Seven new species of Lasioglossum (Dialictus) Robertson, 1902 (Hymenoptera: Halictidae: Halictini) from the Yucatán Peninsula, Mexico
Abstract
Lasioglossum is a large genus of halictid bees with high species diversity in morphologically rather cryptic species groups. With more than 1900 described species, the taxonomy of the genus is complex and largely unresolved in many regions. For practical reasons, systematic reviews are restricted in scope either geographically or to particular species groups. In this study we focus on the subgenus Dialictus of the genus Lasioglossum from the Yucatán Peninsula in Mexico. In previous studies we identified members of the genus as important pollinators of cash crops in the region, and genetic analyses suggested the existence of seven molecular taxonomic units (mOTU). Based on additional morphological differences, we here describe these mOTUs as novel species, Lasioglossum (Dialictus) yucatanense Landaverde-González sp. nov., L. (D.) paxtoni Landaverde-González sp. nov., L. (D.) ameshoferi Landaverde-González sp. nov., L. (D.) aureoviride Landaverde-González & Husemann sp. nov., L. (D.) paralepidii Gardner sp. nov., L. (D.) milpa Landaverde-González sp. nov. and L. (D.) nanotegula Landaverde-González & Husemann sp. nov., and provide keys and images to assist in their identification.
References
Ågren L. & Svensson B. 1982. Flagellar sensilla of Sphecodes bees (Hymenoptera, Halictidae). Zoologica Scripta 11: 45–54. https://doi.org/10.1111/j.1463-6409.1982.tb00517.x
Ascher J.S. & Pickering J. 2021. Discover Life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). Available from http://www.discoverlife.org/mp/20q?guide=Apoidea_species [accessed 15 Mar. 2021].
Ayala R., Terry G. & Bullock S.H. 1993. The native bees of México. In: Ramamoorthy T., Bye R., Lot A. & Fa J. (eds) Biological Diversity of México: Origins and Distribution: 177–227. Oxford University Press, New York.
Barber B.R. & Klicka J. 2010. Two pulses of diversification across the Isthmus of Tehuantepec in a montane Mexican bird fauna. Proceedings of the Royal Society B, Biological Sciences 277 (1694): 2675–2681. https://doi.org/10.1098/rspb.2010.0343
Bonatti V., Simões Z.L.P., Franco F.F. & Francoy T.M. 2014. Evidence of at least two evolutionary lineages in Melipona subnitida (Apidae, Meliponini) suggested by mtDNA variability and geometric morphometrics of forewings. Naturwissenschaften 101 (1): 17–24. https://doi.org/10.1007/s00114-013-1123-5
Bookstein F. 1991. Morphometric Tools for Landmark Data. Geometry and Biology. University Press, Cambridge, UK.
Dardón M.J., Landaverde-González P., Yurrita C., Vásquez M. & Ayala R. 2020. Rediscovering the diversity of Guatemalan bumblebees (Hymenoptera: Apoidea: Bombus Latreille 1802). International Journal of Scientific Research in Biological Sciences 7 (2): 1–14. https://doi.org/10.26438/ijsrbs/v7i6.114
DeSalle R., Egan M.G. & Siddall M. 2005. The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philosophical Transactions of the Royal Society of London B, Biological Sciences 360 (1462): 1905–1916. https://doi.org/10.1098/rstb.2005.1722
Duennes M.A., Petranek C., Diez de Bonilla E.P., Mérida-Rivas J., Martinez-López O., Sagot P., Vandame R. & Cameron S.A. 2017. Population genetics and geometric morphometrics of the Bombus ephippiatus species complex with implications for its use as a commercial pollinator. Conservation Genetics 18: 553–572. https://doi.org/10.1007/s10592-016-0903-9
Eickwort G.C. 1969. A comparative morphological study and generic revision of the augochlorine bees (Hymenoptera: Halictidae). University of Kansas Science Bulletin 48: 325–524. https://doi.org/10.5962/bhl.part.11227
Ellis M.D. 1914. New bees of the genus Halictus (Hym.) from United States, Guatemala and Ecuador. Journal of the New York Entomological Society 22 (3): 218–223.
Engel M., Hinojosa-Díaz I. & Yáñez-Ordóñez O. 2007. The Augochlora-like Dialictus from Guatemala and Southern México (Hymenoptera: Halictidae). Acta Zoológica Mexicana 23: 125–134. https://doi.org/10.21829/azm.2007.233596
Engel M.S. 2001. Three new Habralictellus bee species from the Caribbean (Hymenoptera: Halictidae). Solenodon 1: 33–37.
Engel M.S. 2006. The Sphecodes of Cuba (Hymenoptera: Halictidae). Acta Zoologica Cracoviensia 49B: 73–78. https://doi.org/10.3409/000000006783995355
Engel M.S. 2011. A new species of Dialictus from Sombrero Island, Anguilla (Hymenoptera, Halictidae). ZooKeys 86: 61–68. https://doi.org/10.3897/zookeys.86.909
Ferreira V., Aguiar C., CostaI M. & Silva J. 2011. Morphometric analysis of populations of Centris aenea Lepeletier (Hymenoptera: Apidae) from Northeastern Brazil. Neotropical Entomology 40: 97–102. https://doi.org/10.1590/S1519-566X2011000100014
Ferrusquía-Villafranca I. 1993. Geology of México: a synopsis. In: Ramamoorthy T.P., Bye R., Lot A. & Fa J. (eds) Biological Diversity of México: Origins and Distribution: 3–108. Oxford University Press, New York.
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 (7): 806–817. https://doi.org/10.1080/24701394.2019.1665036
Francoy T.M., Rodrigues Prado P.R., Gonçalves L.S., da Fontoura Costa L. & de Jong D. 2006. Morphometric differences in a single wing cell can discriminate Apis mellifera racial types. Apidologie 37: 91–97. https://doi.org/10.1051/apido:2005062
Francoy T.M., Grassi M.L., Imperatriz-Fonseca V.L., de Jesús May-Itzá W. & Quezada-Euán J.J.G. 2011. Geometric morphometrics of the wing as a tool for assigning genetic lineages and geographic origin to Melipona beecheii (Hymenoptera: Meliponini). Apidologie 42: e499. https://doi.org/10.1007/s13592-011-0013-0
Francoy T.M., de Faria Franco F. & Roubik D.W. 2012. Integrated landmark and outline-based morphometric methods efficiently distinguish species of Euglossa (Hymenoptera, Apidae, Euglossini). Apidologie 43: 609–617. https://doi.org/10.1007/s13592-012-0132-2
Francoy T.M., Bonatti V., Viraktamath S. & Rajankar B.R. 2016. Wing morphometrics indicates the existence of two distinct phenotypic clusters within population of Tetragonula iridipennis (Apidae: Meliponini) from India. Insectes Sociaux 63 (1): 109–115. https://doi.org/10.1007/s00040-015-0442-2
Galvani G.L., Settembrini B.P. & Roig-Alsina A.H. 2008. Morphology of antenna sensilla in Doeringiella nobilis (Hymenoptera: Apidae). Journal of the Kansas Entomological Society 81: 142–152. Available from https://www.jstor.org/stable/25086429 [accessed 16 Dec. 2022].
Galvani G., Roig-Alsina A. & Settembrini B. 2012. Distribution and morphometric studies of flagellar sensilla in Emphorini bees (Hymenoptera, Apoidea). Micron 43: 673–687. https://doi.org/10.1016/j.micron.2011.12.003
Galvani G.L., González-Vaquero R., Guerra Navarro C. & Settembrini B. 2016. Antennal sensilla of cleptoparasitic and non-parasitic bees in two subfamilies of Apidae. Apidologie 48: 437–449. https://doi.org/10.1007/s13592-016-0486-y
Gardner J. & Gibbs J. 2020. The “red-tailed” Lasioglossum (Dialictus) (Hymenoptera: Halictidae) of the western Nearctic. European Journal of Taxonomy 725: 1–242. https://doi.org/10.5852/ejt.2020.725.1167
Genaro J.A. & Franz N.M. 2008. The bees of greater Puerto Rico (Hymenoptera: Apoidea: Anthophila). Insecta Mundi 40: 1–24.
Gibbs J. 2009a. Integrative taxonomy identifies new (and old) species in the Lasioglossum (Dialictus) tegulare (Robertson) species group (Hymenoptera, Halictidae). Zootaxa 2032 (1): 1–38. https://doi.org/10.11646/zootaxa.2032.1.1
Gibbs J. 2009b. New species in the Lasioglossum petrellum species group identified through an integrative taxonomic approach. The Canadian Entomologist 141: 371–396. https://doi.org/10.4039/n09-020
Gibbs J. 2010. Revision of the metallic species of Lasioglossum (Dialictus) in Canada (Hymenoptera, Halictidae, Halictini). Zootaxa 2591 (1): 1–382. https://doi.org/10.11646/zootaxa.2591.1
Gibbs J. 2011. Revision of the metallic Lasioglossum (Dialictus) of eastern North America (Hymenoptera: Halictidae: Halictini). Zootaxa 3073 (1): 1–216. https://doi.org/10.11646/zootaxa.3073.1.1
Gibbs J. 2016. Bees of the family Halictidae Thomson, 1869 from Dominica, Lesser Antilles (Hymenoptera: Apoidea). European Journal of Taxonomy 180: 1–50. https://doi.org/10.5852/ejt.2016.180
Gibbs J. 2018a. DNA barcoding a nightmare taxon: assessing barcode index numbers and barcode gaps for sweat bees. Genome 61 (1): 21–31. https://doi.org/10.1139/gen-2017-0096
Gibbs J. 2018b. Bees of the genus Lasioglossum (Hymenoptera: Halictidae) from Greater Puerto Rico, West Indies. European Journal of Taxonomy 400: 1–57. https://doi.org/10.5852/ejt.2018.400
Gibbs J., Packer L., Dumesh S. & Danforth B.N. 2013. Revision and reclassification of Lasioglossum (Evylaeus), L. (Hemihalictus) and L. (Sphecodogastra) in eastern North America (Hymenoptera: Apoidea: Halictidae). Zootaxa 3672 (1): 1–117. https://doi.org/10.11646/zootaxa.3672.1.1
González-Vaquero R. & Galvani G.L. 2016. Antennal sensilla analyses as useful tools in the revision of the sweat-bee subgenus Corynura (Callistochlora) Michener (Hymenoptera: Halictidae). Zoologischer Anzeiger 262: 29–42. https://doi.org/10.1016/j.jcz.2016.03.006
Gutiérrez-García T.A. & Vázquez-Domínguez E. 2013. Consensus between genes and stones in the biogeographic and evolutionary history of Central America. Quaternary Research 79: 311–324. https://doi.org/10.1016/j.yqres.2012.12.007
Harris RA. 1979. A glossary of surface sculpturing. Occasional Papers in Entomology 28: 1–31.
Klingenberg C. 2011. MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11: 353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x
Landaverde-González P., Moo-Valle J., Murray T., Paxton R., Quezada-Euán J. & Husemann M. 2017a. Sympatric lineage divergence in cryptic Neotropical sweat bees (Hymenoptera: Halictidae: Lasioglossum). Organisms, Diversity and Evolution 17: 251–265. https://doi.org/10.1007/s13127-016-0307-1
Landaverde-González P., Quezada-Euán J.J.G., Theodorou P., Murray T.E., Husemann M., Ayala R., Moo-Valle H., Vandame R. & Paxton R.J. 2017b. Sweat bees on hot chillies: provision of pollination services by native bees in traditional slash-and-burn agriculture in the Yucatán Peninsula of tropical Mexico. Journal of Applied Ecology 54: 1814–1824. https://doi.org/10.1111/1365-2664.12860
Landaverde-González P., Menes M., Melgar S., Bustamante D. & Monroy C. 2020. Common pattern of distribution for Mesoamerican Triatoma dimidiata suggest geological and ecological association. Acta Tropica 204: e105329. https://doi.org/10.1016/j.actatropica.2020.105329
Maechler M., Rousseeuw P., Struyf A., Hubert M. & Hornik K. 2022. cluster: Cluster Analysis Basics and Extensions. R package version 2.1.3. Available from https://CRAN.R-project.org/package=cluster [accessed 16 Dec. 2022].
McColl R. 2005. Encyclopedia of World Geography. Facts on File, Inc., New York.
Michener C.D. 2007. The Bees of the World. 2nd ed. John Hopkins University Press, Baltimore.
Mittermeier R.A., Robles-Gil P., Hoffmann M., Pilgrim J.D., Brooks T.B., Mittermeier C.G., Lamoreux J.L. & Fonseca G.A.B. 2004. Hotspots Revisited: Earth’s Biologically Richest and Most Endangered Ecoregions. CEMEX, México City, Mexico.
Morrone J.J. 2006. Biogeographic areas and transition zones of Latin America and the Carribbean islands based on panbiogeographic and cladistic analyses of the entomofauna. Annual Review of Entomology 51: 467–494. https://doi.org/10.1146/annurev.ento.50.071803.130447
Moure J.S. & Hurd P.D. 1987. An Annotated Catalog of the Halictid Bees of the Western Hemisphere (Hymenoptera: Halictidae). Smithsonian Institution Press, Washington, D.C.
Mulcahy D.G., Morrill B.H. & Mendelson III J.R. 2006. Historical biogeography of lowland species of toads (Bufo) across the Trans-Mexican Neovolcanic Belt and the Isthmus of Tehuantepec. Journal of Biogeography 33: 1889–1904. https://doi.org/10.1111/j.1365-2699.2006.01546.x
Myers N., Mittermeier A.R., Mittermeier C., da Fonseca F.A. & Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853–858. https://doi.org/10.1038/35002501
Ominami Y., Kamimura T. & Takagi K. 2018. Features and applications of the new TM4000 series of tabletop microscopes. Engineering materials. Hitachi High-Tech GLOBAL. Available from https://www.hitachi-hightech.com/global/sinews/technical_explanation/110301/ [accessed 16 Dec. 2022].
R Core Team. 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from https://www.r-project.org/ [accessed 16 Dec. 2022].
Ratnasingham S. & Hebert P.D.N. 2013. A DNA-based registry for all animal species: the barcode index number (BIN) system. PLoS ONE 8 (7): e66213. https://doi.org/10.1371/journal.pone.0066213
Robertson C. 1902. Some new or little-known bees-II. The Canadian Entomologist 34: 48–49. https://doi.org/10.4039/Ent3448-2
Rohlf F. 2013. tpsDig v.2.17. Department of Ecology and Evolution, State University of New York, Stony Brook, New York.
Smith 1879. Descriptions of New Species of Hymenoptera in the Collection of the British Museum. British Museum, London. https://doi.org/10.5962/bhl.title.60089
Urueña A., Martínez-López V., de Jesús May-Itzá W., Quezada-Euán J.J.G. & De la Rúa P. 2022. Morphometric and genetic analyses show differentiation of the widely distributed stingless bee Nannotrigona perilampoides (Hymenoptera: Meliponini) across geographic regions in Mexico. Journal of Apicultural Research 61 (5): 609–618. https://doi.org/10.1080/00218839.2022.2093576
Wcislo W. 1990. A new species of Lasioglossum from Costa Rica (Hymenoptera: Halictidae). Journal of Kansas Entomological Society 63: 450–543.
Wcislo W. 1995. Sensilla numbers and antennal morphology of parasitic and non-parasitic bees (Hymenoptera: Apoidea). International Journal of Insect Morphology and Embryology 24: 63–81. https://doi.org/10.1016/0020-7322(94)E0006-B
Wiley E.O. & Mayden R.L. 2000. The evolutionary species concept. In: Wheeler Q.D. & Meier R. (eds) Species Concepts and Phylogenetic Theory: A Debate: 70–89. Columbia University Press, New York.
Zerene Systems. 2018. Zerene Stacker. Zerene Systems LLC, Richland, WA.
Copyright (c) 2023 Patricia Landaverde-González, Joel Gardner, Humberto Moo-Valle, José Javier G. Quezada-Euán, Ricardo Ayala, Martin Husemann
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.
