J. HYM.RES. Vol. 17(1), 2008, pp. 110-115

Nest Structure, Seasonality, and Host Plants of aethiops (: , ) in the Andes

(VHG) Department of Ecology and Evolutionary Biology, Haworth Hall, 1200 Sunnyside Avenue, University of Kansas, Lawrence, Kansas 66045-7523, USA; email: [email protected] (MO) Instituto de Investigacidn de Recursos Bioldgicos Alexander von Humboldt, Villa de Leyva, Boyacii, Colombia; email: [email protected]

Abstract.-Thygatw is a Neotropical genus of 30 species of solitary occurring from Mexico to Argentina. Information on the nesting biology is only available for a single species, T. analis, from southern Brazil. We studied the nest architecture, seasonality, and host plants of T. aethiops in two localities in the Eastern Andes of Colombia (- 2700-2900 m). Bees nested singly or forming aggregations in flat ground or sloping surfaces. Nests were deep (39-59 cm) and consisted of an unlined but smooth long main tunnel meandering downward from the surface. Nests had three to seven nearly vertical cells, which were located singly at the ends of short vertical tunnels that descended from the main tunnel. The older brood was located closer to the nest entrance, indicating a progressive nest development. Monthly sampling and appraisal of museum specimens showed that, although females were more commonly collected than males, both sexes were present year- round. We present a list of 32 plant species (27 genera in 18 families), including exotic, native, and cultivated plants used by T. aethiops in Colombia. The most noticeable differences from T. analis are in the pattern of nest development and seasonality. Thygatw aethiops builds nests in a progressive manner and it is likely to be multivoltine, whereas T. analis has a regressive nest development (i.e., older brood located far from the entrance) and a single generation per year. Long-term studies on different populations are required to determine if T, aethiops has continuous brood production or if larval diapause occurs at some point during the year.

The purpose of this paper is to provide common species of the genus. Nests of this information on the nest architecture, sea- species are frequently found in grazing sonality and host plants of Thygater aethiops pastures, city parks, gardens, and along (Smith) at higher elevations in the Colom- sidewalks in towns and densely populated bian Andes. Thygater Holmberg is a Neo- cities such as BogotA (Gonzalez and Engel tropical genus of 30 species of solitary bees 2004, Gonzalez et al. 2005). occurring from Mexico to Argentina (Ur- We studied the nesting biology of T. ban 1967, 1999). The biology of Thygater is aethiops in two localities in the Eastern still poorly known. Information on the Andes of Colombia (- 2700-2900 m), and nesting biology is only available for a compared it with that of T. analis. We single species, T. analis (Lepeletier), from describe the nest and, based on monthly southern Brazil (Michener and Lange 1958, samplings and examination of museum Rozen 1974). Thygater aethiops is widely specimens, we show that both sexes of T. distributed in the Neotropical region, aethiops are present year-round, visiting occurring from Costa Rica to Argentina, flowers of exotic, native, and cultivated and is largely sympatric with T. analis in plants. The nesting biologies of both most of its range (Urban 1967). In Colom- species are very similar, except for the bia, T. aethiops is found between 1400 and pattern of nest development and seasonal- 3500 m of elevation and is the most ity. Thygater aethiops builds nests in a 300 Males 0Females 250 -Rainfall

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Month Fig. 1. Seasonal collections of Thygater aethiops at high altitudes (2700-2900 m) in the Andes of Colombia. Monthly surveys were done in 1999 in La Calera (Departamento of Cundinamarca), except in January, April, May, June and December. To complete the seasonal cycle, we used the number of museum specimens collected in La Calera and contiguous areas during those months. Females were more commonly collected than males (X2.001[221 = 534.1, P < 0.001) every month, and the female/male ratios were not homogeneous among months (X2,O5,111 = 28.9, P < 0.001). The total number of individuals is indicated at the top of each column. progressive manner (i.e., older brood lo- Mondofiedo is a semiarid area highly cated near the entrance, thus first to be disturbed by cattle ranching, gravel extrac- completed), and is likely to be multivoltine, tion, and waste dumping whose soils are whereas T. analis has regressive nest very compacted, shallow, and strongly development and a single generation per eroded (details in Gonzalez and Chiivez year. However, long-term studies on dif- 2004). The soils in La Calera are looser and ferent populations are required to deter- less eroded than in Mondofiedo, and mine if T. aethiops has continuous brood primarily used to grow potato, corn, beans, production or if larval diapause occurs at and wheat (IGAC 1996). Annual rainfall in some point during the year, and to detect La Calera is bimodal (Fig. I), with higher any variation in nest development depend- monthly precipitation than in Mondofiedo. ing on soil conditions. We excavated the nests using a geologcal pick, hand shovel, wood chisels and a MATERIAL AND METHODS pocketknife. Prior to excavation, and in order to trace the nest structure, we used a syringe Study sites and nest excavations to inject into the tunnel a slurry of plaster-of- The nesting biology of T. aethiops was Paris and water, which was allowed to studied by VG during December 2004 harden for about 2-5 minutes; we then in Mondofiedo (2720 m, 4"39'52.9"N, excavated the nests. We measured nest 74"17'2"W), whereas the seasonality and features in the field using a caliper. Maxi- host plants were studied in 1999 by MO in mum nest depth was measured from the nest La Calera (2900 m, 4"43'22"N, 73"5B118"W). entrance to the bottom of the deepest cell. Seasonality Table 1. Measurements (cm) of some structures of eight nests of Thygater aethiops. f: mean value, 2 : We collected bees on flowers and exam- standard error, R : range, N : sample size. Samples ined museum specimens to determine the varied in number because, to increase variation, we seasonal cycle of T. aethiops in La Calera. measured remains of nest structures (e.g., cells, Bees were collected when they appeared to tunnels) that we found during excavations. - - - be more active, frequently between 8:00 Nest structure .f + R N and 11:OO am, and from one to three days - - - Nest density (nests/m2) each month depending on weather condi- Inter-nest distance tions. Once we identified and sexed them, Maximum nest depth bees were released. Thygateu aethiops is the Tumulus only species of the genus occurring in La Length Calera. However, we decided to capture Width Nest entrance them because sometimes it was difficult for Main tunnel us to distinguish T. aethiops females from Length small, black workers of the bumble Diameter Bombus atratus Franklin (Apidae, Bombini). Laterals Males and females of T. aethiops were easy Length Diameter to distinguish in the field because, as in Cell depth other eucerines, males have longer anten- Number of cells per nest nae that surpass the base of the abdomen. Cell dimensions The monthly surveys in La Calera were Length Diameter done during the year of 1999, except in January, April, May, June, and December. To complete the seasonal cycle, we used the number of museum specimens collect- boldt (IAvH), Villa de Leyva, Boyaca, and ed in La Calera and contiguous areas the Museo Entomol6gico Francisco Luis during those months. We used a G-test Gallego, Universidad Nacional de Colom- (Sokal and Rohlf 2000) to compare percent- bia in Medellin (MEFLG). ages of males and females of T. aethiops, RESULTS and to determine if female/male (F/M) ratios were homogeneous among months. Nest architecture

Host plants Nest measurements are given in Table 1. Nests were found singly or forming aggre- We recorded the plants visited by T. gations in flat ground or sloping surfaces. aethiops in La Calera, and also extracted The nest sites were either barren or sparsely floral records from data from specimen covered with grasses in areas frequently labels. We examined about 300 specimens well exposed to the sun (Figs 2, 3). Nest of T. aethiops deposited in the Snow entrances were circular and when nests Entomological Museum, University of were active, irregular tumuli extended Kansas, USA (SEM), National Museum of downward from the nest entrances. Nests Natural History, Washington, D.C. were deep, and consisted of an unlined but (USNM), and the following Colombian smooth long main tunnel meandering institutions: Laboratorio de Investigaciones downward from the surface (Fig. 4). Cells en Abejas, Departamento de Biologia (LA- were nearly vertical and placed singly at the BUN), and the Museo de Historia Natural, ends of short laterals, or vertical tunnels that Instituto de Ciencias Naturales (ICN) in descended from the main tunnel. Once the BogotA, Instituto de Investigaci6n de Re- cells were completed, these vertical tunnels cursos Biol6gicos Alexander von Hum- were filled with loose, coarse soil (Fig. 5). Figs 2-5. Nests of Thygatev aethiops. 2, single nest in flat ground; note the tumulus around nest entrance. 3, cluster of nests in a barren, sloping surface; all nest entrances are encircled and one of them is indicated by an arrow. 4, an excavated nest showing the meandering main tunnel, indicated by a white solid line. 5, detailed view of a cell in saggital section; A, main tunnel; B, short laterals filled with loose soil after cell completion; C, whitish spidenveb- like layer, likely a mass of mold hyphae, found in most of excavated cells (nest measurements in Table 1).

The cells were excavated in the soil and small larvae and pollen. Older brood was were not separable from the substrate. The located closer to the nest entrance, indicat- three to seven cells per nest were con- ing progressive nest development. Numer- structed at different depths. The cells were ous old burrows and remains of cocoons elongated, with a concave spiral closure from older generations were commonly inside, slightly wider at the bottom than found during excavations. top, and lined with a "wax-like" secreted material resembling those of other eucerine Associated organisms bees. In most cells, the upper one third of We found empty puparia of an unknown the inner wall was covered with a thin, fly inside three sealed cells that had a whitish spiderweb-like layer (Fig. 5). We perforation (2.0-2.6 mm in diameter) in the did not examine it under the microscope, cell closure. Each cell had from two to six but it might be a mass of mold hyphae. As puparia, about 3.8 mm long and 1.5 mm described for Thygateu (Rozen 1974, Packer wide, among debris. 1987), larval feces were incorporated with- in the dark brown, paper-like cocoon. The Seasonal cycle basal one third of the cell contained liquid The monthly sampling in La Calera and provisions with the egg floating on the appraisal of museum specimens revealed surface. Cell contents ranged from eggs to that both sexes are present on every month of the year (Fig. 1).Moreover, females were Their nests consist of a long, unlined, main more commonly collected than males tunnel from which short laterals, ending in (X2.001[221 = 534.1, P < 0.001), and the F/ a single vertical elongated cell, branch off; M ratios were not homogeneous among these laterals are filled with soil once cells months (X2.O5 = 28.9, P < 0.001). F/M are completed. The most noticeable differ- ranged from about 2:l in January to 31:l in ence from T. analis is the pattern of nest October (Fig. 1). development. We inferred from the distri- bution of young and old brood in the Host plants excavated nests, that T. aethiops builds Both males and females were recorded nests in a progressive manner (i.e., older from 32 plants species (27 genera in 18 brood located near the entrance, thus, first families), including exotic, native, and to be completed) whereas it is regressive in cultivated plants. Females were recorded T. analis (older brood located far from the from the most plants. Records for males are entrance). However, we examined nests of indicated with an asterisk. AGAPANTHA-T. aethiops from a single population and CEAE:Crinum africanum L'Heritier de Bru- only during the dry season, so we do not telle*. ASTERACEAE:Baccharis sp., Senecio know if the nest development pattern sp., Vernonia canescens Kunth. BALSAMINA- varies among localities, with time of year, CEAE:Impatiens balsamina Linnaeus. BRASSI- or with soil hardness. CACEAE:Brassica napus Linnaeus*, B. nigra The monthly surveys in La Calera and (Linnaeus)", Raphanus raphanistrurn Lin- the appraisal of museum specimens naeus*. CAESALPINACEAE:Cassia tomentosa showed that males and females are present Linnaeus. CONVOLWLACEAE:Convolvulus throughout the year. In La Calera, females sp., Ipomoea congesta R. Br. CUCURBITACEAE:were more frequently collected than males, Cyclanthera pedata Scrad, Sechium edule and the F/M ratios varied significantly Swartz. FABACEAE:Desmodium uncinatum among months (Fig. 1). We did not deter- (Jacquin),Phaseolus vulgaris Linnaeus*, Tri- mine adult longevity but unless adults folium pratense Linnaeus*, T. repens Lin- have an extraordinary long life, the pres- naeus*. LAMIACEAE:Salvia cuatrecasana ence of both sexes indicates that T. aethiops Epling*, S. bogotensis Benth*. MALVACEAE:must be multivoltine. In contrast, due to Hibiscus grandiflorus Juss. Ex Candolle. seasonality in southern Brazil, T. analis MELASTOMATACEAE:Tibouchina sp. PAPA- over-winters as postdefecating larvae and VERACEAE:Papaver somniferum Linnaeus*. emerge as adults during the summer. PASSIFLORACEAE:Passipora mollissima L.H. Thygater analis is the most widespread Bailey. ROSACEAE:Rubus sp*. RUBIACEAE:species of the genus, occurring from Coffea arabica Benth, Palicourea sp. RUTA- tropical to subtropical lowlands to high CEAE:Citrus aurantium Linnaeus. SOLANA-altitudes in the Andes (Urban 1967) and CEAE:Cyphomandra betacea (Cav.) Sendtn, thus could have multiple generations per Solanum tuberosum Poepp ex Walp*, S. year in more tropical environments as does lycioides Linneaus. Solanum sp. TROPAEO-T. aethiops. However, we do not know if T. LACEAE:Tropaeolum majus Linnaeus*. aethiops has continuous brood production or if larval diapause occurs at some point DISCUSSION during the year, as it has been observed in The nest architecture of T. aethiops is very other Andean solitary bees, such as Antho- similar to that described for T. analis, the phora walteri Gonzalez (Apidae, Antho- only species of Thygater whose nests have phorini) (Gonzalez and Chiivez 2004). been studied (Michener and Lange 1958, Thygater aethiops seems to use a wide Rozen 1974). Both species nest solitarily or range of exotic, native, and cultivated in aggregations in flat or sloping ground. plants for pollen and nectar (e.g., Impatiens, Salvia spp, and Solanum tuberosum, respec- LITERATURE CITED tively). Our records agree with the appar- Gonzalez, V. H. and F. Chiivez. 2004. Nesting biology of ent polylectic diet of Thygater, as inferred a new high Andean bee, Anthophora walteri Gonza- by Urban (1967) based on scarce floral lez (Hymenoptera: Apidae: Anthophorini). Journal records. Also, as previously noted for some of the Kansas Entomological Society 77: 584-592. Thygafer species (Urban 1967), females of T. and M. S. Engel. 2004. The Tropical Andean aethiops buzz pollinate flowers with por- bee fauna (Insecta: Hymenoptera: Apoidea), with examples from Colombia. Entomologische Abhan- icidal anthers (e.g., Solanum). It might be dlungen 62: 65-75. interesting to explore the use of T. aethiops , M. Ospina, and D. Bennett. 2005. Abejas as a crop pollinator of tomatoes (Solanum altoandinas dz Colombia: Guia de campo. Institute lycopersicum Linnaeus) or Inca berries de Investigaci6n de Recursos Biol6gicos Alexan- (Physalis peruviana Linnaeus), both Solana- der von Humboldt, Bogoti, D.C., Colombia. 80 pp. ceae species with poricidal anthers that are IGAC. 1996, Diccionario Geogrlifico de Colombia. Insti- tuto Geogrifico Agustin Codazzi, Bogoti, Colom- extensively cultivated in the Andean re- bia, 2504 pp. gion. Undoubtedly, research on adult Michener, C. D. and R. B. Lange. 1958. Observations longevity, brood production, and other on the ethology of Neotropical Anthophorine biological aspects of T. aefhiops are needed. bees (Hymenoptera: Apoidea). The University of Kansas Science Bulletin 39: 69-96. ACKNOWLEDGMENTS Packer, L. 1987. A description of the mature larvae and cocoon of the bee Thygater (Hymenoptera: We are greatly indebted to each of the individuals Anthophoridae). Journal of the Nezu York Entonzo- who allowed us to visit their collections; M. S. logical Society 95: 23-27. Engel, Z. Falin (SEM), D. Furth (USNM), G. Nates Rozen, J. G. 1974. Nesting biology of the Eucerini bee (LABUN),F. Fernandez, G. Amat, E. Florez (ICN),J. E. Thygater analis (Hymenoptera: Anthophoridae). Castillo (IAvH), and A. Smith, J. Quiroz (MEFLG). We Journal of the New York Entomological Society 82: also thank E. Palacio and B. Mantilla for their help in 230-234. the field; P. Sepulveda, B. Alexander, C. Rasmussen, Sokal, R. R. and F. J. Rohlf. 2000. Biometry. The G. Broad, J. Neff, and two anonymous reviewers principles and practice of statist ics in biological provided valuable comments on the manuscript. The research. Third Edition. W. H. Freeman and University of Kansas (KU), Undergraduate Program Company, New York, USA, xix + 887 pp. in Biology, Department of Ecology and Evolutionary Urban, D. 1967. As espbcies do g@nero Thygater Biology, KU General Research Fund and US-Israel Holmberg, 1884. Boletim da Universidade Federal Binational Science Foundation grant 2000-259 (to D. do Paranli (Zoologia) 2: 177-307. Smith and Y. Lubin) provided financial support for . 1999, Esp6cies novas de Thygater Holmberg VG through teaching assistantships and laboratory (Hymenoptera, Apoidea, Anthophoridae). Revista facilities. Brasileira de Zoologia 16: 213-220.