doi:10.12741/ebrasilis.v10i1.672 e-ISSN 1983-0572 Publication of the project Entomologistas do Brasil www.ebras.bio.br Creative Commons Licence v4.0 (BY-NC-SA) Copyright © EntomoBrasilis Copyright © Author(s) Scientific Note/Comunicação Científica Notes on the nesting biology of five species of (: ) in the Brazilian Amazon

Fernando da Silva Carvalho-Filho¹ & Favizía Freitas de Oliveira²

1. Museu Paraense Emílio Goeldi, Coordenação de Zoologia. 2. Universidade Federal da Bahia.

EntomoBrasilis 10 (1): 64-68 (2017)

Abstract. Orchid (Euglossini) are medium to large-sized species with fully or partially metallic body that are relatively common in the Neotropical Region. Nevertheless, the nesting biology of many species remains unknown. Therefore, the objective of this paper is to provide new information on the nesting biology of five species of Euglossini found in urban and forested sites of Brazilian Amazon. The nests ofEufriesea pulchra (Smith) and chalybeata Friese were recorded for the first time, found in an active nest of the Azteca sp. and in a fallen rotting tree, respectively. The nest of Euglossa townsendi (Linnaeus) was found in the leaf of an ornamental plant Cordyline sp. (Asparagaceae), also newly recorded. Euglossa intersecta Latreille was recorded nesting in an abandoned termite nest, and Cockerell was found nesting in a tubular metal window handle.

Keywords: ; ; ; Euglossa; Nest.

Notas sobre a biologia de nidificação de cinco espécies de Euglossini (Hymenoptera: Apidae) na Amazônia Brasileira

Resumo. As abelhas-da-orquídea (Euglossini) possuem tamanho médio a grande, corpo parcialmente ou completamente metálico e são relativamente comuns na região Neotropical. Apesar disso, a biologia de nidificação da maioria das espécies permanece desconhecida. Portanto, o objetivo deste estudo e fornecer novas informações sobre a biologia de nidificação de cinco espécies de Euglossini encontradas em área urbana e florestada da Amazônia Brasileira. Os ninhos de Eufriesea pulchra (Smith) e Euglossa chalybeata Friese foram registrados pela primeira vez, encontrados dentro de ninho de formiga Azteca sp. e em uma árvore apodrecida caída, respectivamente. O ninho de Euglossa townsendi Cockerell foi registrado pela primeira vez em uma folha da planta ornamental Cordyline sp. (Asparagaceae). Euglossa intersecta Latreille foi registrada nidificando dentro de um ninho abandonado de cupim e Euglossa cordata (Linnaeus) foi encontrada nidificando em uma maçaneta tubular de metal de uma janela.

Palavras-Chave: Abelha; Apinae; Eufriesea; Euglossa; Ninho.

he corbiculate apines (pollen-basket bees) comprise dens of small mammals and land crabs, in aerial nests made of about 890 described species divided in four tribes: Apini resin and attached to the undersides of leave or twigs, and in (honey bees), Meliponini (stingless bees), Bombini buildings. (bumble bees) and Euglossini (orchid bees) (Ma r t i n s et al. 2014). The orchid bees are the only ones that do not exhibit The bees of this tribe are relatively common within their large colonies, and they may be solitary, communal, semisocial, areas of geographical distribution, and many species have a or social. In addition, some species are cleptoparasites in nests fully or partially metallic body (Ra m í r e z et al. 2002; Ca m e r o n of other orchid bees (Ra m í r e z et al. 2002). 2004), making them attractive to professionals and amateur collectors. Males are attracted to various aromatic compounds The Euglossini is Neotropical in distribution and comprises (Wi l l i a m s & Wh i t t e n 1983), making them easily collectable, 187 species of medium to large-sized (8.5-29.0 mm length), and consequentially they are well represented in entomological moderately to densely hairy bees arranged in five current genera: collections. In spite of this, the nests of orchid bees are difficult ; Eufriesea; Euglossa; ; and (Ra m í r e z to find in natural substrates, and the nesting biology of many et al. 2002; Mi c h e n e r 2007; Ma r t i n s et al. 2014). Information species remains undocumented (Ra m í r e z et al. 2002). Therefore, about the known nesting biology of orchid bees was summarized the objective of this study is to provide new information about by Ra m í r e z et al. (2002), reporting that these bees nest in hollow the nesting biology of five species of Euglossini found in Brazilian trees, in bamboo stems, under tree bark, in wooden boxes made Amazon. by humans, in ground cavities, under rocks, inside active nest of and termites, in abandoned carton nests of social , The observations on euglossine nesting biology reported here and in nests of carpenter bees excavated in wood, in abandoned were made in Belém, state of Pará, , in three distinct

Edited by:  Corresponding author: Funding agencies: Wesley Dáttilo Fernando da Silva Carvalho-Filho  Without funding declared

Article History:  [email protected]  No ORCID record Received: 10.xii.2016 Accepted: 25.ii.2017

www.periodico.ebras.bio.br 65 Notes onthenestingbiologyoffivespeciesEuglossini… a nest of ant of nest a recorded nesting in a rotting cacao pod that was also occupied by of species undetermined An nests. carton ta uuly ae fly tog ealc oy (W body) metallic strong fully a have usually (that most of that from different quite pattern color to similar very is and Amazon Brazilian in length) mm largest 19 (about the of one is species This attention. intersecta oai valida [Monacis Dolichoderinae another of nest the in found were cells whose Kimsey, lucifera ant nest. The other species nesting in active ant nest is of record second the and species this of biology nest the of record first the is This 2). and resin 1 (Figures yellow a with cemented wood reddish of pieces small of (Figure 1). tree The lemon cells were a attached to of the tree branch bark and a composed of underside the on ground the from Azteca the of species ant an of nest carton active small a inside pulchra of nest the 2009, November 5 on site, MPEG the In the entomologicalcollectionofMPEG. (Kempf)] in Panama (K (Glossuropoda of nest the 2012, August 12 on site, MPEG the in Also it isrestrictedtothecladeformedby if or clade these in behavior widespread a is nests ant in nesting the as However, two. biology of these of species sister the is (Mócsary) of species sister is lucifera E. aooi ky ad eecitos f pce (K species with of redescriptions individuals, and identified keys previously taxonomic with comparison identified were by laboratory specimens The the adults. in of were emergence boxes the until plastic Nests in maintained 48°26’25.14”W). and collected (1°25’20.32”S (PEUt) do Estadual Parque the Utinga in forest urban protected a in 3) and 2) in a house in the urban center (1°25’49.50”S 48°27’09.84”W); Museu of campus research Paraense Emílio the Goeldi (MPEG) (1°27’06.00”S 48°26’37.85”W); in border forest 1) localities: W otos (K portions color pattern with strong metallic areas interspersed with darker Bees nesting in termite nests are not common among common not are nests termite in nesting Bees et al.2002). of hypothesis phylogenetic the In 1986). R from different families nest on nests of p (saaaee (iue 7 n 8 i te border the plant in 8) ornamental and 7 introduced (Figures the (Asparagaceae) sp. of Cordyline leaf folded live a inside The nest of without excessivehumidityfor example( environment, nest regulated a provide and/or excavated be can that substrate large a is it because nests termite prefer bees that possible is it nests, occupied and abandoned both utilize bees in active nests of nests active in aggregate termite nests, since it has been previously recorded nesting only rigid a arboreal abandoned and forming active utilizes species another, This 4). (Figure one to one fused tightly resin, of cells black 28 of cluster a containing nest, termite the the termite nest, and it was located in a chamber in the center of The opening of the nest was in the middle of the basal surface of ground. the from m 1.70 about fork tree a in located 3) (Figure (probably nest termite abandoned cm) 22 x (19 (R among widespread is habit this but species, for the bees (C bees the for advantage protective offer termites the that suggested been has i b u o n e t t i h a E. pulchra E. m z e r í k 2004; Forel (Formicidae: Dolichoderinae) located about 70 cm 70 about located Dolichoderinae) (Formicidae: Forel 1983;

Sih, otiig sre o tre el, a found was cells, three of series a containing (Smith), 20) De o hs te eair of behavior the this, to Due 2002). al. et E. ornata is unknown, it is not possible to assess if the Euglossa ( Latreille i m Crematogaster limata Crematogaster N y e s (14-19 mm length) (Figures 5, 6) in also having a having also in 6) 5, (Figures length) mm (14-19 C intersecta ) o j i r r a e a m 1982; m Nasutitermes o i s é n o r e

. 2012). However, as some species of species some as However, 2012). al. et etn i a emt ns cuh our caught nest termite a in nesting & F & Euglossa i 2004). Most species of m C y e s a i r a r r e m aril, a fud nie small a inside found was Latreille, 1982), a species that also constructs n o r e , and pulchra, E. ) townsendi 2011). All bees are deposited in deposited are bees All 2011). sp. (Z sp. 04. ay pce o bees of species Many 2004). Smith in Costa Rica (Y Rica Costa in Smith E. luciferaandpulchra. Eufriesea = i h c c u Nasutitermes Dolichoderus C R o j i r r a

Cockerell was found Euglossa a . 1969; al. et m z e r í species Eufriesea Euglossa Eufriesea ornata Eufriesea Euglossa Eufriesea have a nesting in active in nesting etal.2012). Nasutitermes

. (2010), al. et i m spp. and it have been have y e s Eufriesea Eufriesea a i l l i Euglossa Euglossa Euglossa species R species validus 1982; a m m g n u o z e r í s & )

on leafs: on of species three only and general nesting pattern for the species of the subgenus f abo (G bamboo of made nests trap in are species this of records nesting only The caps. the of construction the in difference noticeable a without located was and about 90 cm resin from the ground. dark The walls of of the cells were made soft and cells leaf six The about 2010. contained June 13 on MPEG the in forest secondary a of Augusto, S.C. & C.A. Garófalo, 2004. Nesting biology and social and biology Nesting 2004. Garófalo, C.A. & S.C. Augusto, thank AdrianoMacielforFigures11to13. We version. English the editing with help and manuscript the of revision for (MPEG) Overal L. William Dr. to grateful are We The nest of nest The sites, asobservedhere. et al. 2008), where it also utilizes human made objects as nesting produce irregular clusters of cells (C cells of clusters irregular produce subgenus the of species The tree. fallen a in 2004). However, the nests of nests the However, 2004). ap et ad n odn oe (R boxes wooden in and nests cordata E. resin. in tubular objects; such as trap nests made of bamboo cane, and brown pinkish of cells of species Many three contained nest (Figure The pass to 10). female the for enough large just hole circular small a was there which in wall resinous black and pink a with metal tube (Figure 9). The upper opening of the tube was sealed cm 8 vertical a is handle window The 10). and 9 (Figures 2011 of nest a found we handle window metallic tubular a of hollow the Inside of thesubgenus (Euglossa to secondary forests (D forests secondary and vegetation, savanna-like grasslands, environments, dry and specie s.s., whose biology is known, seems to be cavity nesting (C Carrijo, T.F., R.B. Gonçalves & R.G. Santos, 2012. Review of bees neotropical of biology and Phylogeny 2004. S.A., Cameron, biology of this species and the first record of record first the and species this of biology the on information first the is This 13). and 12 (Figures resin of mass rounded small a of composed caps with fashion comb-like a in arranged and shape in spheroid resin, brown dark of made cells 10 about contained nest The 12). and 11 (Figures 2007 July inside a large rottingfallentreein a primary forest ofPEUton 5 (G the nest as observed in it and containing cavity the of limitation species spatial to related be to seems same the of inside feature variable a is pattern (Glossurella Dressler (see Dressler ó r a E. tutr of structure 0218- DOI: 141-149. 59: Apicotermitinae). Termitidae, (Isoptera, of nests in Apidae), bee, as guests in termite nests, with a new record of the communal DOI: ento.49.072103.11585 377-404. Entomology, of 49: Review Annual (Euglossini). bees orchid 0760-2. DOI: 51: 400-409. Sociaux, Insectes Euglossini). Apidae, (Hymenoptera, f (Glossura o l a Euglossa (Smith, 1879) (Hymenoptera, (Hymenoptera, 1879) (Smith, obscura Gaesochira Euglossa x. Euglossa etal. ) championi has previously been recorded nesting in abandoned in nesting recorded been previously has ) Euglossa dodsoni R ó r a 1998). a Glossurella ) m ACKNOWLEDGMENTS cordata Euglossa f z e r í chalybeata Euglossa ( ( o l a ( Euglossa c u Euglossa Moure;

https://dx.doi.org/10.1007/s00040-004- https://dx.doi.org/10.1007/s00040-012- (Glossura are aerial such as that found in the species REFERENCES . 2002 and references therein). The therein). references and 2002 al. et t al. et k Euglossa e 1902), as well as in cities (L cities in as well as 1902), mro, 1925 Emerson, banksi Anoplotermes 5. (Linnaeus) is adapted to live in open in live to adapted is (Linnaeus) Euglossa https://dx.doi.org/10.1146/annurev. have already been recorded nesting recorded been already have . 1993; ) Hwvr te el arrangement cell the However, . cordata ) Euglossa) Euglossa E. Cheesman; championi ( ) Carvalho-Filho &deOliveira(2017) Glossura (Euglossa chalybeata have been recorded nesting recorded been have A o t s u g u a m a m ( n o r e Lnau) n 0 July 20 on (Linnaeus) Glossurella z e r í e-ISSN 1983-0572 townsendi ) & townsendi ) 2004) as observed as 2004) annectans

Glossura

20) The 2002). al. et nets Sociaux, Insectes Friese Euglossa G ó r a f )

Cockerell o l a was found was z e p ó turbinifex Euglossa Euglossa Dressler seems to seems 2004), and nesting a -U m n o r e e b i r E.

Janeiro - Abril 2017 - www.periodico.ebras.bio.br EntomoBrasilis 10 (1): 64-68

1 2

3 4

5 6

Figures 1-6. (1) Cells of Eufriesea pulchra inside the opened Azteca sp. ant nest, lateral view; (2) Cell of Eufriesea pulchra with larva, latero-dorsal 66 view; (3) Termite nest with arrow pointing to the nest entrance of Euglossa intersecta, ventral view; (4) Termite nest piece containing the cells of Euglossa intersecta, lateral view; (5) Habitus of Eufriesea pulchra, dorsal view; (6) Habitus of Euglossa intersecta, dorsal view. Scale bars = 1 cm, except in Figure 3 where it represents 3.5 cm.

e-ISSN 1983-0572 Janeiro - Abril 2017 - www.periodico.ebras.bio.br EntomoBrasilis 10 (1): 64-68

7 8 9

10 11

12 13

Figures 7-13. (7) Dry leaf with cells of Euglossa townsendi, ventral view. (8) Dry leaf with cells of Euglossa townsendi with arrows pointing to cell exits, dorsal view; (9) Window handle utilized as nest site by Euglossa cordata, lateral view; (10) Nest opening of Euglossa cordata inside window 67 handle, ventral view; (11) Fallen trunk with a cluster of cells of Euglossa chalybeata, dorsal view; (12) Cluster of cells of Euglossa chalybeata inside trunk, dorsal view; (13) Cluster of cells of Euglossa chalybeata removed from trunk, lateral view. Scale bars = 2 cm, except in Figure 10 where it represents 2.5 cm.

e-ISSN 1983-0572 Janeiro - Abril 2017 - www.periodico.ebras.bio.br EntomoBrasilis 10 (1): 64-68

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Suggestion citation:

Carvalho-Filho, F.S. & F.F. de Oliveira, 2017. Notes on the nesting biology of five species of Euglossini (Hymenoptera: Apidae) in the Brazilian Amazon. EntomoBrasilis, 10 (1): 64-68. Available on: doi:10.12741/ebrasilis.v10i1.672 68

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