Delimitation of Molecular Operational Taxonomic Units (MOTU) and euglossine bees diversity in two altitudinal gradients of northern Colombia
Article Sidebar
Main Article Content
The tribe Euglossini (orchid bees) is vital for tropical pollination, making their diversity and distribution across altitudinal gradients crucial for ecological studies and conservation. This study assesses Euglossini diversity in northern Colombia’s Sierra Nevada de Santa Marta and Serranía del Perijá, focusing on altitudes from 600 to 2200 meters above sea level (m a.s.l.). Using Barcode Index Numbers (BIN) and the COI gene, 1258 male specimens were collected, with 415 individuals sequenced. We identified 21 Molecular Operational Taxonomic Units (MOTUs), from which BOLD: AEF4646 (Eufriesea) was identified as the most variable, BOLD: AEF4645 (Eufriesea) as the most divergent molecular species, and also species like BOLD: AAC0547 (Euglossa) are widely distributed in both SNSM and SP at 800 and 1000 m a.s.l., while BOLD: AAC3172 (Euglossa) is strongly associated with 800 m a.s.l. communities. Additionally, BOLD: ABY5852 (Euglossa) prefers sites between 1400 m and 1800 m a.s.l. Diversity analyses revealed no significant differences in species richness between the gradients, but richness declined with altitude. Eufriesea and Euglossa species were broadly distributed in the Sierra Nevada, while Euglossa and Eulaema dominated the Serranía del Perijá. Beta diversity analyses showed distinct distribution patterns, with intermediate elevations marking a transition zone. Above 2000 m a.s.l., evolutionary processes likely sustain Euglossini populations, emphasizing the role of these regions in bee diversification.
Abrahamczyk, S., Gottleuber, P., Matauschek, C., & Kessler, M. (2011). Diversity and community composition of euglossine bee assemblages (Hymenoptera: Apidae) in Western Amazonia. Biodiversity And Conservation, 20(13), 2981-3001. https://Doi.Org/10.1007/S10531-011-0105-1
Aguilera Díaz, M. (2016). Serranía Del Perijá: Geografía, Capital Humano, Economía Y Medio Ambiente. Documentos De Trabajo Sobre Economía Regional, 249, 17-99. https://doi.org/10.32468/dtseru.249
Ahmed, S., Ibrahim, M., Nantasenamat, C., Nisar, M. F., Malik, A. A., Waheed, R., Ahmed, M. Z., Ojha, S. C., & Alam, M. K. (2022). Pragmatic applications and universality of DNA barcoding for substantial organisms at species level: A review to explore a way forward. Biomed Research International (2022), 846485,. https://Doi.Org/10.1155/2022/1846485
Andrade Correa, M., Aponte Gutiérrez, A., Ardila Reyes, M., Arellano P., H., Campos, M., Calvo Roa, N., Carreño Vega, E., Carvajal Cogollo, J., Casallas Pabón, D., Cuervo, A., Jaramillo Justinico, A., Lynch, J., Niño Arias, L., Medina Rangel, G., Moreno Á., R., Muñoz Saba, Y., Rangel Churio, J., Rivera Díaz, O., Ruiz, D & Rodríguez Ortiz, E. (2019). Colombia Diversidad Biótica XVIII: Biodiversidad y territorio de la Serranía del Perijá, (Cesar - Colombia). Universidad Nacional de Colombia. Facultad de Ciencias.
Ascher, J. S., & Pickering, J. (2020). Discover Life Bee Species Guide and World Checklist (Hymenoptera: Apoidea: Anthophila). https://www.discoverlife.org/mp/20q?guide=Apoidea_species
Bonilla-Gómez, M. A., & Nates-Parra, G. (1992). Abejas euglosinas de Colombia (Hymenoptera: Apidae). I. Claves ilustradas. Caldasia, 17(1), 149-172. https://revistas.unal.edu.co/index.php/cal/article/view/35750
Burnham, K. P., & Overton, W. S. (1978). Estimation of the size of a closed population when capture probabilities vary among animals. Biometrika, 65(3), 625-633. https://doi.org/10.1093/biomet/65.3.625
Cardoso, P., Rigal, F., & Carvalho, J. C. (2015). BAT – Biodiversity Assessment Tools, an R package for the measurement and estimation of alpha and beta taxon, phylogenetic and functional diversity. Methods in Ecology and Evolution, 6(2), 232-236. https://doi.org/10.1111/2041-210X.12310
Colwell, R. K. (2013). Estimates: Statistical Estimation of Species Richness and Shared Species from Samples. Version 9. User’s Guide and Application. http://purl.oclc.org/estimates
Dec, E., & Alves-Dos-Santos, I. (2019). Species distribution of Euglossini bees (Hymenoptera: Apidae) at an altitudinal gradient in northern Santa Catarina. Sociobiology, 66(4), 568-574. https://Doi.Org/10.13102/Sociobiology.V66i4.3436
DeSalle, R., Egan, M. G., & Siddall, M. (2005). The unholy trinity: Taxonomy, species delimitation and DNA barcoding. Philosophical Transactions of the Royal Society B: Biological Sciences, 360(1462), 1905-1916. https://Doi.Org/10.1098/Rstb.2005.1722
Dressler, R. L. (1982). Biology of the orchid bees (Euglossini). Annual Review of Ecology and Systematics, 13, 373-394. https://Doi.Org/10.1146/Annurev.Es.13.110182.002105
Floren, A., Von Rintelen, T., Hebert, P. D. N., De Araujo, B. C., Schmidt, S., Balke, M., Narakusumo, R. P., Peggie, D., Ubaidillah, R., Von Rintelen, K., & Müller, T. (2020). Integrative ecological and molecular analysis indicate high diversity and strict elevational separation of canopy beetles in tropical mountain forests. Scientific Reports, 10(1), 1-12. https://Doi.Org/10.1038/S41598-020-73519-W
Freitas, B. M., Imperatriz-Fonseca, V. L., Medina, L. M., Kleinert, A. D. M. P., Galetto, L., Nates-Parra, G., & Quezada-Euán, J. (2009). Diversity, threats and conservation of native bees in the Neotropics. Apidologie, 40(3), 332-346). https://Doi.Org/10.1051/Apido/2009012
González, V. H., Bennett, D. J., & Ospina, M. (2005). Abejas Altoandinas De Colombia. Guía De Campo. In Instituto De Investigación De Recursos Biológicos Alexander Von Humboldt.
Hill, M. O. (1973). Diversity and evenness: A unifying notation and its consequences. Ecology, 54(2), 427-432. https://Doi.Org/10.2307/1934352
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(4), 998-1002. https://Doi.Org/10.1111/J.1471-8286.2006.01428.X
Janzen, D., & Hallwachs, W. (2019). How a tropical country can DNA barcode itself. IBOL Barcode Bulletin, 9(1). https://Doi.Org/10.21083/Ibol.V9i1.5526
Josse, C., Cuesta, F., Navarro, G., Barrena, V., Cabrera, E., Chacón-Moreno, E., … & Tovar, A. (2009). Ecosistemas de los Andes del Norte y Centro. Bolivia, Colombia, Ecuador, Perú y Venezuela. Secretaría General de la Comunidad Andina, Programa Regional ECOBONA-Intercooperation, CONDESAN-Proyecto Páramo Andino, Programa BioAndes, EcoCiencia, NatureServe, IAvH, LTA-UNALM, ICAEULA, CDC-UNALM, RUMBOL SRL. Lima, Perú.
Kindt, R. (2024). Biodiversity R: Package for Community Ecology and Suitability Analysis. The Comprehensive R Archive Network. https://cran.r-project.org/web/packages/BiodiversityR/index.html
Kress, W. J., & Erickson, D. L. (2008). DNA barcodes: Genes, genomics, and bioinformatics. Proceedings of the National Academy of Sciences, 105(8), 2761-2762. https://Doi.Org/10.1073/Pnas.0800476105
López-Uribe, M. M., & Del Lama, M. A. (2007). Molecular Identification of Species of The Genus Euglossa Latreille (Hymenoptera: Apidae, Euglossini). Neotropical Entomology, 36(5), 712-720. Https://Doi.Org/10.1590/S1519-566X2007000500012
Magurran, A. E., & Magurran, A. E. (1988). Why diversity? Ecological diversity and its measurement, 1-5. https://doi.org/10.1007/978-94-015-7358-0
Malpica-Topete, A. (2012). Divergencia genética y morfológica entre poblaciones migratorias y sedentarias de Selasphorus Platycercus (Aves: Trochilidae),
[Tesis de maestría, INECOL Instituto de Ecología]. Repositorio INECOL. http://inecol.repositorioinstitucional.mx/jspui/handle/1005/51
Martínez-Puc, J. F., & Merlo-Maydana, F. E. (2014). Importancia de la diversidad de abejas (Hymenoptera: Apoidea) y amenazas que enfrenta en el ecosistema tropical de Yucatán, México. Journal of the Selva Andina Animal Science, 1(2), 28-34. http://www.scielo.org.bo/scielo.php?script=sci_arttext&pid=S2311-25812014000200004&lng=es&tlng=es
McFadden, C. S., Gonzalez, A., Imada, R., Shi, S. S., Hong, P., Ekins, M., & Benayahu, Y. (2019). Molecular operational taxonomic units reveal restricted geographic ranges and regional endemism in the Indo-Pacific octocoral family Xeniidae. Journal of Biogeography, 46(5), 992-1006. https://Doi.Org/10.1111/Jbi.13543
Mohammadi, S., & Ahmadzadeh, F. (2024). Revealing hidden diversity and community dynamics of land snails through DNA barcoding: implications for conservation and ecological studies. Frontiers in Ecology and Evolution, 12. https://doi.org/10.3389/fevo.2024.1329581
Moreno, C. E. (2001.). M&T-Manuales y Tesis SEA, Vol. 1. Primera Edición. Métodos para medir la biodiversidad. http://Entomologia.Rediris.Es/Sea
Murren, C. J. (2002), Effects of habitat fragmentation on pollination: pollinators, pollinia viability and reproductive success. Journal of Ecology, 90, 100-107. https://doi.org/10.1046/j.0022-0477.2001.00638.x
Nates-Parra, G. (2016). Iniciativa Colombiana de Polinizadores: Abejas ICPA. Universidad Nacional de Colombia.
Nates-Parra, G., Alejandro Parra, H., Rodríguez, A., Baquero, P., & Vélez, D. (2006). Abejas silvestres (Hymenoptera: 2013Apoidea) en ecosistemas urbanos: estudio en la ciudad de Bogotá y sus alrededores. Revista Colombiana de Entomología, 32(1), 77-84. https://Doi.Org/10.25100/Socolen.V32i1.9369
Nemésio, A., & Vasconcelos, H. L. (2013). Beta diversity of orchid bees in a tropical biodiversity hotspot. Biodiversity and Conservation, 22(8), 1647-1661. Https://Doi.Org/10.1007/S10531-013-0500-X
Noriega, J. A., & Realpe, E. (2018). Altitudinal turnover of species in a Neotropical peripheral mountain system: A case study with dung beetles (Coleoptera: Aphodiinae and Scarabaeinae). Environmental Entomology, 47(6), 1376-1387.https://doi.org/10.1093/ee/nvy133
Nunes, C. A., Braga, R. F., Figueira, J. E. C., De Siqueira Neves, F., & Fernandes, G. W. (2016). Dung Beetles Along a Tropical Altitudinal Gradient: Environmental Filtering on Taxonomic and Functional Diversity. Plos ONE, 11(6), e0157442. https://Doi.Org/10.1371/Journal.Pone.0157442
Oksanen, J., Simpson, G, Blanchet, F., Kindt, R., Legendre, P., Minchin, P., O'Hara, R., Solymos, P., Stevens, M., Szoecs, E., Wagner, H., Barbour, M., Bedward, M., Bolker, B., Borcard, D., Borman, T., Carvalho, G., Chirico, M., De Caceres, M., Durand, S., Evangelista, H., FitzJohn, R., Friendly, M., Furneaux, B., Hannigan, G., Hill, M., Lahti, L., McGlinn, D., Ouellette, M., Ribeiro Cunha, E., Smith, T., Stier, A., Ter Braak, C., Weedon, J. (2024). vegan: Community Ecology Package. R package version 2.7-0, https://vegandevs.github.io/vegan/.
Oliveira, M. L. de ., & Campos, L. A. de O. (1996). Preferência por estratos florestais e por substâncias odoríferas em abelhas Euglossinae (Hymenoptera, Apidae). Revista Brasileira De Zoologia, 13(4), 1075-1085. https://doi.org/10.1590/S0101-81751996000400025
Otero, J. T., & Sandino, J. C. (2003). Capture rates of male euglossine bees across a human intervention gradient, Chocó region, Colombia. Biotropica, 35(4), 520-529. https://Doi.Org/10.1111/J.1744-7429.2003.Tb00608.X
Parra-H., A., & Nates-Parra, G. (2012). The ecological basis for biogeographic classification: An example in orchid bees (Apidae: Euglossini). Neotropical Entomology, 41(6), 442-449. https://Doi.Org/10.1007/S13744-012-0069-1
Parra-H., A., Otero, J. T., Sandino, J. C., & Ospina T, R. (2016). Abejas de las orquídeas (Hymenoptera: Apidae: Euglossini) y su importancia como polinizadoras de amplio rango en ecosistemas naturales. En G Nates Parra (Ed) Iniciativa Colombiana de Polinizadores. (pp. 141-156). Universidad Nacional de Colombia. https://promotepollinators.org/wp-content/uploads/sites/507/2019/11/abejas-polinizadoras-ebook-40217.pdf
Paz, A., Gonzalez, M., & Crawford, A. J. (2011). Códigos de barras de la vida: Introducción y perspectiva. Acta Biológica Colombiana, 3(16), 161-176. https://revistas.unal.edu.co/index.php/actabiol/article/view/19782/28016
Pearson, D. L., & Dressler, R. L. (1985). Two-Year Study of Male Orchid Bee (Hymenoptera: Apidae: Euglossini) Attraction to Chemical Baits in Lowland South- Eastern Perú. Journal of Tropical Ecology, 1(1), 37-54 https://Doi.Org/10.1017/S0266467400000067
Pérez-Buitrago N.; Mojica-Candela L. J.; Agudelo-Martínez, J. C. (2022). Variación estacional de abejas euglosinas (Apidae: Euglossini) en el norte de la Orinoquia colombiana. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, 46(179), 470-481, https://doi.org/10.18257/raccefyn.1636
Prieto, C. & Rodriguez, G. (2007). A new species of Penaincisalia (Lepidoptera: Lycaenidae: Eumaeini) from the high Andes of Colombia. Zootaxa, 1660(1), 61-68. https://doi.org/10.11646/zootaxa.1660.1.5
Prieto, C., Bálint, Zs., Boyer, P. & Micó, E. (2008). A review of the "browni group" of Penaincisalia with notes on their distribution and variability (Lepidoptera: Lycaenidae: Eumaeini). Zootaxa, 1941(1), 1-24. https://doi.org/10.11646/zootaxa.1941.1.1
Prieto C. & Vargas, M. A. (2016). Elfin butterflies of the genus Rhamma Johnson (Lepidoptera: Lycaenidae: Theclinae): A review of the Colombian species. Zootaxa, 4093(3), 323-342. https://doi.org/10.11646/zootaxa.4093.3.2
Prieto, C., Grishin, N., Hausmann, A. & Lorenc-Brudecka, J. (2016). The Penaincisalia amatista species-group (Lepidoptera: Lycaenidae, Eumaeini) in Colombia, insights from mt DNA barcodes and the description of a new species. Systematics and Biodiversity, 14(2), 171-183. https://doi.org/10.1080/14772000.2015.1112314
Prieto, C., Faynel, C., Robbins, R., & Hausmann, A. (2021). Congruence between morphology-based species and barcode index numbers (Bins) in Neotropical Eumaeini (Lycaenidae). Peerj, 9. https://Doi.Org/10.7717/Peerj.11843
Prieto, C., Pinilla, C., Lorenc-Brudecka, J. & Balke, M. (2024). Integrative description of Thaeides ramoni sp. nov. (Lepidoptera: Lycaenidae), a sympatric sibling species of Thaeides theia (Hewitson, 1870) found in the Sierra Nevada de Santa Marta, Colombia. Zootaxa, 5501(1), 181-190. https://doi.org/10.11646/zootaxa.5501.1.9
Prosierra, F. (2018). Prosierra | División Político-Administrativo. http://Www.Prosierra.Org/Index.Php/La-Sierra-Nevada/La-Sierra-Parte-1/Division-Politico-Administrativo
R Core Team (2021). R: A Language and Environment for Statistical Computing_. R Foundation for Statistical Computing, Vienna, Austria. <https://www.R-project.org/>.
Ramírez, S., Dressle, R. L. &Ospina, M., (2002). Abejas euglosinas (Hymenoptera: Apidae) de la región Neotropical: Listado de especies con notas sobre su biología. Biota Colombiana, 3(1), 7-118. https://revistas.humboldt.org.co/index.php/biota/article/view/108
Ramos, Y. J. A., Romero, E., & Gálvez, D. (2022). Vertical stratification in orchid bees (Apidae: Euglossini)? A meta-analysis. Apidologie, 53(26). https://Doi.Org/10.1007/S13592-022-00939-0
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), e66213https://Doi.Org/10.1371/Journal.Pone.0066213
Ribeiro Pinto, A., Do Carmo Silveira, G., Gaglianone, M. C. & Freitas, L. (2019). Abrupt decrease in the diversity of Euglossini bees (Hymenoptera: Apidae) in a montane rainforest, Journal of Apicultural Research, 58(5), 682- 693, https://doi.org/10.1080/00218839.2019.1637223
Rubio, G. D. (2015). Diversidad de arañas (Araneae, Araneomorphae) en la selva de montaña: un caso de estudio en las yungas argentinas. Graellsia, 71(2), e029. http://dx.doi.org/10.3989/graellsia.2015.v71.134.
Sheffield, C. S., Hebert, P. D. N., Kevan, P. G., & Packer, L. (2009). DNA barcoding a regional bee (Hymenoptera: Apoidea) fauna and its potential for ecological studies. Molecular Ecology Resources, 9(Suppl. 1), 196-207. Https://Doi.Org/10.1111/J.1755-0998.2009.02645.X
Silveira, F. A., Pinheiro-Machado, C., Alves, I., Kleinert, A. De M. P., & Imperatriz-Fonseca, V. L. (2002). Taxonomic constraints for the conservation and sustainable use of wild pollinators – The Brazilian wild bees. The Conservation Link Between Agriculture and Nature - Ministry of Environment, 41-50.
Smith, M. A., Fisher, B. L., & Hebert, P. D. N. (2005). DNA barcoding for effective biodiversity assessment of a hyperdiverse arthropod group: The ants of Madagascar. Philosophical Transactions of the Royal Society B: Biological Sciences, 360(1462), 1825-1834. https://Doi.Org/10.1098/Rstb.2005.1714
Smith, E. P., & van Belle, G. (1984). Nonparametric estimation of species richness. Biometrics, 40(1), 119-129. https://doi.org/10.2307/2530750
Sofia, S. H., de Paula, F. M. D., Santos, A. M. D., Almeida, F. S., & Sodré, L. M. (2005). Genetic structure analysis of Eufriesea violacea (Hymenoptera, Apidae) populations from southern Brazilian Atlantic rainforest remnants. Genetics and Molecular Biology, 28(3), 479-484. https://doi.org/10.1590/S1415-47572005000300026
Stein, A., Gerstner, K., & Kreft, H. (2014). Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecology Letters, 17(7), 866-880. https://doi.org/10.1111/ele.12277
Tamura, K., Stecher, G. & Kumar, S. (2021).MEGA11: Molecular Evolutionary Genetics Analysis version 11. Molecular Biology and Evolution, 38(7), 3022-3027. https://doi.org/10.1093/molbev/msab120
Tobias-Loaiza, M. & Tamaris-Turizo, C. E. (2019). Odonatos de la Sierra Nevada de Santa Marta, Colombia: una lista preliminar Ciencias Naturales Artículo original. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, 43(167), 212-218. https://doi.org/10.18257/raccefyn.832
Tonhasca, A., Blackmer, J. L., & Albuquerque, G. S. (2002a). Within-habitat heterogeneity of euglossine bee populations: A re-evaluation of the evidence. Journal of Tropical Ecology, 18(6), 929-933. Https://Doi.Org/10.1017/S0266467402002602
Tonhasca, A., Blackmer, J. L., & Albuquerque, G. S. (2002b). Abundance and diversity of euglossine bees in the fragmented landscape of the Brazilian Atlantic forest. Biotropica, 34(3), 416-422. https://Doi.Org/10.1111/J.1744-7429.2002.Tb00555.X
Velásquez-Tibata, J., Salaman, P. & Graham, C. (2012). Effects of climate change on species distribution, community structure, and conservation of birds in protected areas in Colombia. Regional Environmental Change, 13, 235-248. https://doi.org/10.1007/s10113-012-0329-y
Villarreal, H., Álvarez, M., Córdoba, S., Escobar, F., Fagua, G., Gast, F., Mendoza, H., Ospina, M., & Umaña, A. M. (2004). Manual de métodos para el desarrollo de inventarios de biodiversidad. Programa de inventarios de Biodiversidad. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt. Bogotá, Colombia. pp: 185-227.
Wickham, H. (2016). ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York. ISBN 978-3-319-24277-4, https://ggplot2.tidyverse.org
Will, K. W., Mishler, B. D., & Wheeler, Q. D. (2005). The perils of DNA barcoding and the need for integrative taxonomy. Systematic Biology, 54(5), 844-851. https://Doi.Org/10.1080/10635150500354878
Wong, E. H. K., Shivji, M. S., & Hanner, R. H. (2009). Identifying sharks with DNA barcodes: Assessing the utility of a nucleotide diagnostic approach. Molecular Ecology Resources, 9(Suppl. 1), 243-256. https://Doi.Org/10.1111/J.1755-0998.2009.02653.X
Accepted 2025-05-14
Published 2025-06-30
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
Authors retain the copyright on their work and are responsible for the ideas expressed in them. Once a manuscript is approved for publication, authors are asked for a publication license for the term of legal protection, for all territories that allows the use, dissemination and disclosure of the same.