*Dirección para correspondencia:

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Abstract

The orchid bees are a very important group of pollinators distributed in the Neotropics. Although a lot of studies concerning male euglossine bees have been done in this region, few works have so far been carried out in the Cerrado biome. This manuscript has the main objective to present the orchid bee community from a Gallery Forest in the Northeastern Brazilian Cerrado ]]> Eulaema was the most representative group of euglossine bees in relation to the total number of the sampled individuals, accounting for 50.6% of bees followed by Euglossa (26.6%), Eufriesea (15.2%) and Exaerete (7.6%). The most frequent species were Eulaema nigrita (27.8%), Eulaema ]]> (19%) and Euglossa cordata (18.3%). Many species typical of forested environments were found in samples, like Euglossa avicula, Euglossa violaceifrons and Eulaema meriana, emphasizing the role played by the Gallery Forests as bridge sites to connect the two great biomes of Amazonia and Atlantic Forest. The occurrence of Exaerete guaykuru represents the second record of this species for the Neotropical ]]> Eufriesea species appeared at the baits only in the wet season. The hourly frequency of bees at scent baits showed a clear preference for the morning period, where 87.9% visited the baits from 07:00 to 12:00hr. The euglossine bee fauna found in the Northeastern Maranhão Cerrado is represented chiefly by species of large geographic distribution and by some forest bee species, where their occurrence is maybe related to to the ]]>

Key words: diversity, Euglossini, Exaerete guaykuru, Cerrado, scent bait.

Resumen

Las abejas de las orquídeas son un grupo muy importante de polinizadores distribuido en el Neotrópico, incluyendo Brasil. Aunque una gran cantidad de estudios sobre las abejas euglosinas se han hecho en esa región, pocos trabajos han sido hasta ahora llevado a cabo en el bioma del Cerrado. Este manuscrito tiene como objetivo principal mostrar la ]]> Euglossa (26.6%), Eufriesea (15.2%) y Exaerete (7.6%). Las especies ]]> Eulaema nigrita (27.8%), cingulata Eulaema (19%) y Euglossa cordata (18.3%). Muchas especies típicas de los ambientes forestales fueron capturadas, como Euglossa avicula, Euglossa violaceifrons y Eulaema meriana. La aparición de Exaerete guaykuru representa el segundo registro de ]]> Eufriesea apareció sobre todo en la estación lluviosa. Las abejas mostraron una clara preferencia por el período de la mañana, donde el 87.9% visitó los cebos aromáticos entre 07:00 y las 12:00hr. La fauna de abejas euglosinas está representada principalmente por especies de distribución geográfica amplia y por algunas ]]>

Palabras clave: diversidad, Euglossini, Exaerete guaykuru, Cerrado, cebos aromáticos.

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Cerrado is the designation given to the Brazilian savanna vegetation. The Cerrado landscape is characterized by extensive savanna formations crossed by Gallery Forests and stream valleys. It occupies an area of two million km2 accounting for 23% of the Brazilian territory, being exceeded only by the Amazonian forest (Ratter et al. 1997). Biologically, Cerrado is the richest savanna in the entire world (Castro et al. 1999).

This biome has been largely disturbed and such changes may truly have huge consequences to the biodiversity maintenance (Klink & Machado 2005). In the last 35 years, more than half of the Brazilian Cerrado has been transformed into pasture, agricultural crops and other uses, and, in Northeastern Maranhão, the deforestation process continues to be intense, ]]>

Euglossini bees, also known as orchid bees, are an important group of Neotropical pollinators. This tribe is composed of five genera and about 200 species (Cameron 2004, Moure et al. 2007). They are characterized by their very long tongues ]]>

Euglossine bees show close ]]> et al. 2008). Studying euglossine bees in a threatened landscape is very important for future research, where the impact on how the land-use changes affecting the abundance and community composition can be better evaluated.

In this vast tropical savanna biome, even with the continuous deforestation process, few works have been made on the euglossine bee fauna (Rebêlo & Cabral 1997, Nemésio & Faria 2004, Anjos-Silva et al. 2006, Carvalho et al. 2006, Alvarenga et al. ]]>

Material and methods

]]> The study area is in the Northeastern part of Maranhão state, Brazil (3º44’17’’ S - 43º20’29’’ W), about 300km far away from São Luís, the capital of the state. The Maranhão state Cerrado occupies a large transitional area positioned between three Brazilian regions: North, Northeast and Central-West. The research was undertaken in a Gallery Forest situated in Chapadinha, one of the 33 Maranhão municipalities found in the Cerrado zone, which occupies 30 percent of the geographical area of the state. The Gallery Forest grows along the ]]> et al. 2008). It is bordered on the North-Northeast side by urbanized areas; on the North-Northwest side by the University campus and on the South-Southeast side by Cerrado vegetation. The reserve is composed of a mosaic of vegetation types, such as Riparian and Gallery Forests, “Campo Cerrado” (a savannic ]]> et al. 2008).

In the region the climate is hot and semihumid with an annual average temperature ranging from 28°C-30°C (Fig. 1). There is a precipitation regime of 1 600-2 000mm/year. The region undergoes a dry season, from July to December, ]]>

The bee captures were carried out monthly from September 2007 to May 2009, between 07:00 and 17:00hr, by means of odoriferous baits. The scent lures used to attract males were eucalyptol (1.8-cineole) (Biodinâmica ®), eugenol (clove oil) (Biodinâmica®) and vanillin (4-hydroxy-3-methoxybenzaldehyde) ]]>

The specimens were ]]>

]]> Results

Over this 21-month follow-up study, a total of 158 individuals and 14 species distributed in the four genera of euglossine bees were recorded. Eulaema Lepeletier was represented by 80 individuals and three species, Euglossa Latreille (42 individuals; seven species), Eufriesea Cockerell (24 individuals; two species) and Exaerete Hoffmannsegg (12 individuals; two species) (Table 1). The most frequent species at baits were Eulaema nigrita (Lepeletier, 1841), accounting for 27.8% of the total sampled individuals, followed by Eulaema ]]> (Fabricius, 1804) (19%) and Euglossa cordata (Linnaeus, 1758) (18.3%).

The most attractive scent bait was eucalyptol (11 species; 86 individuals), followed by vanillin (seven species; 44 individuals) and eugenol (six species; 27 individuals). E. nigrita was the most frequent species collected at ]]> E. cordata (39.5% and 34.8%, respectively). Vanillin was more visited by E. cingulata and E. surinamensis (Linnaeus, 1758), both accounting for 27.2% of the collected individuals at that scent. Eugenol was represented mainly by E. cingulata (55.5%).

]]> The genus Eulaema was the most representative group of euglossine bees in relation to the total number of the sampled individuals, accounting for 50.6% of bees followed by Euglossa (26.6%), Eufriesea (15.2%) and Exaerete (7.6%) (Table 1).

]]> The euglossine bees were sampled mainly in the dry season, where 62.5% of the individuals were captured in that period (Table 2). However, these results are not statistically significant (p<0.05). E. cordata occurred exclusively in the dry period and the Eulaema species were mostly found in the dry season. E. ]]> and the two more frequent Eulaema species E. nigrita and E. cingulata accounted for 83.8% of the sampled bees, being responsible for the seasonality configuration observed herein. Eufriesea species appeared at the baits only in the wet season, with one individual of E. ]]> (Friese, 1925) sampled in the dry period.

The hourly frequency of bees at scent baits showed a clear preference for the morning period, where 87.9% visited the baits from 7:00 to 12:00hr (Table 3). The statistical analysis showed significant difference (p<0.05) between the morning and afternoon samples, regarding the number of individuals and species. ]]> Euglossa cordata males were present during all morning period while E. nigrita and E. cingulata appeared more frequently at the baits early in the morning. The males of both Eufriesea species visited the baits all morning and reaching two more hour intervals at the beginning of the afternoon period, particularly in the rainy days.
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Discussion

The three most frequent species surveyed in the Itamacaoca Reserve Gallery Forest are commonly found in open and dry Neotropical areas. E. nigrita is generally found in ]]> et al. 2004) and it is one of the fewer euglossine species found in the caatinga, a semi-arid brazilian ecosystem characterized by scrub vegetation and presenting a low and highly seasonal rainfall (Lopes et al. 2007). The orchid bee E. cordata is well represented in open, disturbed and dry areas (Silva ]]> E. securigera (Dressler, 1982) (Lopes et al. 2007). Eulaema cingulata, like Eulaema nigrita and Euglossa cordata, are a species commonly found in forested areas (Silva & Rebêlo 1999, Nemésio & Silveira 2007) and in the Brazilian Cerrado (Silva & Rebêlo 1999, Rebêlo & Cabral 1997, Mendes et al. ]]> et al. 2006).

Euglossa avicula (Dressler, 1982) has been found in Amazonian forested areas (Oliveira & Campos 1995, Silva & Rebêlo 1999). In the Cerrado landscape it was recorded from a riparian forest in Northeastern Maranhão by Carvalho et al. (2006). Euglossa pleosticta (Dressler, 198) ]]> et al. 2007). Euglossa modestior (Dressler, 1982) is found in Amazonian basin and has already been described from the Cerrado zones of ]]> Euglossa violaceifrons (Rebêlo & Moure, 1995) was recorded from Brazilian forests of South Maranhão (Silva & Rebêlo 1999) and Northeast of São Paulo state, Southeastern Brazil (Rebêlo & Moure 1996). Eufriesea nigrescens has been recorded from the Amazonian basin and Paraguay as well as the open areas of Maranhão state (Rebêlo 2001, Silva et al. 2009). Eulaema meriana (Olivier, 1789) was collected for the first time in the Cerrado landscape. It is a typical species found in forested areas (Silva & Rebêlo 1999, Oliveira & Campos 1995) avoiding urban environments (Parra-H & Nates-Parra 2007).

In this context, the occurrence of ]]> Exaerete guaykuru (Anjos-Silva & Rebêlo, 2006) in the Gallery Forest of Northeastern Cerrado represents the second record for the Neotropical region, since this species was recently described from a Gallery Forest environment of Mato Grosso state, Brazil (Anjos-Silva & Rebêlo 2006). However, it is extremely important to protect those kinds of habitats because so many species of animals are profoundly responsive to environmental disturbances and use the Gallery Forest zones as refuge sites inside the degradation context of the Cerrado vegetation (Moura & Schlindwein 2009).

Eulaema species were the predominant visitors to the odoriferous baits, different from the results obtained by other researches in the Neotropical region using a similar methodology, showing that Euglossa is the most expressive group at the scent baits, in both individuals and species (Janzen et al. ]]> et al. 2006). The two Eulaema species more sampled in the gallery forest, E. nigrita and E. cingulata, accounted together for 46.8% of the total number of individuals. These species have a large geographic distribution and one of them, E. nigrita, is ]]>

Eulaema male activities are favored by satisfactory climate conditions and thus visit the scent baits early in the morning as already observed by Silva & Rebêlo (1999). ]]> Euglossa species arrive late at the scent baits and the hot and dry climate conditions appear to be the main limiting factors. Eulaema species are large, black and have densely pubescent thoraces and Euglossa species are smaller, lack external pubescence and are brightly colored, metallic blue or green (Rebêlo 2001). The morphological aspects and the pubescence have an effect on the flight activity of Eulaema species (Casey et al. 1985) where the thoracic temperature can be maintained high at low temperature conditions favoring them to visit the baits early.

The most frequent species captured in the gallery forest of Maranhão Cerrado depicted an unfamiliar seasonality curve that is divergent from the most researches undertaken in the Neotropics in which a high number of species and individuals ]]> E. cordata, E. cingulata and E. nigrita were responsible for that unusual pattern of seasonal distribution. But, in view of the statistical analysis, there is no significant difference between the two seasons. Silva et al. (2009) observed that E. cingulata and E. cordata were most frequently found in the dry period in the eastern Maranhão “restinga”. The same pattern was observed by ]]> et al. (2008) in forest fragments of Paraiba State. Neves & Viana (1999) observed that most sampled euglossine males in riparian forest in areas of Bahia semi-arid region occurred after the rainy season and the increased flower production together with a moderate temperature and humidity favored that seasonal distribution pattern. In that research, 50% of the captured individuals were E. cordata (Neves & ]]>

Euglossine bees are usually found at baits in the morning period (Braga 1976, Neves & Viana 1999, Bezerra & Martins 2001, Silva & Rebêlo 2002), where the weather conditions are favorable to bee activities. In the studied area, the weather conditions were represented chiefly by increasing temperature and decreasing humidity along the day, forcing bees to occur mostly in the morning period (from seven am to noon), where ]]> good climate conditions and floral ]]> et al. 2009, Oliveira et al. 2011) and this may explain the male euglossine bee activity at the baits.

In conclusion, the euglossine bee fauna found in the Northeastern Maranhão Cerrado is represented chiefly by species of large geographic distribution. Some forest bee ]]>

Acknowledgments

I would like to acknowledge José Manuel Macário Rebêlo by helpful support in the species identification.

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*Correspondencia a: Francinaldo S. Silva: Centro de Ciências Agrárias e Ambientais, s/n, Rodovia MA 230, Campus IV, Bairro Boa Vista, Chapadinha, Maranhão, Brazil. CEP: 65500-000; sandflybr@yahoo.com.br

1. Centro de Ciências Agrárias e Ambientais, s/n, Rodovia MA 230, Campus IV, Bairro Boa Vista, Chapadinha, Maranhão, Brazil. CEP: 65500-000; sandflybr@yahoo.com.br

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