Nesting habits of Centris (Hemisiella) dichrootricha (Hymenoptera: Apidae) in the Northern Cerrado of Brazil / Hábito de nidificación de Centris (Hemisiella) dichrootricha (Hymenoptera: Apidae) en el Cerrado Norte de Brasil

Abstract:The Neotropical bee Centris (Hemisiella) dichrootricha is a solitary bee that nests in pre-existing cavities that occur in the rain forest. This study describes the nesting biology of C. dichrootricha and its preference for nesting in Cerrado and gallery forest habitats. The study was conducted from January 2012 and December 2013, in Mirador State Park in the municipality of Formosa da Serra Negra, Maranhão State, Brazil. For this, wooden trap-nests of 6, 8, 10, 12, 14 and 16 mm in diameter were used; a total of 300 trap-nests were placed in the gallery forest and Cerrado areas, respectively. Traps were monitored monthly and all completed nests were collected and replaced with empty ones. The nests were then taken to the laboratory to analyze bee development and emergence, nests characteristics and parasites presence. The species used 29 of the trap-nests, which had diameters of 8, 10, 12 and 14 mm. A total of 87 C. dichrootricha specimens emerged. The nests were parasitized by two bee species, Mesocheira bicolor (Apinae) and Coelioxys sp. (Megachilinae), and one fly species, Antrax sp. (Diptera). The highest nesting incidence of 72.4 % was observed in the gallery forest, whereas only 27.6 % in the Cerrado; this difference in habitat use was significant (χ² = 5.56; p < 0.05; DF = 1). For the nests that were built in the gallery forest, 80.9% of the soil originated from the Cerrado. The females were significantly larger than the males (F1, 76 = 595.19; p < 0.001). There were 11 pollen types that belonged to six families. Pollen of the family Malpighiaceae was most frequently used, with four species represented (Byrsonima crassifolia, B. rotunda, B. spicata and Heteropterys sp.). C. dichrootricha showed a preference for nesting in cavities of various diameters in gallery forest sites. The present study provides a novel description of the nesting habits and biology of C. dichrootricha in habitats of Central/Southern Maranhão. C. dichrootricha primarily used resources from the Cerrado, including soil to build their nests, pollen and floral oils; we concluded that gallery forest and Cerrado areas are intrinsically related to the maintenance of local populations of this species. Rev. Biol. Trop. 64 (3): 1041-1056. Epub 2016 September 01.

ResumenCentris (Hemisiella) dichrootricha es una especie de abeja solitaria neotropical, que anida en cavidades preexistentes y vive en la selva tropical. El presente estudio describe la biología de anidación de C. dichrootricha y su preferencia de nidificación por áreas en Cerrado y Bosque de Galería. El área de estudio se localiza en el Parque Estadual de Mirador, municipio de Formosa da Serra Negra, Maranhão. El método empleado fue el de nidos trampa de madera de diferentes diámetros, 6, 8, 10, 12, 14 y 16 mm, colocándose 300 nidos trampa por área. Las trampas fueron monitoreadas mensualmente y todos los nidos terminados fueron recogidos y sustituidos por otros vacíos. Los nidos completos fueron llevados al laboratorio para analizar el desarrollo de la abeja, la emergencia, las características de los nidos y la presencia de parásitos. La especie ocupó 29 nidos de los diámetros de 8, 10, 12 y 14 mm. Emergieron 87 individuos de C. dichrootricha. Los nidos fueron parasitados por tres especies: Mesocheira bicolor (Apinae), Coelioxys sp. (Megachilinae) y Antrax sp. (Diptera). En el Bosque de Galería se presentó la mayor nidificación (72.4 %) y en el Cerrado solamente 27.6 %, de esta forma, hubo diferencias significativas entre los hábitats (χ² = 5.56; p < 0.05; G. L.= 1). Los nidos fundados en el bosque de galería presentaron 80.9 % de sedimento originario del Cerrado. Las hembras fueron significativamente más grandes que los machos (F1, 76 = 595.19; p < 0.001). Hubo 11 tipos de polen pertenecientes a seis familias. Los tipos de polinización de la familia Malpighiaceae fueron los más representativos, con cuatro especies: Byrsonima crassifolia, B. rotunda, B. spicata y Heteropterys sp. C. dichrootricha mostró preferencia por nidificar en cavidades con diámetros variados y en el bosque de galería. El presente estudio contribuye con la descripción de los hábitos de nidificación y la biología de la especie para las áreas de Cerrado en la región centrosur de Maranhão. C. dichrootricha utilizó en su mayoría recursos provenientes del Cerrado, tanto sedimento para construir el nido, como material polínico y aceite floral. Estós datos indican que el bosque de galería y el Cerrado están intrínsecamente relacionados con el mantenimiento y conservación de C. dichrootricha.

Nesting habits of Centris (Hemisiella) dichrootricha (Hymenoptera: Apidae) in the Northern Cerrado of Brazil.

The Neotropical bee Centris (Hemisiella) dichrootricha is a solitary bee that nests in pre-existing cavities that occur in the rain forest. This study describes the nesting biology of C. dichrootricha and its preference for nesting in Cerrado and gallery forest habitats. The study was conducted from January 2012 and December 2013, in Mirador State Park in the municipality of Formosa da Serra Negra, Maranhão State, Brazil. For this, wooden trap-nests of 6, 8, 10, 12, 14 and 16 mm in diameter were used; a total of 300 trap-nests were placed in the gallery forest and Cerrado areas, respectively. Traps were monitored monthly and all completed nests were collected and replaced with empty ones. The nests were then taken to the laboratory to analyze bee development and emergence, nests characteristics and parasites presence. The species used 29 of the trap-nests, which had diameters of 8, 10, 12 and 14 mm. A total of 87 C. dichrootricha specimens emerged. The nests were parasitized by two bee species, Mesocheira bicolor (Apinae) and Coelioxys sp. (Megachilinae), and one fly species, Antrax sp. (Diptera). The highest nesting incidence of 72.4 % was observed in the gallery forest, whereas only 27.6 % in the Cerrado; this difference in habitat use was significant (χ² = 5.56; p < 0.05; DF = 1). For the nests that were built in the gallery forest, 80.9% of the soil originated from the Cerrado. The females were significantly larger than the males (F1, 76 = 595.19; p < 0.001). There were 11 pollen types that belonged to six families. Pollen of the family Malpighiaceae was most frequently used, with four species represented (Byrsonima crassifolia, B. rotunda, B. spicata and Heteropterys sp.). C. dichrootricha showed a preference for nesting in cavities of various diameters in gallery forest sites. The present study provides a novel description of the nesting habits and biology of C. dichrootricha in habitats of Central/Southern Maranhão. C. dichrootricha primarily used resources from the Cerrado, including soil to build their nests, pollen and floral oils; we concluded that gallery forest and Cerrado areas are intrinsically related to the maintenance of local populations of this species.

Comunidade de abelhas (Hymenoptera, Apoidea) em ecossistema de dunas na Praia de Panaquatira, São José de Ribamar, Maranhão, Brasil / Community of bees (Hymenoptera, Apoidea) in the coastal sand dunes at Panaquatira beach, São José de Ribamar, Maranhão, Brazil

Comunidade de abelhas (Hymenoptera, Apoidea) em ecossistema de dunas na Praia de Panaquatira, São José de Ribamar, Maranhão, Brasil. Foi analisada a estrutura da comunidade de Apoidea de uma área restrita de dunas primárias em São José de Ribamar, Maranhão, Brasil. Amostragens foram realizadas quinzenalmente durante um ano com metodologia padronizada totalizando 24 coletas. As coletas ocorreram no período das 12:00 às 18:00 h no primeiro dia e das 6:00 às 12:00 h no segundo, realizadas por dois coletores. Um total de 3305 indivíduos de 31 espécies pertencentes a quatro famílias (Apidae>Halictidae>Megachilidae>Andrenidae em número de indivíduos) foram coletadas nas flores. Centris com 14 espécies e 890 indivíduos foi o gênero mais rico e abundante. O padrão de abundância e riqueza foi bastante semelhante ao de outros habitats de dunas no nordeste brasileiro. Das espécies amostradas, 61 por cento foram representadas por menos de 36 indivíduos e apenas 5 espécies foram muito abundantes com mais de 177 indivíduos: Apis mellifera Linnaeus, Centris (Centris) leprieuri Spinola, Eulaema (Apeulema) nigrita Lepeletier, Eufriesea surinamensis Linnaeus e Xylocopa (Neoxylocopa) cearensis Ducke. As abelhas estiveram presentes durante todo o ano, apresentando picos de abundância no período de maior precipitação. A atividade diária foi maior entre 06:00 e 11:00 h, quando a temperatura aumentava e a umidade relativa decrescia.

The community structure of Apoidea of a restricted area of primary dunes in São José de Ribamar, Maranhão, Brazil was analyzed. Standardized samples were taken for one year, 2 times a month, from 12:00 a.m. to 6:00 p.m. on the first day and from 6:00 a.m. to 12:00 a.m. on the second by two collectors. A total of 3305 individuals of 31 species, belonging to four families (Apidae > Halictidae > Megachilidae > Andrenidae) were collected. Centris with 14 species and 890 individuals was the richest and most abundant genus. The abundance pattern and the richness were very similar to other sand dunes habitats in northeast Brazil. Of the total of bees sampled, 61 percent were represented by less than 36 individuals. The five most abundant species (more than 177 individuals) were: Apis mellifera Linnaeus, Centris (Centris) leprieuri Spinola, Eulaema nigrita Lepeletier, Eufriesea surinamensis Linnaeus and Xylocopa (Neoxylocopa) cearensis Ducke. Bees were active throughout the year, with abundance peaks in the highest rainfall periods. Daily activity was greatest between 06:00 and 11:00 a.m., when relative humidity decreased and the temperature increased.

[Euglossina bees (Hymenoptera: Apidae) in an area with sandbanks in the northeast of the state of Maranhão, Brazil]. / Abelhas Euglossina (Hymenoptera: Apidae) em área de restinga do nordeste do Maranhão.

The bees of subtribe Euglossina are an important component of neotropical fauna and have greater species diversity in tropical forests than in spits. They play an important role in the pollination of several plant species and are considered good indicators of environmental conditions. From February 2005 to January 2006, a total of 429 specimens belonging to three genera [Euglossa (Latreille), Eulaema (Lepeletier) and Eufriesea (Cockerell)] and 14 species were collected. Eulaema cingulata (Fabricius) (24.5%), Euglossa cordata (L.) (20.5%) and Eufriesea nigrescens (Friese) (19.8%) were the most abundant species, representing 64.8% of all bees collected. Rainfall was the environmental variable with the greatest relative influence on species composition, particularly for some species of Eufriesea. Euglossa cordata and Eg. gaianii Dressler nested in trap nests, suggesting they are resident species. The larger number of individuals and greater richness of species compared with data available in the literature may result from the great variety of plant species found in the areas adjacent to the collection site.

Abelhas Euglossina (Hymenoptera: Apidae) em área de restinga do nordeste do Maranhão / Euglossina Bees (Hymenoptera: Apidae) in an area with sandbanks in the northeast of the State of Maranhão, Brazil

As abelhas da subtribo Euglossina são importantes elementos da fauna neotropical, ocorrendo em maior diversidade em floresta tropical que em área de restinga. Essas abelhas são responsáveis pela polinização de inúmeras espécies de plantas, sendo consideradas boas indicadoras das condições ambientais. De fevereiro/2005 a janeiro/2006 foram coletados 429 indivíduos pertencentes a três gêneros [Euglossa (Latreille), Eulaema (Lepeletier) e Eufriesea (Cockerell)] e 14 espécies. As espécies mais frequentes foram Eulaema cingulata (Fabricius) (24,5 por cento), Euglossa cordata (L.) (20,5 por cento) e Eufriesea nigrescens (Friese) (19,8 por cento), constituindo 64,8 por cento dos indivíduos. Pluviosidade foi a variável ambiental que teve maior importância relativa sobre a variação da composição de espécies, pelo menos para algumas espécies de Eufriesea. Eg. cordata e Eg. gaianii Dressler nidifi caram em ninhos armadilhas colocados na área, o que sugere que são espécies residentes. A grande abundância e riqueza de espécies, quando comparadas a outros trabalhos, podem ser devidas ao mosaico de distintas formações vegetais encontrado nas áreas adjacentes ao sítio específico de coleta.

The bees of subtribe Euglossina are an important component of neotropical fauna and have greater species diversity in tropical forests than in spits. They play an important role in the pollination of several plant species and are considered good indicators of environmental conditions. From February 2005 to January 2006, a total of 429 specimens belonging to three genera [Euglossa (Latreille), Eulaema (Lepeletier) and Eufriesea (Cockerell)] and 14 species were collected. Eulaema cingulata (Fabricius) (24.5 percent), Euglossa cordata (L.) (20.5 percent) and Eufriesea nigrescens (Friese) (19.8 percent) were the most abundant species, representing 64.8 percent of all bees collected. Rainfall was the environmental variable with the greatest relative influence on species composition, particularly for some species of Eufriesea. Euglossa cordata and Eg. gaianii Dressler nested in trap nests, suggesting they are resident species. The larger number of individuals and greater richness of species compared with data available in the literature may result from the great variety of plant species found in the areas adjacent to the collection site.

Nidificação de Centris (Hemisiella) tarsata Smith (Hymenoptera, Apidae, Centridini) em ninhos-armadilha no Nordeste do Maranhão, Brasil / Nidification of Centris (Hemisiella) tarsata Smith (Hymenoptera, Apidae, Centridini) in trap nests in Northeast Maranhão, Brazil

Este trabalho teve como objetivo obter dados sobre a ecologia da nidificação de Centris (Hemisiella) tarsata Smith em três ecossistemas: mata ciliar (MC), mata mesofítica (MM) e eucaliptal (EC), utilizandose ninhos-armadilha confeccionados em gomos de bambu, distribuídos em diferentes alturas: 1,5 m e 5-12 m do solo. Foram obtidos 41 ninhos: 31 no EC e 10 na MM, a maioria no estrato superior e com maior freqüência de nidificações ocorrendo no período de estiagem. A razão sexual foi de 1,9:1 (fêmeas/ machos) no EC e de 1,08:1 na MM. Cerca de 22 por cento dos ninhos do EC e 40 por cento da MM foram parasitados por Mesocheira bicolor (Fabricius, 1804) (Hymenoptera, Apidae) e Coelioxys sp. (Hymenoptera, Megachilidae). A análise polínica revelou predominância de grãos de pólen de Banisteriopsis sp. (Malpighiaceae) e Cassia sp. (Caesalpiniaceae) no EC e de espécies de Caesalpiniaceae Kunth. e Banisteriopsis Robinson na MM.

This work had as objective to obtain ecological data of Centris (Hemisiella) tarsata Smith's nidification in three ecosystems: riparian forest (MC), mesophitic forest (MM) and eucalyptal (EC), using trap nests made by bamboo canes, distributed in differentiated heights: 1,5 m and 5-12 m high. A total of 41 nests were collected: 31 in EC and 10 in MM, the majority in the upper strata and with the largest frequency of nesting occurring in the dry season. The sex ratio was of 1.9:1 (females/ males) in EC and of 1.08:1 in MM. About 22 percent of nests of the EC and 40 percent of MM were parasitized by Mesocheira bicolor (Fabricius 1804) (Hymenoptera, Apidae) and Coelioxys sp. (Hymenoptera, Megachilidae). The pollinic analyses showed a higher quantity of pollen grains of Banisteriopsis sp. (Malpighiaceae) and Cassia sp. (Caesalpiniaceae) in EC area and a species of Caesalpiniaceae Kunth. and Banisteriopsis Robinson in MM area.

[Nesting biology of Centris flavifrons (Friese) (Hymenoptera: Apidae, Centridini), one of the main pollinators of Byrsonima crassifolia L. Kunth in Maranhão, Brazil]. / Aspectos da biologia de nidificação de Centris flavifrons (Friese) (Hymenoptera: Apidae, Centridini), um dos principais polinizadores do murici (Byrsonima crassifolia L. Kunth, Malpighiaceae), no Maranhão.

The Centridini has almost 176 species distributed mainly in the tropic regions of America. Although they are considered key pollinators in the maintenance of many vegetal species, data about their bionomics are restrict. Nesting activity is known for 11 species, out of the 21 that are considered pollinators of murici, Byrsonima crassifolia L. Kunth, a valuable biomonitoring specie. A study of the nesting biology of Centris flavifrons (Friese) was conducted in the state of Maranhão, Brazil, during the active period of the adults (May through December). Nests were aggregated. The females excavated their nests on flat surfaces of hard soils. Fifteen nests were dug and we only found cells in six of them. The nests architecture consisted of a single unbranched tunnel, with only one cell in the vertical position at the end, which was 25 cm to 50 cm away from the entrance. Nocturnal activity was observed in the nests building. The pollen analysis of the contents of four cells allowed to identify 23 floral species, six of them Malpighiaceae. Six floral species were registered visiting C. flavifrons by the first time: Lecythis lurida (Miers) Mori, Hymenea courbaril L., Myrcea sp., Protium sp., Tetrapterys sp. and Thalisia sp.

Aspectos da biologia de nidificação de Centris flavifrons (Friese) (Hymenoptera: Apidae, Centridini), um dos principais polinizadores do murici (Byrsonima crassifolia L. Kunth, Malpighiaceae), no Maranhão / Nesting biology of Centris flavifrons (Friese) (Hymenoptera: Apidae, Centridini), one of the main pollinators of Byrsonima crassifolia L. Kunth in Maranhão, Brazil

Os Centridini compreendem cerca de 176 espécies distribuídas principalmente nas regiões tropicais da América. Mesmo considerados polinizadores-chave na manutenção de muitas espécies vegetais, dados sobre sua bionomia são ainda restritos. Há relatos sobre a nidificação de 11 espécies, das 21 diagnosticadas como polinizadoras do murici, Byrsonima crassifolia L. Kunth, uma espécie valiosa para o biomonitoramento. Um estudo da biologia de nidificação de Centris flavifrons (Friese) foi conduzido no Maranhão durante o período de atividade dos adultos (maio a dezembro). Os ninhos estavam agregados. As fêmeas escavaram seus ninhos em solo plano e compactado. Quinze ninhos ativos foram escavados, sendo que em apenas seis foram encontradas células. O túnel era simples, sem ramificações, com uma única célula na sua porção terminal, situada entre 25 cm e 50 cm de profundidade. Foi observada atividade noturna na construção dos ninhos. A análise polínica do aprovisionamento de quatro células permitiu identificar 23 espécies florais, das quais seis espécies de Malpighiaceae. Foram registradas seis espécies florais que ainda não haviam sido encontradas visitando C. flavifrons: Lecythis lurida (Miers) Mori, Hymenea courbaril L., Myrcea sp., Protium sp., Tetrapterys sp. e Thalisia sp.

The Centridini has almost 176 species distributed mainly in the tropic regions of America. Although they are considered key pollinators in the maintenance of many vegetal species, data about their bionomics are restrict. Nesting activity is known for 11 species, out of the 21 that are considered pollinators of murici, Byrsonima crassifolia L. Kunth, a valuable biomonitoring specie. A study of the nesting biology of Centris flavifrons (Friese) was conducted in the state of Maranhão, Brazil, during the active period of the adults (May through December). Nests were aggregated. The females excavated their nests on flat surfaces of hard soils. Fifteen nests were dug and we only found cells in six of them. The nests architecture consisted of a single unbranched tunnel, with only one cell in the vertical position at the end, which was 25 cm to 50 cm away from the entrance. Nocturnal activity was observed in the nests building. The pollen analysis of the contents of four cells allowed to identify 23 floral species, six of them Malpighiaceae. Six floral species were registered visiting C. flavifrons by the first time: Lecythis lurida (Miers) Mori, Hymenea courbaril L., Myrcea sp., Protium sp., Tetrapterys sp. and Thalisia sp.