ore JHR 74: 65-81 (2019) JOURNAL OF | *0eeriewed opevaccetsjoural doi: 10.3897/jhr.74.39 191 ME Hymenopter a http://jhr.pensoft.net The Inzrational Society of ymenopterists. RESEARCH Flower use by late nineteenth-century orchid bees (Eufriesea surinamensis, Hymenoptera, Apidae) nesting in the Catedral Basilica Santa Maria la Antigua de Panama Paola Galgani-Barraza', Jorge Enrique Moreno!, Sofia Lobo’, Wendy Tribaldos?*, David W. Roubik', William T. Wcislo' | Smithsonian Tropical Research Institute (STRI), Panama, Apartado 0843-03092, Balboa, Panama 2 Dalmdtica Conservacao e Restauro, Rua da zona Industrial de Covilhé, n4236 4620-276, Lustosa — Lou- sada, Portugal 3 Comité Arquidiocesano Amigos Iglesias Casco Antiguo, Panamd 4 Independent museologist, educator and journalist. Costa del Este, Avenida Centenario, Edificio PMG — Panama City, Panama Corresponding author: William T- Weislo (WcisloW @si.edu) Academic editor: /. Neff | Received 18 August 2019 | Accepted 24 November 2019 | Published 30 December 2019 http://zoobank. org/2F25B4 1 C-9797-4302-9A02-C9E923B24224 Citation: Galgani-Barraza P, Moreno JE, Lobo S, Tribaldos W, Roubik DW, Wcislo WT (2019) Flower use by late nineteenth-century orchid bees (Eufriesea surinamensis, Hymenoptera, Apidae) nesting in the Catedral Basilica Santa Maria la Antigua de Panama. Journal of Hymenoptera Research 74: 65-81. https://doi.org/10.3897/jhr.74.39191 Abstract A recent restoration of the Basilica Cathedral in Casco Viejo, Panama, revealed that prior to 1871-1876 female orchid bees (Eufriesea surinamensis) built large nesting aggregations high above the main altar, based on physical evidence dating to a nineteenth-century restoration. Bees constructed cells in approxi- mately 120 clusters in six different aggregations on the reredos (“altarpiece”). Palynological analyses of cell contents showed that bees visited 48 species of plants, representing 43 genera and 23 families. Contents of bee cells reflect elements of floristic diversity surrounding Panama City that are seen in historical con- temporaneous photographs of the nesting site and environs. Copyright Paola Galgani-Barraza et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 66 Paola Galgani-Barraza et al. / Journal of Hymenoptera Research 74: 65-81 (2019) Resumen Una restauracién reciente de la Catedral Basilica en el Casco Viejo de la ciudad de Panama reveld que las hembras de abejas solitarias (Eufriesea surinamensis) nidificaron en lo alto de su retablo mayor previo a 1871-1876, basada en evidencia fisica de una restauracién del siglo XIX. Las abejas construyeron celdas en aproximadamente 120 grupos de seis agregaciones diferentes en este retablo. Un andlisis de los granos de polen dentro de estos nidos demostré que las abejas visitaron 48 especies de plantas que representan 43 géneros y 23 familias. Los elementos de la diversidad floristica en la ciudad de Panama se pueden observar en fotografias histéricas de esta época del sitio de anidacién y sus alrededores. Keywords Euglossini, pollination, floral utilization, nesting sites, historical reconstruction Introduction The Euglossini is a diverse Neotropical taxon comprised of five genera and nearly 200 species of beautiful, often brilliantly colored and metallic bees (Dressler 1982; Ramirez et al. 2002; Cameron 2004; Roubik and Hanson 2004). Males are well-known for their behavior in collecting chemical fragrances, mainly from orchids and thereby pollinating them (Dressler 1982). Females are more secretive. Their nests generally are dispersed and difficult for us to locate (reviewed by Ramirez et al. 2002; Wcislo et al. 2012). Conse- quently, relatively little is known about females’ behavior, including which plants they visit to collect floral resources for food (pollen and nectar) and nest-building materials (resin and wood fragments), and which plants they pollinate. Orchid bees tend to be denizens of natural forests and adjacent biomes (Dressler 1982; Roubik and Hanson 2004). Some species tolerate disturbances due to human activities (e.g., Lopez-Uribe et al. 2008; Brosi 2009), and one species established itself in Florida USA, well outside its native range (Pemberton and Wheeler 2006). Based on limited information, females tend to gather pollen and nectar from many flowers, and do not specialize on specific host plant taxa (e.g., Cortopassi-Laurino et al. 2009; Villanueva-Gutierrez et al. 2013). For most euglossine species, however, there are no data on pollen preference and utilization. The genus Eufriesea contains about 52 species of large bees (13-27 mm long), many of which are brilliantly metallic in color, while others have striking bands of yellow and black hairs (Michener 2007). They are mainly neotropical-forest-loving creatures, though species extend to southern Argentina and north to Sinaloa and Chi- huahua, México (Kimsey 1982). Eufriesea surinamensis is widely distributed from cen- tral México to southern Brazil, occurring in forested, cultivated and disturbed habitats, up to 1100 m (Kimsey 1982; Roubik and Hanson 2004). Nests consist of exposed, adjacent brood cells (~-13 x 22 mm) constructed of plant resin mixed with numer- ous small pieces of tree bark wood (Bennett 1972; Myers and Loveless 1976; Kimsey 1982). Isolated cells or aggregated clusters are situated on natural sheltered cavities and crevices, such as under overhanging rocky banks or in cliff caves, within rotten hollows in termite nests, under dead bark, or inside bamboo internodes (op. cit.). Females also Pollen use by orchid bees 67 readily use sheltered human-built structures (e.g., under flooring, eaves, and trestles). A female constructs a cell, in which she places a cache of pollen mixed with nectar, lays an egg, and seals the cell. The larva feeds on the pollen and nectar, and later defecates the undigested pollen remains on an interior wall of the cell, coincident with the develop- ment of pupal features within the larval exoskeleton (Rozen 2018). Multiple females may build cells in close proximity to cells built by others, re-use the cells, and defend them from take-over, but they do not cooperate and are aggressive to neighbors (Myers and Loveless 1976). Nesting sites are likely re-used over a number of years by successive generations (Bennett 1972; Myers and Loveless 1976; Young 2012). Floral resources used by E. surinamensis are little known, and we know of no pub- lished palynological studies of brood cell contents. Males are readily attracted by the scent vanillin in forested regions, and visit the orchids Notylia, Pterostemma, Peristeria, and Sievekingia (Orchidaceae) (Roubik and Hanson 2004). Based on specimen label data, Kimsey (1982) reports that females visited Solanum sp. (Solanaceae) and Cassia sp. (Fabaceae) for pollen, and also visited Psidium guajava (Myrtaceae), Petastoma patel- liferum (Bignoniaceae), and Argyeria speciosa (Convolvulaceae) for unknown purposes. Here we provide an analysis of pollen grains recovered from old brood cells of £. surinamensis nesting in an urban setting in late nineteenth-century Panama. ‘The nest- ing sites were within the Basilica Cathedral, which was consecrated in 1796 (Calvo 1999). An extensive restoration was completed in 2018, in preparation for the con- secration of a new altar by Pope Francis. While restoring the reredos (“altarpiece’; Fig. 3A), workers discovered large numbers of bee cell clusters in numerous locations; many cells were covered with gold leaf and other golden material applied during an ear- lier restoration more than a century ago. These golden bee cells reliably date the time of nest cell construction prior to the years 1871—1876, when restoration workers repaired damage from an 1870 fire (Calvo 1999; Lobo and Tribaldos unpublished MS). In the face of changing environments, and recognizing that bees play key roles in most ecosystems as primary pollinators, we looked to the past to analyze histori- cal data on pollen use by orchid bees, FE. surinamensis, living in a human-modified environment. Our study provides a baseline for comparative studies with contempo- rary populations in natural environments. The unusual nesting site—within the first Cathedral on terre firme in the Americas—helps call attention to Francis’ urgent plea in Laudato Si (2015, §42), for the need to increase investment in research to better understand the functions of natural ecosystems and their component species, and how these are being shaped by significant environmental modifications resulting from collective human behavior. Material and methods Bee nests or cell clusters were discovered during restoration work of the Basilica Ca- thedral in Casco Viejo, Panama (8°57'N, 79°32'W) in 2018 by S. Lobo and other restorers working for Dalmatica Conservacao e Restauro. W. Tribaldos then brought 68 Paola Galgani-Barraza et al. / Journal of Hymenoptera Research 74: 65-81 (2019) them to the attention of scientists at the Smithsonian Tropical Research Institute (STRI). These cells were carefully removed using chisels, spatulas and related restora- tion tools, and were sent to STRI. Twenty-seven brood cells were selected for analyses from the recovered cells. Following chemical washes to isolate pollen grains at STRI’s Center for Tropical Paleoecology & Archaeology (CTPA), we carried out standard palynological proce- dures (methods in Roubik and Moreno 1991). Subsequently, permanent microscope preparations were made using glycerin jelly as a mounting medium and paraffin as a sealant. Transects of all preparations were made at 40x magnification using a Nikon Eclipse-Ni binocular scope in order to identify all pollen types. Both biological bright light and differential interference contrast (DIC) microphotographs were obtained at 100x magnification using a Nikon DS-Ril. The magnification of the camera lens of the Nikon scope was 0.7x, yielding a final magnification of 700 times unless indicated otherwise (Plates 1-5). Each photograph displays its own scale (in microns), but pho- tographs in each plate are not to the same scale. Photographs are alphabetically sorted in families, genera and species. Palynology and pollen grain recognition was based on Moore et al. (1991) and Punt et al. (2007). Botanical names were established at the species level if possible, by comparisons with local and regional pollen atlases, STRI collections and botanical inventories (e.g., Croat 1978; Roubik and Moreno 1991; Moreno et al. 2014). The taxonomic status of botanical names was updated using the Tropicos on-line database (Missouri Botanical Garden 2019), following the new an- giosperm phylogeny classification (APG IV 2016), and a new subfamily classification of the Leguminosae (LPWG 2017; Banks and Lewis 2018). External fragments of nests, mainly small pieces of bark, were subjected to chemical analyses to obtain the siliceous fraction containing phytoliths for possible identifica- tion [methods from Piperno (2006) and using a reference collection at STRI’s CTPA]. Voucher specimens of the bee cells and pupae are in the STRI Dry Reference Col- lection, which also houses the remaining unprocessed nest cells. Results The nesting site was surrounded by a mosaic of disturbed forest and open land (Figs 1, 2). Brood cells (N = ~550) of Eufriesea surinamensis were distributed among approximately 120 clusters or aggregations on the six capitals behind and above the al- tar (Fig. 3A), built in the crevices and scrolls of the capitals of the columns (Fig. 3B, C), at heights comparable to upper understory and lower canopy in adjacent natural for- ests. Nests were found in clusters (Fig. 4A, D) or in isolation. (Fig. 4E). Wood frag- ments were used extensively in nest construction (Fig. 4C, E); three different phyto- liths were recovered from these fragments, but they are common to many species of woody plants, including Vismia (Hypericaceae) and could not be identified further (D. Piperno in 4tt. 2019). Nest cells must have been constructed prior to restoration work to repair fire damage (see Introduction). The nineteenth-century restorers left the bee Pollen use by orchid bees 69 Plate |. Eudicots. Acanthaceae: Avicennia germinans (|) Amaranthaceae: aff. Chenopodium sp. (2) Anac- ardiaceae: Spondias sp. aff. S. mombin (3) Apocynaceae: Malouetia guatemalensis (4) Mandevilla sp. aff. M. villosa (5) Prestonia sp. (6) Stemmadenia grandiflora (1) Thevetia ahouai (8) Asteraceae: undetermined (9) Bignoniaceae: Arrabidaea sp. (10) (x100) (Red circle = DIC photo). cells in place and covered them with gold leaf and golden paint (Figs 3C, 4). Pupal re- mains were found in seven cells (Fig. 5A), which allowed us to identify the bee species (Fig. 5B). Taxonomic identification of pollen grains showed that bees used 48 species of plants, representing 43 genera and 23 families (Table 1 and Plates 1-5). 70 Paola Galgani-Barraza et al. / Journal of Hymenoptera Research 74: 65-81 (2019) Plate 2. Bignonaceae: aff. Ceratophytum tetragonolobum (11) Tabebuia sp. (12) Boraginaceae: Cordia sp. aff. C. spinescens (13) Heliotropium procumbens (14) Cannabaceae: Celtis sp. (15) Combretaceae: Conocar- pus erectus (16) Laguncularia racemosa (17) Euphorbiaceae: Alchornea sp. aff. A. latifolia (18) Croton sp. (19) (x100) (Red circle = DIC photo). Pollen use by orchid bees Fl Plate 3. Fabaceae-Caesalpinioideae: Mimosa sp. (20) Fabaceae-Cercidoideae: Bauhinia guianensis (21) Bauhinia reflexa (22) Fabaceae-Papilionoideae: Dioclea reflexa (23) Machaerium sp. (24) Malvaceae-Bomba- coideae: Bombacopsis quinata (25) Pseudobombax septenatum (26) Malvaceae-Grewioideae: aft. Heliocarpus sp. (27) Melastomataceae: Miconia sp. (28) Myrtaceae: Eugenia sp. (29) (x100) (Red circle = DIC photo). 72 Paola Galgani-Barraza et al. / Journal of Hymenoptera Research 74: 65-81 (2019) Plate 4. Rubiaceae: aff. Faramea sp. (30) Genipa americana (31) Macrocnemum glabrescens (32) Psycho- tria sp. (33) Sapindaceae: Cupania sp. (34) Serjania sp.1 (35) Serjania sp.2 (36) Sapotaceae: Pouteria sp. (37) Solanaceae: Solanum sp. (38) (x100) (Red circle = DIC photo). Pollen use by orchid bees V8) Plate 5. Tetrameristaceae: Pelliciera rhizophorae (39) Monocots. Arecaceae: Undetermined sp.1 (40) Undetermined sp.2 (41) Bromeliaceae: Vriesea sp. (42) Costaceae: Costus sp.1 (43) Costus sp.2 (44) Cos- tus sp.3 (45) Costus sp.4 (46) Poaceae: aff. Zea mays (47) Undetermined sp. (48) FERN SPORES. Cy- atheaceae: Cyathea sp. (49) Selaginellaceae: Selaginella sp. (50) UNDETERMINED. Fungal sp.1 (51) Fungal sp.2 (52) Fungal sp.3 (53) (x100) (Blue circle = 60X) (Red circle = DIC photo) 74 Paola Galgani-Barraza et al. / Journal of Hymenoptera Research 74: 65-81 (2019) Table |. List of plants identified from pollen grains recovered of nest cells of Eufriesea surinamensis L. from Casco Viejo, Panama, and sujective estimates of their relative occurrence. Family Genus/Species Relative occurrence Eudicots Acanthaceae Avicennia germinans Common Amaranthaceae aff. Chenopodium sp. Rare Anacardiaceae Spondias sp. aff. S. mombin Rare Apocynaceae Malouetia guatematensis Scarce Apocynaceae Manadevilla sp. aff. M. villosa Scarce Apocynaceae Prestonia sp. Common Apocynaceae Stemmadenia grandiflora Rare Apocynaceae Thevetia ahouai Rare Asteraceae Undetermined Rare Bignoniaceae Arrabidaea sp. Common Bignoniaceae aff. Ceratophytum tetragonolobum Common Bignoniaceae Tabebuia sp. Common Boraginaceae Cordia sp. aff. C. spinescens Scarce Boraginaceae Heliotropium procumbens Common Cannabaceae Celtis sp. Abundant Combretaceae Conocarpus erectus Abundant Combretaceae Laguncularia racemosa Scarce Euphorbiaceae Alchornea sp. aff. A. latifolia Rare Euphorbiaceae Croton sp. Rare Fabaceae-Caesal pinioideae Mimosa sp. Rare Fabaceae-Cercidoideae Bauhinia guianensis Common Fabaceae-Cercidoideae Bauhinia reflexa Common Fabaceae-Papilionoideae Dioclea reflexa Rare Fabaceae-Papilionoideae Machaerium sp. Rare Malvaceae-Bombacoideae Bombacopsis quinata Rare Malvaceae-Bombacoideae Pseudobombax septenatum Rare Malvaceae-Grewioideae aff. Heliocarpus sp. Rare Melastomataceae Miconia sp. Frequent Myrtaceae Eugenia sp. Frequent Rubiaceae Faramea sp. Common Rubiaceae Genipa americana Scarce Rubiaceae Macrocnemum glabrescens Scarce Rubiaceae Psychotria sp. Rare Sapindaceae Cupania sp. Scarce Sapindaceae Serjania sp.1 Common Sapindaceae Serjania sp. 2 Common Sapotaceae Pouteria sp. Rare Solanaceae Solanum sp. Rare Tetrameristaceae Pelliciera rhizophorae Scarce Monocots Arecaceae Undetermined sp. 1 Rare Arecaceae Undetermined sp. 2 Rare Bromeliaceae aff. Vriesea sp. Rare Costaceae Costus sp. 1 Common Costaceae Costus sp. 2 Common Costaceae Costus sp. 3 Common Costaceae Costus sp. 4 Common Poaceae aff. Zea mays Rare Poaceae Undetermined Rare Others Cyatheaceae Polypodium sp. Contaminant Selaginellaceae Selaginella sp. Contaminant Fungal? Undetermined 1 Fungal? Undetermined 2 Fungal? Undetermined 3 Pollen use by orchid bees 75 Discussion Eufriesea surinamensis females nesting in a Cathedral in an urban area in nineteenth- century Panama were catholic in their flower preferences, visiting a diverse array of flowering trees, shrubs and grasses to collect food and nest-building materials, consistent with the known behavior of other orchid bees. They visited more than twice the number of plant species used by related FEuglossa in a present-day urban area of Brazil (Pinto et al. 2019), comparable to the 45 plant species used by two species of Euglossa in Yucatan, México (Villanueva-Gutierrez et al. 2013). The species composition of the collected pollen reflects a mixed-age Neotropical secondary forest, with a mosaic landscape of forest and open areas, as seen in Muybridge’s landscape photographs (Figs 1, 2). The bees visited understory species such as Costus (Costaceae) that do well in full sunlight, such as gaps or along forested roads or openings, as well as canopy trees like Pseudobombax (Malvaceae-Bombacoideae) (“barrigén”) that typically are found in more mature forests (Croat 1978). Orchid bees are long-tongued bees (Michener 2007), a trait that facilitates the col- lection of nectar from flowers that have deep and fused corollas (Endress 1994), provid- ing them with a rich nectar source (e.g., Apocynaceae of Table 1). Additionally, other flowers are structured such that the bee must grab the flower while buzzing to vibrate free the pollen (Buchmann 2015), which provide a rich protein source. Other important nectar flowers were likely Avicennia germinans (Acanthaceae), Heliotropium procumbens Figure |. Environs of the Eufriesea surinamensis nesting site in Casco Viejo, Panama in 1875, as seen from the summit of Cerro Ancén. A white tower of the Cathedral where bees were nesting is visible in the distant background in the center of the peninsula. Photo by Eadweard Muybridge, courtesy of the Smithsonian American Art Museum; gift of Mitchell and Nancy Steir. 76 Paola Galgani-Barraza et al. / Journal of Hymenoptera Research 74: 65-81 (2019) Figure 2. Panama City’s waterfront and surrounding area as seen from the shoreline of Casco Viejo, Panama in 1875. The large building in the left foreground is La Casa de la Marina, near El Palacio de las Garzas (Presidential Palace). The bees were nesting approximately 160 m in-land. The peak of Cerro Ancén is approximately 1.6 km distant. Photo by Eadweard Muybridge, courtesy of the Smithsonian American Art Museum; gift of Mitchell and Nancy Steir. i | = F { 24 bs 4 N iii Figure 3. Locations of nest cell aggregations of Eufriesea surinamensis within the Cathedral in Casco Viejo, Panama A restored reredos showing the capitals above the columns where the historical bee cells were found (black arrows) B a scroll removed during the contemporary restoration, showing bee cells within its crevices and golden material applied during the nineteenth-century restoration C close-up of scrolls on a capital showing painted bee cells from the prior restoration. Pollen use by orchid bees i) Figure 4. Eufriesea surinamensis cells painted during the nineteenth-century restoration A close-up of a cell cluster recovered from a capital B isolated cell entrance that was painted over C isolated cell entrance showing the abundance of bark fragments as a main resource for nest construction D cell cluster covered in golden paint E exterior view of an isolated cell, covered with golden leaf; the cell entrance faces right. (Boraginaceae), Bauhinia spp. (Fabaceae- Cercidoideae), Eugenia sp. (Myrtaceae), Fara- mea sp. (Rubiaceae) and Serjania spp. (Sapindaceae). Plants that were likely important protein sources include Costus (Costaceae), Celtis sp. (Cannabaceae), Conocarpus erectus (Combretaceae), Miconia sp. (Melastomataceae), and species of Bignoniaceae (Table 1). 78 Paola Galgani-Barraza et al. / Journal of Hymenoptera Research 74: 65-81 (2019) A Figure 5. Eufriesea surinamensis reared from cells A head, lateral, dorsal and ventral views of recovered bees B habitus drawing and head of exemplar (STRI-Portal; https://www.stricollections.org/portal/taxa/ index.php?taxon=48960). Together, these species comprise about half of the total taxa reported. Some of the spe- cies, though rare in this sample, likely contributed to the diet of E. surinamensis, while other species may be present from visits to plants collecting resin or nesting materials, or be contaminants (e.g., the two fern spores and fungal species reported). The pollen list also contains elements of a coastal forest with mangroves, including one species (Pel- liciera rhizophorae, Tetrameristaceae) that today is extremely rare in central Panama (Cas- tillo-Cardenas et al. 2016). The precise foraging range of these bees is unknown, but E. surinamensis females in Costa Rica's Osa Peninsula were capable of navigating home from distances as far as 23 km (Janzen 1971). Thus, the foraging range of the Cathedral bees likely extended far beyond Cerro Ancén (Fig. 2), approximately to present-day towns of Tocumen, La Chorrera, and Gamboa, depending on outbound flight direction. Today in central Panama, including the Panama City metropolitan region, these bees are confined to remote forested areas of the central isthmus (Roubik and Ackerman 1987), and there have been no detailed studies of female nesting biology. Accordingly, we now need to collect comparative data on the biology and distribution of contempo- rary populations of E. surinamensis in central Panama and elsewhere in the Neotropics, to better understand how these bees are responding to changing environments. Conclusions Palynological studies of the contents of orchid bee brood cells indicate that late-nine- teenth century Panama City was surrounded by a patchwork of tropical forests suf- ficient to sustain nesting populations of what today is a forest-dwelling species of bee. Pollen use by orchid bees 72) Acknowledgements We are grateful to the entire group of collaborators from Dalmatica Conservacao e Res- tauro-represented here by Sofia Lobo-for their interest in understanding which biologi- cal agents cause damage to our cultural heritage. ‘The staff of the Comité Arquidiocesano Amigos Iglesias Casco Antiguo and the Consorcio la Antigua helped in providing ac- cess to the samples and to the site. Current and former STRI colleagues contributed as follows: Jorge Ceballos helped with microscopy; Marleny Rivera and Jorge Aleman took photos of the bees and the nest cells, respectively; Carlos Jaramillo, Rick Condit, Stanley Heckadon, Joe Wright, and Jeff Hall provided helpful botanical or historical information; Dolores Piperno and Irene Holst analyzed phytoliths and provided related information; Lina Gonzalez helped with graphics; and Annette Aiello first recognized the recovered materials as hymenopteran nest cells, and brought them to the attention of WTW. We are especially grateful to our Smithsonian colleagues, John Jacob and Richard Sorensen of the Smithsonian American Art Museum, who promptly provided high- resolution copies of the original Muybridge photographs in their collection, and related information. Margarita Lopez-Uribe, Santiago Ramirez, and Jack Neff provided many helpful and thoughtful comments, and corrections, which improved the manuscript. References Angiosperm Phylogeny Group IV (2016) An update of the angiosperm phylogeny group clas- sification for orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181: 1-20. https://doi.org/10.1111/boj.12385 Banks H, Lewis G (2018) Phylogenetically informative pollen structures of “caesalpiniod” pol- len (Caesalpinioideae, Cercidoideae, Detarioideae, Dialioideae and Duparquetioideae: Fa- baceae). Botanical Journal of the Linnean Society 187: 59-86. https://doi.org/10.1093/ botlinnean/boy005 Bennett FD (1972) Observations on Exaerete spp. and their hosts Eulaema terminata and Eu- plusia surinamensis (Hymen., Apidae, Euglossine) in Trinidad. Journal of the New York Entomological Society 80: 118-124. Brosi B (2009) ‘The effects of forest fragmentation on euglossine bee communities (Hy- menoptera: Apidae: Euglossini). Biological Conservation 142: 414-423. https://doi. org/10.1016/j.biocon.2008.11.003 Buchmann SL (2015) The Reasons for Flowers: Their History, Culture, Biology, and How They Change our Lives. Scribner, New York, 352 pp. Cameron SA (2004) Phylogeny and biology of neotropical orchid bees (Euglossini). Annual Review of Entomology 49: 377-404. https://doi.org/10.1146/annurev. ento.49.072103.115855 Calvo AC (1999) La Ciudad Imaginada: El Casco Viejo de Panama. Ministerio de la Presiden- cia, Panama, 300 pp. Castillo-Cardenas F, Sanjur O, Toro-Perea N (2016) Differences in sculpture and size of pollen grains: new morphological evidence of diversification in Pelliciera rhizophorae, an ancient 80 Paola Galgani-Barraza et al. / Journal of Hymenoptera Research 74: 65-81 (2019) Neotropical mangrove species. Palynology 40: 302-307. https://doi.org/10.1080/019161 22.2015.1045050 Cortopassi-Laurino M, Zillikens A, Steiner J (2009) Pollen sources of the orchid bee Euglossa an- nectans Dressler 1982 (Hymenoptera: Apidae, Euglossini) analyzed from larval provisions. Genetics and Molecular Research 8: 546-556. https://doi.org/10.4238/vol8-2kerr013 Croat T (1978) Flora of Barro Colorado Island. Stanford University Press (Palo Alto), Stan- ford, 956 pp. Dressler RL (1982) Biology of the orchid bees (Euglossini). Annual Review of Ecology & Sys- tematics 13: 373-394. https://doi.org/10.114G6/annurev.es.13.110182.002105 Endress PK (1994) Diversity and Evolutionary Biology of Tropical Flowers. Cambridge Uni- versity Press, Cambridge, 420 pp. Francis P (2015) Laudato Si. The Vatican Press, Rome, 183 pp. Janzen DH (1971) Euglossine bees as long-distance pollinators of tropical plants. Science 171: 203-205. https://doi.org/10.1126/science.171.3967.203 Kimsey LS (1982) Systematics of bees of the genus Eufriesea, University of California Publica- tions in Entomology 95: 1-125. Legume Phylogeny Working Group (2017) A new subfamily classification of the Legumi- nosae based on a taxonomically comprehensive phylogeny. Taxon 66: 44—77. https://doi. org/10.12705/661.3 Lépez-Uribe MM, Oi CA, del Lama MA (2008) Nectar-foraging behavior of euglossine bees (Hymenoptera: Apidae) in urban areas. Apidologie 39: 410-418. https://doi.org/10.1051/ apido:2008023 Michener CD (2007) The Bees of the World (2° ed.). The Johns Hopkins University Press, Baltimore, 953 pp. Missouri Botanical Garden (2019) Tropicos online database. http://www.tropicos.org Moore PD, Webb JA, Collinson ME (1991) Pollen Analysis (24 ed.). Blackwell Scientific Pub- lications, Oxford, 216 pp. Moreno JE, Vergara D, Jaramillo C (2014) Las colecciones palinoldégicas del Instituto Smithso- nian de Investigaciones Tropicales (STRI), Panama. Boletin de la Asociacién Latinoameri- cana de Paleobotanica y Palinologia (ALPP) 14: 207-222. Myers J, Loveless MD (1976) Nesting aggregations of the euglossine bee Euplusia surinamensis (Hymenoptera: Apidae): individual interactions and the advantage of living together. The Canadian Entomologist 108: 1-6. https://doi.org/10.4039/Ent1081-1 Pemberton RW, Wheeler GS (2006) Orchid bees don’t need orchids: evidence from the naturali- zation of an orchid bee in Florida. Ecology 87: 1995-2001. https://doi.org/10.1890/0012- 9658(2006)87[1995:OBDNOE]2.0.CO;2 Pinto RS, Silva AG, Régo MMC, Albuquerque PMC (2019) Pollen analysis of the post-emer- gence residue of Euglossa bees (Apidae: Euglossini) nesting in an urban fragment. Sociobi- ology 66: 88-96. https://doi.org/10.13102/sociobiology.v66i1.3434 Piperno DR (2006) Phytoliths. Altamira Press, Oxford, 238 pp. Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A (2007) Glossary of pollen and spore terminology. Review of Paleobotany and Palynology 143: 1-81. https://doi.org/10.1016/j. revpalbo.2006.06.008 Pollen use by orchid bees 81 Ramirez S, Dressler RL, Ospina M (2002) Abejas euglosinas (Hymenoptera: Apidae) de la Regién Neotropical: Listado de especies con notas sobre su biologia,” Biota Colombiana 3: 7-118. Roubik DW, Ackerman JD (1987) Long-term ecology of euglossine orchid-bees (Apidae: Eu- glossini) in Panama. Oecologia 73: 321-333. https://doi.org/10.1007/BF00385247 Roubik DW, Hanson PA (2004) Abejas de Orquideas de la America Tropical / Orchid Bees of Tropical America. Inbio, Costa Rica, 370 pp. Roubik DW, Moreno JE (1991) Pollen and spores of Barro Colorado Island. Missouri Botani- cal Garden, Monographs in Systematic Botany 36: 1-268. Rozen Jr JG (2018) On egg eclosion and larval development in euglossine bees. American Mu- seum Novitates 3910: 1-15. https://doi.org/10.1206/3910.1 Villanueva-Gutierrez R, Quezada-Euan J, Eltz T (2013) Pollen diets of two sibling orchid bee species, Euglossa, in Yucatan, southern Mexico. Apidologie 44: 440-446. https://doi. org/10.1007/s13592-013-0194-9 Wceislo DO, Vargas G, Ihle KE, Wcislo WT (2012) Nest construction behavior by the or- chid bee Euglossa hyacinthina. Journal of Hymenoptera Research 29: 15-20. https://doi. org/10.3897/jhr.29.4067 Young AM (2012) Notes on emergence of orchid bees, Eufriesea surinamensis (L.) Apidae: Euglossinae) in Costa Rican nest cell aggregations. Journal of the Kansas Entomological Society 85: 378-379. https://doi.org/10.2317/0022-8567-85.4.378