3 F. silvestrii 1P 1 N. testaceicornis 1P;1C 2 F. schrottkyi 1C 1 P. droryana 1P 1P 1P 3 P. remota 1C 1 Total 2 19 14 26 61

P Plastic trap-nests, C cardboard trap-nests overall low number of swarms (χ2 =3.33; experiments), swarming does not occur random- P>0.05; n=12) (Figure 3). ly throughout the year. Most swarming attempts During the first year, there was a significant occurred during months that correspond to the correlation (rs=0.8; P<0.005) between monthly ending of the dry and beginning of the wet average temperature and number of swarms. season (spring and summer) in the southern Again, no significant pattern emerged in the hemisphere (n=25), with only six swarming second year (rs=–0.39; P>0.005). events occurring on the dry season (autumn and For T. angustula (the most abundant stingless winter) (χ2=13.25; P<0.005; n=31). For T. bee species occupying the trap-nests in the 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). 34 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 were never occupied by stingless bees. Howev- we found no annual pattern for swarming er, there was one exception: a F. schrottkyi behavior (χ2=3.33; P>0.05; n=6). There were colony shared a trap-nest with a Camponotus not enough data for other species to allow sp. colony. further analysis.

3.4. Material attractiveness 4. DISCUSSION

Plastic trap-nests showed to be the most Different trap-nests methodologies have been attractive for stingless bees since eight swarms successfully used to attract stingless bee were attracted to them, as compared to one swarms. Inoue et al. (1993) used bamboo and swarm to Styrofoam and none to cardboard wooden boxes of ca. 2 L as trap-nests and trap-nests (χ2=12.67; P<0.005). Eight of those succeeded in attracting one stingless bee species swarms were T. angustula and one F. varia. ( () minangkabau) out of 24 which swarmed in the area, resulting in 6 % of 3.5. Limitations of trap-nests the traps being occupied. In a different study site in Ribeirão Preto, 11.46 % of the trap-nests Some factors, such as direct sunlight, exces- were occupied: 3 by Scaptotrigona sp. and 8 by sive moisture inside the containers, and use by T. angustula using plastic trap-nests identical to other , might have influenced the suc- the ones used in this experiment (Alvarenga cess rate of swarm attraction to the trap-nests. 2008). In southern Brazil, (Malkowski et al. Spiders and were the most common 2006) obtained 22 % occupation (30 colonies) competitors for the nesting sites occupying by T. angustula using a similar method, and 19 % of plastic trap-nests and 5 % of cardboard Witter et al. (2007) related that Plebeia nig- trap-nests. Trap-nests were also occasionally riceps used a wooden trap-nest. Trap-nests are occupied used by a social (Polybia efficient in a range of different areas and occidentalis, Hymenoptera, ) stingless bee species. In this study, we showed (Table IV). Nests occupied by other animals that at least nine different stingless bee species Trap-nests for stingless bees (Hymenoptera, Meliponini) 35

Table IV. Trap-nests occupied by animals other than stingless bees settled in the larger volumes. In stingless bees. general, larger volumes can be considered more efficient, as they attract a larger number of swarms Occupant n Total percentage and species. Trap-nests of 2 and 3 L attracted 40 swarms of seven different species, as compared to Spiders 20 C; 12 P 8 21 swarms of four different species for 0.5- and 1- Ants 27 C; 21 P 12 L trap-nests. Species with small body size usually 4 C 1 build small nests (Hubbell and Johnson 1977), Spiders and ants 3 C; 5 P 2 such as F.schrottkyi, P. droryana and T. angustula, Wasps and ants 2 C 0.5 which occupied both small and large volume trap- Total 94 23.5 nests. On the other hand, species with large body size would generally build large nests (Hubbell P Plastic trap-nests, C cardboard trap-nests and Johnson 1977): S. bipunctata and F. vari a only occupied large trap-nests (2.0 and 3.0 L). colonized trap-nests and give some hints about Although N. testaceicornis and F. silvestrii were preferential season, volume and material. only found in the small volume trap-nests, based Nine out of 21 species found on the on our data, we predict that they would also be University campus were attracted to the trap- able to settle in a larger volume trap-nest. nests. Four of them build their nests at 1 m Swarming in social bees usually occurs during height on average (F. schrottkyi, N. testaceicor- the reproductive seasons, which are periods with nis, S. bipunctata and T. angustula), two at favorable environmental conditions, i.e. food avail- about 3 m (F. varia and T. clavipes) and for the ability and temperature (Winston 1991). Resources other two there are no data (F. silvestrii and P. availability is an important factor in colony remota) (Freitas 2001). The other species build reproduction because during this process about their nests between 2 and 10 m high, which may 30 % of mother colony will move to the daughter have influenced the diversity of species colony, producing 20–50 % more brood cells and attracted to trap-nests since they were installed about double the amounts of and honey pots at approximately 1.5 m high. Another factor that (Inoue et al. 1984; van Veen and Sommeijer 2000). may influence the attractiveness of trap-nests to Slaa (2006) observed that the foundation of new particular species is the nesting habits of the stingless bee colonies was more frequently during species. Out of 19 species sampled by Freitas the dry season in the lowland dry tropics. In our (2001) at Riberão Preto campus, 5 build their study, there was a trend towards swarming events nests in the ground, on walls, trees or inside occuring in the end of dry season (spring) (18 out termite nests (Trigona fuscipenis, Trigona hya- of 50), and in the first year, the average temper- linata, , helleri and ature and the number of swarms in the trap-nests latitarsis) (Wille and Michener 1973; were positively correlated, showing that there was Michener 1974; Freitas 2001). These species an increase in the number of swarms during the will most likely not be attracted to trap-nests. warmer seasons, i.e. spring and summer. Therefore, Natural stingless bee nest sizes vary widely we recommend placing trap-nests in early spring. amongst different species. Nests of some species During the second year, lower swarming rates are smaller than 0.5 L, while others can be over were observed both at Ribeirão Preto campus and 300 L (Inoue et al. 1993). It has been observed that Aretuzina farm, not only into the trap-nests but stingless bee species are limited by a minimum also into the old wooden hives, to which no volume and diameter cavities but not by a swarming was observed. This difference between maximum (Hubbell and Johnson 1977; Eltz et the first year and the second year of experiment al. 2003). Honey bees also prefer nesting sites may have been influenced by many factors such with larger volumes (Seeley and Buhrman 2001). as weather conditions and nesting site availability In this study, we also observed a trend where the (Inoue et al. 1993; Roubik and Wolda 2001). 36 R.C. Oliveira et al.

Also, it has been shown that most colonies are cause an increase in solitary bees (Steffan- not able to reproduce in two consecutive years Dewenter and Schiele 2008) as well as stingless (Slaa 2006). This suggests to us that the colonies bee populations (Inoue et al. 1984). These were suffering from a lack in nesting site studies were corroborated by our results show- availability before the first year of experiments ing that the trap-nest can be a useful tool to help and, once the first trap-nests were settled, this in the conservation of natural stingless bee demand was fulfilled and prevented swarming in populations in the future. 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 ACKNOWLEDGEMENTS trap-nests. In the material attractiveness experi- ment, we observed that plastic trap-nests were This work was financed by the São Paulo Research more attractive to stingless bee swarms (n=8) Foundation (FAPESP - 04/15801-0) and National than cardboard (n=0) or Styrofoam (n=1). Council for Scientific and Technological Development (CNPq - 112818/2007-2 for RCO). We are thankful to However, the lower swarming rates were gener- Ayrton Neto, Denise Alves and Tomer Czaczkes for the ally observed during the second year of experi- suggestions on the manuscript, Rafael Silva and Ayrton mentsandnotonlyinthecardboardtrap-nests. Neto for helping in the field work. We thank also to Trap-nests were also occupied by other Klaus Hartfelder, James Nieh and the anonymous animals such as ants, spiders, and wasps. In referees. Finally, we would like to thank Dr. Paulo Sumatra, Indonesia, ants occupied 50 % of the Nogueira Neto, in particular, for allowing us to work in trap-nests (Inoue et al. 1993). Ants were also the the Aretuzina farm and for all his suggestions. and we major competitors for nesting sites in our study would like to dedicate this paper to him for the occasion (12 %), showing that these animals compete for of his ninetieth anniversary. the nesting sites with stingless bees. In only one instance, a colony swarmed into an occupied Nids-pièges pour abeilles sans aiguillon (Hymenoptera, trap-nest. On that occasion, F. schrottkyi built its Meliponini) nest in a nest occupied by an ant species Abeille sans aiguillon / piègeage / essaimage / (Camponotus spp.). testaceicor- Meliponini nis is known to build nests associated with Camponotus species (Camargo and Pedro 2008), but this type of association has never Fallennester für Stachellose Bienen (Hymenoptera, Meliponini) been described before for F. schrottkyi. Most stingless bees build their nests in trees Stachellose Bienen / Fallennest / Schwärmen / (Roubik 1983, 2006; Nogueira-Neto 1997; Eltz Meliponini et al. 2003). Deforestation is therefore a serious threat to the conservation of stingless bee REFERENCES populations. It has been shown that non- fragmented are required to maintain Alvarenga, P.E.F., (2008) Levantamento da fauna de stingless bee communities (Brosi et al. 2008). abelhas (Hymenoptera, , Meliponina) na From 1988 to 2010, deforestation in the mata Santa Tereza, estação ecológica de Ribeirão Preto-SP, e limitantes da densidade de seus ninhos. Amazon rainforest proceeded on average at Master thesis, FFCLRP-USP. 16,773 km2/year (INPE 2011) and the Atlantic Brosi, B.J., Daily, G.C., Shih, T.M., Oviedo, F., Duran, rainforest has already lost ca. 90 % of its natural G. (2008) The effects of forest fragmentation on bee vegetation in about 200 years of exploitation communities in tropical countryside. J. Appl. Ecol. – (Ribeiro et al. 2009). Stingless bees appear to 45, 773 783 suffer from lack of suitable nesting sites, and Camargo, J.M.F., Pedro, S.R.M. (2003) Neotropical Meliponini: The genus Partamona Schwarz, 1939 deforestation exacerbates this problem. Howev- (Hymenoptera, Apidae, ) - bionomy and er, experimental addition of nesting sites can biogeography. Rev. Bras. Entomol. 47,311–372 Trap-nests for stingless bees (Hymenoptera, Meliponini) 37

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