A revision of the simplex species group of the cleptoparasitic bee genus Triepeolus Robertson, 1901 (Hymenoptera: Apidae)
Abstract
Species of the cleptoparasitic bee genus Triepeolus Robertson, 1901 (Hymenoptera: Apidae: Nomadinae) of which the female has a trapezoidal or triangular pseudopygidial area with bright, reflective setae and a concave apical margin are revised. This entirely New World group includes the widely known species T. simplex Robertson, 1903 and is thus termed the simplex species group. A total of 18 species in the T. simplex group are recognized as valid, of which seven are newly named and described—T. apache sp. nov., T. eumeniformis sp. nov., T. hirsutus sp. nov., T. oblongimacula sp. nov., T. parahirsutus sp. nov., T. paucipunctatus sp. nov., and T. shoshone sp. nov., all from North America. Eleven redundant names are newly synonymized under three valid ones as follows: Epeolus rugulosus Cockerell, 1917 syn. nov., E. metatarsalis Friese, 1921 syn. nov., and T. bilunatus Cockerell, 1949 syn. nov. under Triepeolus mexicanus (Cresson, 1878); E. lectiformis Cockerell, 1925 syn. nov., T. lusor Cockerell, 1925 syn. nov., and T. junctus Mitchell, 1962 syn. nov. under T. rhododontus Cockerell, 1921; and E. permixtus Cockerell, 1923 syn. nov., T. brunnescens Cockerell & Sandhouse, 1924 syn. nov., T. pacis Cockerell, 1925 syn. nov., E. sarothrinus Cockerell, 1929 syn. nov., and E. sarothrinus var. confluens Cockerell, 1929 syn. nov. under T. segregatus (Cockerell, 1900). Species limits were established using an integrative systematics approach, namely considering morphological and biogeographic evidence as well as DNA barcode data. Taxon concepts are revised for all species in the T. simplex group, with morphological diagnoses and keys presented to enable their identification. Known information on the ranges and ecology of the treated species is summarized.
References
Ascher J.S. & Pickering J. 2023. Discover Life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). Available from https://www.discoverlife.org/mp/20q?guide=Apoidea_species [accessed 25 Oct. 2023].
Bivand R., Pebesma E. & Gomez-Rubio V. 2013. Applied Spatial Data Analysis with R, Second Ed. Springer, NY.
Brèthes J. 1909. Hymenoptera paraguayensis. Anales del Museo Nacional de Buenos Aires 12: 225–256.
Brumley R.L. 1965. A Revision of the Bee Genus Epeolus Latreille of Western America North of Mexico. MSc thesis, Utah State University, Logan, UT.
Cockerell T.D.A. 1900. Notes on New Mexico bees. The Canadian Entomologist 32: 361–364. https://doi.org/10.4039/Ent32361-12
Cockerell T.D.A. 1904. II.—Some parasitic bees. Annals and Magazine of Natural History 13: 33–42. https://doi.org/10.1080/00222930409487052
Cockerell T.D.A. 1907. XII.—Descriptions and records of bees.—XV. Annals and Magazine of Natural History 20: 59–68. https://doi.org/10.1080/00222930709487301
Cockerell T.D.A. 1917. XXXIII.—Descriptions and records of bees.—LXXVII. Annals and Magazine of Natural History 20: 298–304. https://doi.org/10.1080/00222931709487008
Cockerell T.D.A. 1921. The epeoline bees of the American Museum Rocky Mountain expeditions. American Museum Novitates 23: 1–16. Available from http://hdl.handle.net/2246/3249 [accessed 25 Oct. 2023].
Cockerell T.D.A. 1923. VII: Expedition of the California Academy of Sciences to the Gulf of California in 1921: the bees (I). Proceedings of the California Academy of Sciences, Fourth Series 12: 73–103. Available from https://www.biodiversitylibrary.org/page/15974955 [accessed 25 Oct. 2023].
Cockerell T.D.A. 1925a. LXXIV.—Descriptions and records of bees.—CVII. Annals and Magazine of Natural History 16: 621–629. https://doi.org/10.1080/00222932508633354
Cockerell T.D.A. 1925b. XI: bees in the collection of California Academy of Sciences. Proceedings of the California Academy of Sciences, Fourth Series 14: 185–215. Available from https://www.biodiversitylibrary.org/page/3159828 [accessed 25 Oct. 2023].
Cockerell T.D.A. 1929. Some Californian parasitic bees. The Pan-Pacific Entomologist 5: 101–105. Available from https://www.biodiversitylibrary.org/page/53413846 [accessed 25 Oct. 2023].
Cockerell T.D.A. 1949. Bees from Central America, principally Honduras. Proceedings of the United States National Museum 98: 429–490. Available from https://www.biodiversitylibrary.org/page/15695293 [accessed 25 Oct. 2023].
Cockerell T.D.A. & Sandhouse G. 1924. Parasitic bees (Epeolinae and Melectinae) in the collection of the California Academy of Sciences. Proceedings of the California Academy of Sciences, Fourth Series 13: 305–324. Available from https://www.biodiversitylibrary.org/page/3137831 [accessed 25 Oct. 2023].
Creedy T.J., Norman H., Tang C.Q., Chin K.Q., Andujar C., Arribas P., O’Connor R.S., Carvell C., Notton D.G. & Vogler A.P. 2020. A validated workflow for rapid taxonomic assignment and monitoring of a national fauna of bees (Apiformes) using high throughput DNA barcoding. Molecular Ecology Resources 20: 40–53. https://doi.org/10.1111/1755-0998.13056
Cresson E.T. 1878. Descriptions of new North American Hymenoptera in the collection of the American Entomological Society. Transactions of the American Entomological Society 7: 61–136. https://doi.org/10.2307/25076368
Cresson E.T. 1916. The Cresson Types of Hymenoptera. Memoirs of the American Entomological Society 1, American Entomological Society, Philadelphia, PA. Available from https://www.biodiversitylibrary.org/page/6513948 [accessed 25 Oct. 2023].
Folmer O., Black M., Hoeh W., Lutz R. & Vrijenhoek R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.
Françoso E., Zuntini A.R., Ricardo P.C., Silva J.P.N., Brito R., Oldroyd B.P. & Arias M.C. 2019. Conserved numts mask a highly divergent mitochondrial-COI gene in a species complex of Australian stingless bees Tetragonula (Hymenoptera: Apidae). Mitochondrial DNA Part A 30: 806–817. https://doi.org/10.1080/24701394.2019.1665036
Friese H. 1921. Nachtrag zur Bienenfauna von Costa Rica. Stettiner Entomologische Zeitung 82: 74–98. Available from https://www.biodiversitylibrary.org/page/8963054 [accessed 25 Oct. 2023].
Friese H. 1925. Neue neotropische Bienenarten, zugleich II. Nachtrag zur Bienenfauna von Costa Rica (Hym.). Stettiner Entomologische Zeitung 86: 1–41.
Genaro J.A. 1999. Revisión del género Triepeolus en Cuba (Hymenoptera: Apidae), con descripción de dos especies nuevas. Caribbean Journal of Science 35: 215–220.
Gibbs J., Ascher J.S., Rightmyer M.G. & Isaacs R. 2017. The bees of Michigan (Hymenoptera: Apoidea: Anthophila), with notes on distribution, taxonomy, pollination, and natural history. Zootaxa 4352: 1–160. https://doi.org/10.11646/zootaxa.4352.1.1
Graenicher S. 1911. Bees of northwestern Wisconsin. Bulletin of the Public Museum of the City of Milwaukee 1: 221–249.
Hajibabaei M., Janzen D.H., Burns J.M., Hallwachs W. & Hebert P.D.N. 2006. DNA barcodes distinguish species of tropical Lepidoptera. Proceedings of the National Academy of Sciences 103: 968–971. https://doi.org/10.1073/pnas.0510466103
Hebert P.D.N., Cywinska A., Ball S.L. & deWaard J.R. 2003a. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London Series B, Biological Sciences 270: 313–321. https://doi.org/10.1098/rspb.2002.2218
Hebert P.D.N., Ratnasingham S. & deWaard J.R. 2003b. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London Series B, Biological Sciences 270: S96–S99. https://doi.org/10.1098/rsbl.2003.0025
Hebert P.D.N., Penton E.H., Burns J.M., Janzen D.H. & Hallwachs W. 2004. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences 101: 14812–14817. https://doi.org/10.1073/pnas.0406166101
Hernández-Triana L.M., Prosser S.W., Rodríguez-Perez M.A., Chaverri L.G., Hebert P.D.N. & Gregory T.R. 2014. Recovery of DNA barcodes from blackfly museum specimens (Diptera: Simuliidae) using primer sets that target a variety of sequence lengths. Molecular Ecology Resources 14: 508–518. https://doi.org/10.1111/1755-0998.12208
Hijmans R.J. 2022. raster: Geographic Data Analysis and Modeling. R package version 3.5-21. Available from https://CRAN.R-project.org/package=raster [accessed 25 Oct. 2023].
Holmberg E.L. 1886. Sobre ápidos nómadas de la República Argentina. Anales de la Sociedad Científica Argentina 22: 272–286.
Ivanova N.V., deWaard J.R. & Hebert P.D.N. 2006. An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes 6: 998–1002. https://doi.org/10.1111/j.1471-8286.2006.01428.x
Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S., Duran C., Thierer T., Ashton B., Meintjes P. & Drummond A. 2012. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111–120. https://doi.org/10.1007/BF01731581
Messing J. 1983. New M13 vectors for cloning. Methods in Enzymology 101: 20–78. https://doi.org/10.1016/0076-6879(83)01005-8
Michener C.D. 1954. Bees of Panamá. Bulletin of the American Museum of Natural History 104: 1–175. Available from http://hdl.handle.net/2246/1183 [accessed 25 Oct. 2023].
Michener C.D. 2007. The Bees of the World, Second Edition. The Johns Hopkins University Press, Baltimore, MD.
Mitchell T.B. 1962. Bees of the eastern United States. Volume II. North Carolina Agricultural Experiment Station Technical Bulletin 152: 1–557.
Moure J.S. 1955. Notas sôbre Epeolini sulamericanos (Hymenopt. – Apoidea). Dusenia 6: 115–138.
Moure J.S., Urban D. & Melo G.A.R. 2007. Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region. Sociedade Brasileira de Entomologia, Curitiba, Brazil.
Onuferko T.M. 2017. Cleptoparasitic bees of the genus Epeolus Latreille (Hymenoptera: Apidae) in Canada. Canadian Journal of Arthropod Identification 30: 1–62. https://doi.org/10.3752/cjai.2017.30
Onuferko T.M. 2018. A revision of the cleptoparasitic bee genus Epeolus Latreille for Nearctic species, north of Mexico (Hymenoptera, Apidae). ZooKeys 755: 1–185. https://doi.org/10.3897/zookeys.755.23939
Onuferko T.M. 2019. A review of the cleptoparasitic bee genus Epeolus Latreille, 1802 (Hymenoptera: Apidae) in the Caribbean, Central America and Mexico. European Journal of Taxonomy 563: 1–69. https://doi.org/10.5852/ejt.2019.563
Onuferko T.M. & Sheffield C.S. 2022. A new species of Epeolus Latreille, 1802 (Hymenoptera: Apidae) from western North America. Insecta Mundi 940: 1–12.
Onuferko T.M., Bogusch P., Ferrari R.R. & Packer L. 2019. Phylogeny and biogeography of the cleptoparasitic bee genus Epeolus (Hymenoptera: Apidae) and cophylogenetic analysis with its host bee genus Colletes (Hymenoptera: Colletidae). Molecular Phylogenetics and Evolution 141: 1–14. https://doi.org/10.1016/j.ympev.2019.106603
Onuferko T.M., Rightmyer M.G., Melo G.A.R. & Roig-Alsina A. 2024. A revision of the South American species of the cleptoparasitic bee genus Triepeolus Robertson, 1901 (Hymenoptera: Apidae). European Journal of Taxonomy 931: 1–50. https://doi.org/10.5852/ejt.2024.931.2505
Packer L. & Graham L. 2020. Four new species of Isepeolini (Hymenoptera; Apidae) from northern Chile. BMC Zoology 5: 3. https://doi.org/10.1186/s40850-020-00052-8
Pebesma E. 2018. Simple features for R: standardized support for spatial vector data. The R Journal 10: 439–446. https://doi.org/10.32614/RJ-2018-009
Pebesma E. & Bivand R. 2005. Classes and methods for spatial data in R. R News 5: 9–13.
Pebesma E. & Bivand R. 2023. Spatial Data Science: with Applications in R. Chapman and Hall/CRC, NY. https://doi.org/10.1201/9780429459016
Prentice M.A. 1998. The Comparative Morphology and Phylogeny of Apoid Wasps (Hymenoptera: Apoidea). PhD thesis, University of California, Berkeley, CA.
Ratnasingham S. & Hebert P.D.N. 2007. BOLD: the Barcode of Life Data System (www.barcodinglife.org). Molecular Ecology Notes 7: 355–364. https://doi.org/10.1111/j.1471-8286.2007.01678.x
Ratnasingham S. & Hebert P.D.N. 2013. A DNA-based registry for all animal species: the Barcode Index Number (BIN) system. PloS ONE 8: e66213. https://doi.org/10.1371/journal.pone.0066213
Rightmyer M.G. 2004. Phylogeny and classification of the parasitic bee tribe Epeolini (Hymenoptera: Apidae, Nomadinae). Scientific Papers, Natural History Museum, The University of Kansas 33: 1–51.
Rightmyer M.G. 2006. A Phylogenetic Analysis of the Bee Tribe Epeolini, With a Review of the Genus Triepeolus. PhD thesis, University of Kansas, Lawrence, KS.
Rightmyer M.G. 2008. A review of the cleptoparasitic bee genus Triepeolus (Hymenoptera: Apidae).—Part I. Zootaxa 1710: 1–170. https://doi.org/10.11646/zootaxa.1710.1.1
Robertson C. 1903. Synopsis of Epeolinae. The Canadian Entomologist 35: 284–288. https://doi.org/10.4039/Ent35284-10
Robertson C. 1929. Flowers and Insects. Lists of Visitors of Four Hundred and Fifty-three Flowers. The Science Press Printing Company, Lancaster, PA. https://doi.org/10.5962/bhl.title.11538
Roig-Alsina A. 1989. A revision of the bee genus Doeringiella (Hymenoptera, Anthophoridae, Nomadinae). The University of Kansas Science Bulletin 53: 576–621. Available from https://www.biodiversitylibrary.org/page/2973094 [accessed 25 Oct. 2023].
Romankova T. 2004. Ontario bees of tribe Epeolini: Epeolus Latreille and Triepeolus Robertson (Hymenoptera: Apidae, Nomadinae). Journal of the Entomological Society of Ontario 135: 87–99.
Rozen J.G. Jr 1966. The larvae of the Anthophoridae (Hymenoptera, Apoidea). Part 2. The Nomadinae. American Museum Novitates 2244: 1–38. Available from http://hdl.handle.net/2246/3273 [accessed 25 Oct. 2023].
Rozen J.G. Jr 1989. Two new species and the redescription of another species of the cleptoparasitic bee genus Triepeolus with notes on their immature stages (Anthophoridae: Nomadinae). American Museum Novitates 2956: 1–18. Available from https://www.biodiversitylibrary.org/page/62309460 [accessed 25 Oct. 2023].
Rozen J.G. Jr. 2001. A taxonomic key to mature larvae of cleptoparasitic bees (Hymenoptera: Apoidea). American Museum Novitates 3309: 1–27. https://doi.org/10.1206/0003-0082(2001)309<0001:ATKTML>2.0.CO;2
RStudio Team. 2022. RStudio: Integrated Development Environment for R. RStudio, PBC, Boston, MA. Available from https://posit.co/ [accessed 25 Oct. 2023].
Santos D., Ribeiro G.C., Cabral A.D. & Sperança M.A. 2018. A non-destructive enzymatic method to extract DNA from arthropod specimens: Implications for morphological and molecular studies. PLoS ONE 13: e0192200. https://doi.org/10.1371/journal.pone.0192200
Scarpulla E.J. 2018. Four submarginal cells on a forewing of Melitoma taurea (Say) (Hymenoptera: Apidae), and a summary of known records of atypical and variable numbers of submarginal cells. Insecta Mundi 667: 1–28.
Schrottky C. 1913. La distribución geográfica de los himenópteros argentinos. Anales de la Sociedad Científica Argentina 75: 180–286.
Smith M.A. & Fisher B.L. 2009. Invasions, DNA barcodes, and rapid biodiversity assessment using ants of Mauritius. Frontiers in Zoology 6: 31. https://doi.org/10.1186/1742-9994-6-31
Teucher A. & Russell K. 2023. rmapshaper: client for ‘mapshaper’ for ‘Geospatial’ Operations. R package version 0.5.0. Available from https://cran.r-project.org/package=rmapshaper [accessed 25 Oct. 2023].
Veit M.F., Ascher J.S., Milam J., Morrison F.R. & Goldstein P.Z. 2021. A checklist of the bees of Massachusetts (Hymenoptera: Apoidea: Anthophila). Journal of the Kansas Entomological Society 94: 81–157. https://doi.org/10.2317/0022-8567-94.2.81
Vergara C.H. & Ayala R. 2002. Diversity, phenology and biogeography of the bees (Hymenoptera: Apoidea) of Zapotitlán de las Salinas, Puebla, Mexico. Journal of the Kansas Entomological Society 75: 16–30.
Webb D.W. 1980. Primary insect types in the Illinois Natural History Survey Collection, exclusive of the Collembola and Thysanoptera. Illinois Natural History Survey Bulletin 32: 55–191. Available from https://www.biodiversitylibrary.org/page/14798686 [accessed 25 Oct. 2023].
Copyright (c) 2024 Thomas M. Onuferko, Molly G. Rightmyer
This work is licensed under a Creative Commons Attribution 4.0 International License.
Creative Commons Copyright Notices
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License (CC BY 4.0) that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are NOT ALLOWED TO post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to taxonomic issues.
