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Report of the nest of Megachile (Moureapis) benigna (Hymenoptera: Megachilidae) from an urban environment, Rio de Janeiro, Brazil

Registro do ninho de Megachile (Moureapis) benigna (Hymenoptera: Megachilidae) em uma área urbana do Rio de Janeiro, Brasil

ABSTRACT

One nest of Megachile (Moureapis) benigna Mitchell, 1930 (Hymenoptera: Megachilidae) was collected using trap-nests in a forest fragment (Atlantic Forest biome) into an urban matrix in Rio de Janeiro, Brazil, in October/2017. The nest architecture and larval food are presented providing initial data for management and conservation of this species in cities.

KEYWORDS
Leafcutter bee; pollen; solitary bee; trap-nest; urban ecology

RESUMO

Um ninho de Megachile (Moureapis) benigna Mitchell, 1930 (Hymenoptera: Megachilidae) foi coletado usando ninhos-armadilha em um fragmento de floresta (bioma Mata Atlântica) em uma área urbana no Rio de Janeiro, Brasil, em outubro/2017. A arquitetura do ninho e o alimento larval são apresentados fornecendo dados iniciais para o manejo e conservação desta espécie nas cidades.

PALAVRAS-CHAVE
Abelha cortadora de folhas; abelha solitária; ecologia urbana; ninho-armadilha; pólen

Cities have been historically seen as non-suitable places for a diverse fauna, but in the last decades several reports from research conducted in urban areas have shown modest to great richness of wild insect species harboured, especially in non-tropical areas (Hall et al., 2017Hall, D. M.; Camilo, G. R.; Tonietto, R. K.; Ollerton, J.; Ahrné, K.; Arduser, M.; Ascher, J. S.; Baldock, K. C. R.; Fowler, R.; Frankie, G.; Goulson, D.; Gunnarsson, B.; Hanley, M. E.; Jackson, J. I.; Langellotto, G.; Lowenstein, D.; Minor, E. S.; Philpott, S. M.; Potts, S. G.; Sirohi, M. H.; Spevak, E. M.; Stone, G. N. & Threlfall, C. G. 2017. The city as a refuge for insect pollinators. Conservation Biology 31(1):24-29. doi: 10.1111/cobi.12840.
https://doi.org/10.1111/cobi.12840...
). Focusing on bees (Hymenoptera: Anthophila), information about their ecology in urban areas shows that cities and urban environments at general are prone to sustain viable populations with implications for conservation, changing the view that those anthropic areas are sink for the fauna living there (Hall et al., 2017Hall, D. M.; Camilo, G. R.; Tonietto, R. K.; Ollerton, J.; Ahrné, K.; Arduser, M.; Ascher, J. S.; Baldock, K. C. R.; Fowler, R.; Frankie, G.; Goulson, D.; Gunnarsson, B.; Hanley, M. E.; Jackson, J. I.; Langellotto, G.; Lowenstein, D.; Minor, E. S.; Philpott, S. M.; Potts, S. G.; Sirohi, M. H.; Spevak, E. M.; Stone, G. N. & Threlfall, C. G. 2017. The city as a refuge for insect pollinators. Conservation Biology 31(1):24-29. doi: 10.1111/cobi.12840.
https://doi.org/10.1111/cobi.12840...
).

Most research assessing the status of bee fauna in cities are conducted in Europe and North America (Hernandez et al., 2009Hernandez, J. L.; Frankie, G. W. & Thorp, R. W. 2009. Ecology of urban bees : areview of current knowledge and directions for future study. Cities and the Environment 2(1):1-15.; Hall et al., 2017Hall, D. M.; Camilo, G. R.; Tonietto, R. K.; Ollerton, J.; Ahrné, K.; Arduser, M.; Ascher, J. S.; Baldock, K. C. R.; Fowler, R.; Frankie, G.; Goulson, D.; Gunnarsson, B.; Hanley, M. E.; Jackson, J. I.; Langellotto, G.; Lowenstein, D.; Minor, E. S.; Philpott, S. M.; Potts, S. G.; Sirohi, M. H.; Spevak, E. M.; Stone, G. N. & Threlfall, C. G. 2017. The city as a refuge for insect pollinators. Conservation Biology 31(1):24-29. doi: 10.1111/cobi.12840.
https://doi.org/10.1111/cobi.12840...
). In the tropics, little research has addressed this issue (Hernandez et al., 2009; Costa & Gonçalves, 2019Costa, C. C. F. & Gonçalves, R. B. 2019. What do we know about Neotropical trap-nesting bees? Synopsis about their nest biology and taxonomy. Papeis Avulsos de Zoologia 59:e20195926. doi: 10.11606/1807-0205/2019.59.26.
https://doi.org/10.11606/1807-0205/2019....
) which rise concern about the situation of the bee fauna in this region. Specifically, concern is brought about the Megachile species in the Neotropical region whose bionomy is largely unknown, despite the diversity of this genus in the Neotropics with estimative of over 600 species (Raw, 2007Raw, A. 2007. An annotated catalogue of the leafcutter and mason bees (genus Megachile) of the Neotropics. Zootaxa 1601:1-127. ). Some data regarding the biology of species placed in Megachile exist, but taxonomic impediment has made difficult the acquisition of new information (Costa & Gonçalves, 2019Costa, C. C. F. & Gonçalves, R. B. 2019. What do we know about Neotropical trap-nesting bees? Synopsis about their nest biology and taxonomy. Papeis Avulsos de Zoologia 59:e20195926. doi: 10.11606/1807-0205/2019.59.26.
https://doi.org/10.11606/1807-0205/2019....
).

Popularly known as leafcutter bees, Megachile use leaf or petal for lining their brood cells, and most of the knowledge gathered from its species comes from pre-existing cavity nesters (Michener, 2007Michener, C. D. 2007. The Bees of the World. 2ed. Baltimore, The Johns Hopkins University Press. 953p.). Also, there are reports of disruptive behaviours of Megachile species using plastic fragment for building their nests, indicating human activity deeply affecting their ecology (MacIvor & Moore, 2013MacIvor, J. S. & Moore, A. E. 2013. Bees collect polyurethane and polyethylene plastics as novel nest materials. Ecosphere 4(12):1-6. doi: 10.1890/ES13-00308.1.
https://doi.org/10.1890/ES13-00308.1...
; Allasino et al., 2019Allasino, M. L.; Marrero, H. J.; Dorado, J. & Torretta, J. P. 2019. Scientific note: first global report of a bee nest built only with plastic. Apidologie 50(2):230-233. doi: 10.1007/s13592-019-00635-6.
https://doi.org/10.1007/s13592-019-00635...
; Quintos-Andrade et al., 2021Quintos-Andrade, G.; Torres, F. & Vivyan, P. 2021. Observation of Megachile saulcyi (Guérin-Méneville, 1844) (Hymenoptera: Megachilidae) using plastic for nest construction in Chile. Revista Chilena de Entomología 47(2):201-204.).

In Brazil, there is a modest knowledge over Megachile species (Costa & Gonçalves, 2019Costa, C. C. F. & Gonçalves, R. B. 2019. What do we know about Neotropical trap-nesting bees? Synopsis about their nest biology and taxonomy. Papeis Avulsos de Zoologia 59:e20195926. doi: 10.11606/1807-0205/2019.59.26.
https://doi.org/10.11606/1807-0205/2019....
). Authors report leafcutter bees visiting species of Asteraceae and Fabaceae (Garófalo et al., 2004Garófalo, C. A.; Martins, C. F. & Alves-dos-Santos, I. 2004. The Brazilian solitary bee species caught in trap nests. Solitary Bees Conservation, Rearing and Management for Pollination (Table 1):77-84.), but some species in Amazonia, collect pollen from Arecaceae species (Marinho et al., 2018Marinho, D.; Muniz, D. B. & Azevedo, G. G. 2018. Nesting biology of three Megachile (Hymenoptera: Megachilidae) species from eastern Amazonia, Brazil. Revista Brasileira de Entomologia 62(2):97-106. doi: 10.1016/j.rbe.2018.03.002.
https://doi.org/10.1016/j.rbe.2018.03.00...
). Additionally, ruderal plants, those mainly use in gardening, have also been pointed as important source of food for these bees (Schlindwein, 2004Schlindwein, C. 2004. Abelhas solitárias e flores: especialistas são polinizadores efetivos? Anais do 55 Congresso Nacional de Botânica 55:1-8.). Presenting data from urban areas regarding Megachile is an important initiative for thinking about conservation biology in cities.

Megachile (Moureapis) benigna Mitchell, 1930 was studied by Teixeira et al. (2008) at São José do Ubá in the State of Rio de Janeiro and by Cardoso & Silveira (2012Cardoso, C. F. & Silveira, F. A. 2012. Nesting biology of two species of Megachile (Moureapis) (Hymenoptera: Megachilidae) in a semideciduous forest reserve in Southeastern Brazil. Apidologie 43(1):71-81. doi: 10.1007/s13592-011-0091-z.
https://doi.org/10.1007/s13592-011-0091-...
) in the State of Minas Gerais and. Both studies accounted for seasonality and nest architecture of this species in natural areas of Atlantic Forest and the former found no nest in urban or disturbed areas. In this context, this study presents the description of the nest of M. benigna Mitchell, 1930 collected in urban areas as well as the first pollen record used by this species to feed their immatures.

MATERIAL AND METHODS

The area where this study was carried out comprehended the Jardim Botânico do Rio de Janeiro (22°58’14”S, 43°13’8”W, henceforth referred to as JBRJ), a park at the city of Rio de Janeiro, Brazil. Trap nests made of bamboo cane (22 cm in length and diameter ranging from 0.4-2.4 cm), rubber hose (15 cm in length ranging from 1.27-0.79 cm) and plastic straws (10 cm in length and 0.5 cm of diameter) were placed between April/2017 to February/2019 in the JBRJ area as described in Marinho & Vivallo (2020Marinho, D. & Vivallo, F. 2020. Unveiling the trap-nesting bees and wasps’ fauna (Hymenoptera: Apocrita) and associated organisms of the Jardim Botânico do Rio de Janeiro, Brazil. Papeis Avulsos de Zoologia 60:e20206049. doi: 10.11606/1807-0205/2020.60.49.
https://doi.org/10.11606/1807-0205/2020....
). The pollen load in the brood cells of the nest was analysed using the acetolys process following the Erdtman protocol modified by Lieux (1980Lieux, M. H. 1980. Acetolysis applied to microscopical honey analysis. Grana 19(1):57-61.). Three slides per cells were made, and 300 pollen grains by slide were counted. The vouchers of this study were recorded by photography (Figs 1-6), but only the pollen slides remain deposited at the Universidade Federal do Rio de Janeiro, since the emerged female (Fig. 1) and the nest (Fig. 2) were lost in a fire that burned down the Museu Nacional on September, 2018.

Figs 1-4.
Megachile (Moureapis) benigna Mitchell, 1930: 1, female spawned from the nest (habitus, lateral view); 2, nest collected in the trap-nest; 3, brood cell and round-shaped fragments of leaf forming the cell opercula; 4, different shapes of leaf fragments employed by the female foundress for nest building.

Figs 5, 6.
Pollen grains found in the pollen slides analysed from the nest: 5, Cyrtocymura sp. (Asteraceae); 6, Type Fabaceae pollen grain. Pollen grains magnified 40x. Scale bars = 10 µm.

RESULTS

The M. benigna nest was collected in October/2017 (Marinho & Vivallo, 2020Marinho, D. & Vivallo, F. 2020. Unveiling the trap-nesting bees and wasps’ fauna (Hymenoptera: Apocrita) and associated organisms of the Jardim Botânico do Rio de Janeiro, Brazil. Papeis Avulsos de Zoologia 60:e20206049. doi: 10.11606/1807-0205/2020.60.49.
https://doi.org/10.11606/1807-0205/2020....
). It was built in a bamboo cane with 12 of diameter, its bottom against the node wall of the culm. The external wall of the nest was tightly attached to the inner skin of the bamboo trap. So, it was removed sliding an A4 sheet between the nest and the trap to take it out. The entire nest was built using leaf fragments that seemed tender visually and when touched (Figs 2-4). Two layers of leaf fragments covered the brood cells, those on the outermost side of the nest were round-shaped at the edges whereas those in contact with the brood cells had a truncated side (Fig. 3). The leaf fragment cupping the bottom of the nest was almost entirely rounded. This nest was 8.5 cm long, its averaged width was 1.2 cm + 0.9 cm + 1 cm measured at the entrance, middle part, and bottom, respectively.

The three brood cells were arranged linearly, with the opercula of the brood cell facing the bottom of the next cell ahead. Each cell was built with subtrapezoidal leaf fragments, their bottom formed by bent leaf fragments. The cells were built with five leaf fragments tightly fasten together, its rear side formed by bent fragments, conferring to the cell a cylindrical shape (Fig. 3). The brood cells had their measurements as follows (cm): cell 1 -length: 1.7; cell 2 - length:1.1; cell 3 - length:1.1; all cells had 0.7 of width. Cell opercula varied in number of leaf fragments, the innermost cell with five rounded leaf pieces; the middle one with two leaf pieces; and the outermost cell with 11 leaf pieces.

Nest provision of the three cells was moistened with nectar, the pollen load yellow. Eggs were oviposited onto the pollen mass, and the larva when hatched from the egg started feeding at intervals, eating the provision under its body. The middle cell was found empty, although it was fully provisioned and sealed as though if ready for oviposition. The immature from the outermost cell died due to handling in the laboratory. Only the female of the innermost cell emerged (Fig. 1). Analysis of the pollen load revealed 98.56% of the pollen mass consisting of Cyrtocymura sp. (Asteraceae) (Fig. 5) and the 1.34% remaining of an unidentified species belonging to the Fabaceae family (Fig. 6).

DISCUSSION

This is the first nest of M. benigna reported for an urban area. Previous studies recorded this species nesting only in natural areas (Teixeira et al., 2011Teixeira, F. M.; Schwartz, T. A. C. & Gaglianone, M. C. 2011. Biologia da nidificação de Megachile (Moureapis) benigna Mitchell. EntomoBrasilis 4(3):92-99. doi: 10.12741/ebrasilis.v4i3.140.
https://doi.org/10.12741/ebrasilis.v4i3....
; Cardoso & Silveira, 2012Cardoso, C. F. & Silveira, F. A. 2012. Nesting biology of two species of Megachile (Moureapis) (Hymenoptera: Megachilidae) in a semideciduous forest reserve in Southeastern Brazil. Apidologie 43(1):71-81. doi: 10.1007/s13592-011-0091-z.
https://doi.org/10.1007/s13592-011-0091-...
) and reveal the potential of cities as conservation areas. Comparatively with other Megachile species placed in the subgenus Moureapis Raw, 2002 (Moure et al., 2012Moure, J. S.; Melo, G. A. R. & DalMolin, A. 2012. Megachilini Latreille, 1802. In: Moure, J. S.; Urban, D. & Melo, G. A. R. eds. Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region - online version. Available at <Available at http://www.moure.cria.org.br/catalogue >. Accessed May/27/2021.
http://www.moure.cria.org.br/catalogue...
), M. benigna is the best-known species so far, with accounts of its nest architecture, seasonality, and the different habitats where it occurs (Teixeira et al., 2011Teixeira, F. M.; Schwartz, T. A. C. & Gaglianone, M. C. 2011. Biologia da nidificação de Megachile (Moureapis) benigna Mitchell. EntomoBrasilis 4(3):92-99. doi: 10.12741/ebrasilis.v4i3.140.
https://doi.org/10.12741/ebrasilis.v4i3....
; Cardoso & Silveira, 2012Cardoso, C. F. & Silveira, F. A. 2012. Nesting biology of two species of Megachile (Moureapis) (Hymenoptera: Megachilidae) in a semideciduous forest reserve in Southeastern Brazil. Apidologie 43(1):71-81. doi: 10.1007/s13592-011-0091-z.
https://doi.org/10.1007/s13592-011-0091-...
).

In the Northeast of Rio de Janeiro, M. benigna nests were built between October and March (Teixeira et al., 2011Teixeira, F. M.; Schwartz, T. A. C. & Gaglianone, M. C. 2011. Biologia da nidificação de Megachile (Moureapis) benigna Mitchell. EntomoBrasilis 4(3):92-99. doi: 10.12741/ebrasilis.v4i3.140.
https://doi.org/10.12741/ebrasilis.v4i3....
), matching the period the nest reported in this study was collected at the JBRJ. Teixeira et al. (2011Teixeira, F. M.; Schwartz, T. A. C. & Gaglianone, M. C. 2011. Biologia da nidificação de Megachile (Moureapis) benigna Mitchell. EntomoBrasilis 4(3):92-99. doi: 10.12741/ebrasilis.v4i3.140.
https://doi.org/10.12741/ebrasilis.v4i3....
) did not collect M. benigna nests in urban or anthropogenetic areas, whereas the nest collected at the JBRJ brings evidence that this species may inhabit in urban areas as well.

The nest architecture found matches remarkably with the populations assessed by Cardoso & Silveira (2012Cardoso, C. F. & Silveira, F. A. 2012. Nesting biology of two species of Megachile (Moureapis) (Hymenoptera: Megachilidae) in a semideciduous forest reserve in Southeastern Brazil. Apidologie 43(1):71-81. doi: 10.1007/s13592-011-0091-z.
https://doi.org/10.1007/s13592-011-0091-...
, Fig. 1), with tender leaves used to build the nest, and the resemblance of the nest habitus. Teixeira et al. (2011Teixeira, F. M.; Schwartz, T. A. C. & Gaglianone, M. C. 2011. Biologia da nidificação de Megachile (Moureapis) benigna Mitchell. EntomoBrasilis 4(3):92-99. doi: 10.12741/ebrasilis.v4i3.140.
https://doi.org/10.12741/ebrasilis.v4i3....
) reported nests built with petals and the use of mud beneath it, forming two layers, the outer layer made of petals and the inner layer made of mud. However, the two nests that they report as being of M. benigna, which differ greatly of the other 15 they collected, probably were of some Megachile (Chrysosarus) species, since the females of this subgenus have no cutting edges in their mandibles, which would explain the use of petals in nest building, besides the use of mud. Other aspects regarding the nest architecture of M. benigna such as leaf fragment shape match with this study and the one presented by Cardoso & Silveira (2012Cardoso, C. F. & Silveira, F. A. 2012. Nesting biology of two species of Megachile (Moureapis) (Hymenoptera: Megachilidae) in a semideciduous forest reserve in Southeastern Brazil. Apidologie 43(1):71-81. doi: 10.1007/s13592-011-0091-z.
https://doi.org/10.1007/s13592-011-0091-...
).

The brood cell totally provisioned with pollen and nectar, but curiously with no egg, was unseen to our knowledge, even though the innermost and outermost cell had one egg each. The probable explanation for this is some type of failure at the bee oviposition mechanism, or even the fact that the bee was elder and running out of eggs. Vestibular and intercalary cells differ in the sense that they are not provisioned (Krombein, 1967Krombein, K. V. 1967. Trap-nesting wasps and bees. Life histories, nests and associates. Washington, Smithsonian Press. 570p.), and it is a difficult strategy that spend time and effort for load an entire brood cell for leaving it with no offspring.

The knowledge on the food sources used by Megachile in the Neotropics is limited, despite its high diversity (Raw, 2007Raw, A. 2007. An annotated catalogue of the leafcutter and mason bees (genus Megachile) of the Neotropics. Zootaxa 1601:1-127. ). The subgenus Moureapis seems to be oligolectic, in the light of data reported so far. Schlindwein (1998Schlindwein, C. 1998. Frequent oligolecty characterizing a diverse bee-plant community in a xerophytic bushland of subtropical Brazil. Studies on Neotropical Fauna and Environment 33:46-59.) reported females of Megachile apicipennis Schrottky, 1902 visiting flowers of Asteraceae and other females of an unidentified species of Megachile visiting flowers of Asteraceae and Cactaceae. These observations agree with the pollen analysed from brood cells of other species belonging to the Moureapis subgenus: for Megachile maculata Smith, 1853 in the transition of the Cerrado and Atlantic Forest, it harvested pollen from Baccharis and Vernonia flowers (Asteraceae) predominantly (Sabino et al., 2016Sabino, W. O.; Bastos, E. M. A. F. & Antonini, Y. 2016. Trophic-niche of the leaf cutter bee Megachile (Moureapis) maculata (Hymenoptera: Megachilidae) in Southeastern Brazil. Journal of the Kansas Entomological Society 89(4):373-381. doi: 10.2317/0022-8567-89.4.373.
https://doi.org/10.2317/0022-8567-89.4.3...
); and M. benigna at the JBRJ, in the Atlantic Forest, pollen from Cyrtocymura flowers (this report). Interestingly, Buschini et al. (2009Buschini, M. L. T.; Rigon, J. & Cordeiro, J. 2009. Plants used by Megachile (Moureapis) sp. (Hymenoptera: Megachilidae) in the provisioning of their nests. Brazilian Journal of Biology 69(4):1187-1194. doi: 10.1590/S1519-69842009000500025.
https://doi.org/10.1590/S1519-6984200900...
) reported an unidentified species of Megachile (Moureapis) provisioning its cells with pollen of two Ludwigia species (Onagraceae), L. sericea (Cambess.) H. Hara and L. peruviana (L.) H. Hara, in the Araucaria Forest of the Brazilian South, which may point to some variation in the subgenus level, but fidelity of pollen foraging by females of one species. The food source report made by M. benigna in this study is presented with confidence based on the study of Dorado et al. (2011Dorado, J.; Vázquez, D. P.; Stevani, E. L. & Chacoff, N. P. 2011. Rareness and specialization in plant-pollinator networks. Ecology 92(1):19-25.) that observed reliability on data extracted from pollen loads analysed from trap-nests.

Acknowledgements

We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPES, Finance Code 001, for partly funding this research, and the Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq for the grant to DM (proc. 131188/2017-8). We thank the personnel of the Jardim Botânico do Rio de Janeiro, especially Maria Lúcia Teixeira Moscatelli, for the help provided; Claudia Barbieri for kindly identifying the pollen types. This article is part of the SIGMA Project nº 21565MN/UFRJ. It is the contribution nº60 from the HYMN. Museu Nacional VIVE!!!

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    » https://doi.org/10.1007/s13592-019-00635-6
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    » https://doi.org/10.1890/ES13-00308.1
  • Marinho, D.; Muniz, D. B. & Azevedo, G. G. 2018. Nesting biology of three Megachile (Hymenoptera: Megachilidae) species from eastern Amazonia, Brazil. Revista Brasileira de Entomologia 62(2):97-106. doi: 10.1016/j.rbe.2018.03.002.
    » https://doi.org/10.1016/j.rbe.2018.03.002
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  • Raw, A. 2007. An annotated catalogue of the leafcutter and mason bees (genus Megachile) of the Neotropics. Zootaxa 1601:1-127.
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    » https://doi.org/10.2317/0022-8567-89.4.373
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Publication Dates

  • Publication in this collection
    25 Feb 2022
  • Date of issue
    2022

History

  • Received
    31 Aug 2021
  • Accepted
    12 Jan 2022
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