COMMUNITY OF MALE EUGLOSSINI BEES ( HYMENOPTERA : APIDAE ) IN A SECONDARY FOREST , ALCÂNTARA , MA , BRAZIL

From September, 92 to August, 93 bee sampling was done in a secondary forest near the Pepital River, in Alcântara, MA, in order to study the local Euglossini fauna. Five aromatic compounds were used: eucaliptol, eugenol, methyl salicylate, vanillin, and benzoate. Four hundred sixty-seven male Euglossini bees were captured, distributed in 4 genus and 19 species. Euglossa was the most abundant and with high diversity (302 specimens and 14 species), followed by Eulaema (121; 3), Eufriesea (41; 1), and Exaerete (3; 1). The species which more frequently visited the bait were Euglossa piliventris (141 specimens; 30.19%), Euglossa cingulata (113; 24.21%), Euglossa ignita (45; 9.64%), Eufriesea pulchra (41; 8.78%), and Euglossa gaianii (33; 7.07%) corresponding to 79.88% of the sampling universe. The bees were active throught the year, however during the rainy season more activity and diversity were observed. The most attractive essence was eucaliptol (44.32% specimens and 84.21% species). In spite of this study having been done in a forest fragment, a secondary vegetation area smaller than other areas studied in Maranhão, it showed a significant diversity rate. This result reinforces the importance of fragments in the conservation of local bee communities.

Male euglossine bees are the only pollinators of some orchids, e.g.Gongora, Castasctum, and Coryanthes.They are attracted to the essences produced by these orchids' flowers.The collection of these essences is by special pads on the tarsi of the forelegs and storage is in the pockets in the hind tibia (Bennett, 1972).
The use of these essences is not so well understood.However, Dodson (1970), Williams (1982), and Williams & Whitthen (1983) report that they can be used as a sexual attractant.
Although Maranhão State presents wide diversity of natural plant formations (Brasil, 1991), concern for the composition of euglossini community only began in the last decade with the work of Gomes (1991) and Fernandes (1991) in São Luís (north of the state), Silva & Rebelo (1999) in the pre-Amazonian region (west of the state), and Rebelo & Cabral (1997) in the wet littoral of Maranhão.Most of the state continues to have unknown euglossine fauna, in spite of accelerated devastation of the natural environment.

Study site
The study site is located on the west littoral of the Maranhão State, on the west side of São Marcos Bay, between coordinates 2°23'00''S and 44°25'00''W.
The sample site is 25 km away from Alcântara city, along the Pepital River.The weather is warm and humid with an average temperature of around 25°C (annual variation between 0.8 and 3.2°C) and pluviometric index between 1,000 and 1,800 mm (Feitosa, 1983).Medium (8-10 m) and small trees compose the vegetation.The other side of the Pepital River has a plane area saturated during the rainy period and with occurrence of Mauritia flexuosa (buriti), Euterpe oleracea (juçara), Clusia sp. e Toccoca sp.

Sample
The survey was done from September 1992 to August 1993, in intervals of 28 and 30 days.The sampling activities were performed in two consecutive days, the first from 12:00 to 6:00 p.m. and the second from 6:00 a.m. to 12:00 p.m.
Five aromatic compounds were utilized to attract the male euglossine bees: eucaliptol, eugenol, methyl salicylate, vanillin, and benzil benzoate in cotton balls attached to twine.
The chemical baits were put at an average height of 2.0 m, at an average distance of 7 m.Every two hours, the baits were filled with the respective essence.The baits were observed every hour, but to avoid over-sampling the collector remained at each essence bait for only 12 minutes per observation.The bees were captured with an entomological net, after visiting the baits and killed in a jar with ethyl acetate (C 4 H 8 ) 2 ).They were kept in plastic bags with identification (capture hour and bait).They are now preserved in the entomological collection of Maranhão Federal University.
The temperature, relative humidity, and rain fall data were obtained in the Metereologic Station of Ponta da Madeira Terminal -CVRD (São Luís), 20 km from the sample site.
Comparing these results to those of Gomes, 1991 (1,728 specimens and 13 species), Fernandes, 1991 (428 and 9), Silva & Rebelo, 1999 (1,740  and 37), and Ferreira, 1994 (69 and 11), all done in Maranhão State, shows that the largest diversity and fauna abundance were obtained by Silva & Rebelo (1999) in a 10,000 ha area in the Forest Reserve of Vale do Rio Doce in Buriticupu, an Amazonian region of the state (Table 1).In spite of the present study having been done in a forest fragment along the Pepital River, a secondary vegetation area smaller than the study areas cited above, its results were second in specific diversity.Although Powell & Powell (1987) noted that there were fewer nisitors of the Euglossini species in accordance with fragment size, it also shows that in the absence of big forested areas, the small ones are utilized as refuges by fauna.This result reinforces the importance of developing conservation studies in fragments of natural ecosystems.This can also be argued because in 1988, 31.02% of Maranhão State's original forest areas were devastated, and 2.11% of the remaining area were located in fragments smaller than 10,000 ha, as cited by Skole & Tuckers (1993).
The species which more frequently visited the baits were Euglossa piliventris (141 specimens, 30.19%The Euglossini were active throughout the year, however during rainy period more activity and specific diversity were observed.More active specimens representing 17.13% of the total specimens sampled, occurred in March 1993, the rainiest period, and the least activity was observed in September-November 1992 (Fig. 1 and Table 3).Strong rains probably explain the reduced activity registered in April.
Euglossa piliventris was present during the whole year, especially in December (32 specimens, representing 65.31% of the total sampled during that month).The dominance of this species contradicts the results in the studies of Silva & Rebelo (1999), Powell & Powell (1987), and Oliveira & Campos (1995), in which this species was rare.The most abundant species of Euglossa (E.piliventris, E. ignita, and E. gaianii) weren't necessarily the same in other surveys in forest areas in Maranhão.Gomes (1991) and Fernandes (1991) reported E. chalybeata and E. ignita as the most abundant, a justificable similarity because they sampled the same area, the Sacavém Forest Reserve (760 ha), in São Luís.However, Silva & Rebelo (1999) obtained dominance of E. pleostica, E. truncata and E. avicula.Janzen et al. (1982) argue that shifts of Euglossini populations and communities in different or isolated geographic habitats are acculiarly frequent.
Among the three species sampled of the genera Eulaema, E. cingulata were active during the entire sampling period, with more activity in February and March 1993.E. nigrita and E. meriana were represented by few specimens, but all were sampled in the rainy period.The low frequency of E. nigrita, in this area reinforces data showing this species, preference for open and dry areas (Ducke, 1902;Zucchi et al., 1969;Rebelo & Garófalo, 1991).In Buriticupu, transition of forest and "cerrado", E. nigrita was one of the most frequent bees found (Silva & Rebelo, 1999).Before this study, the only wet forest where it was frequently sampled was São Luís, where the vegetation is more similar to that of the Amazon region as observed by Gomes (1991) and Fernandes (1991).
The genus Eufriesea normally occurs in few months of the year (Ackerman et al., 1982;Ackerman, 1983).In this study it was represented by just one species, E. pulchra, observed visiting the baits during almost the whole year, except in September and December 1992.
Exaerete smaragdina, parasites of euglossinis nests (Kinsey, 1979), had three specimens sampled in October 1992and May 1993. Janzen (1981) reported that although many euglossini populations can remain active during the entire years; they must reduce their population size and can thus remain in some sites according to the resources available.
According to Dressler (1968) and Williams & Dodson (1972), the seasonal patterns can be explained by the movement pattern of the species.
However, Ackerman (1983), in studying the diversity and seasonality of euglossini males in Central Panama, verified that seasonal patterns of nidification and emerging of the bees could propably cause the seasonal fluctuation of abundance.Zimmerman & Madrinan (1988) verified that young males visit odorific substances, because they need to collect these substances before establishing territories while old males visit nectar sources.Rebelo & Garófalo (1991) observed that 77% of the males collecting odorific substances were young.The seasonal variation in preference for odorific substances can be related to the orchid floration patterns (Oliveira & Campos, 1996).
The eucaliptol also attracted most species, 16 of the 19 sampled.It failed to attract E. townsendi, E. mourei and Eufriesea pulchra.Silva & Rebelo (1999) found benzil benzoate attracted Eufriesea pulchra, Exaerete smaragdina, and Euglossa cordata, but in Alcântara this essence attracted only one specimen of Exaerete smaragdina, even with the presence of the other species mentioned above.
Euglossa augaspis and E. viridifrons also demonstrated a preference for a specific compound; 61.11% and 87.5% of their specimens were attracted to vanillin.
The other Euglossa species were represented by less than ten specimens, making a detailed analysis about their preferences for chemical compounds more difficult.
Eulaema cingulata was strongly attracted to eugenol, as indicated B ' Janzen (1981), Janzen et al. (1982) and Morato et al. (1992).The other species of this genus were E. meriana, attracted to methyl salicitate and eucaliptol, and E. nigrita, attracted to eucaliptol and vanillin.Discussion about their preferences for the baits in the sample site is almost impossible because they were represented by a reduced number of individuals.

TABLE 1 Frequency of male Euglossini bees collected at menthyl salicylate, eucaliptol, vanillin, eugenol and benzyl benzoate, in Alcântara, MA, from September 1992 to August 1993.
E. ignita and E. gaianii were active for almost the whole year, except in October and November 1992.Euglossa augaspis was strongly seasonal, being in activity during September and October/ 1992 and from May to August 1993.Another species with strong preference for some period of the year was E. viridifrons, active in December 1992 and January 1993, absent in February and active again in March and April.Although E. mourei, E. modestior, E. intersecta, E. townsendi, E. truncata, E. fimbriota, and E. laevicincta were represented by few specimens, they also demonstrated evidences of seasonality.These species were active especially in April and August 1993, corresponding to the end of the rainy and beginning of the dry season.