Abstract
Alien plants may provide considerable benefits to biodiversity in urban areas while showing low to moderate risk of negative impacts. Here, we evaluated the ecological role of the alien tree Bombax ceiba when interacting with nectar-feeding birds, including its potential for negative impacts as an invasive plant in an urban area in Brazil. At the community level, network analysis of 70 bird species interacting with flowers from 73 plant species showed B. ceiba to be one of the few "hub" plant species, indicating its importance as a nectar resource for urban birds. Specifically, B. ceiba flowers attracted 38 bird species with different habits (feeding guilds and habitat requirements), most of which fed on nectar, while some also consumed floral parts. On the other hand, the semiquantitative risk assessment for B. ceiba regarding potential negative impacts on native species and ecosystems indicated only a moderate risk, suggesting an overall benefit of keeping this tree species in the urban landscape. In this context, we highlight that the function, not only the origin of a species, may be used to plan "biophilic" cities through urban greening. Moreover, possible suppression of alien plants should consider the ecological role these species play in urban areas. Given that proper assessment of risk factors is carried out, urban afforestation with some alien plant species can promote biodiversity and ecosystem services by providing key resources during food scarcity for the fauna.
Similar content being viewed by others
Availability of data and material
Data are available as supplementary material. Any queries should be directed to the first author.
Code availability (software application or custom code)
Not applicable.
References
Aizen MA, Morales CL (2020) Impacts of nonnative plants on plant-pollinator interactions. In: Traveset A, Richardson DM (eds) Plant Invasion: The role of biotic interactions. CABI, Wallingford, pp 241–255. https://doi.org/10.1079/9781789242171.0241
Alvey AA (2006) Promoting and preserving biodiversity in the urban forest. Urban For Urban Green 5(4):195–201. https://doi.org/10.1016/j.ufug.2006.09.003
Araújo FP, Barbosa AAA, Oliveira PE (2011) Floral resources and hummingbirds on an island of flooded forest in Central Brazil. Flora 206(9):827–835. https://doi.org/10.1016/j.flora.2011.04.001
Aronson MFJ, LaSorte FA, Nilon CH et al (2014) A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drives. Proc R Soc Lond B 281(1780):20133330. https://doi.org/10.1098/rspb.2013.3330
Aslan CE, Rejmánek M (2010) Avian use of introduced plants: ornithologist records illuminate interspecific associations and research needs. Ecol Appl 20(4):1005–1020. https://doi.org/10.1890/08-2128.1
Beckett SJ (2016) Improved community detection in weighted bipartite networks. R Soc Open Sci 3(1):140536. https://doi.org/10.1098/rsos.140536
Berthon K, Thomas F, Bekessy S (2021) The role of “nativeness” in urban greening to support animal biodiversity. Landsc Urban Plan 205:103959. https://doi.org/10.1016/j.landurbplan.2020.103959
Bhattacharya A, Mandal S (2000) Pollination biology in Bombax ceiba Linn. Curr Sci 79:1706–1712
Blackburn TM, Essl F, Evans T et al (2014) A unified classification of alien species based on the magnitude of their environmental impacts. PLoS Biol 12(5):e1001850. https://doi.org/10.1371/journal.pbio.1001850
Blanco G, Hiraldo F, Tella JL (2018) Ecological functions of parrots: An integrative perspective from plant life cycle to ecosystem functioning. Emu 118(1):36–49. https://doi.org/10.1080/01584197.2017.1387031
Chace JF, Walsh JJ (2006) Urban effect on native birds: a review. Landsc Urban Plan 74(1):46–69. https://doi.org/10.1016/j.landurbplan.2004.08.007
Conser C, Seebacher L, Fujino DW, Reichard S, DiTomaso JM (2015) The development of a plant risk evaluation (PRE) tool for assessing the invasive potential of ornamental plants. PLoS One 10(3):e0121053. https://doi.org/10.1371/journal.pone.0121053
Corlett RT (2005) Interaction between birds, fruit bats and exotic plants in urban Hong Kong, south China. Urban Ecosyst 8(3):275–283. https://doi.org/10.1007/s11252-005-3260-x
Cronk Q, Ojeda I (2008) Bird-pollinated flowers in an evolutionary and molecular context. J Exp Bot 59(4):715–727. https://doi.org/10.1093/jxb/ern009
Cruden RW, Hermann SM (1983) Studying nectar? Some observations on the art. In: Bently B, Elias T (eds) The biology of nectaries. Columbia University Press, New York, pp 223–241
Deshpande P, Sharm R, Lehikoinen A, Thorogood R (2023) Native fauna interact differently with native and alien trees in a tropical megacity. Sci Total Environ 868:161683. https://doi.org/10.1016/j.scitotenv.2023.161683
Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite Package: Analysing Ecological Networks. R News 8:8–11
Filardi FLR, Barros F, Baumgratz JFA et al (2018) Brazilian flora 2020: innovation and collaboration to meet target 1 of the global strategy for plant conservation (GSPC). Rodriguesia 69(4):1513–1527. https://doi.org/10.1590/2175-7860201869402
Francisco MR, Lunardi VO, Galetti M (2002) Massive seed predation of Pseudobombax grandiflorum (Bombacaceae) by parakeets Brotogeris versicolurus (Psittacidae) in a forest fragment in Brazil. Biotropica 34(4):613–615. https://doi.org/10.1111/j.1744-7429.2002.tb00582.x
Francisco MR, Lunardi VO, Guimaraes PR Jr, Galetti M (2008) Factors affecting seed predation of Eriotheca gracilipes (Bombacaceae) by parakeets in a Cerrado fragment. Acta Oecol 33(2):240–245. https://doi.org/10.1016/j.actao.2007.11.002
Franklin DC (1999) Opportunistic nectarivory: an annual dry season phenomenon among birds in monsoonal Northern Australia. Emu 99(2):135–141. https://doi.org/10.1071/MU99016
Freitas WK, Magalhães LMS, Santana CAA, Pereira RE Jr, Souza LCM, Toledo RAB, Garção BR (2020) Tree composition of urban public squares located in the Atlantic Forest of Brazil: a systematic review. Urban For Urban Green 48:126555. https://doi.org/10.1016/j.ufug.2019.126555
Goodenough AE (2010) Are the ecological impacts of alien species misrepresented? A review of the “native good, alien bad” philosophy. Comm Ecol 11(1):13–21. https://doi.org/10.1556/ComEc.11.2010.1.3
Gray ER, van Heezik Y (2016) Exotic trees can sustain native birds in urban woodlands. Urban Ecosyst 19(1):315–329. https://doi.org/10.1007/s11252-015-0493-1
Hanisch E, Johnston R, Longnecker N (2019) Cameras for conservation: wildlife photography and emotional engagement with biodiversity and nature. Hum Dimens Wildl 24(3):267–284. https://doi.org/10.1080/10871209.2019.1600206
Hassan OM (2018) Leaf litter of Bombax ceiba L. threatens plant cover and floristic diversity in a new urban ecosystem. Flora 242:22–30. https://doi.org/10.1016/j.flora.2018.03.004
Horta MB, Bhakti T, Cordeiro PF, Carvalhoribeiro SM, Fernandes GW, Goulart F (2018) Functional connectivity in urban landscapes promoted by Ramphastos toco (Toco Toucan) and its implications for policy making. Urban Ecosyst 21(6):1097–1111. https://doi.org/10.1007/s11252-018-0789-z
Jain V, Verma SK, Sharma SK, Katewa SS (2011) Bombax ceiba Linn.: as an umbrella tree species in forests of southern Rajasthan. India. Res J Environ Sci 5(8):722–729. https://doi.org/10.3923/rjes.2011.722.729
Johnson SD, Nicolson SW (2008) Evolutionary associations between nectar properties and specificity in bird pollination systems. Biol Lett 4(1):49–52. https://doi.org/10.1098/rsbl.2007.0496
Kendle AD, Rose J-E (2000) The aliens have landed! What are the justifications for “native only” policies in landscape plantings? Landsc Urban Plann 47(1–2):19–31. https://doi.org/10.1016/S0169-2046(99)00070-5
Khanduri VP, Kumar KS (2017) Reproductive effort and success in Bombax ceiba L. in a tropical forest of Mizoram, Indo-Burma region of North-East India. Braz J Bot 40(1):157–166. https://doi.org/10.1007/s40415-016-0327-2
Krebs JC (1989) Ecological Methodology. Harper Collins Publishers Inc, New York
Kumar Rai P, Singh JS (2020) Invasive alien plant species: their impact on environment, ecosystem services and human health. Ecol Indic 111:106020. https://doi.org/10.1016/j.ecolind.2019.106020
Lorenzi H, Bacher LB, Torres MAV (2018) Árvores e arvoretas exóticas no Brasil: madeiras, ornamentais e aromáticas. Instituto Plantarum de Estudo da Flora, Nova Odessa
Liu J, Slik F (2022) Are street trees friendly to biodiversity? Landsc Urban Plan 218:104304. https://doi.org/10.1016/j.landurbplan.2021.104304
Luck GW, Davidson P, Boxall D, Smallbone L (2011) Relations between urban bird and plant communities and human well-being and connection to nature. Conserv Biol 25(4):816–826. https://doi.org/10.1111/j.1523-1739.2011.01685.x
Maruyama PK, Bonizário C, Marcon AP, D’Angelo G, Silva MM, Silva Neto EN, Marçal O Jr (2019) Plant-hummingbird interaction networks in urban areas: generalization and the importance of trees with specialized flowers as a nectar resource for pollinator conservation. Biol Conserv 230:187–194. https://doi.org/10.1016/j.biocon.2018.12.012
McDonald R, Beatley T (2021) Biophilic cities: vision and emerging principles. In: McDonald R, Beatley T (eds) Biophilic Cities for an Urban Century: Why Nature is Essential for Success of Cities. Palgrave Pivot, Cham, pp 63–85. https://doi.org/10.1007/978-3-030-51665-9_5
McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127(3):247–260. https://doi.org/10.1016/j.biocon.2005.09.005
Mendes-Rodrigues C, Oliveira PE, Marinho RC, Romero R, Ranal MA (2019) Are the alien species of Melastomataceae and Bombacoideae a potential risk for Brazilian Cerrado? Open Acc Lib J 6(3):e5156. https://doi.org/10.4236/oalib.1105156
Moreira JL, Ribas-Hernández P, Lobo JA (2017) Toucans (Ramphastos ambiguus) facilitate resilience against seed dispersal limitation to a large-seeded tree (Virola surinamensis) in a human-modified landscape. Biotropica 49(4):502–510. https://doi.org/10.1111/btp.12427
Moro MF, Westerkamp C, de Araújo FS (2014) How much importance is given to native plants in cities’ treescape? A case study in Fortaleza. Brazil Urban for Urban Green 13(2):365–374. https://doi.org/10.1016/j.ufug.2014.01.005
Nackley LL, West AG, Skowno AL, Bond WJ (2017) The nebulous ecology of native invasions. Trends Ecol Evol 32(11):814–824. https://doi.org/10.1016/j.tree.2017.08.003
Nascimento VT, Agostini K, Souza CS, Maruyama PK (2020) Tropical urban areas support highly diverse plant-pollinator interactions: An assessment from Brazil. Landsc Urban Plann 198:103801. https://doi.org/10.1016/j.landurbplan.2020.103801
Nghiem TPL, Wong KL, Jeevanandam L, Chang CC, Tan LYC, Goh L, Carrasco LR (2021) Biodiverse urban forests, happy people: Experimental evidence linking perceived biodiversity, restoration, and emotional wellbeing. Urban For Urban Green 59:127030. https://doi.org/10.1016/j.ufug.2021.127030
Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. Proc Natl Acad Sci USA 104(50):19891–19896. https://doi.org/10.1073/pnas.0706375104
Pacheco JF, Silveira LF, Aleixo A et al (2021) Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee—second edition. Ornithol Res 29(1):94–105. https://doi.org/10.1007/s43388-021-00058-x
Panlasigui S, Spotswood E, Beller E, Grossinger R (2021) Biophilia beyond the building: applying the tools of urban biodiversity planning to create biophilic cities. Sustainability 13(5):2450. https://doi.org/10.3390/su13052450
Patefield WM (1981) Algorithm AS159. An efficient method of generating r x c tables with given row & column totals. Appl Stat 30(1):9–97. https://doi.org/10.2307/2346669
Peres CA (2000) Identifying keystone plant resources in tropical forests: the case of gums from Parkia pods. J Trop Ecol 16(2):287–317. https://doi.org/10.1017/S0266467400001413
Peters WE, Carlos TA, Mello MAR, Rice RA, Tallamy DW, Caudill SA, Fleming TH (2016) Using plant-animal interactions to inform tree selection in tree-based agroecosystems for enhanced biodiversity. Bioscience 66(12):1046–1056. https://doi.org/10.1093/biosci/biw140
Pyšek P, Pergl J, Essl F et al (2017) Naturalized alien flora of the world: species diversity, taxonomic and phylogenetic patterns, geographic distribution and global hotspots of plant invasion. Preslia 89(3):203–274
Pyšek P, Jarošík V, Hulme PE, Pergl J, Hejda M, Schaffner U, Vilà M (2012) A global assessment of alien invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species’ traits and environment. Global Change Biol 18(5):1725–1737. https://doi.org/10.1111/j.1365-2486.2011.02636.x
R Development Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org
Raju AJS, Rao SP, Rangaiah K (2005) Pollination by bats and birds in the obligate outcrosser Bombax ceiba L. (Bombacaceae), a tropical dry season flowering tree species in the Eastern Ghats forests of India. Ornithol Sci 4(1):81–87. https://doi.org/10.2326/osj.4.81
Ramsden L, Ho PY (1995) Regeneration of Bombax ceiba L. in Hong Kong. Memo Hong Kong Nat Hist Soc 20:223–231
Richardson DM, Pyšek P, Rejmánek M, Barbour MG, Panetta FD, West CJ (2000) Naturalization and invasion by alien plants: concepts and definition. Divers Distrib 6(2):93–107. https://doi.org/10.1046/j.1472-4642.2000.00083.x
Richardson DM, Rejmánek M (2011) Trees and shrubs as invasive alien species, a global review. Divers Distrib 17(5):788–809. https://doi.org/10.1111/j.1472-4642.2011.00782.x
Riley CB, Herms DA, Gardiner MM (2018) Exotic trees contribute to urban forest diversity and ecosystem services in inner-city Cleveland, OH. Urban for Urban Green 29:367–376. https://doi.org/10.1016/j.ufug.2017.01.004
Rocca MA, Sazima M (2010) Beyond hummingbird-flowers: the other side of ornithophily in the Neotropics. Oecol Aust 14(1):67–99. https://doi.org/10.4257/oeco.2010.1401.03
Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasion 8:927–939. https://doi.org/10.1007/s10530-005-5103-3
Şekercioğlu ÇH (2002) Impacts of birdwatching on human and avian communities. Environ Conserv 29(3):282–289. https://doi.org/10.1017/S0376892902000206
Şekercioğlu ÇH (2006) Increasing awareness of avian ecological function. Trends Ecol Evol 21(8):464–471. https://doi.org/10.1016/j.tree.2006.05.007
Sick H (1997) Ornitologia Brasileira. Editora Nova Fronteira, Rio de Janeiro
Silva JMC (1995) Birds of the Cerrado region, South America. Steenstrupia 21:69–92
Silva PA (2018) Bird-flower interactions in an urban area: Ceiba pubiflora provides nectar and promotes biodiversity in the city. Urban for Urban Green 36:42–49. https://doi.org/10.1016/j.ufug.2018.10.003
Silva PA (2019) Flower eating by the Toco Toucan (Ramphastos toco) in an anthropogenic landscape during the dry season. Ornitol Neotrop 30:51–55
Silva PA, Silva LL, Brito L (2020) Using bird-flower interactions to select native tree resources for urban afforestation: the case of Erythrina velutina. Urban For Urban Green 51:126677. https://doi.org/10.1016/j.ufug.2020.126677
Sjöman H, Morgenroth J, Sjöman JD, Sæbø A (2016) Diversification of the urban forest—Can we afford to exclude exotic tree species? Urban for Urban Green 18:237–241. https://doi.org/10.1016/j.ufug.2016.06.011
Tella JL, Hiraldo F, Pacífico E, Díaz-Luque JÁ, Dénes FV, Fontoura FM, Guedes N, Blanco G (2020) Conserving the diversity of ecological interactions: The role of two threatened macaw species as legitimate dispersers of “megafaunal” fruits. Diversity 12(2):45. https://doi.org/10.3390/d12020045
Terborgh J (1986) Keystone plant resources in the tropical forest. In: Soulé ME (ed) Conservation Biology: The Science of Scarcity and Diversity. Sinauer Associates, Sunderland, pp 330–344
van Kleunen M, Pyšek P, Dawson W et al (2019) The global naturalized alien flora (GloNAF) database. Ecology 100(1):e02542. https://doi.org/10.1002/ecy.2542
Vitorino BD, Frota AVB, Maruyama PK (2021) Ecological determinants of interactions as key when planning pollinator-friendly urban greening: a plant-hummingbird network example. Urban For Urban Green 2021:127298. https://doi.org/10.1016/j.ufug.2021.127298
Westerkamp C (1990) Bird-flowers: hovering versus perching exploitation. Bot Acta 103(4):366–371. https://doi.org/10.1111/j.1438-8677.1990.tb00176.x
Wood EM, Esaian S (2020) The importance of street trees to urban avifauna. Ecol Appl 30(7):e02149. https://doi.org/10.1002/eap.2149
Zar H (1999) Biostatistical Analysis, 4th edn. Prentice-Hall Inc, Upper Saddle River
Zenni RD, Ziller SR (2011) An overview of invasive plants in Brazil. Braz J Bot 34(3):431–446. https://doi.org/10.1590/S0100-84042011000300016
Acknowledgements
We thank Camila S. Souza for her help with the network figure. We also thank an anonymous reviewer and the associate editor, J. Kollmann, for suggestions that improved the presentation of our study. The first author dedicates this paper to his mother (In Memoriam).
Funding
This study is part of an independent project conducted by the first author over many years. Although aided by researchers with support from Coordination for Higher Education Staff Development, CAPES (i.e., LLS and BMR), this investigation, in particular, did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. PKM had funding from Fundação de Amparo à Pesquisa do Estado de Minas Gerais - FAPEMIG (RED-00253-16 and APQ-01151-22).
Author information
Authors and Affiliations
Contributions
PAS contributed to the research conception and design. PAS, AGC, ACSG, LLS, LB, and BMR collected the data. PAS and PKM performed data analysis and wrote the first draft of the manuscript. All authors commented on the manuscript and approved the final version.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors have no relevant financial or nonfinancial interest to disclose.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Silva, P.A., Cherutte, A.G., Gomes, A.C.S. et al. The ecological role and potential impact of an alien tree highly attractive to native nectar-feeding birds in urban areas. Urban Ecosyst 26, 1029–1040 (2023). https://doi.org/10.1007/s11252-023-01345-9
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11252-023-01345-9