Neotropical Entomology ISSN: 1519-566X Journal Homepage

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Ecology, Behavior and Bionomics Long-Term Male Aggregations of Euglossa melanotricha Moure (Hymenoptera: Apidae) on Fern Fronds Serpocaulon triseriale (Pteridophyta: Polypodiaceae) MD e Silva1, ACR Andrade-Silva2, M Silva3 1Lab de Ecologia da Polinizaçao – ECOPOL, Instituto de Biologia, Depto de Botânica, Univ Federal da Bahia, Salvador, BA, Brasil 2Lab de Comportamento e Ecologia de Insetos Sociais, Depto de Biologia/FFCLRP, Univ de São Paulo, Ribeirão Preto, SP, Brasil 3Lab de Entomologia, Depto de Ciências Biológicas, Univ Estadual de Feira de Santana, Feira de Santana, BA, Brasil

Keywords Abstract Dormitory, Euglossini, interaction, sleeping site A communal dormitory of male orchid bees, Euglossa melanotricha Moure, was monitored over a one-year period, when they passed the Correspondence night in the fronds of a Serpocaulon triseriale (Polypodiaceae) fern. Marília D e Silva, Lab de Ecologia da The bees used the same fronds continuously, moving to neighboring Polinizaçao – ECOPOL, Instituto de Biologia fronds as senescence set in. As many as 49 males were observed – Depto de Botânica, Univ Federal da Bahia, together on any one night, clinging to the midribs on the abaxial Campus Universitário de Ondina, Rua Barão do Jeremoabo s/n, Ondina, 40170-115, Salvador, BA, Brasil; [email protected] males returned to the same site to pass the night continuously over surfacea number of upof months,to five fern and blades were withobserved their makingmandibles. physical A number contact of with one another without provoking agonistic behavior. Males of Edited by Fernando B Noll – UNESP E. melanotricha appeared to prefer sleeping at sites close to nests and potential sources of odoriferous essences, such as orchids Received 04 March 2011 and accepted 07 (Orchidaceae). June 2011

Introduction although the selection of sites is an unknown process.

Male solitary bees do not generally pass the night in defense (Treisman 1975, Hoogland & Sherman 1976, maternal nests like females, but tend to aggregate in AzevedoThe benefits & Faria of Jr aggregation 2007), thermoregulation may include anti-predator (Yom–Tov et other locations, forming communal dormitories (Alves- al dos-Santos et al 2009). These dormitories are locations at which a number of individuals of the same or from 1976), more efficient access to females (Wagner 1993) congregateand the synchronous as a consequence rearing of environmentalor education ofrestrictions, offspring close to one another (Adams 1999). such(Emlen as & the Demong scarcity 1975). of appropriate However, males roosts, may rather also simply than differentThree speciestypes of gather communal to rest fordormitories a few hours, have generally been et al et al 2004): facultative & Linsley (1960) suggested that the gregarious behavior (formed during migrations), diapause (in response to maybehavioral have a or protective social factors function, (Endringer but when males 2004). begin Evans to seasonalidentified variation) in insects and (Endringer circadian (nocturnal roosting of congregate (preliminary concentration), they are more groups of male bees). In the latter case, the same sites exposed to certain types of predators (Mallet & Gilbert may be used continuously over many years by successive et al 2004). generations of insects (Mallet & Gilbert 1995). In bees, A number of studies have focused on aggregations this type of behavior has only been observed in males, in1995, Apoidea Oliveira (Linsley & Castro 1962, 2002, MiyanagaEndringer & Maeta 1998,

Stehmann & Semir 2001, Alves-dos-Santos et al 2009), although most have involved relatively short-term and qualitative observations. The paucity of long-term studies, topof 0.1. of the In January torax, to 2002, determine all males which in individualsthe aggregation returned (n = that have monitored dormitories over a number of years to23) the were site, marked and their with frequency permanent of visitation. opaque white ink on locating(Alcock males1998), in theor experimentalwild and determining approaches their preferred (Wcislo The bee species was identified by Dr. André Nemésio nocturnal2003) is probably roosts. In due addition, primarily males to rarely the difficulties use sites for of MG,of the Brazil, Laboratório based on de ten Ecologia specimens, e Sistemática which were de deposited Abelhas, more than a few days. In fact, most observations refer to Depto de Zoologia, Univ Federal de Minas Gerais (UFMG), the use of sites for only a single night. In the present study, aggregations of male orchid bees of the species Euglossa in his collection. The plant species was identified by melanotricha Moure were observed continuously MSc Maria Lenise Silva Guedes, curator of the Herbário using fern fronds Serpocaulon triseriale as communal statisticsAlexandre (means Leal Costa, and standard Univ Federal deviations) da Bahia, were BA, provided Brazil, dormitories over an extended period. where the voucher specimen is deposited. Descriptive

by Microsoft Excel 2007, and Pearson’s correlation Material and Methods coefficient was calculated in BioEstat 5.0. Results The present study was conducted in an urban residential area of 0.5 ha located in the municipality of Campo The aggregation of E. melanotricha

observed on two blades of a S. triseriale males fern. wasAll males first Formoso in the Chapada Diamantina region in the state abandonedobserved on the January site in the11th, following 2002, when morning 23 males(07:00 were am), climateof Bahia, is Brazilhot and (10°30’17.71”S,40º19’10.99”W). semi-arid (BSh) (Köppen 1948), Local with altitude ranges from 400 m to 800 masl. The region’s Fifty-six cultivated orchids belonging to eight species rainy season from March to August (Bahia 2010). but 30 specimens returned in the afternoon (4:00 pm). annualThe precipitation orchid bees of 302the genusmm to Euglossa1,935 mm, are and essentially a marked Neotropical in distribution, with a total of 122 recognized were observed in the study area, which would flower at species (Nemésio 2009). They are found from Paraguay different times over the course of the year, although with 49some males overlap of E in. melanotricha the flowering were period observed (Fig 1). occupying Indies, except for a single species in Jamaica, Euglossa Between October 2002S. triserialand Octobere 2003, up to jamaicensisto Mexico, but (Silveira are absent et from al 2002, Chile andMoure most et of al the 2007). West the mean number of males observed together in the Euglossa melanotricha is found in southern, central, primarily five fern blades of . During this period, and eastern Brazil (Moure et al 2007), typically in open S. triseriale frond between vegetation, such as the savanna and semi-arid habitats dormitory varied was 9.2 ± 12.2 (range = 1-49, n = 342). of the Cerrado and Caatinga biomes, respectively. The The first male landed on the species appears to be most abundant in Cerrado habitats 4:30 pm and 08:50 pm (mean = 6:25 pm ± 02:08 dp, n = (Nemésio & Faria Jr 2004, Alvarenga et al. 2007). midrib342), and of otherthe basal males region would of continue the blade to (Figarrive 2). for The around hind Serpocaulon triseriale, formerly known as Polypodium the next hour. The first bee clings with its mandibles to the triseriale, is very common throughout most of Brazil 25 Number of species Number of individuals ﬂowering (Labiak & Hirai 2010). It is frequently used as a decorative plant, and is tolerant to wide variations in humidity 20 and temperature. Observations of the number of males present at the communal dormitory were initiated in 15

10 onwards,January 2002, daily and records continued were until kept December of the time 2003, at which when maleswe finalized began to our occupy observations. the site at theFrom end October of each afternoon,2002 and and when they left in the morning. Observations were 5 conducted in two sessions, one between 05:00 am and 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Month 10:00 am (07:15 am ± 01:30, n = 342), and the other Fig 1 Orchid species observed at the study site in Campo Formoso, thebetween temperature 4:30 pm and and relative 8:50 pm humidity (6:25 pm of the± 02:08, air were n = recorded331). During using these a thermo-hygrometer observations, over with a total an accuracyof 600h, Brazil, and the number of individuals flowering each month between Neotrop Entomol 40(5): 548-552 © 2011 Sociedade Entomológica do BrasilOctober 2002 and October 2003. 549 Euglossa melanotricha Male Aggregations on Fern Fronds Silva et al

100 Temperature Humidity Male abundance 90 80 70 60

50 Mean 40 30 20 10 0 Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Set Oct Month Euglossa melanotricha males congregating Fig 2 Aggregation of Euglossa melanotricha males on a Serpocaulon on fronds of Serpocaulon triseriale between October 2002 and triseriale frond. Males preferred to rest at the midrib of the blades Fig 3 Abundance of and were closely grouped. October 2003. legs of the male were free, and were rubbed continuously the dormitory to pass the night, there was no strict over the surface of its body, as if spreading some kind of bees confirmed that while individuals did return to substance over the body. The second male to arrive took returned to the dormitory on seven consecutive nights, site fidelity. Of the 23 marked males, only five (21.7%) just below the second, and so on. day of observation. up aThis similar behavior position would a little continue below the until first themale, blade the third was and only two (8.7%) were still using the site on the 17th fully occupied, with the last male located a little below the medial region of the blade. Males arriving later would Discussion begin to occupy a neighboring blade in the same manner. Males tended to be grouped very closely together, and The use of the same roosts over long periods of time would sometime interact, but were never aggressive by different males may be related to the presence towards one another. On a number of occasions, recently- arrived males were observed touching the antennae or abundance of orchids, particularly Catasetum, Notylia and other part of the body of a resting male when settling into Ocyndiumof many natural(Fig 1). These nests orchids (N = 14) are importantand the relative sources position. The same fern fronds were used consecutively of odoriferous essences to males, which visited them for up to 14 days, until their natural senescence impeded E. their use. At this point, the E. melanotricha males would melanotricha bees are born in the warmer months and, begin occupying a new blade, generally beside the one asduring a consequence, the flowering there period. were We more observed males thatin the more roost. previously occupied (Fig 2). The mean number of males occupying the dormitory less time searching for an appropriate roost each night, per night was higher during the dry season, between allowingAlternatively, them site to investfidelity more would energy allow the males following to spend day in the search for the odoriferous essences used to attract females. In addition, the presence of natural nests, betweenSeptember the and number February of males(Z = 5.68, in theP < aggregation0.0001, n = 395) and associated with the certainty of the emergence of virgin (Fig 3). Despite this variation, no correlation was found females, and adequate overnight shelter would be extra incentives for the males to stay in this area. either ambient temperature (r = 0.006, P = 0.90, n = 342) There are few records in the Apoidea of males using theor humidity activity of(r E=. 0.03melanotricha P = 0.65; nmales = 342). in forestedOn rainy areasdays, the same dormitory over long periods (Alves-dos-Santos withinmost of the the same males region remained as the instudy the siteaggregation. indicate that Data they on et al 2009). In fact, studies of males of Augochlorella are active throughout the year, but are more abundant neglectula during the dry season, in particular in November and Idiomelissodes duplocincta (Cockerell) in Arizona (Alcock (Cockerell) in Panama (Wcislo 2003) and On sunny days, males dispersed from the dormitory data indicate that this behavior may be related to the high atDecember around 7:00(ACR am Andrade-Silva, and returned pers. a little comm.). later (8:00 pm). mobility1998) recorded of males, no which sleeping travel site relatively fidelity. long However, distances the On cloudy days, they left later, at around 10:00 am, and searching for virgin females or for areas with high abandon the dormitory. Observations of the marked move on emerging from their nests, as suggested for landed earlier, starting at 3:00 pm. Few males did not concentrations of flowers towards which these females 550 Neotrop Entomol 40(5): 548-552 © 2011 Sociedade Entomológica do Brasil Silva et al Euglossa melanotricha Male Aggregations on Fern Fronds the aggregation of males in Centris fuscata (Lepeletier) reviewers for their critical analysis and suggestions for (Azevedo & Faria Jr. 2007). the improvement of an early version of this manuscript. Females of E. melanotricha (Moure) usually construct their nests in ground holes, cavities in buildings or fellowship. mounds (Sakagami et al 1967, Augusto & Garófalo 2007). We also thank FAPESB for granting Maise Silva a post-doc Although the nesting behavior of females is well-known, the behavior of the males is rarely described. According References dense aggregations, maintain contact with one another, Adams AAY (1999) Communal rosting in insects. http://colostate. andto the use classification the same dormitories of Alcock (1998), continuously they congregate over periods in htm.Accessed in June 2010. of a number of months. The lack of agonistic interactions edu/Depts/Entomology/courses/en507/papers1999/yackel. indicates that the species is characterized by some level of Alcock J (1998) Sleeping aggregation of the Idiomelissodes sociality, as recorded in other species of the superfamily duplocincta (Cockerell) (Hymenoptera: Anthophorini) and their Apoidea (Alcock 1998, Azevedo & Faria Jr 2007). One interpretation of the continued use of the possible function. J Kans Entomol Soc 71: 74-84. dormitory site is that males of E. melanotricha mark the S. triseriale fronds with pheromones in order to facilitate Alvarenga PEF, Freitas RF, Algusto SC (2007) Diversidade de the task of locating the site in the following afternoon. Euglossini (Hymenoptera, Apidae) em áreas de cerrado do Triangulo Mineiro. Biosci J 23: 30-37. Male sleeping aggregations of solitary oil-colleting bees in Brazil Alves-dos-Santos I, Gaglianone MC, Naxara SRC, Engel MS (2009) In this case, the male that “decides” to return to the maledormitory presumably earlier releaseswill be able a signal to find odor, the which site relativelyindicates (Centridini, Tapinotaspidini, and Tetrapediini; Hymenoptera: Euglossa (Euglossa) itseasily, location and then to other signal males, to the allowing following these males. individuals The first Apidae). Gen Mol Res 8: 515-524. melanotricha (Hymenoptera: Apidae) no solo do Cerrado. to follow the trail and aggregate at the site. Males that Augusto SC, Garófalo CA (2007) Nidificação de arrive earlier will be able to occupy the internal portion of the blade, where they will be better protected from Neotrop Entomol 36: 153-156. Phacellodomus rufifrons nocturnal predators. Azevedosolitary AA, bee Faria species Jr LRR (Apidae: (2007) Centridini) Nets of in southeastern Brazil. Most of the hypotheses used to explain aggregating (Wied, 1821) (Aves: Furnariidae) as sleeping shelter for a behavior in males of Apoidea favor anti-predator strategies and thermoregulation (Miy Anaga & Maeta Lundiana 8: 53-55. 1998, Alves-dos-Santos 1999, Stehmann & Semir 2001, Bahia (2010) Superintendência de Recursos Hídricos (Ba). Oliveira & Castro 2002, Alves-dos-Santos et al 2009). The Secretaria de Meio Ambiente e Recursos Hídricos. Plano present study indicates that the local abundance of natural Diretor de Recursos Hídricos - Bacia do Itapicurú. Salvador, nests, the eclosion of virgin females throughout the year, a SRH, 501p. breeding in a colonial bird: a new hypothesis. Science 188: essences may have favored the persistence of males of E. Emlen ST, Demong MJ (1975) Adaptive significance of synchronized melanotrichasafe shelter to inspend the area the night for such and a the relatively availability long of period floral 1029-1031. of time. However, further studies are needed to investigate Helicoinus the frequency of aggregations of E. melanotricha males in Endringererato (Lepidoptera, FB, Silva PR, Nymphalidae).Lutz LV (2004) NaturezaHipóteses on evolutivas line 2: 1-9. sobre a origem e manutenção dos dormitórios comunais de substrate is related to the availability of locations with concentrationsurban areas, and of whether orchids the or prolongedis a common use behaviorof a specific in Evansh E, Linsley EG (1960) Notes on a sleeping aggregation of the species. It would also be important to verify whether solitary bees and wasps. Bull Soc Calif Acad Sci 59: 30-37. Hoogland JL, Sherman PW (1976) Advantages and disadvantages marked males abandon the dormitory due to the loss of of bank swallow (Riparia riparia) coloniality. Ecol Monogr 46: theirmale characteristicmarking may odor,affect impeding their behavior, their recognition and whether by 33-58. Labiak PH, Hirai R (2010) Polypodiaceae in lista de espécies da flora do Brasil. Jardim Botânico do Rio de Janeiro. (http:// the other members of the “group”. Aculeate Hymenoptera. Acknowledgments floradobrasil.jbrj.gov.br/2010/FB091766). Linsley E (1962) Sleeping aggregations of II Ann Entomol Soc Am 55 2: 148-164(17). Koppen W (1948) Climatologia. México, Fondo de Cultura We are grateful to Ana Maria Galvão Dantas e Silva Económica. 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