Abstract
Despite the importance of parks and vegetation remnants in supporting the fauna in urban areas, not much is known about the structure of interaction networks of plants and pollinators occurring in these habitats. Hummingbirds are the main vertebrate pollinators in the Americas, contributing to the reproductive success of several plant species. The objective of this study was to evaluate the interactions between hummingbirds and the flowers used as resources in green areas within the city of Campo Grande, Brazil. We recorded a total of 63 interactions between six hummingbirds and 24 plant species. Fabaceae and Bignoniaceae were the most representative families, with seven and five species visited, respectively. Most of the visited species (75%) are native and common in urban ornamentation. The network of interactions was modular (Q = 0.481), presented an intermediate value of specialization (H2’ = 0.532) and a high core-periphery structure (CPness = 0.83). The plants Bauhinia variegata, Handroanthus heptaphyllus, Inga edulis, Prestonia tomentosa and Psiguria ternata, and the hummingbird Eupetomena macroura were the most central species in the network. In the dry period we recorded the greatest number of floral resources and the highest number of visits. The green areas within the municipality of Campo Grande offer resources that favor the permanence of hummingbirds in the city throughout the year, with native non-ornithophilous plants species characterized as important resources. The information presented here can be useful for understanding the structuring processes and the functioning of anthropically modified interactive communities.
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References
Arborday (2020) The Arbor Day Foundation and the Food and Agriculture Organization of the United Nations (FAO) Recognize Tree Cities of the World. https://www.arborday.org/media/pressreleases/pressrelease.cfm?id=471. Accessed 11 April 2020
Agostini K, Sazima M (2003) Ornamental plants and their resources for bees on the campus of the State University of Campinas, state of São Paulo. Brazil Bragantia 62:335–343. https://doi.org/10.1590/S0006-87052003000300001
Araujo AC, Sazima M (2003) The assemblage of flowers visited by hummingbirds in the “capões” of Southern Pantanal, Mato Grosso do sul, Brazil. Flora 198:1–9. https://doi.org/10.1078/0367-2530-00116
Araujo AC, González AMM, Sandel B et al (2018) Spatial distance and climate determine modularity in a cross-biomes plant–hummingbird interaction network in Brazil. J Biogeogr 4:1846–1858. https://doi.org/10.1111/jbi.13367
Baldock KC, Goddard MA, Hicks DM, Kunin WE, Mitschunas N, Osgathorpe, Potts SG, Robertson KM, Scott AV, Stone GN, Vaughan IP, Memmott J (2015) Where is the UK’s pollinator biodiversity? The importance of urban areas for flower-visiting insects. Proc. Natl Acad Sci USA 1:1–3. https://doi.org/10.1098/rspb.2014.2849
Barbosa-Filho WG, Araujo AC (2013) Flowers visited by hummingbirds in an urban Cerrado fragment, Mato Grosso do sul, Brazil. Biota Neotrop 13:4–5. https://doi.org/10.1590/S1676-06032013000400001
Batagelj V, Mrvar A (2004) Pajek - analysis and visualization of large networks. In: Jünger M, Mutzel P (eds) Graph drawing Software. Mathematics and visualization. Springer, Berlin, Heidelberg, pp 77–103. https://doi.org/10.1007/978-3-642-18638-7_4
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Beckett SJ (2016) Improved community detection in weighted bipartite networks. R Soc Open Sci 1:1–18. https://doi.org/10.1098/rsos.140536
Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. Ecology 6:1–12. https://doi.org/10.1186/1472-6785-6-9
Bogiani PA (2012) Interaction network between hummingbirds and flowers in the Pantanal do Miranda. Dissertation (Master in Ecology and Conservation) - Federal University of Mato Grosso do Sul. Campo Grande, MS
Buzato S, Sazima M, Sazima I (2000) Hummingbird-pollinated floras at three Atlantic Forest sites. Biotropica 32:824–841. https://www.jstor.org/stable/2663920
Cariveau D, Winfree R (2015) Causes of variation in wild bee responses to anthropogenic drivers. Curr Opin Insect Sci 1:104–109. https://www.10.1016/j.cois.2015.05.004
Carvalheiro LG, Biesmeijer JC, Benadi G et al (2014) The potential for indirect effects between co-flowering plants via shared pollinators depends on resource abundance, accessibility and relatedness. Ecol Lett 17:1389–1399. https://doi.org/10.1111/ele.12342
Danieli-Silva A, Souza JMT, Donatti AJ, Campos RP, Silva JV, Freitas L, Varassin IG (2012) Do pollination syndromes cause modularity and predict interactions in a pollination network in tropical high-altitude grasslands? Oikos 121:35–43. https://doi.org/10.1111/j.1600-0706.2011.19089.x
Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analysing ecological networks. R News 8:8–11
Faegri K, Van der pijl L (1976) The principles of pollination ecology. Pergamon Press 3:248. https://doi.org/10.1016/C2009-0-00736-3
Flora of Brazil under construction (2020) Botanical Garden of Rio de Janeiro. Available at: http://floradobrasil.jbrj.gov.br/. Accessed 10 August 2018
Fournier LA (1974) A quantitative method for the measurement of phenological characteristics in trees. Turrialba 24:422–423
Fonseca LN, Vizentin-Bugoni J, Rech AR, Alves MS (2015) Plant-hummingbird interactions and temporal nectar availability in a restinga from brazil. An Acad Bras Cienc 87:1–14. https://doi.org/10.1590/0001-3765201520140349
Fründ J, McCann KS, Williams NM (2016) Sampling bias is a challenge for quantifying specialization and network structure: lessons from a quantitative niche model. Oikos 125:502–513. https://doi.org/10.1111/oik.02256
Gallagher RJ, Young JG, Welles BF (2021) A clarified typology of core-periphery structure in networks. Sci Adv 7:1–21. https://doi.org/10.48550/arXiv.2005.10191
Genini J, Morellato LPC, Guimarães PR, Olesen JM (2010) Cheaters in mutualism networks. Biol Lett 6:494–497. https://doi.org/10.1098/rsbl.2009.1021
Grantsau R (1989) The hummingbirds of Brazil. Expression and Culture 2:234
Guedes-Bruni RR, Morim MP, Lima HC, Silvestre LS (2002) Floristic inventory. Methods for botanical studies in the Atlantic Forest. Seropédica, Rio de Janeiro 24–49
IBGE (2018) Territorial division of Brazil and territorial limits. Available at: <https://cidades.ibge.gov.br/brasil/ms/campo-grande/panorama. Accessed 11 March 2018
Irwin RE, Bronstein JL, Manson JS, Richardson L (2010) Nectar robbing: ecological and evolutionary perspectives. Annu Rev Ecol Evol Syst 41:271–292. https://doi.org/10.1146/annurev.ecolsys.110308.120330
Johansen DA (1940) Plant microtechnique. Mcgraw-Hill book, New York, p 523
Li D, Stucky BJ, Deck J, Baiser B, Guralnick RP (2019) The effect of urbanization on plant phenology depends on regional temperature. Nat Ecol Evol 3:1661–1667. https://doi.org/10.1038/s41559-019-1004-1
Machado CG, Coelho AG, Santana CS, Rodrigues M (2007) Hummingbirds and their floral resources in a rocky countryside area of Chapada Diamantina, Bahia. Rev Bras Ornitol 15:215–227. https://doi.org/10.1590/S1519-69842011000400005
Machado CG (2009) Hummingbirds (Aves: Trochilidae) and their floral resources in an area of Caatinga da Chapada Diamantina. Bahia Brazil Zoologia (Curitiba) 26:255–265. https://doi.org/10.1590/S1984-46702009000200008
Machado AO (2012) Diversity of floral resources for hummingbirds in the cerrados of the mining triangle and region. Dissertation (Doctorate in Ecology) - Federal University of Uberlândia. Uberlândia, Minas Gerais. 1, 117
Machado CG (2014) The hummingbird community and the plants they visit in an area of thin cerrado in Chapada Diamantina, Bahia, Brazil. Biosci J 30:1578–1587. https://doi.org/10.1590/bjb.2014.0097
Machado AO, Oliveira PE (2015) β-Diversity of hummingbird plants in Cerrado areas of Central Brazil. Rodriguésia 66:001–019. https://doi.org/10.1590/2175-7860201566101
Marcon AP (2016) Interactions of your hummingbirds and their floral resources in an anthropized environment in southern Brazil. Ornithological news 1:18–24
Martín-González AM, Dalsgaard B, Nogués‐Bravo D et al (2015) The macroecology of phylogenetically structured hummingbird–plant networks. Global Ecol Biogeogr 24, 1212–1224. https://doi.org/10.1111/geb.12355
Martín-González AM, Vazquez DP, Ramos-Jiliberto R, Lee SH, Miele V (2020) Core-periphery structure in mutualistic networks: an epitaph for nestedness? bioRxiv. https://doi.org/10.1101/2020.04.02.021691
Martin-González AM, Allesina S, Rodrigo A, Bosch J (2012) Drivers of compartmentalization in a Mediterranean pollination network. Oikos 121(12):2001–2013. https://doi.org/10.1111/j.1600-0706.2012.20279.x
Maruyama PK, Oliveira GM, Ferreira C, Dalsgaard B, Oliveira PE (2013) Pollination syndromes ignored: importance of non-ornithophilous flowers to neotropical savanna hummingbirds. Naturwissenschaften 100:1061–1068. https://doi.org/10.1007/s00114-013-1111-9
Maruyama PK, Vizentin-Bugoni J, Oliveira GM, Oliveira PE, Dalsgaard B (2014) Morphological and spatio-temporal mismatches shape a neotropical savana plant-hummingbird network. Biotropica 46:740–747. https://doi.org/10.1111/btp.12170
Maruyama PK, Sonne J, Vizentin-Bugoni J et al (2018) Functional diversity mediates macroecological variation in plant-hummingbird interaction networks. Glob Ecol Biogeogr 27:1186–1199. https://doi.org/10.1111/geb.12776
Maruyama PK, Bonizário C, Marcon AP et al (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
Mendonça LB, Anjos L (2003) Bird-flower interactions in Brazil: a review. Ararajuba Seropédica 11:195–205
Mendonça LB, Anjos L (2005) Hummingbirds (Aves, Trochilidae) and their floral resources in an urban area of southern Brazil. Rev Bras Zool 22:51–59. https://doi.org/10.1590/1519-6984.223723
Miele V, Ramos-Jiliberto R, Vázquez DP (2020) Core–periphery dynamics in a plant–pollinator network. J Anim Ecol 89:1670–1677. https://doi.org/10.1111/1365-2656.13217
Neil K, Wu J (2006) Effects of urbanization on plant flowering phenology: a review. Urban Ecosyst 9(3):243–257. https://doi.org/10.1007/s11252-006-9354-2
Nishida SM, Naide SS, Pagnin D (2014) Plants that attract birds and other animals. 1. ed. São Paulo: Academic Culture, 2014. (PROEX Digital-UNESP Collection). Available at: http://hdl.handle.net/11449/126246
Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. Proc. Natl Acad Sci USA 104:19891–19896. 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. https://doi.org/10.1111/j.1600-0706.2010.18644.x
Pestana LTC, Alves FM, Sartori AL (2011) Tree species from urban afforestation in the center of the municipality of Campo Grande, Mato Grosso do Sul, Brazil. Brazilian Society of Urban Forestry Magazine - Revsbau, Piracicaba, 6:01–21. https://doi.org/10.5380/revsbau.v6i3.66471
Raguso RA, Gottsberger G (2017) An ode to osmophores: Stefan Vogel’s seminal contributions to the study of scent. Flora 232:150–152
R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Available at https://www.r-project.org/. Accessed 5 August 2019
Rodrigues LC, Araujo AC (2011) The hummingbird community and their floral resources in an urban forest remnant in Brazil. Braz J Biol 71:611–622. https://doi.org/10.1016/j.flora.2017.02.014
Rocca MA, Machado CG (2010) Protocols for the study of pollination by birds. In: Von Matter S, Straube FC, Accordi IA, Piacentini V, Candido-Jr. JF. Ornitology and conservation: applied science, research, and survey techniques. Rio de Janeiro: Technical Books 1:471–490
Seleme EP, Sartori AB (2009) Floristics and syndromes of dispersion of tree and shrub species in a cerradão in Campo Grande, Mato Grosso do sul. Agroecology notebooks 4:1–4
Semadur (2010) Municipal secretariat for the environment and urban development. Master plan for urban afforestation of Campo Grande, MS (PDAU). Campo Grande: Semadur, 2010. Available at: http://www.capital.ms.gov.br/egov/downloadfile.php?id=3103&filefield=arquivo_dow&table = downloads & key = id_dow & acronym_sec = dpsa>. Accessed 02 October 2019
Shepherdson JP (2018) Observations of territorial behavior of the Antillean Crested Hummingbird (Orthorhyncus cristatus) on St. Eustatius. J Caribb Ornithol 31:48–50
Sick H (1997) Brazilian ornithology. New frontier. Rio de Janeiro 3:206–258
Stiles FG (1981) Geographical aspects of bird-flower coevolution, with particular reference to Central America. Ann Missouri Bot 68:323–351. https://doi.org/10.2307/2398801
Tylianakis JM, Morris RJ (2017) Ecological networks across environmental gradients. Annu Rev Ecol Evol 48:25–48. https://doi.org/10.1146/annurev-ecolsys-110316-022821
Vázquez DP, Morris WF, Jordano P (2005) Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecol Lett 8(10):1088–1094. https://doi.org/10.1111/j.1461-0248.2005.00810.x
Vázquez DP, Aizen MA (2004) Asymmetric specialization: a pervasive feature of plant–pollinator interactions. Ecology 85(5):1251–1257. https://doi.org/10.1890/03-3112
Vizentin-Bugoni J, Maruyama PK, Debastiani VJ, Duarte LDS, Dalsgaard B, Sazima M (2016) Influences of sampling effort on detected patterns and structuring processes of a neotropical plant–hummingbird network. J Anim Ecol 85(1):262–272. https://doi.org/10.1111/1365-2656.12459
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We thank the Graduate Program in Plant Biology (PPGBV/UFMS); CAPES (Coordination for the Improvement of Higher Education Personnel) for the master’s scholarship to VAN (88882.461308/2019-01); FAPEMIG (Minas Gerais State Agency for Research and Development) for a postdoc fellowship for CSS (RED-00253-16); CNPq (National Council for Scientific and Technological Development) for a research fellowship to ACA (307991/2021-0). Ângela Sartori, Flávio Alves and Geraldo Damasceno identified the botanical material, and Pedro Isaac helped in fieldwork. Camila Aoki, Erich Fischer, and Pietro Maruyama provided constructive comments and suggestions on early versions of the manuscript.
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VAN received a MSc fellowship from CAPES (Coordination for the Improvement of Higher Education Personnel - #88882.461308/012019). FAPEMIG (Minas Gerais State Agency for Research and Development) provided a postdoctoral fellowship for CSS (RED-00253-16) and CNPq (National Council for Scientific and Technological Development) provided a research fellowship for ACA (#307991/2021-0).
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Nakamura, V.A., Souza, C.S. & Araujo, A.C. Mass-flowering native species are key in the structure of an urban plant-hummingbird network. Urban Ecosyst 26, 929–940 (2023). https://doi.org/10.1007/s11252-023-01346-8
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DOI: https://doi.org/10.1007/s11252-023-01346-8