Print version ISSN 0085-5626
Rev. Bras. entomol. vol.56 no.1 São Paulo Jan./Mar. 2012
Giselle B. MenezesI; Vania Gonçalves-EstevesII; Esther M. A. F. BastosIII; Solange C. AugustoIV; Maria Cristinna GaglianoneI
ILaboratório de Ciências Ambientais, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Av. Alberto Lamego, 2000, Parque Califórnia, 28013-602 Campos dos Goytacazes-RJ, Brasil. firstname.lastname@example.org; email@example.com
IILaboratório de Palinologia, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, Horto Botânico, São Cristóvão, 20940-040 Rio de Janeiro-RJ, Brasil. firstname.lastname@example.org
IIILaboratório de Recursos Vegetais e Apiterápicos, Fundação Ezequiel Dias, Rua Conde Pereira Carneiro, 80, Gameleira, 30510-010 Belo Horizonte-MG, Brasil. email@example.com
IVLaboratório de Ecologia e Comportamento de Abelhas, Universidade Federal de Uberlândia, Campus Umuarama, Bloco 2D, 38400-902 Uberlândia-MG, Brasil. firstname.lastname@example.org
Nesting and use of pollen resources by Tetrapedia diversipes Klug (Apidae) in Atlantic Forest areas (Rio de Janeiro, Brazil) in different stages of regeneration. The nesting in trap-nests and use of pollen sources in larval food by Tetrapedia diversipes Klug, 1810 (Apidae) was compared between regenerating areas of Atlantic Forest. The study was conducted between April 2008 and October 2009 at União Biological Reserve, Rio de Janeiro, Brazil. T. diversipes nested in 66 trap-nests and showed a peak of nesting during the months of highest rainfall. The most frequent pollen type in brood cells during the wet season was Dalechampia sp. 1. During the dry season, the type Ludwigia sp. was the most frequent, followed by Dalechampia sp. 2. The high frequency of Dalechampia and Ludwigia species in the larval food, observed in both habitats and in the two seasons could be considered relevant for T. diversipes, suggesting highly selective diet based primarily on two plant species unrelated, but similar in size of pollen grains.
Keywords: Atlantic rainforest; Oil collecting bee; Pollen analysis; Tetrapediini; Trap-nests.
Nidificação e uso de fontes de pólen por Tetrapedia diversipes Klug (Apidae) em áreas de Mata Atlântica (Rio de Janeiro, Brasil) em diferentes estágios de regeneração. A nidificação em ninhos-armadilha e o uso de fontes de pólen no alimento larval por Tetrapedia diversipes Klug, 1810 (Apidae) foram comparados entre áreas de Floresta Atlântica em regeneração. O estudo foi realizado entre abril de 2008 e outubro de 2009 na Reserva Biológica União, Rio de Janeiro, Brasil. T. diversipes nidificou em 66 ninhos-armadilha e apresentou um pico de nidificação durante os meses de maior precipitação pluviométrica. O tipo polínico mais frequente nas células de cria durante a estação chuvosa foi Dalechampia sp. 1. Durante a estação seca, o tipo Ludwigia sp. foi o mais frequente, seguido de Dalechampia sp. 2. A alta frequência de espécies de Dalechampia e Ludwigia no alimento larval, observada em ambos os habitats e nas duas estações deve ser considerada um fato relevante para T. diversipes, sugerindo uma dieta altamente seletiva baseada primariamente em duas espécies vegetais não relacionadas, porém semelhantes quanto ao tamanho dos grãos de pólen.
Palavras-chave: Abelha coletora de óleo; Análise polínica; Floresta Atlântica; Ninhos-armadilha; Tetrapediini.
Oil-collecting bees in the Neotropics belong to three tribes: Centridini, Tapinotaspidini and Tetrapediini (Alves-dos-Santos et al. 2007). Traditionally Tetrapediini bees include two genera: Tetrapedia, composed by oil-collecting and nest-constructing bees and Coelioxoides, cleptoparasite species of Tetrapedia (Alves-dos-Santos et al. 2002) although recent phylogenetic analyses do not confirm the monophyly of the tribe (Cardinal et al. 2010).
The genus Tetrapedia comprises solitary bees widely distributed in tropical regions of the Americas and represented by 18 species in Brazil (Moure 2008). Their females commonly nest in cavities in wood, and they may also occupy the inactive nests of other Hymenoptera such as Anthodioctes megachiloides Holmberg, 1903 (Megachilidae) and Trypoxylon (Crabronidae) (Alves-dos-Santos et al. 2002). The reuse of cells from abandoned nests of Polistes simillimus Zikán, 1951 (Vespidae) by Tetrapedia diversipes Klug, 1810 has also been observed (Pinto 2005). In addition to building its nests in pre-existent wood cavities, T. diversipes can also be attracted to trap-nests (Roubik 1987; Alves-dos-Santos et al. 2002; Garófalo et al. 2004; Camillo 2005). This sampling methodology gives access to significant information about nesting species, such as nesting biology, building materials, architecture, and food resources provided for larvae (Garófalo et al. 2004).
Although the biology of T. diversipes is well known (Alves-dos-Santos et al. 2002; Camillo 2005), reports of interaction between this species and food sources are poorly described in the literature, as well as information about its importance as a pollinator. Analysis of the pollen in larval food gives precise information about the range of plants visited and the relative importance of those sources to the bees (Dórea et al. 2010).
Bees are important components of biological communities, not only because of their role as pollinators, but also because they can be very sensitive to the effects of environmental disturbances (Morato & Campos 2000; Steffan-Dewenter 2003; Holzschuh et al. 2010). Among bees, species that specialize in the collection of floral oils compose an important guild of pollinators associated with specific plant groups in several ecosystems, such as the Atlantic Forest, cerrado and restinga (Teixeira & Machado 2000; Gaglianone 2003, 2006; Dunley et al. 2009). Currently, only approximately 7% of the original extent of the Atlantic Forest remains. This is one of the biomes most affected by deforestation (Myers et al. 2000; Morellato & Haddad 2000). In the state of Rio de Janeiro, the process of forest devastation and fragmentation has been quite intense, and currently 18,4% of its original vegetation cover is in either privately or publicly held conservation areas (SOS Mata Atlântica/INPE 2010).
Due to the reduction of natural areas in recent decades, the study of biological processes in altered ecosystems is being emphasized (Saunders et al. 1991; Naeem 2002). Of particular interest are insects with important ecological functions, such as predators, parasites and pollinators; these are frequently used in studies evaluating the effects of habitat loss on biodiversity (Tscharntke 1992; Kevan 1999; Steffan-Dewenter & Tscharntke 2002). However, such studies involving the Atlantic Forest are still rare (Viana et al. 2006; Loyola & Martins 2008, 2009). Comparing nesting parameters in Atlantic Forest areas in different stages of regeneration can indicate preferences and fidelity to certain habitats, providing important information about the handling and conservation of these bees.
The objective of this study is to compare the use of Atlantic Forest habitats in different stages of regeneration by T. diversipes bees by considering trap-nest occupation, seasonality, and sources of pollen.
MATERIAL AND METHODS
This study was carried out at União Biological Reserve (Rebio União) (22º25'40"S, 42º02'06"W), located in the municipalities of Rio das Ostras, Casimiro de Abreu and Macaé, in the northern portion of Rio de Janeiro state, Brazil, between March 2008 and October 2009. The area contains 3126 ha: 2400 ha of dense Atlantic ombrophilous forest vegetation, 215 ha of abandoned eucalyptus plantation interspersed with native vegetation, and the remaining consists of areas altered by human action (IBAMA 2007). In these former plantations, the native species are regenerating themselves and forming an understory (Evaristo 2008). The predominating vegetation is considered one of the best preserved in the coastal lowlands in Rio de Janeiro state, even though there are areas in regeneration that were altered due to selective logging, hunting, introduction of exotic species in the area (eucalyptus and fruit trees), and the construction of high tension power lines and underground ducts for the transportation of combustible materials (IBAMA 2007). The predominant climate in the region is humid tropical, with a median annual temperature of 24ºC and 1658 mm/year of rainfall, of which 75% occurs between October and April (IBAMA 2007).
Twelve sampling sites were selected at Rebio União: six in understory areas of abandoned eucalyptus plantations where there are native species in initial stage of regeneration (henceforth termed eucalyptus with regenerating understory, ERU); and six areas of secondary Atlantic Forest (SAF) in advanced stage of regeneration. An identical number of trap-nests (n = 1440) was installed at the sites monthly. These trap-nests were either bamboo canes of various diameters grouped in sets of three and attached to poles at approximately 1.5m above the ground, or black cardboard tubes varying from 4 to 15 mm in diameter and inserted in wood blocks at the same height. The trap-nests were checked monthly and replaced with new ones after they were closed by the bees. The occupied nests were brought to the laboratory, kept at room temperature and checked daily. The plant species in bloom, within a radius of 200 meters close to the nesting sites in areas of eucalyptus with regenerating understory, were also collected monthly for the development of a reference collection of pollen slides of this area.
After the T. diversipes adults emerged, the trap-nests were opened and the pollen content in the brood cells was removed and stored with glacial acetic acid to acetolysis (see Erdtman 1960). The cell with the highest pollen content from each nest studied was visually selected, and all the pollen content was fixed as the representative sample of the nest. After the samples were acetolyzed, three slides were prepared from each one, and the types of pollen were identified and quantified. The exclusive pollen types were considered as those found uniquely in samples obtained in one habitat and season studied. The qualitative analysis consisted of determining the genera and types of pollen (group of grains with very similar morphology) according to specialized literature (Salgado-Labouriau 1973; Roubik & Moreno 1991) and refe-rence slides from the study area. Quantitative analysis was performed by counting 400 pollen grains per slide and 1200 grains per sampled nest.
The trap-nests occupancy rate was calculated as the ratio between the number of occupied cavities in relation to total cavities available monthly. In order to examine the relation of nesting frequency and emergence of adults per month with climate variables (rain and average temperature), the Spearman (rs) correlation was calculated. The nesting frequency of T. diversipes was compared between areas using the Mann-Whitney (U) test. The sex ratio was calculated using the ratio between the number of females and the number of males that emerged from the nests.
The head width of emerging T. diversipes was taken measuring the distance between the external edges of the eyes at the level of the base of the antenna. The analysis of the Spearman (rs) correlation was used to test the relation between the median width of the head and the diameter class of the cavity from which the individual emerged. The median number of cells per nest was compared between areas using the Mann-Whitney (U) test. The confidence interval for all statistical tests was 5%. The diversity of food sources visited and evenness in their use was calculated using Shannon-Wiener diversity index and evenness test, respectively, according to Magurran (2003). The similarity percentage was used to calculate the similarity of food sources visited between areas, according to Krebs (1989).
Nesting and seasonality. A total of 1440 trap-nests (bamboo canes and cardboard tubes) were available monthly in the twelve sampling sites between March 2008 and October 2009. The study registered 1200 cavities occupied by solitary Hymenoptera (bees and wasps), and of those, 130 were used by oil-collecting bees. The maximum occupation rate per month (occupied trap-nests/available trap-nests) by oil collecting bees was 1.8%. Tetrapedia diversipes was the oil-collecting bee that nested in most of the cavities, building 66 nests, 44 of them between September and January in ERU, and the other 22 between October and June in SAF (Fig. 1). Nesting peak in both habitats was during the rainiest months (Fig. 1). There was a positive correlation between the nesting frequency of T. diversipes and precipitation (rs = 0.57; p < 0.05) and temperature (rs = 0.66; p < 0.05) in the areas of ERU. However, there was no significant correlation between these variables in SAF areas (rs = 0.36; p > 0.05 and rs = 0.17; p > 0.05, respectively). The total number of emerging T. diversipes individuals was 64 males and 53 females in ERU areas (sex ratio 1:0.83), and 33 males and 16 females in SAF areas (sex ratio 1:0.48). Most of T. diversipes adults emerged between November 2008 and April 2009 in both habitats, and the least productive months were August, September and November 2009 (Fig. 2). There was a significant correlation between frequency of emergence and precipitation in ERU areas (rs = 0.45; p < 0.05); however, the same result was not observed in SAF areas (rs = 0.40; p > 0.05). No significant difference was observed in the number of individuals emerging per nest in the habitats studied (U = 140.5 p > 0.05) (Table I).
Nests of T. diversipes were built only in cardboard tubes, and the diameters used in both habitats varied from 4 to 10 mm, with no significant difference in the diameters used between habitats (U = 433.5 p > 0.05) (Table I). Cavities between 6 and 8 mm were the most used and included 65% of the nests built. A total of 117 individuals emerged from nests constructed in the ERU areas, and 49 from those in the SAF areas. The median head width of the emerging T. diversipes individuals was 2.6 ± 0.7mm. There was a significant positive correlation between the cavity size and head width of the emerging individuals (rs = 0.86; p < 0.05). The number of cells built in nests from ERU (n = 164) was higher than that of SAF (n = 76), varying from 1 to 8 cells per nest. There was no significant difference in the median number of cells built per nest between areas (U = 443.0; p > 0.05) (Table I). The cells were always arrayed in rows inside the cavities, and a mixture of oil and sand was used to build the internal nest structure.
Food resources. From nests obtained in the wet season (October 2008, December 2008, and January 2009), eighteen T. diversipes nests from each habitat had enough pollen to be analyzed; while in the dry season (April 2009 and June 2009) only three nests from the eucalyptus with regenerating understory area could be examined, totalling 117 pollen grain slides analyzed.
From wet season nests in ERU, 20 types of pollen (with nine exclusive types) belonging to 12 botanical families were identified (Table II); in SAF, 18 types were identified (with seven exclusive types) belonging to 11 families (Table III). Eleven types were observed in dry season nests from ERU (seven botanical families), including five exclusive types (Table IV).
The most frequent type of pollen in the wet season for both physiognomies was Dalechampia sp. 1 (Fig. 3A and B), with a median frequency of occurrence of 81.4% (ERU) and 90.3% (SAF) in the samples. In addition to its high frequency, Dalechampia sp. 1 was present in all wet season samples from both habitats considered in this study (Table II and III). The similarity percentage for resource use in both habitats during the period considered was 93.54%, even though exclusive types of pollen were observed in both habitats.
Ludwigia sp. (Fig. 3D) was the most frequent type of pollen in ERU during the dry season, followed by another species of Dalechampia that also appeared in this period, Dalechampia sp. 2 (Table IV and Fig. 3C).
According to the pollen analysis, the diversity of food resources was significantly higher in ERU than in the SAF area during the wet season (t = 42.3; df = 19; p < 0.05), and the use of resources was more uniform (Table V). The similarity in food resource use between the dry and wet seasons in ERU was 17.66%. During the dry season, the diversity of food resources used in the ERU area was significantly higher than that observed during the wet season in both the eucalyptus and secondary forest areas (t = 20.5; df = 19; p < 0.05 and t = 47.1; df = 19; p < 0.05, respectively).
The plant species found in bloom near the nesting sites in the ERU area were mainly herbaceous plants. There was a total of 49 species from the families: Annonaceae (1sp.), Apocynaceae (1sp.), Asclepiadaceae (1sp.), Asteraceae (9sp.), Bignoniaceae (3sp.), Capparaceae (2sp.), Celastraceae (1sp.), Convolvulaceae (2sp.), Lamiaceae (1sp.), Leguminosae Caesalpinioidea (2sp.), Leguminosae Faboidea (10sp.), Malpighiaceae (2sp.), Malvaceae (3sp.), Melastomataceae (3sp.), Myrtaceae (2sp.), Rubiaceae (2sp.), Rutaceae (2sp.) and Verbenaceae (2sp.). None of these pollen types were found in larval food from the analyzed cells.
The data obtained in the study showed Tetrapedia diversipes as the most frequent oil collecting bees sampled in trap-nests. This pattern was described by Garófalo et al. (2004) as occurring in other forest fragments studied in the southeast of Brazil. This relatively high abundance of nests is probably due to the low average number of brood cells observed inside the nests of this species. Alves-dos-Santos et al. (2002) also observed that most nests of T. diversipes analyzed in that study had consisted of few cells (2 to 3 cells), and, after building a nest and closing the cells, the same female looked for cavities close to the one used previously to build another nest.
The number of constructed nests was considerably higher in the eucalyptus with regenerating understory (ERU) areas than in the secondary Atlantic Forest (SAF) areas. In general, the abundance of nests built in pre-existent cavities by solitary Hymenoptera species can be related to the existence of appropriate materials for the construction and availability of food resources for adults and larvae (Roubik 1989). In addition, the availability of natural substrates in the environment for nesting has also been indicated as an influential factor in the abundance of nests in traps (Viana et al. 2001). We could not precise if these factors are influencing the highest number of nests in eucalyptus areas. The analysis of cell pollen content showed that most of the plants observed in bloom in this area during the T. diversipes nesting period were not used by these bees to feed the larvae. However, the high abundance of Byrsonima sericea DC (Malpighiaceae) in the eucalyptus area (Evaristo 2008) may have been attractive to this species since floral oils are necessary to build the nest cells (Alves-dos-Santos et al. 2002). Nevertheless, there was a low frequency of pollen grains from this plant in larval food samples, and a low frequency of T. diversipes females has been observed foraging in B. sericea flowers (Menezes & Gaglianone unpubl. data). This data suggest, therefore, that this bee species is using the eucalyptus area mainly for nesting and not for foraging.
Regarding the availability of natural substrates, the habitats considered in this study are very different in their complexity; the richness of plant species found in the secondary forest (Prieto 2008) is superior to that of eucalyptus with regenerating understory (Evaristo 2008). Even though the availability of natural cavities was not directly evaluated in this study, the higher floral richness and higher structural complexity of the forest suggest that the possibilities of natural substrate for nesting are better in the secondary forest environment. If this is indeed the case, the high frequency of nests built by T. diversipes in the traps installed in the area of eucalyptus with regenerating understory may be due to the greater limitation of such resources in this environment. However, T. diversipes is a species easily found in open habitats containing less dense vegetation, which could also justify its greater preference for the area of eucalyptus with regenerating understory. If so, the higher frequency of nests in the eucalyptus area would be expected due to the species' intrinsic preference. Studies about this species in other environments could help clarify this question.
Tetrapedia diversipes nesting activities and emergence were seasonal. There was a significant positive correlation between the frequency of these events and the environmental variables precipitation and temperature in the area of eucalyptus with regenerating understory. Even though this result did not occur in the secondary forest area, the period with the highest nesting and emergence of T. diversipes also corresponded to the months of the hot wet season. These data agree with findings in other regions about T. diversipes seasonality in forest trap-nests (Alves-dos-Santos et al. 2002; Alves-dos-Santos 2003). The authors reported that, in urban forest areas in São Paulo, adult females were observed to nest in the wet season, with peaks of activity from November to December and March to April (Alves-dos-Santos 2003). During the cold dry season (between June and August) bees from this species were in diapause at a mature larval stage (Alves-dos-Santos et al. 2002). Therefore, it was observed that despite climatic differences with the area of the present study, including the less pronounced seasonality and higher median temperatures of the latter, T. diversipes presented a seasonal pattern similar to that observed in areas further south in Atlantic Forest in the state of São Paulo.
It was observed strong preference of T. diversipes by cardboard tubes compared to bamboo canes, although the former is a non-natural substrate. A slight preference for cardboard tubes was also verified by Aguiar et al. (2005) and Nascimento & Garófalo (2010), but these authors found also nests of this species in bamboo canes. Thus, the type of material used for trap-nests can be suggested as an influential factor in the choice of nesting cavity. The variation in cavity diameter used by T. diversipes was positively correlated with the body size of these bees, justifying the high utilization of trap-nest cavities with diameters between 6 and 8 mm, which are compatible with the median body size of the individuals at Rebio União. Larger orifices would demand a greater expenditure of energy both to stock the cells and fill in gaps and, accordingly, were rarely used. A higher use of trap-nests with diameters between 6 and 8 mm was also verified by Cordeiro (2009) in areas of dense ombrophile forest.
The architecture of the nests was similar to nests from urban forest areas (Alves-dos-Santos 2003), as well as nests in semideciduous cerrado forest (sensu lato) (Camillo 2005), particularly regarding the size, arrangement and material used for the cells. This indicates that, regardless of the environment, these characteristics of nesting biology are preserved.
The richness of pollen sources in T. diversipes cells was high, as also observed by Coelho et al. (2010). However, the high abundance of Ludwigia (Onagraceae) and Dalechampia (Euphorbiaceae) species in the larval food observed in both habitats and in both seasons at Rebio União should be considered a relevant fact about T. diversipes, suggesting highly selective diet based primarily on two plant species unrelated, but similar in size of pollen grains. This does not characterized an oligolectic bee, but Tetrapedia diversipes surely is not a true generalist bee. The preferred plant species were not observed in the eucalyptus area, expected fact for Ludwigia, since their species grow preferably in flooded habitats (Ramamoorthy & Zardini 1987). Such a habitat, however, was verified at Rebio União approximately 100 to 200 m from the study area. Although Ludwigia has not been observed in bloom in this flooded habitat, its occurrence there is probably right. Thereby, the high abundance of this pollen type in the larval food corroborates the hypothesis that the bees are using other areas for foraging.
Silveira et al. (1993) and Alves-dos-Santos (1999) also reported on the interaction between T. diversipes and Ludwigia flowers in Atlantic Forest areas in the states of Minas Gerais and Rio Grande do Sul in Brazil, respectively. A study carried out by Sazima & Santos (1982) about the floral biology of the Ludwigia sericea (Cambess.) H. Hara in Campinas, SP, demonstrated that one species of Tetrapedia was the effective pollinator of this plant in the area. This was determined from pollen collecting behavior as well as the frequency and time of permanence on the flowers. Similarly, Gimenes (2002) verified the efficiency of Tetrapedia sp. as a pollinator of Ludwigia elegans (Cambess.) H. Hara in marshy areas of the Parque do Carmo in the city of São Paulo. Other reports in the literature refer to the interaction between Tetrapedia and Euphorbiaceae species (Armbruster & Herzig 1984; Alves dos Santos et al. 2002). In the former study, the authors observed visits of Tetrapedia sp. to Dalechampia tiliifolia Lam. in Panamá in which flowers these bees only collected pollen. The authors did not consider Tetrapedia sp. to be an effective pollinator of Dalechampia tiliifolia, probably because of the contrasting sizes of flowers and bees. The large size of the flowers requires large resin-collecting bees for acting as pollinators. Alves-dos-Santos et al. (2002) reported a high dominance of one Dalechampia species as well as a Croton species (both belong to Euphorbiaceae) observed in pollen samples from T. diversipes nests collected at the University of São Paulo campus. Although flowers of Dalechampia are primary sources of resin for other bees (Armbruster & Webster 1981; Armbruster & Herzig 1984), they seem to be important sources of pollen for T. diversipes. The high frequency of Dalechampia's pollen grains in the analyzed samples and the absence of information on resin collection by Tetrapedia bees, reinforce the evidence that Dalechampia species are important sources of pollen for this bee. Other studies have described the collection of resources by T. diversipes from flowers of other families, such as nectar in Orchidaceae (Oncidium paranaensis Kraenzl.), pollen in Cactaceae (Opuntia sp.) in the city of Curitiba (Singer & Cocucci 1999) and oil in Malpighiaceae (Heteropterys umbelata A. Juss.) in the cerrado of São Paulo (Pedro 1994). It is well known that the oil-collecting behavior of T. diversipes on flowers of Malpighiaceae rarely results in contact with anthers, as the collection of this resource is held by these bees in the underside of the flowers (Rêgo & Albuquerque 1989). As described by Vogel (1990), Tetrapedia bees are illegitimate flower visitors on Malpighiaceae flowers. This behavior explains the low proportion of Malpighiaceae's pollen observed in the analysed samples of T. diversipes in this study.
In general, the diversity of sources used by T. diversipes during the wet season was higher in the area of eucalyptus with regenerating understory than in the secondary forest, even though the frequency of non-dominant pollen types was very low in both areas. The proximity to open and flooded areas, as well as the presence of a great number of vines and ruderal plant species around the area of regenerating forest could have influenced this result.
None of the 49 herbaceous species collected near the T. diversipes nesting sites in the area of eucalyptus with regenerating understory was found in the pollen samples from larval food analyzed. Among the tree-shrub species inventoried in this environment by Evaristo (2008), only the types Byrsonima, Myrcia and Eugenia were found, although with a low frequency (less than 15%). This result suggests that these plants are not been used as primary pollen sources, but oil and nectar. The low frequency of these types may also have resulted from accidental contact with pollen grains from these plants during foraging for other resources. These results reinforce the hypothesis that the area of eucalyptus with regenerating understory at Rebio União is being used by T. diversipes principally as a nesting site since the potential resources in this habitat are insufficient for maintaining the T. diversipes population. Thus, this study has proved that the area of eucalyptus with regenerating understory at Rebio União already does not contain preferred resources for these bees. The management of these areas through the removal of eucalyptus, currently underway, should improve the regeneration of plant species and the habitat diversity. This process is essential for increasing the availability of other important resources to the bees in the União Biological Reserve. Therefore, the monitoring of these bees is necessary to assess possible changes in the community and also to identify plants resources for the bees, including oil plants, which can colonize these areas in later successional stages.
We thank the Instituto Chico Mendes (ICM-Bio) for permission to study at Rebio União (União Biological Reserve), Rio de Janeiro, Brazil (license number 14871-5); to CAPES/PROCAD (158/07) and FAPERJ for financial support for this project (Pensa Rio 09/07) and for the scholarship award to the first author; to Gabriel A. R. Melo (UFPR) for identifying the bee species; to Helmo Siqueira, Marcelle Muniz Barreto, Mariana Scaramussa Deprá (UENF), Alice Maria Fernandes Vilhena and Laice Souza Rabelo (UFU) for assistance in field and laboratory activities.
Aguiar, C. M. L.; C. A. Garófalo & G. F. Almeida. 2005. Trap-nesting bees (Hymenoptera, Apoidea) in areas of dry semideciduous forest and caatinga, Bahia, Brazil. Revista Brasileira de Zoologia 22: 1030-1038. [ Links ]
Alves-dos-Santos, I. 1999. Abelhas e plantas melíferas da mata atlântica, restinga e dunas do litoral norte do Estado do Rio Grande do Sul, Brasil. Revista Brasileira de Entomologia 43: 191-223. [ Links ]
Alves-dos-Santos, I. 2003. Trap-nesting bees and wasps on the University campus in São Paulo, Southeastern Brazil (Hymenoptera: Aculeata). Journal of the Kansas Entomological Society 76: 328-334. [ Links ]
Alves-dos-Santos, I.; I. C. Machado & M. C. Gaglianone. 2007. História natural das abelhas coletoras de óleo. Oecologia Brasiliensis 11: 544-557. [ Links ]
Alves-dos-Santos, I.; G. A. R. Melo & J. G. Rozen, Jr. 2002. Biology and imature stages of the bee tribe Tetrapediini (Hymenoptera: Apidae). American Museum Novitates 3377: 1-45. [ Links ]
Armbruster, W. S. & A. L. Herzig. 1984. Partitioning and sharing of pollinators by four sympatric species of Dalechampia (Euphorbiaceae) in Panama. Annals of the Missouri Botanical Garden 71: 1-16. [ Links ]
Armbruster, W. S. & G. L. Webster. 1981. Sistemas de polinização de duas espécies simpátricas de Dalechampia (Euphorbiaceae) no Amazonas, Brazil. Acta Amazônica 11: 13-17. [ Links ]
Camillo, E. 2005. Nesting biology of four Tetrapedia species in trap-nests (Hymenoptera: Apidae: Tetrapediini). Revista Biología Tropical 53: 175-186. [ Links ]
Cardinal, S.; J. Straka & B. N. Danforth. 2010. Comprehensive phylogeny of apid bees reveals the evolutionary origins and antiquity of cleptoparasitism. Proceedings of the National Academy of Sciences of the United States of America 107: 16207-16211. [ Links ]
Coelho, T. A.; R. B. S. P. Araujo; G. D. Cordeiro; C. I. Silva; C. Krug & I. Alves-dos-Santos. 2010. Rede de interação das plantas visitadas por Tetrapedia diversipes Klug (Apidae: Tetrapediini) revelada por análise polínica do alimento larval. Anais do IX Encontro sobre Abelhas: 455. [ Links ]
Cordeiro, G. D. 2009. Abelhas solitárias nidificantes em ninhos-armadilha em quatro áreas de Mata Atlântica do estado de São Paulo. Master Dissertation, São Paulo, Universidade de São Paulo, 84 p. [ Links ]
Dórea, M. de C.; C. M. L. Aguiar; L. E. R. Figueroa; L. C. L. Lima & F. de A. R. dos Santos. 2010. Pollen residues in nests of Centris tarsata Smith (Hymenoptera, Apidae, Centridini) in a tropical semiarid area in NE Brazil. Apidologie 41: 557-567. [ Links ]
Dunley, B. S.; L. Freitas & L. Galetto. 2009. Reproduction of Byrsonima sericea (Malpighiaceae) in restinga fragmented habitats in southeastern Brazil. Biotropica 41: 692-699. [ Links ]
Erdtman, G. 1960. The acetolized method. A revised description. Svensk Botanisk Tidskrift 54: 561-564. [ Links ]
Evaristo, V. T. 2008. Dinâmica da comunidade e das principais populações arbustivo-arbóreas de mata atlântica em plantios abandonados de eucalipto Corymbia citriodora (Hook.) K.D.Hill & L.A.S. Johnson. Master Thesis, Campos dos Goytacazes, Universidade Estadual do Norte Fluminense Darcy Ribeiro, 141 p. [ Links ]
Gaglianone, M. C. 2003. Abelhas da tribo Centridini na Estação Ecológica de Jataí (Luiz Antonio, SP): composição de espécies e interações com flores de Malpighiaceae, p. 279-284. In: G. A. R. Melo & I. Alves-dos-Santos (eds.). Apoidea Neotropica: Homenagem aos 90 anos de Jesus Santiago Moure. Criciúma, Editora UNESC, 320 p. [ Links ]
Gaglianone, M. C. 2006. Centridini em remanescentes de Mata Atlântica: diversidade e interações com flores. Anais do VII Encontro sobre Abelhas: 335-340. [ Links ]
Garófalo, C.A.; C. F. Martins & I. Alves-dos-Santos. 2004. The Brazilian solitary bee species caught in trap nests, p. 77-84. In: B. M. Freitas & J. O. P. Pereira (eds.). Solitary bees: conservation, rearing and management for pollination. Fortaleza, Imprensa Universitária, 285 p. [ Links ]
Gimenes, M. 2002. Estudo da atividade diária das abelhas visitantes (Hymenoptera, Apoidea) nas flores de Ludwigia elegans (Camb.) Hara (Onagraceae). Acta Biologica Leopoldensia 24: 47-56. [ Links ]
Holzschuh, A.; I. Steffan-Dewenter & T. Tscharntke. 2010. How do landscape composition and configuration, organic farming and fallow strips affect the diversity of bees, wasps and their parasitoids? Journal of Animal Ecology 79: 491-500. [ Links ]
IBAMA - Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis. 2007. Plano de Recuperação dos Eucaliptais da Reserva Biológica União. Rio das Ostras, IBAMA, 141 p. [ Links ]
Kevan, P. G. 1999. Pollinators as bioindicators of the state of the environment: species, activity and diversity. Agriculture, Ecosystems & Environment 74: 373-393. [ Links ]
Krebs, C. J. 1989. Ecological Methodology. New York, Harper and Row Publishers, 654 p. [ Links ]
Loyola, R. D. & R. P. Martins. 2008. Habitat structure components are effective predictors of trap-nesting Hymenoptera diversity. Basic and Applied Ecology 9: 735-742. [ Links ]
Loyola, R. D. & R. P. Martins. 2009. On a habitat structure-based approach to evaluating species occurrence: cavity-nesting Hymenoptera in a secondary tropical forest remnant. Journal of Insect Conservation 13: 125-129. [ Links ]
Magurran, A. E. 2003. Measuring Biological Diversity. Oxford, Wiley-Blackwell, 260 p. [ Links ]
Morato, E. F & L. A. de O. Campos. 2000. Efeitos da fragmentação florestal sobre vespas e abelhas solitárias em uma área da Amazônia Central. Revista Brasileira de Zoologia 17: 429-444. [ Links ]
Morellato, L. P. C. & C. F. B. Haddad. 2000. Introduction: The Brazilian Atlantic Forest. Biotropica 32: 786-792. [ Links ]
Moure, J. S. 2008. Tetrapediini Michener & Moure, 1957. In: J. S. Moure; D. Urban & G. A. R. Melo (Orgs). Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region. Available at: http://www.moure.cria.org.br/catalogue (accessed on 9 July 2011). [ Links ]
Myers, N.; R. A. Mittermeier; C. G. Mittermeier; G. A. B. da Fonseca & J. Kent. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853-858. [ Links ]
Naeem, S. 2002. Ecosystem consequences of biodiversity loss: the evolution of a paradigm. Ecology 83: 1537-1552. [ Links ]
Nascimento, A. L. O. & C. A. Garófalo. Abelhas (Hymenoptera, Apoidea) ndificando em ninhos-armadilha no Parque Estadual da Serra do Mar, Ubatuba, SP. Anais do IX Encontro sobre Abelhas: 139-146. [ Links ]
Pedro, S. R. M. 1994. Interação entre abelhas e flores em uma área de cerrado no NE do estado de São Paulo: abelhas coletoras de óleo (Hymenoptera: Apoidea: Apidae). Anais do I Encontro sobre Abelhas: 243-255. [ Links ]
Pinto, N. P. O. 2005. Estudo de caso: a reutilização de células de ninho abandonado de Polistes (Aphanilopterus) simillimus Ziká, 1951 (Hymenoptera: Vespidae, Polistinae) por Tetrapedia (Tetrapedia) diversipes Klug, 1810 (Hymenoptera: Apidae, Apinae). Revista de Etologia 7: 67-74. [ Links ]
Prieto, P. V. 2008. Efeitos de borda sobre o sub-bosque da Mata Atlântica de terras baixas na Reserva Biológica União-RJ. Master Thesis, Rio de Janeiro, Instituto de Pesquisas Jardim Botânico do Rio de Janeiro/Escola Nacional de Botânica Tropical, 123 p. [ Links ]
Ramamoorthy, T. P.; E. M. Zardini. 1987. The systematics and evolution of Ludwigia sect. Myrtocarpus sensu lato (Onagraceae). Monographs in Systematic Botany from the Missouri Botanical Garden 19: 1-120. [ Links ]
Rêgo, M. M. C & P. M. C. Albuquerque. 1989. Comportamento das abelhas visitantes de murici, Byrsonima crassifólia (L.) Kunth, Malpighiaceae. Boletim do Museu Paraense Emílio Goeldi, série Zoologia, 5: 179-193. [ Links ]
Roubik, D. W. 1989. Nesting and reproductive biology, p. 161-206. In: D. W. Roubik (ed.). Ecology and Natural History of Tropical Bees. Cambridge, University Press, 514 p. [ Links ]
Roubik, D. W. 1987. Notes on the biology of anthophorid bee Tetrapedia and the mite Chaetodactylus panamensis Baker, Roubik and Delfinado-Baker (Acari: Chaetodactylidae) International Journal of Acarology 13: 75-76. [ Links ]
Roubik, D. W. & J. E. Moreno. 1991. The pollen and spores of Barro Colorado Island. Monographs in Systematic Botany from the Missouri Botanical Garden 36: 1-268. [ Links ]
Salgado-Labouriau, M. L. 1973. Contribuição à Palinologia dos Cerrados. Rio de Janeiro, Academia Brasileira de Ciências, 273 p. [ Links ]
Saunders, D. A; R. J. Hobbs & C. R. Margules. 1991. Biological consequences of ecosystem fragmentation: A review. Conservation Biology 5: 18-32. [ Links ]
Sazima, M. & J. U. M. dos Santos. 1982. Biologia floral e insetos visitantes de Ludwigia sericea (Onagraceae). Boletim do Museu Paraense Emílio Goeldi 54: 1-10. [ Links ]
Silveira, F. A.; L. B. Rocha; J. R. Cure & M. J. F. Oliveira. 1993. Abelhas silvestres (Hymenoptera, Apoidea) da Zona da Mata de Minas Gerais. II. Diversidade, abundância e fontes de alimento em uma pastagem abandonada em Ponte Nova. Revista Brasileira de Entomologia 37: 595-610. [ Links ]
Singer, R. B. & A. A. Cocucci. 1999. Pollination mechanisms in four sympatric southern Brazilian Epidendroideae orchids. Lindleyana 14: 47-56. [ Links ]
SOS Mata Atlântica/Instituto Nacional de Pesquisas Espaciais (INPE). 2010. Atlas dos remanescentes florestais da Mata Atlântica período 2008-2010, Relatório Parcial. Rio de Janeiro, Fundação SOS Mata Atlântica, 60 p. [ Links ]
Steffan-Dewenter, I. 2003. Importance of habitat area and landscape context for species richness of bees and wasps in fragmented orchard meadows. Conservation Biology 17: 1036-1044. [ Links ]
Steffan-Dewenter, I. & T. Tscharntke. 2002. Insect communities and biotic interactions on fragmented calcareous grasslands-A mini review. Biological Conservation 104: 275-284. [ Links ]
Teixeira, L. M. & I. C. Machado. 2000. Sistemas de polinização e reprodução de Byrsonima sericea DC (Malpighiaceae). Acta Botanica Brasilica 14: 347-357. [ Links ]
Tscharntke, T. 1992. Fragmentation of Phragmites habitats, minimum viable population size, habitat suitability, and local extinction of moths, midges, flies, aphids, and birds. Conservation Biology 6: 530-536. [ Links ]
Viana, B. F.; F. O. Silva; A. M. P. Kleinert. 2001. Diversidade e sazonalidade de abelhas solitárias (Hymenoptera: Apoidea) em dunas litorâneas no Nordeste do Brasil. Neotropical Entomology 30: 245-251. [ Links ]
Viana, B. F.; A. M. Costa de Melo & P. D. Drumond. 2006. Variação na estrutura do habitat afetando a composição de abelhas e vespas solitárias em remanescentes florestais urbanos de Mata Atlântica no Nordeste do Brasil. Sitientibus, série Ciências Biológicas, 6: 282-295. [ Links ]
Vogel, S. 1990. History of the Malpighiaceae in the light of pollination ecology. Memoirs of the New York Botanical Garden 55: 130-142. [ Links ]
Editor: Eduardo A. B. Almeida