Caio C. C. Missagia, Cassio J. O. Mendes, Maria Alice S. Alves
{"title":"Performance of pollinators of the tropical bromeliad <i>tillandsia stricta</i> sol. (Bromeliaceae) in the Atlantic Forest, Rio de Janeiro","authors":"Caio C. C. Missagia, Cassio J. O. Mendes, Maria Alice S. Alves","doi":"10.1080/17550874.2023.2261927","DOIUrl":null,"url":null,"abstract":"ABSTRACTBackground Most bromeliad (Bromeliaceae) species have specialised flowers for specific pollinators, establishing a mutualistic relationship. However, other animals may also pollinate bromeliads, though it is logical to assume that specialised flowers are more compatible with one specific group of pollinators.Aims We compared the performance of a hummingbird (Thalurania glaucopis) and a butterfly (Heliconius erato) as pollinators of flowers classified as ornithophilous of the bromeliad Tillandsia stricta (Bromeliaceae).Methods We applied the single visit method with seed counting, and measured corolla tube length of flowers. We also conducted observations on plants to determine the effectiveness of pollination by the hummingbird and the butterfly.Results Both animal species pollinated flowers, although the hummingbird was a more frequent and effective pollinator, resulting in greater seed production. The corolla tube length of T. stricta was a significant predictor of seeds produced per flower following interactions with the hummingbird, but not with the butterfly.Conclusion Our results indicate a more intimate flower – pollinator relationship between T. stricta and the hummingbird than the butterfly in this population of the bromeliad in Rio de Janeiro, Brazil.KEYWORDS: Atlantic ForestBrazilBromeliaceaefloral syndromehummingbirdspollinationDisclaimerAs a service to authors and researchers we are providing this version of an accepted manuscript (AM). Copyediting, typesetting, and review of the resulting proofs will be undertaken on this manuscript before final publication of the Version of Record (VoR). During production and pre-press, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal relate to these versions also. AcknowledgementsResearch in Pedra Branca State Park (PEPB: Parque Estadual da Pedra Branca) was authorised by the Rio de Janeiro State Environment Institute (INEA: Instituto Estadual do Ambiente) through permit number 008/2015. The authors thank PEPB for logistical support. They are also grateful to Stephen Ferrari for his review of the English text. The authors also thank the editors (including the subject editor, Richard Abbott) and the anonymous reviewers for the valuable contributions which greatly improved the manuscript. Funding for this study was provided by the Brazilian Coordination for Higher Education Personnel Training (CAPES: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) by granting C.C.C.M. a doctoral research scholarship and C.J.O.M with a master’s scholarship (this study was financed in part by CAPES—Finance Code 001). The Rio de Janeiro State Research Foundation (FAPERJ: Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro) provided C.C.C.M. with a grant (DSC-10 process E_01/201.955/2017) and supported the research of M.A.S.A. (CNE processes E-26/203191/2015, E-26/202.835/2018, E-26/201126/2022). The Brazilian National Research Council (CNPq: Conselho Nacional de Desenvolvimento Científico e Tecnológico) provided M.A.S.A. with a research fellowship (PQ processes 305798/2014-6, 306.579/2018-9, 308615/2022-0), who was also supported by a productivity fellowship from Rio de Janeiro State University (Prociência, UERJ/FAPERJ).Authors’ contributionsCCCM conceived the study and designed the methods; CCCM collected the data; CCCM and CJOM analysed the data; CCCM and CJOM led the writing of the manuscript. MASA participated in the writing, contributing with important intellectual content and revision, and financial support through her research grants. All the authors contributed fundamentally to the drafts and gave final approval for publication.Declaration of interest statementThe corresponding author confirms that this work does not present any type of conflict of interest.Data archiving statementThe data were published in the Zenodo Repository (DOI: 10.5281/zenodo.6299296), with a one-year embargo (until December 31 2023).Figure 1. Inflorescence of Tillandsia stricta (Bromeliaceae) with available flowers (purple) for visitors. Photograph: XXX.Display full sizeFigure 2. Corolla tube length of the flowers of Tillandsia stricta (Bromeliaceae) visited by hummingbirds (Thalurania glaucopis) and butterflies (Heliconius erato) in Pedra Branca State Park, Rio de Janeiro, Brazil.Display full sizeFigure 3. Relationship between the corolla tube length and seed production of Tillandsia stricta (Bromeliaceae) following interactions with hummingbirds (Thalurania glaucopis) in Pedra Branca State Park, Rio de Janeiro, Brazil.Display full sizeReferences Aizen MA, Harder LD. 2007. Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology, 88(2), 271–281. https://doi.org/10.1890/06-1017 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Almeida JM, Missagia CCC, Alves, MAS., Jia, Z-Y. 2022. Effects of the availability of floral resources and neighboring plants on nectar robbery in a specialized pollination system. Current Zoology, 68(5), 541–548. 10.1093/cz/zoab083 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Altmann J. 1974. Observational study of behavior: sampling. Behaviour, 49(3), 227–267. https://doi.org/10.1080/14794802.2011.585831 [Taylor & Francis Online] [PubMed] [Web of Science ®], [Google Scholar] Aguilar-Rodríguez PA, MacSwiney GMC, Krömer T, García-Franco JG., Knauer A, Kessler M. 2014. First record of bat-pollination in the species-rich genus Tillandsia (Bromeliaceae). Ann Bot, 113(6), 1047–1055. [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Aguilar-Rodríguez PA, Krömer T, García-Franco JG, MacSwiney GMC. 2016. From dusk till dawn: nocturnal and diurnal pollination in the epiphyte Tillandsia heterophylla (Bromeliaceae). Plant Biology, 18(1), 37–45. [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Alvares CA, Stape JL, Sentelhas PC, De Moraes Gonçalves JL, Sparovek G. 2013. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22(6), 711–728. https://doi.org/10.1127/0941-2948/2013/0507 [Crossref] [Web of Science ®], [Google Scholar] Alves MAS, Rocha CFD, Van Sluys M, Bergallo HG. 2000. Guildas de beija-flores polinizadores de quatro espécies de Bromeliaceae de Mata Atlântica da Ilha Grande, RJ, Brasil: composição e taxas de visitação. A Ornitologia No Brasil: Pesquisa Atual e Perspectivas, January, 171–185. [Google Scholar] Armbruster WS, Wright G 2017. The specialization continuum in pollination systems: diversity of concepts and implications for ecology, evolution and conservation. Funct Ecol, 31(1), 88–100. https://doi.org/10.1111/1365-2435.12783 [Crossref] [Web of Science ®], [Google Scholar] Armbruster WS. 1997. Exaptations link evolution of plant–herbivore and plant–pollinator interactions: a phylogenetic inquiry. Ecology, 78(6), 1661–1672.10.1890/0012-9658(1997)078[1661:ELEOPH]2.0.CO;2 [Crossref] [Web of Science ®], [Google Scholar] Armbruster WS, Pélabon C, Bolstad GH, Hansen TF. 2014. Integrated phenotypes: understanding trait covariation in plants and animals. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1649). https://doi.org/10.1098/rstb.2013.0245 [Crossref] [Web of Science ®], [Google Scholar] Astegiano J, Guimarães PR, Cheptou PO, Vida MM, Mandai CY, Ashworth L, Massol F. 2015. Persistence of plants and pollinators in the face of habitat loss: Insights from trait-based metacommunity models. In Advances in Ecological Research (1st ed., Vol. 53). Elsevier Ltd. https://doi.org/10.1016/bs.aecr.2015.09.005 [Crossref], [Google Scholar] Blondel J. 2003. Guilds or functional groups: Does it matter? Oikos, 100(2), 223–231. https://doi.org/10.1034/j.1600-0706.2003.12152.x [Crossref] [Web of Science ®], [Google Scholar] Blüthgen N, Klein AM. 2011. Functional complementarity and specialisation: The role of biodiversity in plant-pollinator interactions. Basic Appl Ecol, 12(4), 282–291. https://doi.org/10.1016/j.baae.2010.11.001 [Crossref] [Web of Science ®], [Google Scholar] Buzato S, Sazima M, Sazima I. 2000. Hummingbird-Pollinated Floras at Three Atlantic Forest Sites. Biotropica, 32(4b), 824–841. https://doi.org/10.1111/j.1744-7429.2000.tb00621.x [Crossref] [Web of Science ®], [Google Scholar] Camargo E, Rodrigues LC, Araujo AC. 2011. Pollination biology and reproduction of Seemannia sylvatica (Kunth) Hanstein (Gesneriaceae) in the Serra da Bodoquena National Park, Mato Grosso do Sul. Biota Neotropica, 11(4), 125–130. https://doi.org/10.1590/S1676-06032011000400013 [Crossref] [Web of Science ®], [Google Scholar] Canela MBF, Sazima, M. 2005. The pollination of Bromelia antiacantha (Bromeliaceae) in Southeastern Brazil: ornithophilous versus melittophilous features. Plant Biology, 7(04), 411–416.10.1055/s-2005-865619 [Crossref] [PubMed], [Google Scholar] Dellinger AS 2020. Pollination syndromes in the 21st century: where do we stand and where may we go? New Phytol, 228(4), 1193–1213. https://doi.org/10.1111/nph.16793 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Egawa S, Hirose K, Itino T. 2020. Geographic changes in pollinator species composition affect the corolla tube length of self-heal (Prunella vulgaris L.): Evidence from three elevational gradients. Ecological Research, 35(5), 819–825. https://doi.org/10.1111/1440-1703.12146 [Crossref] [Web of Science ®], [Google Scholar] Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD 2004. Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst, 35(1), 375–403. https://doi.org/10.1146/annurev.ecolsys.34.011802.132347 [Crossref] [Web of Science ®], [Google Scholar] Freitas L. 2013. Concepts of pollinator performance: Is a simple approach necessary to achieve a standardized terminology? Revista Brasileira de Botanica, 36(1), 3–8. https://doi.org/10.1007/s40415-013-0005-6 [Crossref] [Web of Science ®], [Google Scholar] Fründ J, Linsenmair KE, Blüthgen N. 2010. Pollinator diversity and specialization in relation to flower diversity. Oikos, 119(10), 1581–1590.10.1111/j.1600-0706.2010.18450.x [Crossref] [Web of Science ®], [Google Scholar] Fumero-Cabán JJ, Meléndez-Ackerman EJ 2007. Relative pollination effectiveness of floral visitors of Pitcairnia angustifolia (Bromeliaceae). Am J Bot, 94(3), 419–424. https://doi.org/10.3732/ajb.94.3.419 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Gélvez-Zúñiga I, Teixido AL, Neves ACO, Fernandes GW. 2018. Floral antagonists counteract pollinator-mediated selection on attractiveness traits in the hummingbird-pollinated Collaea cipoensis (Fabaceae) (Fabaceae). Biotropica, 50(5), 797–804. https://doi.org/10.1111/btp.12574 [Crossref] [Web of Science ®], [Google Scholar] Gilbert LE. 1972. Pollen feeding and reproductive biology of Heliconius butterflies. Proceedings of the National Academy of Sciences, 69(6), 1403–1407. https://doi.org/10.1073/pnas.69.6.1403 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Gomes AC, Ferreira BHS, Souza CS, Arakaki LMM, Aoki C, Paggi GM, Sigrist MR. 2020. Adaptive response of extreme epiphyte Tillandsia species (Bromeliaceae) is demonstrated by different sexual reproduction strategies in the Brazilian Chaco. Botanical Journal of the Linnean Society, 192(4), 840–854. https://doi.org/10.1093/botlinnean/boz104 [Crossref] [Web of Science ®], [Google Scholar] Hammer Ø., Harper DA, Ryan, PD. 2001. Past: paleontological statistics software package for educaton and data anlysis. Palaeontologia electronica, 4(1), 1. [Google Scholar] Hernandes FA. 2013. The feather mites (Acari, Astigmata) of the Violet-capped Woodnymph, Thalurania glaucopis (Gmelin) (Aves, Trochilidae), with descriptions of three new species. Zootaxa, 3616(6), 563–577. https://doi.org/10.11646/zootaxa.3616.6.3 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Herrera CM. 1990. Daily patterns of pollinator activity, differential pollinating effectiveness, and floral resource availability, in a summer-flowering Mediterranean shrub. Oikos, 58(3), 277. https://doi.org/10.2307/3545218 [Crossref] [Web of Science ®], [Google Scholar] Irwin RE, Bronstein JL, Manson JS, Richardson L 2010. Nectar robbing: ecological and evolutionary perspectives. Annu Rev Ecol Evol Syst, 41(1), 271–292. https://doi.org/10.1146/annurev.ecolsys.110308.120330 [Crossref], [Google Scholar] Johnson SD, Steiner KE 2000. Generalization versus specialization in plant pollination systems. Trends Ecol Evol. https://doi.org/10.1016/S0169-5347(99)01811-X 15 4 140–143 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Kamke R, Schmid S, Zillikens A, Lopes BC, Steiner J. 2011. The importance of bees as pollinators in the short corolla bromeliad Aechmea caudata in southern Brazil. Flora-Morphology, Distribution, Functional Ecology of Plants, 206(8), 749–756. [Crossref], [Google Scholar] Karron JD 1987. The pollination ecology of co-occuring geographically restricted and widespread species of Astragalus (Fabaceae). Biol Conserv, 39(3), 179–193. https://doi.org/10.1016/0006-3207(87)90033-4 [Crossref] [Web of Science ®], [Google Scholar] Kessler M, Abrahamczyk S, Krömer T. 2020. The role of hummingbirds in the evolution and diversification of Bromeliaceae: unsupported claims and untested hypotheses. Botanical Journal of the Linnean Society, 192(4), 592–608.10.1093/botlinnean/boz100 [Crossref] [Web of Science ®], [Google Scholar] King C, Ballantyne G, Willmer PG. 2013. Why flower visitation is a poor proxy for pollination: measuring single-visit pollen deposition, with implications for pollination networks and conservation. Methods in Ecology and Evolution, 4(9), 811–818. https://doi.org/10.1111/2041-210X.12074 [Crossref] [Web of Science ®], [Google Scholar] Lagomarsino LP, Muchhala N 2019. A gradient of pollination specialization in three species of Bolivian Centropogon. Am J Bot, 106(5), 633–642. https://doi.org/10.1002/ajb2.1276 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Lande R, Arnold SJ. 1983. The measurement of selection on correlated characters. Evolution, 37(6), 1210. https://doi.org/10.2307/2408842 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Leal RLB, Moreira MM, Pinto AR, de Oliveira Ferreira J, Rodriguez-Girones M, Freitas L. 2020. Temporal changes in the most effective pollinator of a bromeliad pollinated by bees and hummingbirds. PeerJ, 8(3), e8836. https://doi.org/10.7717/peerj.8836 [Crossref] [PubMed], [Google Scholar] Legendre P, Legendre L. 2012. Interpretation of ecological structures. In Developments in Environmental Modelling, 24: 521–624. Elsevier. https://doi.org/10.1016/B978-0-444-53868-0.50010-1 [Crossref], [Google Scholar] Leimberger KG, Dalsgaard B, Tobias JA, Wolf C, Betts MG. 2022. The evolution, ecology, and conservation of hummingbirds and their interactions with flowering plants. Biol Rev, 97: 923–959. https://doi.org/10.1111/brv.12828 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Machado CG, Semir J. 2006. Fenologia da floração e biologia floral de bromeliáceas ornitófilas de uma área da Mata Atlântica do Sudeste brasileiro. Revista Brasileira de Botânica, 29(1), 163–174. https://doi.org/10.1590/s0100-84042006000100014 [Crossref], [Google Scholar] Maglianesi MA, Blüthgen N, Böhning-Gaese K, Schleuning M. 2014. Morphological traits determine specialization and resource use in plant-hummingbird networks in the Neotropics. Ecology, 95(12), 3325–3334. https://doi.org/10.1890/13-2261.1 [Crossref] [Web of Science ®], [Google Scholar] Martén-Rodríguez S, Fenster CB, Agnarsson I, Skog LE, Zimmer EA 2010. Evolutionary breakdown of pollination specialization in a Caribbean plant radiation. New Phytol, 188(2), 403–417. https://doi.org/10.1111/j.1469-8137.2010.03330.x [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Miñarro M, García D. 2018. Complementarity and redundancy in the functional niche of cider apple pollinators. Apidologie, 49(6), 789–802. https://doi.org/10.1007/s13592-018-0600-4 [Crossref] [Web of Science ®], [Google Scholar] Missagia CCC, Alves MAS. 2015. The rate of visitation by Amazilia fimbriata (Apodiformes: Trochilidae) influences seed production in Tillandsia stricta (Bromeliaceae). Zoologia, 32(3), 260–262. https://doi.org/10.1590/S1984-46702015000300010 [Crossref] [Web of Science ®], [Google Scholar] Missagia CCC, Alves MAS. 2016. Territorial foraging behavior in the male Violet-capped Woodnymph is dependent on the density of patches of inflorescences of Heliconia spathocircinata Aristeg. (Heliconiaceae) in the Brazilian Atlantic forest. Revista Brasileira de Botanica, 39(4), 1145–1150. https://doi.org/10.1007/s40415-016-0303-x [Crossref] [Web of Science ®], [Google Scholar] Missagia CCC, Alves MAS. 2017. Florivory and floral larceny by fly larvae decrease nectar availability and hummingbird foraging visits at Heliconia (Heliconiaceae) flowers. Biotropica, 49(1), 13–17. https://doi.org/10.1111/btp.12368 [Crossref] [Web of Science ®], [Google Scholar] Missagia CCC, Alves MAS 2018. Does beak size predict the pollination performance of hummingbirds at long and tubular flowers? A case study of a Neotropical spiral ginger. J Zool, 1–7. https://doi.org/10.1111/jzo.12539 305 1 [Crossref] [Web of Science ®], [Google Scholar] Missagia CCC, Verçoza FC. 2011. Fenologia reprodutiva, polinização e frutificação de Heliconia spathocircinata Aristeg. (Heliconiaceae) em fragmento de Floresta Atlântica do município do Rio de Janeiro DOI: 10.5007/2175-7925.2011v24n3p13. Biotemas, 24(3), 13–23. https://doi.org/10.5007/2175/7925.2011v24n3p13 [Crossref], [Google Scholar] Missagia CCC, Verçoza FC. 2014. Influência da disponibilidade de recurso floral no comportamento de forrageamento de Eupetomena macroura (Trochilidae). Atualidades Ornitológicas, 180(February), 4–6. [Google Scholar] Missagia CCC, Verçoza FDC. 2015. Implicações do agrupamento de inflorescências para a taxa de visitação por beija-flores e a produção de frutos de Heliconia bihai (L.) L. (Heliconiaceae) (L.) L. (Heliconiaceae). Biotemas, 28(3), 181. https://doi.org/10.5007/2175-7925.2015v28n3p181 [Crossref], [Google Scholar] Missagia CCC, Mendes CJO, Alves MAS. 2023. Data on flower-pollinator interactions in inflorescences of Tillandsia stricta (Bromeliaceae) in the Atlantic Forest. Rio de Janeiro Brazil. [ Data set]. Zenodo. https://doi.org/10.5281/zenodo.6299296. [Crossref], [Google Scholar] Morgado LN, Rocha CFD. 2016. Diversity of wild bees and their mediated dispersal of pollen from the genus Tillandsia (Bromeliaceae, Tillandsioideae) in an insular area. Athens J Sci, 3(4), 297–307. [Crossref], [Google Scholar] Moura TN, Webber AC, Torres LNM. 2011. Floral biology and a pollinator effectiveness test of the diurnal floral visitors of Tabernaemontana undulata Vahl. (Apocynaceae) in the understory of Amazon Rainforest, Brazil. Acta Botanica Brasilica, 25(2), 380–386. https://doi.org/10.1590/s0102-33062011000200014 [Crossref] [Web of Science ®], [Google Scholar] Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature, 403(6772), 853–858.10.1038/35002501 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Ollerton J, Alarcon R, Waser NM, Price MV, Watts S, Cranmer L, Hingston A, Peter CI, [Google Scholar] Rico-Guevara A, Hurme KJ, Elting R, Russell AL 2021. Bene “fit” assessment in pollination coevolution: mechanistic perspectives on hummingbird bill–flower matching. Integr Comp Biol, 61(2), 681–695.10.1093/icb/icab111 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Ollerton J, Alarcón R, Waser NM, Price MV, Watts S, Cranmer L, Hingston A, Peter CI, Rotenberry J 2009. A global test of the pollination syndrome hypothesis. Ann Bot, 103(9), 1471–1480. https://doi.org/10.1093/aob/mcp031 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Ollerton J, Rech AR, Waser NM, Price MV. 2015. Using the literature to test pollination syndromes - some methodological cautions. Journal of Pollination Ecology, 16(17), 119–125. https://doi.org/10.1016/j.cognition.2008.05.007 [Crossref], [Google Scholar] Ollerton J 2017. Pollinator diversity: distribution, ecological function, and conservation. Annu Rev Ecol Evol Syst, 48, 353–376 1 10.1146/annurev-ecolsys-110316-022919 [Crossref], [Google Scholar] Pellissier L, Albouy C, Bascompte J, Farwig N, Graham C, Loreau M, Maglianesi MA, Melián CJ, Pitteloud C, Roslin T, et al. 2018. Comparing species interaction networks along environmental gradients. Biological Reviews, 93(2), 785–800. https://doi.org/10.1111/brv.12366 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Queiroz JA, Quirino ZGM, Lopes AV, Machado IC. 2016. Vertebrate mixed pollination system in Encholirium spectabile: a bromeliad pollinated by bats, opossum and hummingbirds in a tropical dry forest. J Arid Environ. 125:21–30. doi: 10.1016/j.jaridenv.2015.09.015. [Crossref] [Web of Science ®], [Google Scholar] Ribeiro MC, Martensen AC, Metzger JP, Tabarelli M, Scarano F, Fortin MJ. 2011. The Brazilian Atlantic Forest: A Shrinking Biodiversity Hotspot. In: Zachos, F., Habel, J. (eds) Biodiversity Hotspots. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-20992-5_21Rombaut LM, Capp EJ, Hughes EC, Varley ZK, Beckerman AP, Cooper N, Thomas GH. 2022. The evolution of the traplining pollinator role in hummingbirds: specialization is not an evolutionary dead end. Proceedings of the Royal Society B, 289(1967), 20212484. [Crossref], [Google Scholar] Rosas-Guerrero V, Aguilar R, Martén-Rodríguez S, Ashworth L, Lopezaraiza-Mikel M, Bastida JM, Quesada M, Irwin R 2014. A quantitative review of pollination syndromes: Do floral traits predict effective pollinators? Ecol Lett, 17(3), 388–400. https://doi.org/10.1111/ele.12224 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Santos JC, Nascimento ART, Marzinek J, Leiner N, Oliveira PE. 2017. Distribution, host plants and floral biology of the root holoparasite Langsdorffia hypogaea in the Brazilian savanna. Flora, 226, 65–71. https://doi.org/10.1016/j.flora.2016.11.008 [Crossref] [Web of Science ®], [Google Scholar] Schmid S, Schmid VS, Zillikens A, Harter-Marques B, Steiner J. 2011. Bimodal pollination system of the bromeliad Aechmea nudicaulis involving hummingbirds and bees. Plant Biology, 13(SUPPL. 1), 41–50. https://doi.org/10.1111/j.1438-8677.2010.00348.x [Crossref] [PubMed], [Google Scholar] Schupp EW, Jordano P, Gómez JM, Hille Ris Lambers J 2017. A general framework for effectiveness concepts in mutualisms. Ecol Lett, 20(5), 577–590. https://doi.org/10.1111/ele.12764 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Sletvold N, Tye M, Ågren J, Campbell D 2017. Resource- and pollinator-mediated selection on floral traits. Funct Ecol, 31(1), 135–141. https://doi.org/10.1111/1365-2435.12757 [Crossref] [Web of Science ®], [Google Scholar] Stebbins GL 1970. Adaptive radiation of reproductive characteristics in angiosperms, I: pollination mechanisms. Annu Rev Ecol Syst, 1(1), 307–326. https://doi.org/10.1146/annurev.es.01.110170.001515 [Crossref], [Google Scholar] Tagliati MC, Oliveira HC, Faria APG. 2018. Fenologia reprodutiva, recursos florais e polinização de espécies de Bromeliaceae em um remanescente urbano de floresta atlântica do sudeste brasileiro. IDiversidade e Gestão, 2(2), 139–150. [Google Scholar] Tardivo RC, Araújo, CC, Paixão Souza B. 2020. Tillandsia in Flora do Brasil 2020. Jardim Botânico do Rio de Janeiro. Available at: <http://reflora.jbrj.gov.br/reflora/floradobrasil/FB6407>. Accessed on: 6th Nov. 2021 [Google Scholar] Temeles EJ. 1996. A new dimension to hummingbird-flower relationships. Oecologia, 105, 517–523. 4 10.1007/BF00330015 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Temeles EJ, Rah YJ, Andicoechea J, Byanova KL, Giller GSJ, Stolk SB, Kress WJ 2013. Pollinator-mediated selection in a specialized hummingbird-Heliconia system in the eastern Caribbean. J Evol Biol, 26(2), 347–356. https://doi.org/10.1111/jeb.12053 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Thiele SC, Milcharek O, Santos FL, Kaminski LA 2014. Butterflies (Lepidoptera: Hesperioidea and Papilionoidea) of Porto Mauá, Upper Paraná Atlantic Forest Ecoregion, Rio Grande do Sul State, Brazil. Biota Neotropica, 14(2), 1–10. https://doi.org/10.1590/1676-06032014000613 [Crossref] [Web of Science ®], [Google Scholar] Turner JRG. 1971. Experiments on the demography of tropical butterflies. II. Longevity and home-range behaviour in Heliconius erato. Biotropica, 3(1), 21. https://doi.org/10.2307/2989703 [Crossref], [Google Scholar] Vale MM, Tourinho L, Lorini ML, Rajão H, Figueiredo MSL. 2018. Endemic birds of the Atlantic Forest: traits, conservation status, and patterns of biodiversity. Journal of Field Ornithology, 89(3), 193–206. https://doi.org/10.1111/jofo.12256 [Crossref] [Web of Science ®], [Google Scholar] van der Pijl L. 1961. Ecological aspects of flower evolution. II. Zoophilous flower classes. Evolution, 15(1), 44–59. https://doi.org/10.2307/2405842 [Crossref] [Web of Science ®], [Google Scholar] Vogel S. 1954. Blütenbiologische Typen als Elemente der Sippengliederug, dargestellt anhand der Flora Südafrikas. Fischer, Jena. [Google Scholar] Vogel S. 2006. Floral syndromes: empiricism versus typology. Botanische Jahrbücher, 127(1), 5–11. https://doi.org/10.1127/0006-8152/2006/0127-0005 [Crossref], [Google Scholar] Wang X, Wen M, Qian X, Pei N, Zhang D 2020. Plants are visited by more pollinator species than pollination syndromes predicted in an oceanic island community. Sci Rep, 10(1), 1–12. https://doi.org/10.1038/s41598-020-70954-7 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Waser NM, Chittka L, Price MV, Williams NM., Ollerton, J. 1996. Emphasizing new ideas to stimulate research in ecology. Generalization in pollination systems, and why it matters. Ecology, 77(4), 1043–1060. 10.2307/2265575 [Crossref] [Web of Science ®], [Google Scholar] Weinstein BG, Graham CH, Irwin R 2017. Persistent bill and corolla matching despite shifting temporal resources in tropical hummingbird-plant interactions. Ecol Lett, 20(3), 326–335. https://doi.org/10.1111/ele.12730 [Crossref] [PubMed] [Web of Science ®], [Google Scholar]Additional informationFundingThe work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico [PQ # 305798/2014-6, 306.579/2018-9, 308615/2022-0]; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior [Finance Code 001 (scholarships Master and Doctoral]; Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro [CNE # E-26/203191/2015, 202.835/2018, 201126/2022].","PeriodicalId":1,"journal":{"name":"Accounts of Chemical Research","volume":null,"pages":null},"PeriodicalIF":16.4000,"publicationDate":"2023-09-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Accounts of Chemical Research","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1080/17550874.2023.2261927","RegionNum":1,"RegionCategory":"化学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"CHEMISTRY, MULTIDISCIPLINARY","Score":null,"Total":0}
引用次数: 0
Abstract
ABSTRACTBackground Most bromeliad (Bromeliaceae) species have specialised flowers for specific pollinators, establishing a mutualistic relationship. However, other animals may also pollinate bromeliads, though it is logical to assume that specialised flowers are more compatible with one specific group of pollinators.Aims We compared the performance of a hummingbird (Thalurania glaucopis) and a butterfly (Heliconius erato) as pollinators of flowers classified as ornithophilous of the bromeliad Tillandsia stricta (Bromeliaceae).Methods We applied the single visit method with seed counting, and measured corolla tube length of flowers. We also conducted observations on plants to determine the effectiveness of pollination by the hummingbird and the butterfly.Results Both animal species pollinated flowers, although the hummingbird was a more frequent and effective pollinator, resulting in greater seed production. The corolla tube length of T. stricta was a significant predictor of seeds produced per flower following interactions with the hummingbird, but not with the butterfly.Conclusion Our results indicate a more intimate flower – pollinator relationship between T. stricta and the hummingbird than the butterfly in this population of the bromeliad in Rio de Janeiro, Brazil.KEYWORDS: Atlantic ForestBrazilBromeliaceaefloral syndromehummingbirdspollinationDisclaimerAs a service to authors and researchers we are providing this version of an accepted manuscript (AM). Copyediting, typesetting, and review of the resulting proofs will be undertaken on this manuscript before final publication of the Version of Record (VoR). During production and pre-press, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal relate to these versions also. AcknowledgementsResearch in Pedra Branca State Park (PEPB: Parque Estadual da Pedra Branca) was authorised by the Rio de Janeiro State Environment Institute (INEA: Instituto Estadual do Ambiente) through permit number 008/2015. The authors thank PEPB for logistical support. They are also grateful to Stephen Ferrari for his review of the English text. The authors also thank the editors (including the subject editor, Richard Abbott) and the anonymous reviewers for the valuable contributions which greatly improved the manuscript. Funding for this study was provided by the Brazilian Coordination for Higher Education Personnel Training (CAPES: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) by granting C.C.C.M. a doctoral research scholarship and C.J.O.M with a master’s scholarship (this study was financed in part by CAPES—Finance Code 001). The Rio de Janeiro State Research Foundation (FAPERJ: Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro) provided C.C.C.M. with a grant (DSC-10 process E_01/201.955/2017) and supported the research of M.A.S.A. (CNE processes E-26/203191/2015, E-26/202.835/2018, E-26/201126/2022). The Brazilian National Research Council (CNPq: Conselho Nacional de Desenvolvimento Científico e Tecnológico) provided M.A.S.A. with a research fellowship (PQ processes 305798/2014-6, 306.579/2018-9, 308615/2022-0), who was also supported by a productivity fellowship from Rio de Janeiro State University (Prociência, UERJ/FAPERJ).Authors’ contributionsCCCM conceived the study and designed the methods; CCCM collected the data; CCCM and CJOM analysed the data; CCCM and CJOM led the writing of the manuscript. MASA participated in the writing, contributing with important intellectual content and revision, and financial support through her research grants. All the authors contributed fundamentally to the drafts and gave final approval for publication.Declaration of interest statementThe corresponding author confirms that this work does not present any type of conflict of interest.Data archiving statementThe data were published in the Zenodo Repository (DOI: 10.5281/zenodo.6299296), with a one-year embargo (until December 31 2023).Figure 1. Inflorescence of Tillandsia stricta (Bromeliaceae) with available flowers (purple) for visitors. Photograph: XXX.Display full sizeFigure 2. Corolla tube length of the flowers of Tillandsia stricta (Bromeliaceae) visited by hummingbirds (Thalurania glaucopis) and butterflies (Heliconius erato) in Pedra Branca State Park, Rio de Janeiro, Brazil.Display full sizeFigure 3. Relationship between the corolla tube length and seed production of Tillandsia stricta (Bromeliaceae) following interactions with hummingbirds (Thalurania glaucopis) in Pedra Branca State Park, Rio de Janeiro, Brazil.Display full sizeReferences Aizen MA, Harder LD. 2007. Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology, 88(2), 271–281. https://doi.org/10.1890/06-1017 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Almeida JM, Missagia CCC, Alves, MAS., Jia, Z-Y. 2022. Effects of the availability of floral resources and neighboring plants on nectar robbery in a specialized pollination system. Current Zoology, 68(5), 541–548. 10.1093/cz/zoab083 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Altmann J. 1974. Observational study of behavior: sampling. Behaviour, 49(3), 227–267. https://doi.org/10.1080/14794802.2011.585831 [Taylor & Francis Online] [PubMed] [Web of Science ®], [Google Scholar] Aguilar-Rodríguez PA, MacSwiney GMC, Krömer T, García-Franco JG., Knauer A, Kessler M. 2014. First record of bat-pollination in the species-rich genus Tillandsia (Bromeliaceae). Ann Bot, 113(6), 1047–1055. [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Aguilar-Rodríguez PA, Krömer T, García-Franco JG, MacSwiney GMC. 2016. From dusk till dawn: nocturnal and diurnal pollination in the epiphyte Tillandsia heterophylla (Bromeliaceae). Plant Biology, 18(1), 37–45. [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Alvares CA, Stape JL, Sentelhas PC, De Moraes Gonçalves JL, Sparovek G. 2013. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22(6), 711–728. https://doi.org/10.1127/0941-2948/2013/0507 [Crossref] [Web of Science ®], [Google Scholar] Alves MAS, Rocha CFD, Van Sluys M, Bergallo HG. 2000. Guildas de beija-flores polinizadores de quatro espécies de Bromeliaceae de Mata Atlântica da Ilha Grande, RJ, Brasil: composição e taxas de visitação. A Ornitologia No Brasil: Pesquisa Atual e Perspectivas, January, 171–185. [Google Scholar] Armbruster WS, Wright G 2017. The specialization continuum in pollination systems: diversity of concepts and implications for ecology, evolution and conservation. Funct Ecol, 31(1), 88–100. https://doi.org/10.1111/1365-2435.12783 [Crossref] [Web of Science ®], [Google Scholar] Armbruster WS. 1997. Exaptations link evolution of plant–herbivore and plant–pollinator interactions: a phylogenetic inquiry. Ecology, 78(6), 1661–1672.10.1890/0012-9658(1997)078[1661:ELEOPH]2.0.CO;2 [Crossref] [Web of Science ®], [Google Scholar] Armbruster WS, Pélabon C, Bolstad GH, Hansen TF. 2014. Integrated phenotypes: understanding trait covariation in plants and animals. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1649). https://doi.org/10.1098/rstb.2013.0245 [Crossref] [Web of Science ®], [Google Scholar] Astegiano J, Guimarães PR, Cheptou PO, Vida MM, Mandai CY, Ashworth L, Massol F. 2015. Persistence of plants and pollinators in the face of habitat loss: Insights from trait-based metacommunity models. In Advances in Ecological Research (1st ed., Vol. 53). Elsevier Ltd. https://doi.org/10.1016/bs.aecr.2015.09.005 [Crossref], [Google Scholar] Blondel J. 2003. Guilds or functional groups: Does it matter? Oikos, 100(2), 223–231. https://doi.org/10.1034/j.1600-0706.2003.12152.x [Crossref] [Web of Science ®], [Google Scholar] Blüthgen N, Klein AM. 2011. Functional complementarity and specialisation: The role of biodiversity in plant-pollinator interactions. Basic Appl Ecol, 12(4), 282–291. https://doi.org/10.1016/j.baae.2010.11.001 [Crossref] [Web of Science ®], [Google Scholar] Buzato S, Sazima M, Sazima I. 2000. Hummingbird-Pollinated Floras at Three Atlantic Forest Sites. Biotropica, 32(4b), 824–841. https://doi.org/10.1111/j.1744-7429.2000.tb00621.x [Crossref] [Web of Science ®], [Google Scholar] Camargo E, Rodrigues LC, Araujo AC. 2011. Pollination biology and reproduction of Seemannia sylvatica (Kunth) Hanstein (Gesneriaceae) in the Serra da Bodoquena National Park, Mato Grosso do Sul. Biota Neotropica, 11(4), 125–130. https://doi.org/10.1590/S1676-06032011000400013 [Crossref] [Web of Science ®], [Google Scholar] Canela MBF, Sazima, M. 2005. The pollination of Bromelia antiacantha (Bromeliaceae) in Southeastern Brazil: ornithophilous versus melittophilous features. Plant Biology, 7(04), 411–416.10.1055/s-2005-865619 [Crossref] [PubMed], [Google Scholar] Dellinger AS 2020. Pollination syndromes in the 21st century: where do we stand and where may we go? New Phytol, 228(4), 1193–1213. https://doi.org/10.1111/nph.16793 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Egawa S, Hirose K, Itino T. 2020. Geographic changes in pollinator species composition affect the corolla tube length of self-heal (Prunella vulgaris L.): Evidence from three elevational gradients. Ecological Research, 35(5), 819–825. https://doi.org/10.1111/1440-1703.12146 [Crossref] [Web of Science ®], [Google Scholar] Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD 2004. Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst, 35(1), 375–403. https://doi.org/10.1146/annurev.ecolsys.34.011802.132347 [Crossref] [Web of Science ®], [Google Scholar] Freitas L. 2013. Concepts of pollinator performance: Is a simple approach necessary to achieve a standardized terminology? Revista Brasileira de Botanica, 36(1), 3–8. https://doi.org/10.1007/s40415-013-0005-6 [Crossref] [Web of Science ®], [Google Scholar] Fründ J, Linsenmair KE, Blüthgen N. 2010. Pollinator diversity and specialization in relation to flower diversity. Oikos, 119(10), 1581–1590.10.1111/j.1600-0706.2010.18450.x [Crossref] [Web of Science ®], [Google Scholar] Fumero-Cabán JJ, Meléndez-Ackerman EJ 2007. Relative pollination effectiveness of floral visitors of Pitcairnia angustifolia (Bromeliaceae). Am J Bot, 94(3), 419–424. https://doi.org/10.3732/ajb.94.3.419 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Gélvez-Zúñiga I, Teixido AL, Neves ACO, Fernandes GW. 2018. Floral antagonists counteract pollinator-mediated selection on attractiveness traits in the hummingbird-pollinated Collaea cipoensis (Fabaceae) (Fabaceae). Biotropica, 50(5), 797–804. https://doi.org/10.1111/btp.12574 [Crossref] [Web of Science ®], [Google Scholar] Gilbert LE. 1972. Pollen feeding and reproductive biology of Heliconius butterflies. Proceedings of the National Academy of Sciences, 69(6), 1403–1407. https://doi.org/10.1073/pnas.69.6.1403 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Gomes AC, Ferreira BHS, Souza CS, Arakaki LMM, Aoki C, Paggi GM, Sigrist MR. 2020. Adaptive response of extreme epiphyte Tillandsia species (Bromeliaceae) is demonstrated by different sexual reproduction strategies in the Brazilian Chaco. Botanical Journal of the Linnean Society, 192(4), 840–854. https://doi.org/10.1093/botlinnean/boz104 [Crossref] [Web of Science ®], [Google Scholar] Hammer Ø., Harper DA, Ryan, PD. 2001. Past: paleontological statistics software package for educaton and data anlysis. Palaeontologia electronica, 4(1), 1. [Google Scholar] Hernandes FA. 2013. The feather mites (Acari, Astigmata) of the Violet-capped Woodnymph, Thalurania glaucopis (Gmelin) (Aves, Trochilidae), with descriptions of three new species. Zootaxa, 3616(6), 563–577. https://doi.org/10.11646/zootaxa.3616.6.3 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Herrera CM. 1990. Daily patterns of pollinator activity, differential pollinating effectiveness, and floral resource availability, in a summer-flowering Mediterranean shrub. Oikos, 58(3), 277. https://doi.org/10.2307/3545218 [Crossref] [Web of Science ®], [Google Scholar] Irwin RE, Bronstein JL, Manson JS, Richardson L 2010. Nectar robbing: ecological and evolutionary perspectives. Annu Rev Ecol Evol Syst, 41(1), 271–292. https://doi.org/10.1146/annurev.ecolsys.110308.120330 [Crossref], [Google Scholar] Johnson SD, Steiner KE 2000. Generalization versus specialization in plant pollination systems. Trends Ecol Evol. https://doi.org/10.1016/S0169-5347(99)01811-X 15 4 140–143 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Kamke R, Schmid S, Zillikens A, Lopes BC, Steiner J. 2011. The importance of bees as pollinators in the short corolla bromeliad Aechmea caudata in southern Brazil. Flora-Morphology, Distribution, Functional Ecology of Plants, 206(8), 749–756. [Crossref], [Google Scholar] Karron JD 1987. The pollination ecology of co-occuring geographically restricted and widespread species of Astragalus (Fabaceae). Biol Conserv, 39(3), 179–193. https://doi.org/10.1016/0006-3207(87)90033-4 [Crossref] [Web of Science ®], [Google Scholar] Kessler M, Abrahamczyk S, Krömer T. 2020. The role of hummingbirds in the evolution and diversification of Bromeliaceae: unsupported claims and untested hypotheses. Botanical Journal of the Linnean Society, 192(4), 592–608.10.1093/botlinnean/boz100 [Crossref] [Web of Science ®], [Google Scholar] King C, Ballantyne G, Willmer PG. 2013. Why flower visitation is a poor proxy for pollination: measuring single-visit pollen deposition, with implications for pollination networks and conservation. Methods in Ecology and Evolution, 4(9), 811–818. https://doi.org/10.1111/2041-210X.12074 [Crossref] [Web of Science ®], [Google Scholar] Lagomarsino LP, Muchhala N 2019. A gradient of pollination specialization in three species of Bolivian Centropogon. Am J Bot, 106(5), 633–642. https://doi.org/10.1002/ajb2.1276 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Lande R, Arnold SJ. 1983. The measurement of selection on correlated characters. Evolution, 37(6), 1210. https://doi.org/10.2307/2408842 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Leal RLB, Moreira MM, Pinto AR, de Oliveira Ferreira J, Rodriguez-Girones M, Freitas L. 2020. Temporal changes in the most effective pollinator of a bromeliad pollinated by bees and hummingbirds. PeerJ, 8(3), e8836. https://doi.org/10.7717/peerj.8836 [Crossref] [PubMed], [Google Scholar] Legendre P, Legendre L. 2012. Interpretation of ecological structures. In Developments in Environmental Modelling, 24: 521–624. Elsevier. https://doi.org/10.1016/B978-0-444-53868-0.50010-1 [Crossref], [Google Scholar] Leimberger KG, Dalsgaard B, Tobias JA, Wolf C, Betts MG. 2022. The evolution, ecology, and conservation of hummingbirds and their interactions with flowering plants. Biol Rev, 97: 923–959. https://doi.org/10.1111/brv.12828 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Machado CG, Semir J. 2006. Fenologia da floração e biologia floral de bromeliáceas ornitófilas de uma área da Mata Atlântica do Sudeste brasileiro. Revista Brasileira de Botânica, 29(1), 163–174. https://doi.org/10.1590/s0100-84042006000100014 [Crossref], [Google Scholar] Maglianesi MA, Blüthgen N, Böhning-Gaese K, Schleuning M. 2014. Morphological traits determine specialization and resource use in plant-hummingbird networks in the Neotropics. Ecology, 95(12), 3325–3334. https://doi.org/10.1890/13-2261.1 [Crossref] [Web of Science ®], [Google Scholar] Martén-Rodríguez S, Fenster CB, Agnarsson I, Skog LE, Zimmer EA 2010. Evolutionary breakdown of pollination specialization in a Caribbean plant radiation. New Phytol, 188(2), 403–417. https://doi.org/10.1111/j.1469-8137.2010.03330.x [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Miñarro M, García D. 2018. Complementarity and redundancy in the functional niche of cider apple pollinators. Apidologie, 49(6), 789–802. https://doi.org/10.1007/s13592-018-0600-4 [Crossref] [Web of Science ®], [Google Scholar] Missagia CCC, Alves MAS. 2015. The rate of visitation by Amazilia fimbriata (Apodiformes: Trochilidae) influences seed production in Tillandsia stricta (Bromeliaceae). Zoologia, 32(3), 260–262. https://doi.org/10.1590/S1984-46702015000300010 [Crossref] [Web of Science ®], [Google Scholar] Missagia CCC, Alves MAS. 2016. Territorial foraging behavior in the male Violet-capped Woodnymph is dependent on the density of patches of inflorescences of Heliconia spathocircinata Aristeg. (Heliconiaceae) in the Brazilian Atlantic forest. Revista Brasileira de Botanica, 39(4), 1145–1150. https://doi.org/10.1007/s40415-016-0303-x [Crossref] [Web of Science ®], [Google Scholar] Missagia CCC, Alves MAS. 2017. Florivory and floral larceny by fly larvae decrease nectar availability and hummingbird foraging visits at Heliconia (Heliconiaceae) flowers. Biotropica, 49(1), 13–17. https://doi.org/10.1111/btp.12368 [Crossref] [Web of Science ®], [Google Scholar] Missagia CCC, Alves MAS 2018. Does beak size predict the pollination performance of hummingbirds at long and tubular flowers? A case study of a Neotropical spiral ginger. J Zool, 1–7. https://doi.org/10.1111/jzo.12539 305 1 [Crossref] [Web of Science ®], [Google Scholar] Missagia CCC, Verçoza FC. 2011. Fenologia reprodutiva, polinização e frutificação de Heliconia spathocircinata Aristeg. (Heliconiaceae) em fragmento de Floresta Atlântica do município do Rio de Janeiro DOI: 10.5007/2175-7925.2011v24n3p13. Biotemas, 24(3), 13–23. https://doi.org/10.5007/2175/7925.2011v24n3p13 [Crossref], [Google Scholar] Missagia CCC, Verçoza FC. 2014. Influência da disponibilidade de recurso floral no comportamento de forrageamento de Eupetomena macroura (Trochilidae). Atualidades Ornitológicas, 180(February), 4–6. [Google Scholar] Missagia CCC, Verçoza FDC. 2015. Implicações do agrupamento de inflorescências para a taxa de visitação por beija-flores e a produção de frutos de Heliconia bihai (L.) L. (Heliconiaceae) (L.) L. (Heliconiaceae). Biotemas, 28(3), 181. https://doi.org/10.5007/2175-7925.2015v28n3p181 [Crossref], [Google Scholar] Missagia CCC, Mendes CJO, Alves MAS. 2023. Data on flower-pollinator interactions in inflorescences of Tillandsia stricta (Bromeliaceae) in the Atlantic Forest. Rio de Janeiro Brazil. [ Data set]. Zenodo. https://doi.org/10.5281/zenodo.6299296. [Crossref], [Google Scholar] Morgado LN, Rocha CFD. 2016. Diversity of wild bees and their mediated dispersal of pollen from the genus Tillandsia (Bromeliaceae, Tillandsioideae) in an insular area. Athens J Sci, 3(4), 297–307. [Crossref], [Google Scholar] Moura TN, Webber AC, Torres LNM. 2011. Floral biology and a pollinator effectiveness test of the diurnal floral visitors of Tabernaemontana undulata Vahl. (Apocynaceae) in the understory of Amazon Rainforest, Brazil. Acta Botanica Brasilica, 25(2), 380–386. https://doi.org/10.1590/s0102-33062011000200014 [Crossref] [Web of Science ®], [Google Scholar] Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature, 403(6772), 853–858.10.1038/35002501 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Ollerton J, Alarcon R, Waser NM, Price MV, Watts S, Cranmer L, Hingston A, Peter CI, [Google Scholar] Rico-Guevara A, Hurme KJ, Elting R, Russell AL 2021. Bene “fit” assessment in pollination coevolution: mechanistic perspectives on hummingbird bill–flower matching. Integr Comp Biol, 61(2), 681–695.10.1093/icb/icab111 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Ollerton J, Alarcón R, Waser NM, Price MV, Watts S, Cranmer L, Hingston A, Peter CI, Rotenberry J 2009. A global test of the pollination syndrome hypothesis. Ann Bot, 103(9), 1471–1480. https://doi.org/10.1093/aob/mcp031 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Ollerton J, Rech AR, Waser NM, Price MV. 2015. Using the literature to test pollination syndromes - some methodological cautions. Journal of Pollination Ecology, 16(17), 119–125. https://doi.org/10.1016/j.cognition.2008.05.007 [Crossref], [Google Scholar] Ollerton J 2017. Pollinator diversity: distribution, ecological function, and conservation. Annu Rev Ecol Evol Syst, 48, 353–376 1 10.1146/annurev-ecolsys-110316-022919 [Crossref], [Google Scholar] Pellissier L, Albouy C, Bascompte J, Farwig N, Graham C, Loreau M, Maglianesi MA, Melián CJ, Pitteloud C, Roslin T, et al. 2018. Comparing species interaction networks along environmental gradients. Biological Reviews, 93(2), 785–800. https://doi.org/10.1111/brv.12366 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Queiroz JA, Quirino ZGM, Lopes AV, Machado IC. 2016. Vertebrate mixed pollination system in Encholirium spectabile: a bromeliad pollinated by bats, opossum and hummingbirds in a tropical dry forest. J Arid Environ. 125:21–30. doi: 10.1016/j.jaridenv.2015.09.015. [Crossref] [Web of Science ®], [Google Scholar] Ribeiro MC, Martensen AC, Metzger JP, Tabarelli M, Scarano F, Fortin MJ. 2011. The Brazilian Atlantic Forest: A Shrinking Biodiversity Hotspot. In: Zachos, F., Habel, J. (eds) Biodiversity Hotspots. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-20992-5_21Rombaut LM, Capp EJ, Hughes EC, Varley ZK, Beckerman AP, Cooper N, Thomas GH. 2022. The evolution of the traplining pollinator role in hummingbirds: specialization is not an evolutionary dead end. Proceedings of the Royal Society B, 289(1967), 20212484. [Crossref], [Google Scholar] Rosas-Guerrero V, Aguilar R, Martén-Rodríguez S, Ashworth L, Lopezaraiza-Mikel M, Bastida JM, Quesada M, Irwin R 2014. A quantitative review of pollination syndromes: Do floral traits predict effective pollinators? Ecol Lett, 17(3), 388–400. https://doi.org/10.1111/ele.12224 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Santos JC, Nascimento ART, Marzinek J, Leiner N, Oliveira PE. 2017. Distribution, host plants and floral biology of the root holoparasite Langsdorffia hypogaea in the Brazilian savanna. Flora, 226, 65–71. https://doi.org/10.1016/j.flora.2016.11.008 [Crossref] [Web of Science ®], [Google Scholar] Schmid S, Schmid VS, Zillikens A, Harter-Marques B, Steiner J. 2011. Bimodal pollination system of the bromeliad Aechmea nudicaulis involving hummingbirds and bees. Plant Biology, 13(SUPPL. 1), 41–50. https://doi.org/10.1111/j.1438-8677.2010.00348.x [Crossref] [PubMed], [Google Scholar] Schupp EW, Jordano P, Gómez JM, Hille Ris Lambers J 2017. A general framework for effectiveness concepts in mutualisms. Ecol Lett, 20(5), 577–590. https://doi.org/10.1111/ele.12764 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Sletvold N, Tye M, Ågren J, Campbell D 2017. Resource- and pollinator-mediated selection on floral traits. Funct Ecol, 31(1), 135–141. https://doi.org/10.1111/1365-2435.12757 [Crossref] [Web of Science ®], [Google Scholar] Stebbins GL 1970. Adaptive radiation of reproductive characteristics in angiosperms, I: pollination mechanisms. Annu Rev Ecol Syst, 1(1), 307–326. https://doi.org/10.1146/annurev.es.01.110170.001515 [Crossref], [Google Scholar] Tagliati MC, Oliveira HC, Faria APG. 2018. Fenologia reprodutiva, recursos florais e polinização de espécies de Bromeliaceae em um remanescente urbano de floresta atlântica do sudeste brasileiro. IDiversidade e Gestão, 2(2), 139–150. [Google Scholar] Tardivo RC, Araújo, CC, Paixão Souza B. 2020. Tillandsia in Flora do Brasil 2020. Jardim Botânico do Rio de Janeiro. Available at: . Accessed on: 6th Nov. 2021 [Google Scholar] Temeles EJ. 1996. A new dimension to hummingbird-flower relationships. Oecologia, 105, 517–523. 4 10.1007/BF00330015 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Temeles EJ, Rah YJ, Andicoechea J, Byanova KL, Giller GSJ, Stolk SB, Kress WJ 2013. Pollinator-mediated selection in a specialized hummingbird-Heliconia system in the eastern Caribbean. J Evol Biol, 26(2), 347–356. https://doi.org/10.1111/jeb.12053 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Thiele SC, Milcharek O, Santos FL, Kaminski LA 2014. Butterflies (Lepidoptera: Hesperioidea and Papilionoidea) of Porto Mauá, Upper Paraná Atlantic Forest Ecoregion, Rio Grande do Sul State, Brazil. Biota Neotropica, 14(2), 1–10. https://doi.org/10.1590/1676-06032014000613 [Crossref] [Web of Science ®], [Google Scholar] Turner JRG. 1971. Experiments on the demography of tropical butterflies. II. Longevity and home-range behaviour in Heliconius erato. Biotropica, 3(1), 21. https://doi.org/10.2307/2989703 [Crossref], [Google Scholar] Vale MM, Tourinho L, Lorini ML, Rajão H, Figueiredo MSL. 2018. Endemic birds of the Atlantic Forest: traits, conservation status, and patterns of biodiversity. Journal of Field Ornithology, 89(3), 193–206. https://doi.org/10.1111/jofo.12256 [Crossref] [Web of Science ®], [Google Scholar] van der Pijl L. 1961. Ecological aspects of flower evolution. II. Zoophilous flower classes. Evolution, 15(1), 44–59. https://doi.org/10.2307/2405842 [Crossref] [Web of Science ®], [Google Scholar] Vogel S. 1954. Blütenbiologische Typen als Elemente der Sippengliederug, dargestellt anhand der Flora Südafrikas. Fischer, Jena. [Google Scholar] Vogel S. 2006. Floral syndromes: empiricism versus typology. Botanische Jahrbücher, 127(1), 5–11. https://doi.org/10.1127/0006-8152/2006/0127-0005 [Crossref], [Google Scholar] Wang X, Wen M, Qian X, Pei N, Zhang D 2020. Plants are visited by more pollinator species than pollination syndromes predicted in an oceanic island community. Sci Rep, 10(1), 1–12. https://doi.org/10.1038/s41598-020-70954-7 [Crossref] [PubMed] [Web of Science ®], [Google Scholar] Waser NM, Chittka L, Price MV, Williams NM., Ollerton, J. 1996. Emphasizing new ideas to stimulate research in ecology. Generalization in pollination systems, and why it matters. Ecology, 77(4), 1043–1060. 10.2307/2265575 [Crossref] [Web of Science ®], [Google Scholar] Weinstein BG, Graham CH, Irwin R 2017. Persistent bill and corolla matching despite shifting temporal resources in tropical hummingbird-plant interactions. Ecol Lett, 20(3), 326–335. https://doi.org/10.1111/ele.12730 [Crossref] [PubMed] [Web of Science ®], [Google Scholar]Additional informationFundingThe work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico [PQ # 305798/2014-6, 306.579/2018-9, 308615/2022-0]; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior [Finance Code 001 (scholarships Master and Doctoral]; Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro [CNE # E-26/203191/2015, 202.835/2018, 201126/2022].
【摘要】背景:大多数凤梨科(Bromeliaceae)物种都有专门的花,为特定的传粉者授粉,建立了互惠关系。然而,其他动物也可能为凤梨花授粉,尽管假设特定的花朵与特定的传粉者群体更相容是合乎逻辑的。目的比较蜂鸟(Thalurania glaucopis)和蝴蝶(Heliconius erato)在凤梨科(bromelia Tillandsia stricta)亲鸟花中的传粉性能。方法采用单次访种法,测量花的花冠管长。我们还对植物进行了观察,以确定蜂鸟和蝴蝶授粉的有效性。结果两种动物都授粉,但蜂鸟是更频繁和有效的传粉者,导致更多的种子产量。花冠管长度是与蜂鸟交互作用后单花种子产量的显著预测因子,而与蝴蝶交互作用后无显著预测因子。结论在巴西里约热内卢的凤梨科植物中,与蝴蝶相比,扁蝽与蜂鸟的传粉关系更为密切。关键词:大西洋森林巴西凤梨科花卉综合征蜂鸟授粉免责声明作为对作者和研究人员的服务,我们提供此版本的已接受稿件(AM)。在最终出版版本记录(VoR)之前,将对该手稿进行编辑、排版和审查。在制作和印前,可能会发现可能影响内容的错误,所有适用于期刊的法律免责声明也与这些版本有关。Pedra Branca州立公园(PEPB: Parque Estadual da Pedra Branca)的研究由里约热内卢国家环境研究所(INEA: Instituto Estadual do Ambiente)授权,许可号为008/2015。作者感谢PEPB的后勤支持。他们也感谢Stephen Ferrari对英文文本的审阅。作者还感谢编辑(包括主题编辑Richard Abbott)和匿名审稿人的宝贵贡献,他们极大地改进了手稿。本研究由巴西高等教育人才培训协调机构(CAPES: coordindena<s:1> ode aperfeioamento de Pessoal de Nível Superior)提供资金,授予c.c.c.m博士研究奖学金和C.J.O.M硕士奖学金(本研究部分由CAPES - finance Code 001资助)。里约热内卢国家研究基金会(FAPERJ: funda<s:1> o Carlos Chagas Filho de Amparo Pesquisa do Estado do Rio de Janeiro)向ccc.c.m.提供了一笔赠款(DSC-10流程E_01/201.955/2017),并支持M.A.S.A. (CNE流程E-26/203191/2015, E-26/202.835/2018, E-26/201126/2022)的研究。巴西国家研究委员会(CNPq: Conselho Nacional de Desenvolvimento Científico e Tecnológico)为M.A.S.A.提供了研究奖学金(PQ流程305798/2014- 6,306.579 /2018- 9,308615 /2022-0),并得到了里约热内卢州立大学(Prociência, UERJ/FAPERJ)的生产力奖学金的支持。scccm构思了研究并设计了方法;CCCM采集数据;CCCM和CJOM分析数据;CCCM和CJOM主导了稿件的撰写。MASA参与了写作,提供了重要的知识内容和修订,并通过她的研究资助提供了财政支持。所有作者都对初稿做出了重要贡献,并最终批准发表。利益声明通讯作者确认本研究不存在任何类型的利益冲突。数据存档声明数据发布在Zenodo知识库(DOI: 10.5281/ Zenodo .6299296)中,禁制期为一年(直到2023年12月31日)。图1所示。凤梨科凤梨花(Tillandsia stricta)花序,可供游客观赏的花(紫色)。照片:XXX。显示完整尺寸图2巴西里约热内卢佩德拉布兰卡州立公园,蜂鸟(Thalurania glaucopis)和蝴蝶(Heliconius erato)对凤梨科凤梨花的花冠管长度的观察。显示完整尺寸图3巴西Pedra Branca州立公园凤梨科花冠管长与蜂鸟(Thalurania glaucopis)相互作用后花冠管长与种子产量的关系显示全尺寸的参考文献。Aizen MA, Harder LD. 2007。扩大花粉限制概念的范围:花粉数量和质量的影响。生态学报,28(2),391 - 391。https://doi.org/10.1890/06-1017 [Crossref] [PubMed] [Web of Science®],[Google Scholar] Almeida JM, Missagia CCC, Alves, MAS。, Jia, Z-Y。2022. 1111 / jofo。[12] [Crossref] [Web Science®],[Google Scholar]。花进化的生态学方面。2亲动物花卉课程。进化,15(1),44-59。https://doi.org/10.2307/2405842 [Crossref] [Web of Science®],[Google Scholar]。[3] [j] [j] [j] [j]; [j] [j]; [j]。费舍尔,耶拿。[Google学术]Vogel S. 2006。花综合症:经验主义与类型学。植物学报,2012(1),5-11。https://doi.org/10.1127/0006-8152/2006/0127-0005 [Crossref], [Google Scholar]王鑫,文敏,钱鑫,裴宁,张东。2020.[链接本文]在一个海洋岛屿群落中,植物被更多的传粉者物种访问,而不是传粉综合征。科学通报,10(1),1 - 12。https://doi.org/10.1038/s41598-020-70954-7 [Crossref] [PubMed] [Web of Science®],[Google Scholar] Waser NM, Chittka L, Price MV, Williams NM。欧尔班。1996。强调新思路,促进生态学研究。传粉系统中的泛化及其重要性。生态学报,32(4),344 - 344。10.2307/2265575 [Crossref] [Web of Science®],[Google Scholar] Weinstein BG, Graham CH, Irwin R 2017。热带蜂鸟-植物相互作用中喙和花冠的持续匹配,尽管时间资源发生了变化。生态学报,20(3),326-335。https://doi.org/10.1111/ele.12730 [Crossref] [PubMed] [Web of Science®],[Google Scholar]其他信息本研究由Conselho Nacional de Desenvolvimento Científico e Tecnológico支持[PQ # 305798/2014- 6,306.579 /2018- 9,308615 /2022-0];坐标aaperfeiaperoamento de Pessoal de Nível高级[财务法规001](硕士和博士奖学金);巴西巴西基金[CNE # E-26/203191/2015, 202.835/2018, 201126/2022]。
期刊介绍:
Accounts of Chemical Research presents short, concise and critical articles offering easy-to-read overviews of basic research and applications in all areas of chemistry and biochemistry. These short reviews focus on research from the author’s own laboratory and are designed to teach the reader about a research project. In addition, Accounts of Chemical Research publishes commentaries that give an informed opinion on a current research problem. Special Issues online are devoted to a single topic of unusual activity and significance.
Accounts of Chemical Research replaces the traditional article abstract with an article "Conspectus." These entries synopsize the research affording the reader a closer look at the content and significance of an article. Through this provision of a more detailed description of the article contents, the Conspectus enhances the article's discoverability by search engines and the exposure for the research.