Best management practices in Agriculture for sustainable use and conservation of pollinators Agreement FAO- S. Paulo University

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1 Best management practices in Agriculture for sustainable use and conservation of pollinators Agreement FAO- S. Paulo University Vera Lucia Imperatriz-Fonseca Ecology Department, Biosciences Institute, S. Paulo University Rua do Matão, travessa 14, n.321. CEP São Paulo, Brasil

2 How to get stingless bees nests in Nature? Considerations on nesting behavior and concerns on resources availability 2

3 Contents Abstract Foreword Best management practices in Agriculture for sustainable use and conservation of pollinators Introduction 1. How to get stingless bees nests in Nature? Considerations on nesting behaviour and concerns on resources availability 2. Forestry and pollinators conservation Trees for bees- Annex 1 Table 1. Plant families and their species used for stingless bees for nesting Table 2. Plant species in alphabetic order used by stingless bees for nesting Table 3. Stingless bees, in alphabetic order, and the trees used by them for nesting Table 4. Brazilian biomes with respective stingless bees species and the plants species used as their nest sites Table 5. World data on stingless bees and the trees used as their nest sites Table 6. Plants recommended for environmental restoration and used as nest sites by Meliponine bees. Bees and their floral resources- Annex 2 Table 1. Plants species used by stingless bees as floral resources Table 2. Plants recommended for environmental restoration in Brazil and used as floral resources for social bees (bumblebees, stingless bees and honeybees). Tetragonisca angustula: Bee plant calendar in an urban garden; trees for nesting and databank of flowers visited Annex 3 General remarks on the importance of Tetragonisca angustula as a flag species Table 1. Floral calendar for social bees in an urban garden Table 2. Floral calendar for Tetragonisca angustula in an urban garden Table 3. Trees used as resources for Tetragonisca angustula Table 4. Floral resources for Tetragonisca angustula in Latin America 3

4 Abstract Stingless bees biodiversity, abundance and nest densities were discussed based on available literature in tropical areas of the world. In this report we focus on resources needed by stingless bees survivorship, mainly shelter and food availability. Their biodiversity is influenced by the quality of their environment. Human activities as logging and habitat disturbance by agricultural areas were also shown to modify their communities. Nests sites for stingless bees are told to be a limit for nests density. Besides, the new rules for stingless bees keeping and meliponaries settlement in Brazil (resolution from CONAMA 343), allow the use of trap nests as a source of nests in nature. Nevertheless, research on the use of trap nests was not done in Brazil concerning stingless bees. The ecological problems related to nesting were discussed, as well the literature on trap nests in stingless bees. Annex 1 show data from trees that are used for stingless bees to nidify in Brazil, in South and Central America and in Asia. The quality of environment has an influence on stingless bees species composition in the community, as well as bees as pollinators influence the natural areas botanical composition through the ecosystem services provided by them. In wet lowland forest at La Selva, more than 50% of canopy species and 36% of subcanopy trees were pollinated by bees (Bawa et al. 1985). A change in the pollinator s community will impact tree composition and the whole food chain. This is very important for activities related to forest use, as logging, and the recommendations for best practices with stingless bees and other bees nests management. The general introduction concerns nesting behavior, resources availability and considerations in logging activity, pollinators and forest composition. Forestry is an important subject in Brazil nowadays. Only a few species of stingless bees are used as pollinators in cultivars, mainly because this is still new approach, a service that was taken for grant until recently. Although they are generalists in their habits, there is a variation in size and preference for different floral sources (Biesmeijer et al., submitted). In Annex 2 are data related to floral resources visited by social bees, including stingless bees, in Brazil. They came for published and unpublished papers, thesis and data of sparse observations mentioned in literature and constitutes a data bank. 4

5 Annex 3 concerns the most common stingless bee in Brazil and in other Latin American countries, Tetragonisca angustula. For this species a list of important floral resources is presented, as well as a floral calendar for them in an urban area. Plant species used as nests sites are also listed. T. angustula is used for crop pollination, and is one of the species for which trap nests are attractive. Its honey is very appreciated and considered as medicinal. Key words: stingless bees, biodiversity, nest sites, trap nests, logging, foraging. resources, 5

6 Best management practices in Agriculture for sustainable use and conservation of pollinators. Foreword Best management practices in Agriculture for sustainable use and conservation of pollinators are focused in recent literature, and mainly by several authors that study pollinators conservation. This means to carry on pesticides (a detailed study is in preparation by Claire Kremen, p. com.) and their use in the crops; transgenic crops and gene flow studies; environmental friendly agricultural practices, including land preparation, in order to keep nests of solitary bees that occur in the soil; agricultural area and maintenance of their borders with native vegetation, or hedges that can keep pollinators; to decrease herbicides use in Agricultural crops, that helps the foraging supply for pollinators and crop attractiveness for them, in larger areas. Agricultural intensification includes a decline in the proportion of natural habitat, an increase in pesticide usage, a decrease of floral resource on farm sites, as well as larger field sizes, crop monocultures, intensive soil and water usages and the use of synthetic fertilizers. Of course, the sustainability of Agriculture following these patterns of land use is under concern by 21 Agenda for Agriculture. All these issues are focused for some crops, mainly those of global commercial importance. The recent International Pollinators Initiative s plan of action really is putting pollinators in the mainstream. Interesting papers focusing the ecosystem services provided by pollinators were recently published, considering also their economic value, and trying to measure this. A good example is related to coffee crops. Although this crop does not depend obligatory on pollinators, Roubik (2002) showed that the feral Africanized bees increased the coffee production in Central America. Also in coffee plantation, de Marco & Coelho (2004), in Brazil, found that the farms near forest fragments had an increase of 14,6% in production, that could be related to pollinating services; Ricketts (2004) and Ricketts et al (2004) pointed out the importance of tropical forest fragments to enhance pollinator s activity in nearby coffee crops. These last studies 6

7 demonstrated the importance of stingless bees (10 species) as well as Africanized honeybees Apis as pollinators. The distance between the crop and the fragment showed that the use of the pollinators in transects along the agricultural areas should increase on 20% the crop production, as well as diminished the peaberries, resulting of unsuccessful pollination. Based on this, and their analyses in three plots, the authors suggested an economic value of the forest providing this ecosystem service and that this pollination service could be paid, by the coffee producers, to the owner of the fragment; they also present an estimate of the economic value of these natural fragments, based on this evaluation. But economics of the pollination services is still rare in literature. Kevan and Phillips (2001) did an estimative for apples, and also present a model to be applied in economic value of crops. Drucker (2004) discussed the economic value of the bee pollination services, and their implications for farm management and policy. Is this paper he presents a selection of studies on economic value of pollination services by bees. Kremen (2004) also considered the importance of bee community as crop pollinators, pointing out that if we keep several bee species from natural environments visiting flowers, the shortage of one species in one year could be compensated by the other visitor s species, diminishing the impact of pollinators shortage on crops. Ricketts (2004) used the same approach considering plots with different percentage of bee species visiting coffee flowers. Although the importance of pollinators in Agriculture (see also weevils for oil palm; bumblebees for tomatoes, among others; solitary bees for apple, pears and alfalfa, for instance; stingless bees for strawberry, guaraná, açaí, coffee, among several other crops; honeybees for several crops) is well known, until now their use is not remarkable in undeveloped countries. But this situation will change very soon, because of new initiatives concerning pollinators use in crops (for instance, the Brazilian Pollinators Initiative) as well as from successful crops competing in world market, resulting from the pollinators use in greenhouses, for instance. Developed countries are working with pollinators shortage, although only a small number of them (a dozen, Kremen 2004) are successful bred for agricultural use. If they are not available nearby due to the intensive agricultural patterns using large areas, they are bought from biotech companies that breed them successfully. These companies are multinational and have the technology of large 7

8 scale breeding. The best example is that of Bombus terrestris use in agriculture (their breeding in laboratory conditions was successful only in 1985; nowadays, companies worldwide sell 1 million of nests per year (Velthuis and Van Doorn, 2004). The introduction of alien pollinators with defined breeding techniques is also undesirable, and studies of ecological impact are asked in importation process. This will stimulate the breading of native pollinators for the same service in countries with capacity building in pollination area. In many tropical and subtropical areas of the world, a new scenario opens focusing stingless bees use as crop pollinators (Maeta et al.,1992; Slaa, 2001; Macias et al., 2001; Cunningham et al., 2002; Malagodi- Braga & Kleinert, 2004; Cruz et al., 2004; other related investigations were recently improved by Brazilian government). Best management practices of pollinators in crops means best economic value, and in this aspect both issues are together. Generally, producers are not interest in resistance (ability to retain community properties under disturbance) or resilience (ability to recover from disturbance) of crops when intensifying Agriculture, but in their economic value in this season. Short time actions and market simulations are important in the producer s decisions on what crop to use in next season. They are linked to unpredictable weather conditions, as well to the market fluctuation on crop values (Kevan and Viana, 2003), as well as to the economic advantage in having better fruits. Long-term activities concerning natural resources are almost not considered. For this document the focus on best practices will be stingless bees (Meliponini). They are the new possibility to face the pollinators shortage in the world. With a high biodiversity, social, having local well-distributed species living in perennial colonies, they are suitable for this new approach. Information around the world on Meliponini was considered related to resources use (as nest sites and bee plants for food). A review was prepared considering nests sites, in order to provide the list of plants that are used as nest sites that could be included in official program of environmental compensation and disturbed area restoration in Brazil. Also the food sources could be included in that list. This program is a government request for those activities that damage the environment, they have to restore additional areas. An infant industry arises with stingless bees breeding in Australia (Heard & Dollin, 2000) and Brazil (Rosso et al., 2001). Their 8

9 potential use in large scale is in crop pollination (Heard, 1999). How to get nests in nature and to breed them successfully is a challenge. Resources availability for them, as food sources, will be discussed. Stingless bees breeding was recently ruled in Brazil. To get nests in Nature, trap nests are allowed. Nevertheless, this is not a conventional practice for us. A complete survey in literature was done in order to discuss this subject and to make recommendation for next steps. References Eltz,T; Brühl, C.A ;Imiyabir, Z & Linsenmair, K. E Nesting and nest trees of stingless bees (Apidae: Meliponini) in lowland dipterocarp forests in Sabah, Malysia, with implications for forest management. Forest Ecology and Management, v. 172, p Cruz D de O, Freitas BM, Silva LA da, Silva SEM da, Bomfim IGA 2004 Use of the stingless bee Melipona subnitida to pollinate sweet pepper (Capsicum annuum L.) flowers in greenhouse. Proceedings of the 8th IBRA International Conference on Tropical Bees and VI Encontro sobre Abelhas, p.661. Cunningham, S; FitzGibbon, F & Heard, T.A The future of pollinators for Australian agriculture. Aust.J. Agric.Res.53: De Marco Jr, P & Coelho, F.M Services performed by the ecosystem: Forest remnants influence agricultural cultures pollination and production. Biodiversity and Conservation, v.13, p Drucker, A.G Economic valuation of the bee pollination services: implications for farm management and policy. In: Freitas & Pereira ed., Solitary bees: conservation, rearing and management for pollination. Fortaleza, p Heard T.A The role of stingless bees in crop pollination. Ann. Rev. Entomol. 44: Heard, T.A. & Dollin, A Stingless bees beekeeping in Australia, snapshot of an infant industry. Bee World, 82: Kevan. P.G. & Phillips,T.P The economics impacts of pollinator declines:an approach to assessing the consequences. Conservation Ecology, v.5, n.1 Kremen, C Pollination services and community composition: does it depend on diversity, abundance, biomass or species traits? In: Freitas & Pereira ed., Solitary bees: conservation, rearing and management for pollination. Fortaleza, p Macias MJO, Quezada-Euan JJG, Parra-Tabla V & Reyes OV 2001 Comportamiento y eficiencia de polinizacion de las abejas sin aguijon (Nannotrigona perilampoides) en el cultivo del tomate (Lycopersicum esculentum M) bajo condiciones de invernadero 9

10 en Yucatan, Mexico. II Seminario Mexicano sobre abejas sin aguijón. Memorias. Mérida, Yucatán, México, pp Maeta Y, Tezuka T, Nadano H, Suzuki K Utilization of the Brazilian stingless bee, Nannotrigona testaceicornis, as a pollinator of strawberries. Honeybee Sci. 13: Malagodi-Braga KS & Kleinert AMP 2004 Could Tetragonisca angustula Latreille (Apinae, Meliponini) be used as strawberry pollinator in greenhouses? Aust. J. of Agric. Res. 55 (7): Ricketts, H. T Tropical forest fragments enhance pollinators activity in nearby coffee crops. Conservation Biology, v. 18, n. 5, p Ricketts, H. T.; Daily, G.C.; Ehrlich. P. R. and Michener, C.D Economic value of tropical forest to coffee production. Proc. of National Academy of Sciences, v. 101, n.34, p Rosso, J.M.L; Imperatriz-Fonseca, V.L & Cortopassi-Laurino, M Meliponicultura en Brasil I: situation en 2001 y perspectivas. II Seminario mexicano sobre abejas sin aguijón-memorias.yucatan, Merida, p Roubik, D.W. (2002)- The value of bees in coffee harvest. Nature 417: 708. Slaa EJ, Sanchez LA, Sandi M & Salazar W A scientific note on the use of stingless bees for commercial pollination in enclosures. Apidologie 31: Velthuis, H.H.W. & van Doorn, A The breeding, commercialization and economic value of bumblebees. In: Freitas & Pereira ed., Solitary bees: conservation, rearing and management for pollination. Fortaleza,

11 How to get stingless bees nests in Nature? Considerations on nesting behavior and concerns on resources availability Vera Lucia Imperatriz Fonseca- Depto. Ecologia, Instituto de Biociências, Universidade de S. Paulo. Rua do Matão, trav. 14, 321. CEP S. Paulo, Brazil INTRODUCTION Stingless bees biodiversity in fragmented Brazilian landscapes A bee review in Boracéia Biological Station, Atlantic Rainforest in S. Paulo, showed that it was the richest bee area sampled until now in Brazil, comprising 255 bee species with 38 stingless bees species. This analyzes was done 3 years round collecting bees on flowers (Wilms et. al., 1996). Bee nests were not recorded. Oliveira (2001) evaluated stingless bees in different seized fragments in Amazonian forest. The used method was collections in forest fragments of 1, 10 and 100ha, as well as continuous forest sites and deforested areas. The bees were colleted in six ways: by honey baits; by collecting clay; by collecting sweat; in flight; in their nests; in flowers. Stingless bees belonging to 37 species were collected 37 in continuous forests, 11 in 100ha fragments, 22 in 10ha fragments, 21 in 1ha fragments and 25 in deforested areas! He mentioned that in four fragments of 10ha and in five fragments of 1ha the number of species found surpassed the number found in 100ha fragment. He also was surprised with the number of species in the deforested area. Another important study concerning different landscapes and stingless bees richness was done in Rondônia (Brown & Albrecht, 2001). These authors analyzed the landscape and used a method of collecting stingless bees species in Vernonia polyanthes, an attractive food source for them, planted near the plots of different landscape quality for samples. They were interested in determining whether deforestation has affected the incidence of Melipona species. They found that M. seminigra abunensis and M. grandis 11

12 were common species, followed by M. rufiventris brachychaeta and M. melanoventer. The rare species were M. schwarzi, M. fuliginosa and M. crinita. Forests are difficult to be sampled (Ramalho, 2004). In Brazil several bee surveys with standard methodology were done until now, mainly in open areas (Pinheiro- Machado et. al., 2002). Data on bee-plant relationship are also available (for a metanalysis, see Biesmejer et. al., submitted). The use of baits (sugar baits, salt baits, chemical baits) as a standard method for biodiversity availability is not common yet in our country, and a methodology must be assessed and tested (see Roubik, 1996 for a standard methodology for stingless bees biodiversity estimates with baits, in Southeast Asia). Stingless bees nests Stingless bees are a diverse and rich group of tropical and Neotropical bees. They live in nests that can be aerial and constructed by themselves (as Trigona spinipes in Brazil and Dactylurina stundigeri in Africa), but generally use natural hollows or man made cavities for establishing their nests. The trees can be also used as a support for aerial nests, including here nests from other social insects, as ants and termites. Scaura latitarsis (Kerr et al., 1967) and Paratrigona impunctata (Camargo & Moure, 1994) in Brazil, are examples of nesting inside termite nests; in Africa, the same occurs for Apotrigona nebulata (Darchen, 1972). Cavities constructed by Atta ants and later abandoned are used as nest sites for Paratrigona subnuda in disturbed habitats (including agro ecosystems) (Imperatriz-Fonseca et al. 1970), and Schwarziana quadripunctata (Camargo, 1974), among many others. Roubik (1983) mentions the variation in nest sites preferences when analyzing bees from Panama and comparing literature, appointing this plasticity in T. mirandula, T. pallens, T. cilipes and T. hypogea. T. cilipes can be found in trunks (Roubik, 1983), inside Azteca ant nests or termite nests (Kerr et al., 1967), showing a broader niche for nests. A plasticity related to nests requirements is also verified towards these species that make their nests in disturbed areas, as Tetragonisca angustula, for instance (see Annex 3). 12

13 Data on trees that hosts colonies of stingless bees are sparse in literature and are listed in Annex 1. The majority of stingless bees species nest in preformed cavities in live trees (Roubik, 1983; Sakagami et al., 1983; Salmah et al., 1990). Other can live in dead trees (as Ptilotrigona lurida mocsaryi and Trigona fulviventris in Brazilian Amazon, Oliveira et al. 1995; T. melanocephala and T. rufibasalis in Sarawak, Malaysia, Samejima et al., 2004), including here those that have already felt (for instance, Duckeola ghiliani, Kerr et al. op. cit.). Stingless bees as Partamona batesi, P. gregaria, P. pearsoni, P. cupira among several others nest inside active termite nests, whether epigeous or arboreous (Camargo & Pedro, 2003). The Partamona genus and nests were recently reviewed and related information show the large variety of nests sites used by this bee genus. According to Camargo & Pedro (op. cit), All species endemic to western Ecuador to Mexico with known nesting habits (P. orizabaensis, P. peckolti, P. xanthogastra, P. bilineata, P. aequatoriana and P. musarum) build their nests in several substrates, nonassociated with termitaria, such as cavities and crevices in walls, among roots of epiphytes and in bases of palm leaves, in abandoned bird nests, under bridges, and in other protected places, except P. peckolti that occasionally occupies termite nests. In South America, on the eastern side of the Andes, only P. epiphytophila and P. helleri nest among roots of epiphytes and other substrates, non-associated with termitaria. In Africa, Darchen showed in his films (Stingless bees in African forests and Apotrigona nebulata, SRFS) how vertebrate as birds and mammals make holes in suitable nest sites, including termite nests, offering possibilities for stingless bees to make their nests in them. Nests can be also found in aggregates [Hypotrigona in Africa (Darchen, 1972); Starr & Sakagami (1987) found 84 colonies of Trigona (Tetragonula) fuscobalteata and T. (Tetragonula) sapiens in a bamboo house with an area of 68m 2 ; Partamona cupira (=orizabaensis, Camargo e Pedro 2003), in Roubik 1983]. 13

14 Hollow trees as shelter and den sites Hollow trees are ultimately found when decayed invertebrates remove heartwood material, usually, water or fire are formed (Gibbons and Lindenmayer, 2002; Martin & Eddie, 1999) and then generally are in older and larger trees, which can be suitable for logging activities. Hollow trees are special environments for many species of mammals in Australia (Lindenmayer et al., 1997;) and birds (Newton, 1994 for a review) both for nesting and hosting. A paucity of tree hollows may limit the abundance and distribution of species. Considered as an unavailable resource, because of logging and forest management, conservation activities supply artificial wood boxes to be offered as nest sites, in order to keep these animals alive in the environment. A good example, in Brazilian wetlands, the Pantanal region, is the work done with an endangered population of the hyacinth macaw, intimately dependent on one species of palm tree the macauba palm, Acrocomia sclerocarpa ( bocaiúva ), where it is also nests. The cutting-down of this palm endangered the survival of the macaw. Dr. Neiva Guedes, who conducted this research, used trap nests constructed with wood, and offered them as nest sites in several places of her study area. The results were excellent, with an increase in the hyacinth macaw population (now with individuals in Pantanal), who is not endangered any more. It is interesting that environmental education was very effective: 42 farms added the conservation program, as well as government centers in other regions. Her method is also being used in Bolivia and other Pantanal areas. Trapnests for macaws were distributed; it was found that 90% of them were occupied by other animals instead of macaws, including local stingless bees (Guedes, p. inf.). She monitors, yearly, 170 artificial nests with hyacinth macaws (see ). The increased probability of a hollow being present in large diameter trees is in part a function of the loss of decay resistance as trees ages. Hollows can be found in trunks (mainly in their base) and in branches. 14

15 How big must be a cavity to keep a stingless bees nest? Stingless bees size and populations varies a lot (see Roubik, 1983), as well as their needs for nest sites. So, they have specific nests requirements, according to their size, population and habitat quality. Very slender cavities (1-5cm wide) were used by smaller bees (Roubik, 1983): Melipona marginata micheneri, T. mirandula, T. jatifornis, etc.. On the other hand, Kerr et al (1967) mention that Melipona semimigra merrilae need more space, because it produced 20 L of honey/year, twice the quantity observed by the rare honeybees found in that region in This situation changed now, with the arrival of Africanized honeybee, and a competition for nest sites was described between Africanized honeybee and Melipona bees in several parts of the country, from dry Caatinga to forests, as described by stingless bee keepers. Some of these descriptions include parrots, Africanized honeybees and stingless bees nests (Bruening, 1990). Roubik (1983) listed the cavities sizes form de Panamanian nests. Camargo, in his several papers on stingless bees nests, also mentions cavities sizes. There is a huge variation here, and each species must be considered in different environments. Cavity size constraints nest development. Inoue et al (1993) mention the cavity volume for three stingless bees species from Sumatra (Trigona canifrons, >30.0 L; Trigona minangkabau, 0.5 L and Trigona fuscobalteata, 0.3 L). Matins et al. (2004) studied the internal diameter and length of 5 Melipona subnitida nests, representing volumes from 2,4 to 8,6L (mean= 5,6L). Cavities sizes for the several stingless bees species varies a lot. Small cavities sometimes constraints nest development. Large cavities are delimited by walls of resin or batumen (a mixture of resin, mud, wax and sometimes pieces of plants) constructed by the bees. 15

16 Competition among stingless bees for nest spacing Stingless bees colonies can be long lived (some Tetragonisca angustula nests are 40 years old at the University campus in S. Paulo; the same for some Melipona bees kept by beekeepers). These colonies, fixed by their nests, can swarm if nest sites are available. Colony density and dispersion modes are important ecological aspects, that will be deeper considered here. Hubbell & Johnson (1977) studied the dispersion patterns of five stingless bees species in Costa Rica, four of them territorial and with uniformly distributed nests. They stated that suitable nest sites availability do not limit colony dispersion. Rather, food limitation is suggested as a limitation. The authors considered that if there are shortages of suitable nest sites, this shortage should be more acute for bee species with nest requirements for larger trees: Trigona fulviventris and T. silvestriana. Nevertheless, these species have nests very uniformly spaced through the forest, an strong limitation against the theory of nesting limitation because they believed that suitable nest sites are themselves not uniformly spaced. They also found that bees occupied only 25 of the 74 potentially available tree species. Another point: some tree species without nests in the study area were known to have nests of these bee species elsewhere in the Guanacaste Province. A second source of evidence against the nest-site limitation was the apparent indiscriminant choice of tree species for nesting. For this study, the marked nests were in low number; they also considered: there is no reason for expecting that every tree species of appropriate diameter is equally likely to have cavities suitable for nest sites, since undoubtedly some species are more prone to cavity formation than others. However, they did not found evidences for trees selectivity as nest sites. Eltz et al. (2002) evaluated the nest density of stingless bees in undisturbed and logged over dipterocarp forests in Sabah, Borneo. They also focused the population control mediated by 1) nest predation; 2) limitation of nest trees; 3) food limitation. Observations, as in the previous study mentioned above, were also 4 years round. They concluded that the abundance of stingless bees in forests in Sabah is chiefly dependent on 16

17 the local availability of food resources. Bee populations strongly benefit from edge effects and increased foraging habitat diversity. The authors found 16,2 nests/ha, far exceeding 2,8 nests/ha in Belalong Forest from Brunei and 2-4 nests/ha in Costa Rica, by Hubbell and Johnson. Roubik, in a 5ha area, found 5,88 nest/ha; Michener (1964) in Panama studied a 64ha area and found 2,17 nests/ha. Eltz et al. (op. cit.) worked in the boundaries of mangroves, and studied the pollen collected by the bees. They concluded that Rizophora, an important mangrove species, was a relevant source of pollen for stingless bees. Mangroves have few plant species, but present in high quantities. In North Brazil, Venturieri et al. (2003) studied the Melipona nests in the mangrove area in Pará, who also produces a lot of honey. There are no available data on nest densities in this area, comparing to those that do not face the mangrove. But Avicennia, one of the 3 plant species of the local mangrove, was one of the main plant sources for these bees. Eltz et al. (2003) also considered the negative impact of logging on stingless bees, in the same area. They analyzed the commercial potential of 142 nest trees of stingless bees in dipterocarp forests in Sabah and concluded that one-third would qualify for harvesting in case of logging operation. Batista et al. (2003) focused on nesting sites in a fragment of Atlantic Rainforest, in Bahia. In an area of 11,3ha containing three habitat types 16 species of stingless bees were found. Tetragonisca angustula was the most abundant species, occurring in all habitats, with 30,7% of found nests. These authors also consider that its ecological plasticity is allied with aggressive patrolling of potential nests cavities, and also to the high swarming rate observe by this bee. Nests were abundant in altered landscape. Artificial offering of nests sites Another possibility of deal with nest sites as a limited resource is to establish artificial trap nests, offering nests sites for stingless bees. Inoue et al. (1993) did these 17

18 experiments in order to know more about the population dynamics of stingless bees. They studied an area of the Horticultural Experimental Station in Lubuk Mintrum, in Sumatra, where the main vegetation was a plantation of tropical fruits (rambutan, N. lappaceum, and durian, D. zibethinus (ca 480x200m, 8-6ha) where 24 species of stingless bees were found. The species Trigona (Tetragonula) minangkabau was the most common, and suitable for their study. They censused tree cavities and possible artificial nesting sites to estimate the number of natural colonies. At these censuses, 2 persons searched 4 days. They also set 362 trap nests in the field, of which 248 were perforated bamboo stems and 114 wood boxes with glass tops. Trap nests were set in January 1981 (100); December 1981/January 1982 (138) December 1982 (75) and October 1983 (49). Nests were observed during 56 months. The results were: 1. Trap nests were used by many animals, as social insects (mainly ants) and vertebrates (geckos, for instance); 2. Only T. (Tetragonula) minangkabau occupied the trap nests; 3. Ants occupied 20% of empty nets; 4. Bees occupied 6% of empty nests; 5. Colonies were found monthly during all experiment; 6. Successful in nest establishment was also recorded This experiment shows that additional nest sites offer can improve the bee density in the area, and that trap nests are suitable only for some species. Antonini & Martins (2002) used trapnests in Cerrado (Brazilian Savanna) without any result, in an area where they found 46 nests of Melipona quadrifasciata. This bee species nested mainly in Caryocar brasiliense, a protected tree from cerrado, abundant in the studied area. Several trees had hollows available for M. quadrifasciata. Sometimes M. quadrifasciata swarms to empty Apis colonies that have wax or food inside. This is common also for other stingless bees: as wax is a costly product, they 18

19 often swarm to empty hives with residues of construction materials, even if they belong to other bee species or in laboratories conditions. This is an indication that trap nests should contain some wax or cerumen inside, in order to be more attractive to the bees. In Brazil, recently stingless bees keepers are using pet bottles as traps nests. In a beekeeping meeting this year in Rio Grande do Sul (Encontro dos meliponicultores) some of them reported that Tetragonisca angustula, a very common stingless bee species and that could be used as crop pollinators for strawberry (Malagodi-Braga and Kleinert, 2004), nested in pet bottles offer as traps. A deeper research on this subject is urgent, and will be suggested in our recommendations. How many stingless bees nests are there in a tree? Hubbell & Johnson (1977) verified in Guanacaste Provincia, Costa Rica, the frequency of nest occupation by tree: 10 sp had 1 nest; 7 species had 2 nests; 4 species, 3 nests; 1 tree species contained 4 nests; 2 species, 5 nests; 1 species was found with 6 nests and 11 nests respectively, Martins et al. (2004) studied the nesting opportunities that trees offer to stingless bees (Meliponini), in the semi-arid Caatinga of Northeast Brazil. Samples consisted mostly of tree trunks, which were kept by Meliponini beekeepers. Nearly 13% of observed nests were in living trees in the field. Seven species of stingless bees, totaling 227 nests, were found in 12 tress species. More than 75% of stingless bees were found in Caesalpinea pyramidalis (49%) and Commiphora leptophloeos (Burseraceae, 33,9%). Furthermore, all bee species nidified in C. pyramidalis. A great part of the nests in trunks were of Melipona subnitida (n=130), of which 50% were found in C. leptophloeos and 22,3% in C. pyramidalis. M. asilvae was predominantly found in C. pyramidalis (92,3%, n=39). One of those C. pyramidalis trees had nine nests: seven of Frieseomelitta varia dispar and two nests of Scaptotrigona aff. depilis. One Schinopsis brasiliensis tree had 19

20 ten nests of Frieseomelitta varia dispar. Those tree species were indicated for nursery in Caatinga, important for environmental restoration. Currently, Caatinga suffers from two main human impacts: the cutting of trees for firewood and its use as cattle land. Some Caatinga regions already have turned into desert. Camargo & Pedro (2004) found in Salvertia convallariodora five nests: Ptilotrigona lurida, Scaptotrigona sp., Tetragona clavipes, Trigona pallens and Melipona compressipes fasciculata. Remarkable is also Campsiandra angustifolia, a tree from Amazon igapós where 23 and 30 nests of Schwarzula sp. were found, in tunnels burrowed by moth larvae. This is a specialized bee species, that live in association with soft scale insects, Cryptostigma sp., that they house and attend (Camargo, 2002). Antonini & Martins (2002) in Brazilian Cerrado found 20% of Caryocar brasiliense trees with two nests of Melipona quadrifasciata, and nests of Frieseomelitta varia, F. silvestri, Partamona cupira, Scaptotrigona postica and Tetragonisca angustula (maximum number in a tree, 13 nests). Stingless bees nests in Asia In Asia, stingless bees nests have been recently studied with different approach by several authors. Sakagami et al described the nests of some Southeast Asian stingless bees. Starr & Sakagami (1987) described nest aggregations of stingless bees in Philippines. Salmah et al. (1990) worked on the influence of human disturbance on stingless bees in Central Sumatra; they found that species diversity and abundance of stingless bees decreased along the disturbed gradient. Roubik (1996) also evaluated diversity of stingless bees in Brunei Darussalan, with salt and sugar baits. Eltz studied the 20

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