A Picky Generalist: Nesting Females of Pseudaugochlora graminea (Halictidae) are Highly Specialized in an Urban Area
DOI:
https://doi.org/10.13102/sociobiology.v71i3.10459Keywords:
Augochlorini, floral preferences, interaction networks, specialized females, polylectic bee, urban areasAbstract
Urban areas act as important shelters to support bee populations, but some guilds, such as generalist species, benefit more than others. We aimed to investigate if the floral preferences of a polylectic species would change throughout the years and if gardening practices such as mowing could affect the females’ floral preferences and, thus, the bee-plant interaction networks in an urban area within a medium- sized city in Brazil. Nesting females of Pseudaugochlora graminea (Fabricius) (Halictidae) were collected and had the pollen grains attached to their scopae removed, acetolyzed, and identified in two different periods: March 2019 and March 2022. Only five plant species were identified in samples from 2019, while 13 species were detected in 2022 despite mowing and plant replacements throughout three years. Among the floral sources observed, both exotic and native species were visited by females for pollen and nectar collection. Despite being a generalist species, all interaction networks between P. graminea females and plant species were highly specialized. Females concentrated their pollen gathering on a few plant species, represented by less than ten individuals in the study area. Mowing led to the destruction of the third most important pollen source in 2019. However, plant replacements may have favored females by some nectar sources seedlings. Our findings demonstrate that gardening practices impacted the floral choices of females of a generalist bee species, whose females established highly specialized interaction networks with plants in an urban area.
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References
Almeida, E.A.B. (2008). Revision of the Brazilian Species of Pseudaugochlora Michener 1954 (Hymenoptera: Halictidae: Augochlorini). Zootaxa, 1679: 1-38.
Araújo, T.N., Pires, L.P., Meireles, D.A.L. & Augusto, S.C. (2021). Individual-resource network between Xylocopa bees and plant resources: generalist species, specialist individuals? Ecological Entomology, 46: 1273-1282.
Baldock, K.C.R., Goddard, M.A., Hicks, D.M., Kunin, W.E., Mitschunas, N., Osgathorpe, L.M., Potts, S.G., Robertson, K.M., Scott, A.V., Stone, G.N., Vaughan, I.P. & Memmott, J. (2015). Where is the UK’s pollinator biodiversity? The importance of urban areas for flower-visiting insects. Proceedings of the Royal Society B: Biological Sciences, 282: 20142849.
Banaszak-Cibicka, W. & Żmihorski, M. (2012). Wild bees along an urban gradient: winners and losers. Journal of Insect Conservation, 6: 331-343.
Banaszak-Cibicka, W., Twerd, L., Fliszkiewicz, M., Giejdasz, K. & Langowska, A. (2018). City parks vs. natural areas –is it possible to preserve a natural level of bee richness and abundance in a city park? Urban Ecosystems, 21: 599-613.
Beal-Neves, M., Ely, C.V., Esteves, M.W., Blochtein, B., Lahm, R.A., Quadros, E.L.L. & Ferreira, P.M.A. (2020). The influence of urbanization and fire disturbance on plant-floral visitor mutualistic networks. Diversity, 12: 1-20.
Bernays, E.A. (2001). Neural limitations in phytophagous insects: Implications for diet breadth and evolution of host affiliation. Annual Review of Entomology, 46: 703-727.
Blüthgen, N., Menzel, F. & Blüthgen, N. (2006). Measuring specialization in species interaction networks. BMC Ecology, 6: 1-12.
Bonet-Ferrer, M. & Vergara, C.H. (2019). Abejas silvestres de un cafetal orgánico en Veracruz, México. Puebla: Fundación Universidad de las Américas, 499 p.
Cane, J.H., Minckley, R.L., Kervin, L.J., Roulston, T.A.H. & Williams, N.M. (2006). Complex responses within a desert bee guild (Hymenoptera: Apiformes) to urban habitat fragmentation. Ecological Applications, 16: 632-644.
Czech, B., Krausman, P.R. & Devers, P.K. (2000). Economic associations among causes of species endangerment in the United States. BioScience, 50: 593-601.
Dormann, C.F. (2011). How to be a specialist? Quantifying specialisation in pollination networks. Network Biology, 1: 1-20.
Dormann, C.F., Gruber, B. & Fründ, J. (2008). Introducing the bipartite package: analysing ecological networks. R News, 8: 8-11.
Dormann, C.F., Fründ, J., Blüthgen, N. & Gruber, B. (2009). Indices, graphs and null models: analyzing bipartite ecological networks. Open Journal of Ecology, 2: 7-24.
Dylewski, Ł., Maćkowiak, Ł. & Banaszak-Cibicka, W. (2019). Are all urban green spaces a favourable habitat for pollinator communities? Bees, butterflies and hoverflies in different urban green areas. Ecological Entomology, 44: 678-689.
Erdtman, G. (1960). The acetolysis method. A revised description. Svensk Botanisk Tidskrift, 54: 561-564.
Fortel, L., Henry, M., Guilbaud, L., Guirao, A.L., Kuhlmann, M., Mouret, H., Rollin, O. & Vaissière, B.E. (2014). Decreasing abundance, increasing diversity, and changing structure of the wild bee community (Hymenoptera: Anthophila) along an urbanization gradient. PLoS ONE, 9: e104679.
Guimarães-Alves, S. & Gaglianone, M.C. (2021). Bee guilds’ responses to urbanization in Neotropics: A case study. Diversity, 13: 365.
Hall, D.M., Camilo, G.R., Tonietto, R.K., Ollerton, J., Ahrné, K., Arduser, M., Ascher, J.S., Baldock, K.C.R., Fowler, R., Frankie, G., Goulson, D., Gunnarsson, B., Hanley, M.E., Jackson, J.I., Langellotto, G., Lowenstein, D., Minor, E.S., Philpott, S.M., Potts, S.G., Sirohi, M.H., Spevak, E.M., Stone, G.N. & Threlfall, C.G. (2017). The city as a refuge for insect pollinators. Conservation Biology, 31: 24-29.
Hülsmann, M., von Wehrden, H., Klein, A.M. & Leonhardt, S.D. (2015). Plant diversity and composition compensate for negative effects of urbanization on foraging bumble bees. Apidologie, 46: 760-770.
IBGE – Instituto Brasileiro de Geografia e Estatística (2024). Cidades. IBGE, Rio de Janeiro. https://cidades.ibge.gov.br/brasil/mg/uberlandia/panorama. (accessed date: 19 June 2024).
Imperatriz-Fonseca, V.L., Alves-dos-Santos, I., Santos-Filho, O.S., Engels, W., Ramalho, M., Wilms, W., Aguilar, J.B.V., Pinheiro-Machado, C.A., Alves, D.A. & Kleinert, A.M.P. (2011). Checklist das abelhas e plantas melitófilas no Estado de São Paulo, Brasil. Biota Neotropica, 11: 631-655.
Lanner, J., Kratschmer, S., Petrović, B., Gaulhofer, F., Meimberg, H. & Pachinger, B. (2020). City dwelling wild bees: how communal gardens promote species richness. Urban Ecosystems, 23: 271-288.
Lowenstein, D.M., Matteson, K.C., Xiao, I., Silva, A.M. & Minor, E.S. (2014). Humans, bees, and pollination services in the city: the case of Chicago, IL (USA). Biodiversity Conservation, 23: 2857-2874.
Martins, K.T., Gonzalez, A. & Lechowicz, M.J. (2017). Patterns of pollinator turnover and increasing diversity associated with urban habitats. Urban Ecosystems, 20: 1359-1371.
McDonald, R.I., Kareiva, P. & Forman, R.T.T. (2008). The implications of current and future urbanization for global protected areas and biodiversity conservation. Biological Conservation, 141: 1695-1703.
McKinney, M.L. (2008). Effects of urbanization on species richness: A review of plants and animals. Urban Ecosystems, 11: 161-176.
Michener, C.D. & Kerfoot, W.B. (1967). Nests and social behavior of three species of Pseudaugochloropsis (Hymenoptera: Halictidae). Journal of the Kansas Entomological Society, 40: 214-232.
Müller, A. & Kuhlmann, M. (2008). Pollen hosts of western palaearctic bees of the genus Colletes (Hymenoptera: Colletidae): the Asteraceae paradox. Biological Journal of the Linnean Society, 95: 719-733.
Nimer, E. & Brandão, A.M.P.M. (1989). Balanço hídrico e clima da região dos cerrados. Rio de Janeiro: IBGE, 166 p.
Osborne, J.L., Martin, A.P., Shortall, C.R., Todd, A.D., Goulson, D., Knight, M.E., Hale, R.J. & Sanderson, R.A. (2008). Quantifying and comparing bumblebee nest densities in gardens and countryside habitats. Journal of Applied Ecology, 45: 784-792.
Rocha-Filho, L.C. & Garófalo, C.A. (2016). Natural history of Tetrapedia diversipes (Hymenoptera, Apidae) in an Atlantic semi-deciduous forest remnant surrounded by coffee crops, Coffea arabica (Rubiaceae). Annals of the Entomological Society of America, 109: 183-197.
Rocha-Filho, L.C., Ferreira-Caliman, M.J., Garófalo, C.A. & Augusto, S.C. (2018). A specialist in an urban area: Are cities suitable to harbour populations of the oligolectic bee Centris (Melacentris) collaris (Apidae: Centridini)? Annales Zoologici Fennici, 55: 135-149.
Roulston, T.H., Cane, J.H. & Buchmann, S.L. (2000). What governs protein content of pollen: Pollinator preferences, pollen-pistil interactions, or phylogeny? Ecological Monographs, 70: 617-643.
Roulston, T.H. & Goodell, K. (2011). The role of resources and risks in regulating wild bee populations. Annual Review of Entomology, 56: 293-312.
Rundlöf, M., Andersson, G.K.S., Bommarco, R., Fries, I., Hederström, V., Herbertsson, L., Jonsson, O., Klatt, B.K., Pedersen, T.R., Yourstone, J. & Smith, H.G. (2015). Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature, 521: 77-80.
Samuelson, A.E., Gill, R.J., Brown, M.J.F. & Leadbeater, E. (2018). Lower bumblebee colony reproductive success in agricultural compared with urban environments. Proceedings of the Royal Society B: Biological Sciences, 285: 20180807.
Senapathi, D., Carvalheiro, L.G., Biesmeijer, J.C., Dodson, C.A., Evans, R.L., McKerchar, M., Morton, R.D., Moss, E.D., Roberts, S.P.M., Kunin, W.E. & Potts, S.G. (2015). The impact of over 80 years of land cover changes on bee and wasp pollinator communities in England. Proceedings of the Royal Society B: Biological Sciences, 282: 20150294.
Steiner, J., Zillikens, A., Kamke, R., Feja, E.P. & Falkenberg, D.B. (2010). Bees and melittophilous plants of secondary Atlantic Forest habitats at Santa Catarina Island, Southern Brazil. Oecologia Australis, 14: 16-39.
Suni, S., Hall, E., Bahu, E. & Hayes, H. (2021). Urbanization increases floral specialization of pollinators. Ecology and Evolution, 12: e8619.
Theodorou, P., Albig, K., Radzevičiūtė, R., Settele, J., Schweiger, O., Murray, T.E. & Paxton, R.J. (2017). The structure of flower visitor networks in relation to pollination across an agricultural to urban gradient. Functional Ecology, 31: 838-847.
Theodorou, P., Radzevičiūtė, R., Lentendu, G., Kahnt, B., Husemann, M., Bleidorn, C., Settele, J., Schweiger, O., Grosse, I. & Wubet, T. (2020). Urban areas as hotspots for bees and pollination but not a panacea for all insects. Nature Communications, 11: 576.
Threlfall, C.G., Walker, K., Williams, N.S.G., Hahs, A.K., Mata, L., Stork, N. & Livesley, S.J. (2015). The conservation value of urban green space habitats for Australian native bee communities. Biological Conservation, 187: 240-248.
United Nations (2018). World Urbanization Prospects: The 2018 Revision. Department of Economic and Social Affairs/Population Division. https://population.un.org/wup/. (accessed date: 2 March 2023).
Vergeron, P. (1964). Interprétation statistique des résultats en matière d`analyse pollinique des miels. Les Annales de l’Abeille, 7: 349-364.
Wastian, L., Unterweger, P.A. & Betz, O. (2016). Influence of the reduction of urban lawn mowing on wild bee diversity (Hymenoptera, Apoidea). Journal of Hymenoptera Research, 49: 51-63.
Zambrano, L., Aronson, M.F.J. & Fernandez, T. (2019). The consequences of landscape fragmentation on socio-ecological patterns in a rapidly developing urban area: A case study of the National Autonomous University of Mexico. Frontiers in Environmental Science, 7: 152.
Zanette, L.R.S., Martins, R.P. & Ribeiro, S.P. (2005). Effects of urbanization on neotropical wasp and bee assemblages in a Brazilian metropolis. Landscape and Urban Planning, 71: 105-121.
Zaninotto, V., Thebault, E. & Dajoz, I. (2023). Native and exotic plants play different roles in urban pollination networks across seasons. Oecologia, 201: 525-536.
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