Effect of green spaces and floral composition on the community of flower visitors in a piedmont city in Argentina
DOI:
https://doi.org/10.25260/EA.24.34.3.0.2379Keywords:
urban greenspaces, flower density, exotic plants, potential urban pollinators, urban environmentAbstract
In cities, human activities transform the native composition of plant communities into a mixture of native and exotic species. This new plant community shapes the composition of floral visitor communities persisting in urban environments. Recognizing the value of the diversity of urban pollinator communities can help quantify the conservation significance of cities. The aims of this work are: 1) to understand the effect of urbanization on flower visitors by comparing pollinator communities in natural and urban landscapes; 2) to quantify the influence of floral resources on floral visitors, and 3) to assess the impact of green spaces in urban environments on the composition of the flower-visitor community. We explored plant communities and floral visitors in five urban green spaces in a low urbanized city in Tucumán, Argentina, and in five natural protected areas located adjacent to the city. We found a greater diversity of flowering plants in the urban environment; mainly represented by exotic plant species and a lower diversity of the pollinator community than in the natural landscape. Pollinator diversity also showed a positive association with plant richness, while it was negatively affected by the proportion of exotic plants and the increase in flower density. Within city, distance to green spaces negatively affects the diversity of pollinators. Our results show that floral visitor communities in urban environments are less diverse than those in natural sites. Therefore, the composition of the plant community in the city, mainly exotic seems to affect communities of urban floral visitors. Our findings suggest that cities without intensive urbanization, and that still share many species with the closest natural space, may focus on urban planning that considers development alternatives that contribute to the conservation of pollinators.
References
Abrahamovich, A. H., N. B. Díaz, and M. Lucia. 2007. Identificación de las “abejas sociales” del género Bombus (Hymenoptera, Apidae) presentes en la Argentina: clave pictórica, diagnosis, distribución geográfica y asociaciones florales. Revista de La Facultad de Agronomía de La Plata 106(2):165-176.
Ahrné, K., J. Bengtsson, and T. Elmquist. 2009. A next-generation approach to the characterization of a non-model plant transcriptome. PLoS ONE 4(5). https://doi.org/10.1371/ journal.pone.0005574.
Álvarez, L. J. 2015. Diversidad de las abejas nativas de la tribu Meliponini (Hymenoptera, Apidae) en Argentina. Tesis Doctoral. Universidad Nacional de la Plata - Facultad de Ciencias Naturales y Museo. La Plata, Buenos Aíres. Argentina.
Álvarez, L. J., C. Rasmussen, and A. H. Abrahamovich. 2016. Nueva especie de Plebeia Schwarz, clave para las especies argentinas de Plebeia y comentarios sobre Plectoplebeia en la Argentina (Hymenoptera: Meliponini). Rev Mus Argentino Cienc Nat 18(1):65-74. https://doi.org/10.22179/REVMACN.18.433.
Amado De Santis, A. A., and N. P. Chacoff. 2020. Urbanization Affects Composition but Not Richness of Flower Visitors in the Yungas of Argentina. Neotropical Entomology 49(4):568-577. https://doi.org/10.1007/s13744-020-00772-z.
Baldock, K. C. R., M. A. Goddard, D. M. Hicks, W. E. Kunin, N. Mitschunas, H. Morse, et al. 2019. A systems approach reveals urban pollinator hotspots and conservation opportunities. Nature Ecology and Evolution 3(3):363-373. https://doi.org/10.1038/s41559-018-0769-y.
Baldock, K. C. R., M. A. Goddard, D. M. Hicks, W. E. Kunin, N. Mitschunas, L. M. Osgathorpe, et al. 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(1803):20142849. https://doi.org/10.1098/rspb.2014.2849.
Banaszak-Cibicka, W., L. Twerd, M. Fliszkiewicz, K. Giejdasz, and A. Langowska. 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(4):599-613. https://doi.org/10.1007/s11252-018-0756-8.
Bates, A. J., J. P. Sadler, A. J. Fairbrass, S. J. Falk, J. D. Hale, and T. J. Matthews. 2011. Changing bee and hoverfly pollinator assemblages along an urban-rural gradient. PLoS ONE 6(8). https://doi.org/10.1371/journal.pone.0023459.
Brose, U., and N. D. Martínez. 2004. Estimating the richness of species with variable mobility. Oikos 105(2):292-300. https://doi.org/10.1111/j.0030-1299.2004.12884.x.
Brothers, D. J., A. T. Finnamore, and F. Fernández. 2006. Superfamilia Vespoidea. Pp. 505-513 in F. Fernández and M. J. Sharkey (eds.). Introducción a los Hymenoptera de la Región Neotropical. Sociedad Colombiana de Entomología and Universidad Nacional de Colombia, Bogotá, Colombia.
Brown, A. D. 2009. Manejo sustentable y conservación de la biodiversidad de un ecosistema prioritario del noroeste argentino. Pp. 13-31 in A. D. Brown, P. G. Blendinger T. Lomáscolo and P. G. Bes (eds.). Selva pedemontana de las Yungas. Historia natural, ecología y manejo de un ecosistema en peligro. Yerba Buena, Tucuman: Ediciones del Subtrópico.
Buchholz, S., and I. Kowarik. 2019. Urbanisation modulates plant-pollinator interactions in invasive vs. native plant species. Scientific Reports 9(1):1-9. https://doi.org/10.1038/s41598-019-42884-6.
Buck, M., N. E. Woodley, A. Borkent, D. M. Wood, T. Pape, J. R. Vockeroth, et al. 2009. Key to Diptera Families. In B. V. Brown, A. Borkent, J. M. Cumming, D. M. Wood, N. E. Woodley and M. A. Zumbado (eds.). Manual of Central American Diptera (Vol. 1). Ottawa: NRC Research Press.
Chalup, A. E. 2021. Mariposas. Pp. 311-318 in Plantas y animales de la sierra San Javier. Ediciones del Subtrópico, Yerba Buena, Tucumán, Argentina.
Conner, J. K., and R. Neumeier. 1995. Effects of black mustard population size on the taxonomic composition of pollinators. Oecologia 104(2):218-224. https://doi.org/10.1007/BF00328586.
Colwell, R. K., and J. A. Coddington. 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 345(1311):101-118. https://doi.org/10.1098/rstb.1994.0091.
Coscarón, M. C., and D. L. Carpintero. 2023. Coreidae. Pp. 182-186 in L. E. Claps, S. Roig-Juñent and J. J. Morrone (eds.). Biodiversidad de Artrópodos Argentinos, vol. 6. Editorial INSUE -UNT, San Miguel de Tucumán, Tucumán, Argentina.
Crawley, M. J. 2007. The R Book. Auction Theory. https://doi.org/10.1016/b978-0-12-374507-1.00050-9.
Dalmazzo, M., R. A. González Vaquero, A. Roig Alsina, and G. Debandi. 2020. Halictidae. Pp. 203-219 in S. Roig-Juñent, L. E. Claps and J. J. Morrone (eds.). Biodiversidad de Artrópodos Argentinos, vol. 4. Editorial INSUE -UNT, San Miguel de Tucumán, Tucumán, Argentina.
Daniels, B., J. Jedamski, R. Ottermanns, and M. Ross-Nickoll. 2020. A “plan bee” for cities: Pollinator diversity and plant-pollinator interactions in urban green spaces. PLoS ONE 15(7 July):1-29. https://doi.org/10.1371/journal.pone.0235492.
Davis, A. Y., E. V. Lonsdorf, C. R. Shierk, K. C. Matteson, J. R. Taylor, S. T. Lovell, and E. S. Minor. 2017. Enhancing pollination supply in an urban ecosystem through landscape modifications. Landscape and Urban Planning 162:157-166. https://doi.org/10.1016/j.landurbplan.2017.02.011.
Dirección de Estadística de la Provincia de Tucumán. (2020). URL: tinyurl.com/3d3zfphd.
Durante, S. P., N. C. Cabrera, and L. E. Gómez de la Vega. 2008. Megachilidae. Pp. 421-433 in L. E. Claps, G. Debandi and S. Roig-Juñent (eds.). Biodiversidad de Artrópodos Argentinos, vol. 2. Editorial Sociedad Entomológica Argentina, Mendoza, Argentina.
Dylewski, Ł., Ł. Maćkowiak, and W. Banaszak-Cibicka. 2019. Are all urban green spaces a favourable habitat for pollinator communities? Bees, butterflies and hoverflies in different urban green areas. Ecological Entomology 44(5):678-689. https://doi.org/10.1111/een.12744.
Dylewski, Ł., Ł. Maćkowiak, and W. Banaszak-Cibicka. 2020. Linking pollinators and city flora: How vegetation composition and environmental features shapes pollinators composition in urban environment. Urban Forestry and Urban Greening 56(July). https://doi.org/10.1016/j.ufug.2020.126795.
Fernández, F., and E. E. Palacio. 2006. Familia Formicidae. Pp. 521-538 in F. Fernández and M. J. Sharkey (eds.). Introducción a los Hymenoptera de la Región Neotropical. Sociedad Colombiana de Entomología and Universidad Nacional de Colombia, Bogotá, Colombia.
Fischer, L. K., J. Eichfeld, I. Kowarik, and S. Buchholz. 2016. Disentangling urban habitat and matrix effects on wild bee species. PeerJ 4:e2729. https://doi.org/10.7717/peerj.2729.
Fitch, G., C. Wilson, P. Glaum, C. Vaidya, M. C. Simao, and M. A. Jamieson. 2019. Does urbanization favour exotic bee species? Implications for the conservation of native bees in cities. Biology Letters 15(12). https://doi.org/10.1098/rsbl.2019.0574.
Flora Argentina y del Conosur. URL: bit.ly/47pWRPS.
Garbuzov, M., R. Schürch, and F. L. W. Ratnieks. 2015. Eating locally: dance decoding demonstrates that urban honey bees in Brighton, UK, forage mainly in the surrounding urban area. Urban Ecosystems 18(2):411-418. https://doi.org/10.1007/s11252-014-0403-y.
Geslin, B., M. Le Féon, Kuhlmann, B. E. Vaissière, and I. Dajoz. 2016. The bee fauna of large parks in downtown Paris, France. Annales de La Societe Entomologique de France 51(5-6):487-493. https://doi.org/10.1080/00379271.2016.1146632.
Giurfa, M., A. Dafni, and P. R. Neal. 1999. Floral symmetry and its role in plant-pollinator systems. International Journal of Plant Sciences 160(6 Suppl.). https://doi.org/10.1086/314214.
Glaum, P., M. C. Simao, C. Vaidya, G. Fitch, and B. Iulinao. 2017. Big city Bombus: Using natural history and land-use history to find significant environmental drivers in bumble-bee declines in urban development. Royal Society Open Science 4(5). https://doi.org/10.1098/rsos.170156.
González, R., and N. S. Carrejo. 1992. Introducción al estudio de los Diptera. 1st edition. Universidad del Valle, Cali, Colombia.
Graffigna, S., R. A. González-Vaquero, J. P. Torretta, and H. J. Marrero. 2024. Importance of urban green areas’ connectivity for the conservation of pollinators. Urban Ecosyst 27:417-426. https://doi.org/10.1007/s11252-023-01457-2.
Grau, A. 2021. Plantas y animales de la sierra de San Javier. 1st ed. Ediciones del Subtrópico. Yerba Buena, Tucumán, Argentina.
Grau, H. R., M. E. Hernández, J. Gutiérrez, N. I. Gasparri, M. C. Casavecchia, E. E. Flores-Ivaldi, and L. Paolini. 2008. A peri-urban neotropical forest transition and its consequences for environmental services. Ecology and Society 13(1):35. https://doi.org/10.5751/ES-02434-130135.
Grimm, N. B., S. H. Faeth, N. E. Golubiewski, C. L. Redman, J. Wu, X. Bai, and J. M. Briggs. 2008. Global change and the ecology of cities. Science 319(5864):756-760. https://doi.org/10.1126/science.1150195.
Gutiérrez Angonese, J. 2015. Historia de uso del territorio en el área peri-urbana de la Sierra de San Javier y el Gran San Miguel de Tucumán, Argentina (1972-2010). Universidad Nacional de Córdoba.
Haedo, J., P. G., Blendinger, and N. I. Gasparri. 2010. Estructura espacial del ensamble de aves en el gradiente de urbanización de Yerba Buena-San Miguel de Tucumán (noroeste de Argentina). Pp. 153-166 in Ecologia de una interfase natural-urbana. La Sierra de San Javier y el Gran San Miguel de Tucuman.
Hall, D. M., G. R. Camilo, R. K. Tonietto, J. Ollerton, K. Ahrné, M. Arduser, et al. 2017. The city as a refuge for insect pollinators. Conservation Biology 31(1):24-29. https://doi.org/10.1111/cobi.12840
National Census of Population, Households, and Housing. 2022. Resultados definitivos: indicadores demográficos por sexo y edad / 1a ed. - Ciudad Autónoma de Buenos Aires : Instituto Nacional de Estadística y Censos - INDEC 2023.
Kearns, C. A., and D. M. Oliveras. 2009. Environmental factors affecting bee diversity in urban and remote grassland plots in Boulder, Colorado. Journal of Insect Conservation 13(6):655-665. https://doi.org/10.1007/s10841-009-9215-4.
Knapp, S., L. Dinsmore, C. Fissore, S. E. Hobbie, I. Jakobsdottir, J. Kattge, et al. 2012. Phylogenetic and functional characteristics of household yard floras and their changes along an urbanization gradient. Ecology 93(8):83-98. https://doi.org/10.1890/11-0392.1.
Lucia, M., L. J. Alvarez, and A. H. Abrahamovich. 2014. Large carpenter bees in Argentina: systematics and notes on the biology of Xylocopa subgenus Neoxylocopa (Hymenoptera: Apidae). Zootaxa 3754(3):201-238. https://doi.org/10.11646/zootaxa.3754.3.1.
Lowenstein, D. M., K. C. Matteson, and E. S. Minor. 2019. Evaluating the dependence of urban pollinators on ornamental, non-native, and ‘weedy’ floral resources. Urban Ecosystems 22(2):293-302. https://doi.org/10.1007/s11252-018-0817-z.
MacInnis, G., E. Normandin, and C. D. Ziter. 2023. Decline in wild bee species richness associated with honey bee (Apis mellifera L.) abundance in an urban ecosystem. PeerJ 11:1-26. https://doi.org/10.7717/peerj.14699.
Maza, N., G. P. López-García, and X. Mengual. 2023. Syrphidae. Pp. 324-346 in L. E. Claps, S. Roig-Juñet and J. J. Morrone (eds.). Biodiversidad de Artrópodos Argentinos, vol. 6. Editorial INSUE UNT, San Miguel de Tucumán, Argentina.
McAlpine, J. F., B. V. Peterson, G. E. Shewell, H. J. Teskey, J. R. Vockeroth, and D. Wood. 1981. Manual of Nearctic Diptera (Vol. 1). Ottawa: Agriculture Canada Monograph No. 27.
McFrederick, Q. S., and G. LeBuhn. 2006. Are urban parks refuges for bumble bees Bombus spp. (Hymenoptera: Apidae)? Biological Conservation 129(3):372-382. https://doi.org/10.1016/j.biocon.2005.11.004.
McIntyre, M. E., N. E. Hostetler, and M. E. McIntyre. 2001. Effects of urban land use on pollinator (Hymenoptera: Apoidea) communities in a desert metropolis. Basic and Applied Ecology 2(3):209-218. https://doi.org/10.1078/1439-1791-00051.
McKinney, E. L. 2008. Effects of urbanization on species richness: A reviw of plants and animals. Urban Ecosystems 11:161-176. https://doi.org/10.1007/s11252-007-0045-4.
Michener, C. D. 2007. The Bees of the World (Second). Baltimore: The Johns Hopkins University Press Baltimore.
Normandin, É., N. J. Vereecken, C. M. Buddle, and V. Fournier. 2017. Taxonomic and functional trait diversity of wild bees in different urban settings. PeerJ 2017(3):1-35. https://doi.org/10.7717/peerj.3051.
Oltra-Carrió, R., J. A. Sobrino, J. Gutiérrez Angonese, A. Gioia, L. Paolini, and A. Malizia. 2010. Estudio del crecimiento urbano, de la estructura de la vegetación y de la temperatura de la superficie del Gran San Miguel de Tucumán , Argentina. Revista de Teledetección 34:69-76.
Osborne, J. L., A. P. Martin, N. L. Carreck, J. L. Swain, M. E. Knight, D. Goulson, et al. 2008. Bumblebee flight distances in relation to the forage landscape. Journal of Animal Ecology 77(2):406-415. https://doi.org/10.1111/j.1365-2656.2007.01333.x.
Persson, A. S., A. Westman, T. J. Smith, M. M. Mayfield, P. Olsson, H. G. Smith, and R. Fuller. 2022. Backyard buzz: human population density modifies the value of vegetation cover for insect pollinators in a subtropical city. Urban Ecosyst 25:1875-1890. https://doi.org/10.1007/s11252-022-01277-w.
Persson, A. S., V. Hederström, I. Ljungkvist, L. Nilsson, and L. Kendall. 2023. Citizen science initiatives increase pollinator activity in private gardens and green spaces. Front Sustain Cities 4:1099100. https://doi.org/10.3389/frsc.2022.1099100.
Potter, A., and G. LeBuhn. 2015. Pollination service to urban agriculture in San Francisco, CA. Urban Ecosystems 18(3):885-893. https://doi.org/10.1007/s11252-015-0435-y.
Roig Alsina, A. 2008. Apiformes. Pp. 373-390 in L. E. Claps, G. Debandi and S. Roig-Juñent (eds.). Biodiversidad de Artrópodos Argentinos, vol. 2. Editorial Sociedad Entomológica Argentina, Mendoza.
Roig Alsina, A. 2013. El género Ceratina en la Argentina: Revisión del subgénero Neoclavicera subg. n. (Hymenoptera, Apidae, Xylocopinae). Revista Del Museo Argentino de Ciencias Naturales, Nueva Serie 15(1):121-143. https://doi.org/10.22179/REVMACN.15.174.
Roig Alsina, A. 2014. Claves para las especies argentinas de Centris (Hymenoptera, Apidae), con descripción de nuevas especies y notas sobre distribución. Revista Del Museo Argentino de Ciencias Naturales Nueva Serie 2(2):171-193. https://doi.org/10.22179/REVMACN.2.154.
Ruz, L., L. Campagnucci, and A. Roig-Alsina. 2008. Andrenidae. Pp. 407-420 in L. E. Claps, G. Debandi and S. Roig-Juñent (eds.). Biodiversidad de Artrópodos Argentinos, vol. 2. Editorial Sociedad Entomológica Argentina, Mendoza.
Sarmiento, C. E., and J. M. Carpenter. 2006. Familia Vespidae. Pp. 539-555 in F. Fernández and M. J. Sharkey (eds.). Introducción a los Hymenoptera de la Región Neotropical. Sociedad Colombiana de Entomología and Universidad Nacional de Colombia, Bogotá, Colombia.
Sattler, T., D. Borcard, R. Arlettaz, F. Bontadina, P. Legendre, M. K. Obrist, and M. Moretti. 2010. Spider, bee, and bird communities in cities are shaped by environmental control and high stochasticity. Ecology 91(11):3343-3353. https://doi.org/10.1890/09-1810.1.
Statistics Directorate of the Province of Tucumán 2020. URL: bit.ly/3tJXgyC.
Theodorou, P., R. Radzevičiūtė, G. Lentendu, B. Kahnt, M. Husemann, C. Bleidorn, et al. 2020. Urban areas as hotspots for bees and pollination but not a panacea for all insects. Nature Communications 11(1):1-13. https://doi.org/10.1038/s41467-020-14496-6.
Threlfall, C. G., K. Walker, N. S. G. Williams, A. K. Hahs, L. Mata, N. Stork, and S. J. Livesley. 2015. The conservation value of urban green space habitats for Australian native bee communities. Biological Conservation 187:240-248. https://doi.org/10.1016/j.biocon.2015.05.003.
Totland, Ø., and I. Matthews. 1998. Determinants of pollinator activity and flower preference in the early spring blooming Crocus vernus. Acta Oecologica 19(2):155-165. https://doi.org/10.1016/S1146-609X(98)80019-2.
Urban, D. 2009. Espécies novas de Anthrenoides Ducke (Hymenoptera, Apidae, Andreninae) da Argentina. Rev Bras Entomol 53(2). https://doi.org/10.1590/S0085-56262009000200005.
Van Rossum, F. 2010. Reproductive success and pollen dispersal in urban populations of an insect-pollinated hay-meadow herb. Perspectives in Plant Ecology, Evolution and Systematics 12(1):21-29. https://doi.org/10.1016/j.ppees.2009.08.002.
Waters, C. N., J. Zalasiewicz, C. Summerhayes, A. D. Barnosky, C. Poirier, A. Gałuszka, et al. 2016. The Anthropocene is functionally and stratigraphically distinct from the Holocene. Science 351(6269). https://doi.org/10.1126/science.aad2622.
Werenkraut, V., F. Baudino, F. Frasca, M. F. Nuñez Sada, and R. Ripa. 2022. Guía de Campo de Vaquitas Argentina. URL: proyectovaquitas.com.ar.
Weiner, C. N., M. Werner, K. E. Linsenmair, and N. Blüthgen. 2014. Land-use impacts on plant-pollinator networks: Interaction strength and specialization predict pollinator declines. Ecology 95(2):466-474. https://doi.org/10.1890/13-0436.1.
Wenninger, A., T. N. Kim, B. J. Spiesman, and C. Gratton. 2016. Contrasting foraging patterns: Testing resource-concentration and dilution effects with pollinators and seed predators. Insects 7(2). https://doi.org/10.3390/insects7020023.
Wenzel, A., I. Grass, V. V. Belavadi, and T. Tscharntke. 2020. How urbanization is driving pollinator diversity and pollination - A systematic review. Biological Conservation 241(November 2019):108321. https://doi.org/10.1016/j.biocon.2019.108321.
Zaninotto, V., E. Thebault, and I. Dajoz. 2023. Native and exotic plants play different roles in urban pollination networks across seasons. Oecologia 201(2):525-536. https://doi.org/10.1007/s00442-023-05324-x.
Downloads
Additional Files
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Franco D. Andrada, Natacha P. Chacoff, Silvia B. Lomáscolo
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors retain their rights as follows: 1) by granting the journal the right to its first publication, and 2) by registering the published article with a Creative Commons Attribution License (CC-BY 4.0), which allows authors and third parties to view and use it as long as they clearly mention its origin (citation or reference, including authorship and first publication in this journal). Authors can make other non-exclusive distribution agreements as long as they clearly indicate their origin and are encouraged to widely share and disseminate the published version of their work.
