Plant–Bee Interaction Network in an Atlantic Forest Fragment of a Neotropical Metropolis
DOI:
https://doi.org/10.13102/sociobiology.v73i2.12408Keywords:
Ecological networks, urban ecology, webs, floral visitors, functional roles, pollinationAbstract
Urbanization is a major driver of biodiversity loss and profoundly alters the structure of species interaction networks. Nevertheless, urban forest remnants may still sustain structurally and functionally diverse pollinator networks. Here, we characterize the structural and functional organization of a plant-bee interaction network within a large Atlantic Forest fragment embedded in a tropical metropolis in northeastern Brazil. We quantified 4,700 plant-bee interactions involving 19 plant and 80 bee species and evaluated network connectance, nestedness, modularity, specialization, and species- level functional roles. The network was relatively sparse, exhibited low nestedness, moderate modularity, and high specialization. Most plant and bee species occupied peripheral positions, whereas a small subset of abundant eusocial stingless bees, particularly Trigona spinipes (Fabricius) and Scaptotrigona tubiba (Smith), functioned as connectors linking interaction modules. No species acted as a true network hub, indicating limited integration among modules. Together, these patterns reveal a network dominated by a few generalists and many low-degree species, consistent with functional filtering in urban landscapes. Despite this, the remnant supported ecologically important interactions involving both generalist and specialized pollinator guilds. Our findings highlight the ecological value of large, heterogeneous urban forest patches, such as Pituaçu Metropolitan Park, and their role in maintaining pollination network structure and function, with important implications for the planning and conservation of urban green areas in tropical cities.
Downloads
References
Aizen, M.A., Sabatino, M. & Tylianakis, J.M. (2012). Specialization and rarity predict nonrandom loss of interactions from mutualist networks. Science, 335: 1486-1489. DOI: https://doi.org/10.1126/science.1215320
Almeida-Neto, M., Guimarães, P.R.J., Loyota, R.D. & Ulrich, W. (2008). A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos, 117: 1227-1239. DOI: https://doi.org/10.1111/j.0030-1299.2008.16644.x
Almeida-Neto, M. & Ulrich, W. (2011). A straightforward computational approach for measuring nestedness using quantitative matrices. Environmental Modelling and Software, 26: 173-178. DOI: https://doi.org/10.1016/j.envsoft.2010.08.003
Alvares, C.A., Stape, J.L., Sentelhas, P.C., de Moraes Gonçalves, J.L. & Sparovek, G. (2013). Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22: 711-728. DOI: https://doi.org/10.1127/0941-2948/2013/0507
Aronson, M. F., Lepczyk, C. A., Evans, K. L., Goddard, M. A., Lerman, S. B., MacIvor, J. S., et al. (2017). Biodiversity in the city: key challenges for urban green space management. Frontiers in Ecology and the Environment, 15: 189-196. DOI: https://doi.org/10.1002/fee.1480
Baldock, K.C.R., Goddard, M.A., Hicks, D.M., Kunin, W.E., Mitschunas, N., Osgathorpe, L.M., 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: 20142849. DOI: https://doi.org/10.1098/rspb.2014.2849
Banaszak-Cibicka, W. & Żmihorski, M. (2012). Wild bees along an urban gradient: winners and losers. Journal of Insect Conservation, 16: 331-343. DOI: https://doi.org/10.1007/s10841-011-9419-2
Bascompte, J., Jordano, P., Melián, C.J. & Olesen, J.M. (2003). The nested assembly of plant-animal mutualistic networks. Proceedings of the National Academy of Sciences of the United States of America, 100: 9383-9387. DOI: https://doi.org/10.1073/pnas.1633576100
Blüthgen, N., Menzel, F. & Blüthgen, N. (2006). Measuring specialization in species interaction networks. BMC Ecology, 6: 9. DOI: https://doi.org/10.1186/1472-6785-6-9
Boscolo, D., Tokumoto, P.M., Ferreira, P.A., Ribeiro, J.W. & Santos, J.S.D. (2017). Positive responses of flower visiting bees to landscape heterogeneity depend on functional connectivity levels. Perspectives in Ecology and Conservation, 15: 18-24. DOI: https://doi.org/10.1016/j.pecon.2017.03.002
Campbell, A.J., Gigante Carvalheiro, L., Gastauer, M., Almeida-Neto, M. & Giannini, T.C. (2019). Pollinator restoration in Brazilian ecosystems relies on a small but phylogenetically-diverse set of plant families. Scientific Reports, 9: 1-11. DOI: https://doi.org/10.1038/s41598-019-53829-4
Cane, J.H. (2005). Bees, Pollination, and the Challenges of Sprawl. In: Nature in Fragments E.A. Johnson & M.W. Klemens (Eds). pp. 109-124. New York: Columbia University Press. DOI: https://doi.org/10.7312/john12778-008
CONDER (1992). Avaliação dos Impactos Ambientais Decorrentes da Implantação do Plano Diretor do Campus Pituaçu. Salvador-BA. pp. 205.
Dormann, C.F., Frund, J., Bluthgen, N. & Gruber, B. (2009). Indices, Graphs and Null Models: Analyzing Bipartite Ecological Networks. The Open Ecology Journal, 2: 7-24. DOI: https://doi.org/10.2174/1874213000902010007
Dormann, C.F. & Strauss, R. (2014). A method for detecting modules in quantitative bipartite networks. Methods in Ecology and Evolution, 5: 90-98. DOI: https://doi.org/10.1111/2041-210X.12139
ECOA. (2013). Animais e Plantas do Parque Metropolitano de Pituaçu – Lista de Espécies. Conservação. http://www.ucsal.br/pesquisa/ecoa/pesq_apresentacao.asp. Centro de Ecologia e Conservação Animal. Accessed on Nov, 19/2025.
Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics, 34: 487-515. DOI: https://doi.org/10.1146/annurev.ecolsys.34.011802.132419
Ferreira, P.A., Boscolo, D., Lopes, L.E., Carvalheiro, L.G., Biesmeijer, J.C., Rocha, P.L.B. da, et al. (2020). Forest and connectivity loss simplify tropical pollination networks. Oecologia, 192: 577-590. DOI: https://doi.org/10.1007/s00442-019-04579-7
Fisogni, A., Hautekèete, N., Piquot, Y., Brun, M., Vanappelghem, C., Ohlmann, M, et al. (2022). Seasonal trajectories of plant-pollinator interaction networks differ following phenological mismatches along an urbanization gradient. Landscape and Urban Planning, 226: 104512. DOI: https://doi.org/10.1016/j.landurbplan.2022.104512
Fortel, L., Henry, M., Guilbaud, L., Guirao, A.L., Kuhlmann, M., Mouret, H., et al. (2014). Decreasing abundance, increasing diversity and changing structure of the wild bee community (Hymenoptera: Anthophila) along an urbanization gradient. PLoS ONE, 9: e104679. DOI: https://doi.org/10.1371/journal.pone.0104679
Fortuna, M.A., Stouffer, D.B., Olesen, J.M., Jordano, P., Mouillot, D., Krasnov, B.R., et al. (2010). Nestedness versus modularity in ecological networks: Two sides of the same coin? Journal of Animal Ecology, 79: 811-817. DOI: https://doi.org/10.1111/j.1365-2656.2010.01688.x
García-Algarra, J., Pastor, J.M., Iriondo, J.M. & Galeano, J. (2017). Ranking of critical species to preserve the functionality of mutualistic networks using the k-core decomposition. PeerJ, 5: e3321. DOI: https://doi.org/10.7717/peerj.3321
Geslin, B., Gauzens, B., Thébault, E. & Dajoz, I. (2013). Plant Pollinator Networks along a Gradient of Urbanisation. PLOS ONE, 8: e63421. DOI: https://doi.org/10.1371/journal.pone.0063421
Giannini, T.C., Garibaldi, L.A., Acosta, A.L., Silva, J.S., Maia, K.P., Saraiva, A.M., et al. (2015). Native and Non-Native Supergeneralist Bee Species Have Different Effects on Plant-Bee Networks. PLOS ONE, 10: e0137198. DOI: https://doi.org/10.1371/journal.pone.0137198
Graf, L.V., Schneiberg, I. & Gonçalves, R.B. (2022). Bee functional groups respond to vegetation cover and landscape diversity in a Brazilian metropolis. Landscape Ecology, 37: 1075-1089. DOI: https://doi.org/10.1007/s10980-022-01430-y
Graf, L.V., Meyer, F.S., Jeronimo, F.F. & Gonçalves, R.B. (2025). Urbanization as a driver of changes in mutualistic networks between bees and plants. Urban Ecosystems, 28: 30. DOI: https://doi.org/10.1007/s11252-024-01639-6
Guimerà, R. & Amaral, L.A.N. (2005). Functional cartography of complex metabolic networks. Nature, 433: 895-900. DOI: https://doi.org/10.1038/nature03288
Haddad, N.M., Brudvig, L.A., Clobert, J., Davies, K.F., Gonzalez, A., Holt, R.D., et al. (2015). Habitat fragmentation and its lasting impact on Earth’s ecosystems. Science Advances, 1: e1500052. DOI: https://doi.org/10.1126/sciadv.1500052
Hagen, M., Kissling, W.D., Rasmussen, C., de Aguiar, M.A.M., Brown, L.E., Carstensen, D.W., et al. (2012). Biodiversity, Species Interactions and Ecological Networks in a Fragmented World. Advances in Ecological Research, 46: 89-210. DOI: https://doi.org/10.1016/B978-0-12-396992-7.00002-2
Hall, D.M., Camilo, G.R., Tonietto, R.K., Ollerton, J., Ahrné, K., Arduser, M., et al. (2017). The city as a refuge for insect pollinators. Conservation Biology, 31: 24-29. DOI: https://doi.org/10.1111/cobi.12840
Harrison, T. & Winfree, R. (2015). Urban drivers of plant-pollinator interactions. Functional Ecology, 29: 879-888. DOI: https://doi.org/10.1111/1365-2435.12486
Herrmann, J., Buchholz, S. & Theodorou, P. (2023). The degree of urbanisation reduces wild bee and butterfly diversity and alters the patterns of flower-visitation in urban dry grasslands. Scientific Reports, 13: 2702. DOI: https://doi.org/10.1038/s41598-023-29275-8
INEMA – Instituto do Meio Ambiente e Recursos Hídricos. Parque Metropolitano de Pituaçu – Histórico. Available at: https://www.ba.gov.br/inema/gestao-2/parques-metropolitanos/ parque-metropolitano-de-pituacu/historico. Accessed date: 19 Nov 2025.
Jordano, P. (1987). Patterns of mutualistic interactions in pollination and seed dispersal. American Naturalist, 129: 657-677. DOI: https://doi.org/10.1086/284665
Kaluza, B.F., Wallace, H.M., Heard, T.A., Minden, V., Klein, A. & Leonhardt, S.D. (2018). Social bees are fitter in more biodiverse environments. Scientific Reports, 8: 12353. DOI: https://doi.org/10.1038/s41598-018-30126-0
Kowarik, I. (2011). Novel urban ecosystems, biodiversity, and conservation. Environmental Pollution, 159: 1974-1983. DOI: https://doi.org/10.1016/j.envpol.2011.02.022
MapBiomas. (2023). Projeto MapBiomas – Coleção 7 da Série Anual de Mapas de Cobertura e Uso da Terra do Brasil. Available at: https://mapbiomas.org.
Marcacci, G., Westphal, C., Rao, V.S., Kumar S., S., Tharini, K.B., Belavadi, V., Noelke, N., Tscharntke, T. & Grass, I. (2023). Urbanization alters the spatiotemporal dynamics of plant-pollinator networks in a tropical megacity. Ecology Letters, 26: 1951-1962. DOI: https://doi.org/10.1111/ele.14324
Martins, A.C., Gonçalves, R.B. & Melo, G.A.R. (2013). Changes in wild bee fauna of a grassland in Brazil reveal negative effects associated with growing urbanization during the last 40 years. Zoologia, 30: 157-176. DOI: https://doi.org/10.1590/S1984-46702013000200006
McKinney, M.L. (2006). Urbanization as a major cause of biotic homogenization. Biological Conservation, 127: 247-260. DOI: https://doi.org/10.1016/j.biocon.2005.09.005
Michener, C. D. (2007). The bees of the world. 2nd ed. Baltimore: The Johns Hopkins University Press, 972p. DOI: https://doi.org/10.56021/9780801885730
Moreira, E.F., Boscolo, D. & Viana, B.F. (2015). Spatial heterogeneity regulates plant-pollinator networks across multiple landscape scales. PLOS One, 10: 1-19. DOI: https://doi.org/10.1371/journal.pone.0123628
Moure, J. S., Urban, D. & Melo, G. A. R. (2025). Catalog of Bees (Hymenoptera, Apoidea) in the Neotropical Region – online version. Available at: https://www.moure.cria.org.br/catalogue.
Normandin, É., Vereecken, N.J., Buddle, C.M. & Fournier, V. (2017). Taxonomic and functional trait diversity of wild bees in different urban settings. PeerJ, 5: e3051. DOI: https://doi.org/10.7717/peerj.3051
Oksanen, J., Simpson, G.L., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., et al. (2001). vegan: Community Ecology Package. DOI: https://doi.org/10.32614/CRAN.package.vegan
Olesen, J.M., Bascompte, J., Dupont, Y.L. & Jordano, P. (2007). The modularity of pollination networks. Proceedings of the National Academy of Sciences of the United States of America, 104: 19891-19896. DOI: https://doi.org/10.1073/pnas.0706375104
Ollerton, J., Winfree, R. & Tarrant, S. (2011). How many flowering plants are pollinated by animals? Oikos, 120: 321-326. DOI: https://doi.org/10.1111/j.1600-0706.2010.18644.x
Olsson, R.L., Brousil, M.R., Clark, R.E., Baine, Q. & Crowder, D.W. (2021). Interactions between plants and pollinators across urban and rural farming landscapes. Food Webs, 27. e00194. DOI: https://doi.org/10.1016/j.fooweb.2021.e00194
Pardee, G.L., Ballare, K.M., Neff, J.L., Do, L.Q., Ojeda, D., Bienenstock, E.J., et al. (2023). Local and landscape factors influence plant-pollinator networks and bee foraging behavior across an urban corridor. Land, 12: 362. DOI: https://doi.org/10.3390/land12020362
Patefield, W.M. (1981). Algorithm AS 159: An Efficient Method of Generating Random R × C Tables with Given Row and Column Totals. Applied Statistics, 30: 91. DOI: https://doi.org/10.2307/2346669
Pereira, J., Ribeiro, M.C., Battiston, F. & Jordán, F. (2022). Reconstruction and variability of tropical pollination networks in the Brazilian Atlantic Forest. Community Ecology, 23. DOI: https://doi.org/10.1101/2021.11.22.469524
Philpott, S.M., Pardee, G., Hsu, J., Kulikowski, A.J., Bichier, P., Liere, H., et al. (2025). Floral richness shapes plant-pollinator networks in urban agroecosystems. Basic and Applied Ecology, 88: 114-127. DOI: https://doi.org/10.1016/j.baae.2025.10.004
Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O. & Kunin, W.E. (2010). Global pollinator declines: Trends, impacts and drivers. Trends in Ecology and Evolution, 25: 345-353. DOI: https://doi.org/10.1016/j.tree.2010.01.007
Ramalho M., Silva M. & Carvalho, G. (2014). Pollinator Sharing in Specialized Bee Pollination Systems: a Test with the Synchronopatric Lip Flowers of Centrosema Benth (Fabaceae). Sociobiology, 61: 189-197. DOI: https://doi.org/10.13102/sociobiology.v61i2.189-197
R Core Team. (2025). R: A Language and Environment for Statistical Computing.
Santos, S.P. (2018). Atuação do Conselho Gestor no Parque Metropolitano de Salvador. Dissertação de Mestrado Profissional em Planejamento Ambiental – Universidade Católica do Salvador – UCSAL, 2018.
Sakagami, S.F., Laroca, S. & Moure, J.S. (1967). Wild bee biocoenotics in São Jose dos Pinhais (PR), South Brazil: preliminary report. Journal of the Faculty of Science Hokkaido University Series VI. Zoology, 16: 253-291.
Sebastián-González, E., Dalsgaard, B., Sandel, B. & Guimarães, P.R. (2015). Macroecological trends in nestedness and modularity of seed-dispersal networks: human impact matters. Global Ecology and Biogeography, 24: 293-303. DOI: https://doi.org/10.1111/geb.12270
Silva M., Ramalho M., Aguiar C.M.L. & Silva, M.D. (2015). Apifauna (Hymenoptera, Apoidea) em uma área de restinga arbórea-mata atlântica na costa atlântica do Nordeste do Brasil. Magistra, Cruz das Almas/BA. 27: 110-121.
Sheykhali, S., Fernández-Gracia, J., Traveset, A., Ziegler, M., Voolstra, C.R., Duarte, C.M., et al. (2020). Robustness to extinction and plasticity derived from mutualistic bipartite ecological networks. Scientific Reports, 10: 1-12. DOI: https://doi.org/10.1038/s41598-020-66131-5
Shochat, E., Lerman, S.B., Anderies, J.M., Warren, P.S., Faeth, S.H. & Nilon, C.H. (2010). Invasion, Competition, and Biodiversity Loss in Urban Ecosystems. BioScience, 60: 199-208. DOI: https://doi.org/10.1525/bio.2010.60.3.6
Simmons, B.I., Cirtwill, A.R., Baker, N.J., Wauchope, H.S., Dicks, L.V., Stouffer, D.B., et al. (2019). Motifs in bipartite ecological networks: uncovering indirect interactions. Oikos, 128: 154-170. DOI: https://doi.org/10.1111/oik.05670
Slaa, E.J., Sánchez Chaves, L.A., Malagodi-Braga, K.S. & Hofstede, F.E. (2006). Stingless bees in applied pollination: practice and perspectives. Apidologie, 37: 293-315. DOI: https://doi.org/10.1051/apido:2006022
Soares, K.O., Lima, M.V., Evangelista-Rodrigues, A., Silva, A.A.F., Silva, F.J.D.A., Lima, A.I.B.L.C., et al. (2021). Factors influencing the foraging behavior of Trigona spinipes (Apidae, Meliponinae). Biological Rhythm Research, 52: 1109-1119. DOI: https://doi.org/10.1080/09291016.2019.1616903
Suni, S., Hall, E., Bahu, E. & Hayes, H. (2022). Urbanization increases floral specialization of pollinators. Ecology and Evolution, 12: e8619. DOI: https://doi.org/10.1002/ece3.8619
Tavares-Brancher, K.P., Graf, L.V., Ferreira-Júnior, W.G., Faria, L.D.B. & Zenni, R.D. (2024). Plant-pollinator interactions in the Neotropics are affected by urbanization and the invasive bee Apis mellifera. Journal of Insect Conservation, 28: 1-11. DOI: https://doi.org/10.1007/s10841-024-00547-6
Theodorou, P. (2022). The effects of urbanisation on ecological interactions. Current Opinion in Insect Science, 52: 100922. DOI: https://doi.org/10.1016/j.cois.2022.100922
Theodorou, P., Albig, K., Radzevičiūtė, R., Settele, J., Schweiger, O., Murray, T.E. & Paxton, R. (2017). The structure of flower visitor networks in relation to pollination across an agricultural to urban gradient. Functional Ecology, 31: 12803. DOI: https://doi.org/10.1111/1365-2435.12803
Tylianakis, J.M., Laliberté, E., Nielsen, A. & Bascompte, J. (2010). Conservation of species interaction networks. Biological Conservation, 143: 2270-2279. DOI: https://doi.org/10.1016/j.biocon.2009.12.004
Rohr, R. P., Saavedra, S. & Bascompte, J. (2014). On the structural stability of mutualistic systems. science, 345: 1253497. https://doi.org/10.1126/science.1253497 DOI: https://doi.org/10.1126/science.1253497
Ulrich, W. & Gotelli, N.J. (2010). Null model analysis of species associations using abundance data. Ecology, 91: 3384-3397. DOI: https://doi.org/10.1890/09-2157.1
United Nations – World Population Prospects (2019) Highlights (ST/ ESA/SER A/423). Department of Economic and Social Affairs Population Division, New York, NY.
Valiente-Banuet, A., Aizen, M.A., Alcántara, J.M., Arroyo, J., Cocucci, A., Galetti, M., et al. (2015). Beyond species loss: The extinction of ecological interactions in a changing world. Functional Ecology, 29: 299-307. DOI: https://doi.org/10.1111/1365-2435.12356
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. DOI: https://doi.org/10.1016/j.landurbplan.2004.02.003
Downloads
Additional Files
Published
How to Cite
Issue
Section
License
Copyright (c) 2026 Maise Silva, Khatianne Correia-Reis, Cândida Maria Lima Aguiar, Emanuelle L. da Silva Brito
This work is licensed under a Creative Commons Attribution 4.0 International License.
Sociobiology is a diamond open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles in this journal without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.
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 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 permitted and encouraged 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 productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
eISSN 2447-8067
