Abstract
The floral traits in Bignoniaceae are claimed as precise determiners of specialized pollination systems. Here, we investigated how such floral traits ensure a highly specialized interaction between Jacaranda rugosa and medium-sized bees by examining visual, and olfactory signaling, as well as mechanical fit to pollinating bees. We also report the efficiency of the system by fitness measures (pollen delivery from anthers; pollen deposition on stigma; fruit and seed set). Jacaranda rugosa probably attracting bees through chromatic and achromatic contrasts of staminode with corolla and pollen mimicry, and floral volatile compounds that are common to other bee-pollinated systems. Fundamental and realized accuracy ensure tight mechanical fit to medium-sized bees. While the natural female component is strongly limited, promoting lower fruit set than pollinated flowers, the floral morphology seems to ensure high male fitness by pollen transfer. Our results demonstrate that floral traits of J. rugosa promote a specialized system for pollination by medium-sized bees, and this process is likely to happen in other species of Bignoniaceae or flowers with similar traits.
Similar content being viewed by others
Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request. Floral visitation photos available at iNaturalist observations code: 109387821-23.
References
Abràmoff, M., Magalhães, P., & Ram, S. J. (2004). Image processing with ImageJ. Biophotonics International, 11, 36–42. https://imagej.nih.gov/ij/docs/pdfs/ImageJPaper
Adams, R. P. (2007). Identification of essential oil components by gas chromatography/mass spectrometry (4th ed.). Carol Stream, I. L. Allured Publishing Corporation.
Alcantara, S., & Lohmann, L. G. (2010). Evolution of floral morphology and pollination systems in Bignonieae (Bignoniaceae). American Journal of Botany, 97, 782–796. https://doi.org/10.3732/ajb.0900182
Alcantara, S., & Lohmann, L. G. (2011). Contrasting phylogenetic signals and evolutionary rates in floral traits of Neotropical lianas. Biological Journal of the Linnean Society, 102, 378–390. https://doi.org/10.1111/j.1095-8312.2010.01567.x
Alonso, C., Vamosi, J. C., Knight, T. M., Steets, J. A., & Ashman, T. (2010). Is reproduction of endemic plant species particularly pollen limited in biodiversity hotspots? Oikos, 119, 1192–1200. https://doi.org/10.1111/j.1600-0706.2009.18026.x
Alves, M. F., Duarte, M. O., Oliveira, P. E., & Sampaio, D. S. (2013). Self-sterility in the hexaploid Handroanthus serratifolius (Bignoniaceae), the national flower of Brazil. Acta Botanica Brasilica, 27, 714–722. https://doi.org/10.1590/S0102-33062013000400010
Alves-dos-Santos, I., Silva, C. I., Pinheiro, M., & Kleinert, A. M. P. (2016). When a floral visitor is a pollinator? Rodriguésia, 67, 295–307. https://doi.org/10.1590/2175-7860201667202
Andrade, K. V. S. A., Rodal, M. J. N., Lucena, M. F. A., & Gomes, A. P. S. (2004). Composição florística de um trecho do Parque Nacional do Catimbau, Buíque, Pernambuco – Brasil. Hoehnea, 31, 337–348.
APAC. (2017). https://www.apac.pe.gov.br/metereologia/monitoramentopluvio.php
Arceo-Gómez, G., & Ashman, T. (2011). Heterospecific pollen deposition: Does diversity alter the consequences? New Phytologist, 192, 738–746. https://doi.org/10.1111/j.1469-8137.2011.03831.x
Armbruster, W. S. (2014). Floral specialization and angiosperm diversity: Phenotypic divergence, fitness trade-offs and realized pollination accuracy. AoB Plants, 6, plu003. https://doi.org/10.1093/aobpla/plu003
Armbruster, W. S., & Muchhala, N. (2009). Associations between floral specialization and species diversity: Cause, effect, or correlation? Ecology and Evolution, 23, 159–179. https://doi.org/10.1007/s10682-008-9259-z
Armbruster, W. S., Di Stilio, V. S., Tuxill, J. D., Flores, T. C., & Velásquez Runk, J. L. (1999). Covariance and decoupling of floral and vegetative traits in nine neotropical plants: A re-evaluation of Berg’s correlation pleiades concept. American Journal of Botany, 86, 39–55. https://doi.org/10.2307/2656953
Armbruster, W. S., Pélabon, C., Hansen, T. F., & Mulder, C. P. H. (2004). Floral integration, modularity, and precision distinguishing complex adaptations from genetic constraints. In M. Pigliucci & K. Preston (Eds.), Phenotypic Integration: Studying the Ecology and Evolution of Complex Phenotypes (pp. 23–49). Nova York.
Armbruster, W. S., Pérez-Barrales, R., Arroyo, J., Edwards, M. E., & Vargas, P. (2006). Three-dimensional reciprocity of floral morphs in wild flax (Linum suffruticosum): A new twist on heterostyly. New Phytologist, 171, 581–590. https://doi.org/10.1111/j.1469-8137.2006.01749.x
Armbruster, W. S., Hansen, T. F., Pélabon, C., Pérez-Barrales, R., & Maad, J. (2009). The adaptive accuracy of flowers: Measurement and microevolutionary patterns. Annals of Botany, 103, 1529–1545. https://doi.org/10.1093/aob/mcp095
Armbruster, W. S., Shi, X. Q., & Huang, S. Q. (2014a). Do specialized flowers promote reproductive isolation? Realized pollination accuracy of three sympatric Pedicularis species. Annals of Botany, 113, 331–340. https://doi.org/10.1093/aob/mct187
Armbruster, W. S., Corbet, S. A., Vey, A. J. M., Liu, S. J., & Huang, S. Q. (2014b). In the right place at the right time: Parnassia resolves the herkogamy dilemma by accurate repositioning of stamens and stigmas. Annals of Botany, 113, 97–103. https://doi.org/10.1093/aob/mct261
Armbruster, W. S., Pélabon, C., Bolstad, G. H., & Hansen, T. F. (2014c). Integrated phenotypes: Understanding trait covariation in plants and animals. Philosophical Transactions of the Royal Society, 369, 20130245. https://doi.org/10.1098/rstb.2013.0245
Armisén, R., & Galatas, F. (2009). Agar. In P. A. Williams, G. O. Phillips (Eds.), Handbook of hydrocalloids (2nd ed., pp. 807–828). Woodhead Publishing, Cambridge, UK, CRC Press.
Berg, R. L. (1960). The ecological significance of correlation pleiades. Evolution, 14, 171–180. https://doi.org/10.2307/2405824
Bernhardt, P. (2005). Pollen transport and transfer by animal pollinators. In A. Dafni, P. G. Kevan, & B. C. Husband (Eds.), Practical pollination biology (pp. 371–380). Cambridge.
Bittencourt, JR, N. S. (2019). Reproductive systems and low outbreeding barriers between Jacaranda cuspidifolia and J. mimosifolia (Jacarandeae, Bignoniaceae). Nordic Journal of Botany, 37, 11. https://doi.org/10.1111/njb.02558
Bittencourt, Jr, N. S., & Semir, J. (2004). Pollination biology and breeding system of Zeyheria montana (Bignoniaceae). Plant Systematics and Evolution, 247, 241–254. https://doi.org/10.1007/s00606-004-0142-2
Bittencourt, Jr, N. S., & Semir, J. (2005). Late-acting self incompatibility and other breeding systems in Tabebuia (Bignoniaceae). International Journal of Plant Sciences, 166, 493–506. https://doi.org/10.1086/428758
Bittencourt, Jr, N. S., & Semir, J. (2006). Floral biology and late-acting self incompatibility in Jacaranda racemosa (Bignoniaceae). Australian Journal of Botany, 54, 315–324. https://doi.org/10.1071/BT04221
Bittencourt, Jr, N. S., Gibbs, P. E., & Semir, J. (2003). Histological study of post-pollination events in Spathodea campanulata Beauv (Bignoniaceae), a species with late-acting self incompatibility. Annals of Botany, 91, 827–834. https://doi.org/10.1093/aob/mcg088
Bittencourt, Jr, N. S., Pereira, Jr. E. J., São-Thiago, P. S., & Semir, J. (2011). The reproductive biology of Cybistax antisyphilitica (Bignoniaceae), a characteristic tree of the South American savannah-like “Cerrado” vegetation. Flora, 206, 872–886. https://doi.org/10.1016/j.flora.2011.05.004
Bohart, G. E., & Nye, W. P. (1960). Insect pollinators of carrots in Utah. Utah Agricultural Experiment Station Bulletin, 419,1–16. https://digitalcommons.usu.edu/cgi/viewcontent.cgi?article=1074&context=piru_pubs&httpsredir=1&referer=
Burger, H., Dötterl, S., & Ayasse, M. (2010). Host-plant finding and recognition by visual and olfactory floral cues in an oligolectic bee. Functional Ecology, 24, 1234–1240. https://doi.org/10.1111/j.1365-2435.2010.01744.x
Cavalcanti, L. C. S., & Corrêa, A. C. B. (2014). Pluviosidade no Parque Nacional do Catimbau (Pernambuco): Seus condicionantes e seus efeitos sobre a paisagem. Geografia, 23, 133–156. https://doi.org/10.5433/2447-1747.2014v23n2p133
Chittka, L. (1992). The colour hexagon: A chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. Journal of Comparative Physiology, 170, 533–543. https://doi.org/10.1007/BF00199331
Chittka, L., & Kevan, P. G. (2005). Flower colour as advertisement. In A. Dafni, P. G. Kevan, & B. C. Husband (Eds.), Practical pollination biology (pp. 157–196). Cambridge, Ontário, Canadá, Enviroquest Ltd. https://www.researchgate.net/publication/231536872_Practical_Pollination_Biology
Choisy, J. D. (1845). Convolvulaceae. In: De Candolle, ed. Prodromus systematics naturalis regni vegetabilis, 9, 323–465.
Cruden, R. W. (1977). Pollen-ovule ratios: A conservative indicator of breeding systems in flowering plants. Evolution, 31, 32–46.
Cruden, R. W. (2000). Pollen grains: Why so many?. In Pollen and pollination (pp. 143–165). Springer, Vienna.
De Jager, M., & Peakall, R. (2019). Experimental examination of pollinator-mediated selection in a sexually deceptive orchid. Annals of Botany, 123, 347–354. https://doi.org/10.1093/aob/mcy083
De Vega, C., Herrera, C. M., & Dötterl, S. (2014). Floral volatiles play a key role in specialized ant pollination. Perspective in Plant Ecology Evolution and Systematics, 16, 1. https://doi.org/10.1016/j.ppees.2013.11.002
Decraene, L. P. R., & Smets, E. F. (2001). Staminodes: Their morphological and evolutionary significance. The Botanical Review, 67, 351–402. https://doi.org/10.1007/BF02858099
Dobson, H. E. M., & Bergström, G. (2000). The ecology and evolution of pollen odors. Plant Systematics and Evolution, 222, 63–87. https://www.jstor.org/stable/23644328
Domingos-Melo, A., Nadia, T. L., Wiemer, A. P., Cocucci, A. A., & Machado, I. C. (2019). Beyond taxonomy: Anther skirt is a diagnostic character that provides specialized noctuid pollination in Marsdenia megalantha (Asclepiadoideae–Apocynaceae). Plant Systematics and Evolution, 305, 103–114. https://doi.org/10.1007/s00606-018-1555-7
Domingos-Melo, A., Milet-Pinheiro, P., Navarro, D. M. A. F., Lopes, A. V., & Machado, I. C. (2020). It’s raining fragrant nectar in the Caatinga: Evidence of nectar olfactory signaling in bat-pollinated flowers. Ecology, 101, e02914. https://doi.org/10.1002/bes2.1640
Dormann, C. F. (2020). Using bipartite to describe and plot two-mode networks in R. R package version, 4, 1–28. https://cloud.r-project.org/web/packages/bipartite/vignettes/Intro2bipartite.pdf
Dötterl, S., & Jürgens, A. (2005). Spatial fragrance patterns in flowers of Silene latifolia: lilac compounds as olfactory nectar guides? Plant Systematics and Evolution, 255, 99–109. https://doi.org/10.1007/s00606-005-0344-2
Dötterl, S., & Vereecken, N. J. (2010). The chemical ecology and evolution of bee–flower interactions: A review and perspectives. Canadian Journal of Zoology, 88, 668–697. https://doi.org/10.1139/Z10-031
Dötterl, S., Wolfe, L. M., & Jürgens, A. (2005). Qualitative and quantitative analyses of flower scent in Silene latifolia. Phytochemistry, 66, 203–213. https://doi.org/10.1016/j.phytochem.2004.12.002
Dyer, A. G., & Chittka, L. (2004). Fine colour discrimination requires differential conditioning in bumblebees. Naturwissenschaften, 91, 224–227. https://doi.org/10.1007/s00114-004-0508-x
Eltz, T., Whitten, W. M., Roubik, D. W., & Linsenmair, K. E. (1999). Fragrance collection, storage, and accumulation by individual male orchid bees. Journal of Chemical Ecology, 25, 157–176. https://doi.org/10.1023/A:1020897302355
Erbar, C., & Enghofer, J. (2001). Untersuchungen zum Reproduktionssystem der Wegwarte (Cichorium intybus, Asteraceae): Pollenportionierung, Narbenbelegung und Pollenschlauchkonkurrenz. Botanische Jahrbücher Fur Systematik, Pflanzengeschichte Und Pflanzengeographie, 123, 179–208.
Fægri, K., & Pijl, L. van der. (1979). Principles of pollination ecology (3rd ed.). Pergamon.
Fang, Q., & Huang, S. Q. (2013). A directed network analysis of heterospecific pollen transfer in a biodiverse community. Ecology, 94, 1176–1185. https://doi.org/10.2307/23435959
Fenster, C. B., & Martén-Rodríguez, S. (2007). Reproductive assurance and the evolution of pollination specialization. International Journal of Plant Sciences, 168, 215–228. https://doi.org/1058-5893/2007/16802-000815.00
Flora do Brasil. (2020). https://www.floradobrasil.jbrj.gov.br
Frazão, A., Lohmann, L. G., Costa, E. R., & Demarco, D. (2020). Structure of long-tubed white corollas: A case study from the trumpet-creeper family (Bignoniaceae). Flora, 268, 151598. https://doi.org/10.1016/j.flora.2020.151598
Gandolphi, G., & Bittencourt, J. R. N. S. (2010). Sistema reprodutivo do Ipê-Branco: Tabebuia roseo-alba (Ridley) Sandwith (Bignoniaceae). Acta Botanica Brasilica, 24, 840–851. https://doi.org/10.1590/S0102-33062010000300026
Gentry, A. H. (1974a). Flowering phenology and diversity in tropical Bignoniaceae. Biotropica, 6, 64–68. https://doi.org/10.2307/2989698
Gentry, A. H. (1974b). Coevolutionary patterns in Central American Bignoniaceae. Annals of the Missouri Botanical Garden, 61, 728–759. https://doi.org/10.2307/2395026
Gentry, A. H. (1976). Bignoniaceae of Sourthern Central America: Distribution and ecological specificity. Biotropica, 8, 117–131. https://doi.org/10.2307/2989632
Gentry, A. H. (1980). Bignoniaceae: Part I (Crescentieae and Tourrettieae). Flora Neotropica Monograph. New York Botanical Garden, 25, 1–130. https://www.jstor.org/stable/4393736
Gentry, A. H. (1982). Neotropical floristic diversity: Phytogeographical connections between Central and South America, pleistocene climatic fluctuations, or an accident of the andean orogeny? Annals of the Missouri Botanical Garden, 69, 557–593.
Gentry, A. H. (1992). Bignoniaceae - Part II (Tribe Tecomeae). Flora Neotropica. New York Botanical Garden, 25, 1–370. https://www.jstor.org/stable/i400045
Gentry, A. H., & Morawetz, W. (1992). Jacaranda. In A. H. Gentry (Ed.), Bignoniaceae - Part II (Tribe Tecomeae). Flora Neotropica Monograph. New York Botanical Garden, 25, 51–105.
Gong, Y. B., & Huang, S. Q. (2014). Interspecific variation in pollen–ovule ratio is negatively correlated with pollen transfer efficiency in a natural community. Plant Biology, 16, 843–847.
Gottsberger, G., & Silberbauer-Gottsberger, I. (2006). Life in the Cerrado, a South American tropical seasonal ecosystem. Pollination and seed dispersal (2nd ed.). Ulm, Germany, Reta Verlag.
Guimarães, E., Di Stasi, L. C., & Maimoni-Rodella, R. C. S. (2008). Pollination biology of Jacaranda oxyphylla with an emphasis on staminode function. Annals of Botany, 102, 699–711. https://doi.org/10.1093/aob/mcn152
Huang, M., Sanchez-Moreiras, A. M., Abel, C., Sohrabi, R., Lee, S., Gershenzon, J., & Tholl, D. (2012). The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-b-caryophyllene, is a defense against a bacterial pathogen. New Phytologist, 193, 997–1008. https://doi.org/10.1111/j.1469-8137.2011.04001.x
Irwin, H. S., & Barneby, R. C. (1982). The American cassiinaea synoptical revision of Leguminosae tribe Cassieae subtribe cassiinaea in the New World (No. 580.744747 M4/v. 35/2).
Jackman, S., Tahk, A., Zeileis, A., Maimone, C., Fearon, J., & Meers, Z. (2020). Package pscl. Political Science Computational Laboratory. Version 1.5.5. https://CRAN.R-project.org/package=pscl
Jain, D. K., & Singh, V. (1979). Studies in Bignoniaceae - VI. Floral anatomy. Proceedings of the Indian Academy of Sciences-Section b, Plant Sciences, 88, 379–390.
Junker, R. R., & Blüthgen, N. (2010). Floral scents repel facultative flower visitors, but attract obligate ones. Annals of Botany, 105, 777–782. https://doi.org/10.1093/aob/mcq045
Jussieu, A. (1843). Monographie des malpighiacées. Archives Du Muséum D’histoire Naturelle, Paris, 3, 255–626.
Knudsen, J. T., Eriksson, R., Gershenzon, J., & Stahl, B. (2006). Diversity and distribution of floral scent. The Botanical Review, 72, 1–120. https://doi.org/10.1663/0006-8101(2006)72[1:DADOFS]2.0.CO;2
Kyogoku, D. (2015). Reproductive interference: Ecological and evolutionary consequences of interspecific promiscuity. Population Ecology, 57, 253–260. https://doi.org/10.1007/s10144-015-0486-1
Lepeletier, A. (1841). Histoire Naturelle des Insects. Hyménoptères. Tome Second. Paris, Librarie Encyclopédique de Roret.
Liu, Y., Jing, S. H., Luo, S. H., & Li, S. H. (2019). Non-volatile natural product in plant glandular trichomes: Chemistry, biological activities and biosynthesis. Natural Product Report, 36, 626–665. https://doi.org/10.1039/C8NP00077H
Lohmann, L., Firetti, F., & Gomes, B. M. (2018). Flora das cangas da Serra dos Carajás, Pará, Brasil: Bignoniaceae. Rodriguésia, 69, 2175–7860. https://doi.org/10.1590/2175-7860201869313
Lunau, K. (1995). Notes on the colour of pollen. Plant Systematics and Evolution, 198, 235–252. https://doi.org/10.1007/BF00984739
Lunau, K. (2000). The ecology and evolution of visual pollen signals. Plant Systematics and Evolution, 222, 89–111. https://doi.org/10.1007/BF00984097
Lunau, K. (2007). Stamens and mimic stamens as components of floral colour patterns. Botanische Jahrbücher Fur Systematik, 127, 13–41. https://doi.org/10.1127/0006-8152/2006/0127-0013
Lunau, K., Unseld, K., & Wolter, F. (2009). Visual detection of diminutive floral guides in the bumble bee Bombus terrestris and in the honey bee Apis mellifera. Journal of Comparative Physiology A, 195, 1121–1130. https://doi.org/10.1007/s00359-009-0484-x Epub 2009 Oct 8.
Lunau, K., Papiorek, S., Eltz, T., & Sazima, M. (2011). Avoidance of achromatic colours by bees provides a private niche for hummingbirds. Journal of Experimental Biology, 214, 1607–1612. https://doi.org/10.1242/jeb.052688
Maia, R., Eliasson, C., Bitton, P. P., & White, T. (2017). Perceptual analysis, visualization and organization of spectral color data in R. Available from: https://mran.microsoft.com/snapshot/2017-04-06/web/packages/pavo/pavo.pdf
Masters, M. T. (1871). Contributions to the natural history of the Passifloraceae. Transactions of the Linnean Society, 237, 5923–6645.
Maués, M. M., Oliveira, P. E. A. M., & Kanashiro, M. (2008). Pollination biology in Jacaranda copaia (Aubl.) D. Don. (Bignoniaceae) at the “Floresta Nacional do Tapajós”, Central Amazon. Brazil. Revista Brasileira De Botânica, 31, 517–527. https://doi.org/10.1590/S0100-84042008000300015
Menzel, R., & Backhaus, W. (1991). Colour vision in insects. In P. Gouras (Ed.), Vision and Visual Dysfunction: The Perception of Colour (6, pp. 262–288). London, MacMillan Press.
Milet-Pinheiro, P., & Schlindwein, C. (2009a). Permanent stigma closure in Bignoniaceae: Mechanism and implications for fruit set in self-incompatible species. Flora, 204, 82–88. https://doi.org/10.1016/j.flora.2007.11.006
Milet-Pinheiro, P., & Schlindwein, C. (2009b). Pollination in Jacaranda rugosa (Bignoniaceae): Euglossine pollinators, nectar robbers and low fruit set. Plant Biology, 11, 131–141. https://doi.org/10.1111/j.1438-8677.2008.00118.x
Milet-Pinheiro, P., Ayasse, M., Schlindwein, C., Dobson, H. E. M., & Dötterl, S. (2012). Host location by visual and olfactory floral cues in an oligolectic bee: Innate and learned behavior. Behavioral Ecology, 23, 531–538. https://doi.org/10.1093/beheco/arr219
Milet-Pinheiro, P., Domingos-Melo, A., Olivera, J. B., Albuquerque, N. S. L., Costa, A. C. G., Albuquerque-Lima, S., Silva, M. F. R., Navarro, D. M. A. F., Maia, A. C. D., Gundersen, L. L., Schubert, M., Dötterl, S., & Machado, I. C. (2021). A Semivolatile floral scent marks the shift to a novel pollination system in Bromeliads. Current Biology, 31, 860–868. https://doi.org/10.1016/j.cub.2020.11.012
Miller, T. J., Raguso, R. A., & Kay, K. M. (2014). Novel adaptation to hawkmoth pollinators in Clarkia reduces efficiency, not attraction of diurnal visitors. Annals of Botany, 113, 317–329. https://doi.org/10.1093/aob/mct237
Morales, C. L., & Traveset, A. (2008). Interspecific pollen transfer: Magnitude, prevalence and consequences for plant fitness. Critical Reviews in Plant Sciences, 27, 221–238. https://doi.org/10.1080/07352680802205631
Moré, M., Amorim, F. W., Benitez-Vieyra, S., Medina, A., Sazima, M., & Cocucci, A. A. (2012). Armament imbalances: Match and mismatch in plant-pollinator traits of highly specialized long-spurred orchids. PLoS ONE, 7, 1–9. https://doi.org/10.1371/journal.pone.0041878
Moré, M., Soteras, F., Ibañez, A. C., Dötterl, S., Cocucci, A. A., & Raguso, R. A. (2021). Floral scent evolution in the genus Jaborosa (Solanaceae): Influence of ecological and environmental factors. Plants, 10, 1512. https://doi.org/10.3390/plants10081512
Ne’eman, G., Jürgens, A., Newstrom-Lloyd, L., Potts, S. G., & Dafni, A. (2010). A framework for comparing pollinator performance: Effectiveness and efficiency. Biological Reviews of the Cambridge Philosophical Society, 85, 435–451. https://doi.org/10.1111/j.1469-185X.2009.00108.x
Nemésio, A. (2009). Orchid bees (Hymenoptera: Apidae) of the Brazilian Atlantic Forest. Zootaxa, 2041, 1–242. https://doi.org/10.11646/zootaxa.2041.1.1
Ng, L., Garcia, J. E., & Dyer, A. G. (2018). Why colour is complex: Evidence that bees perceive neither brightness nor green contrast in colour signal processing. FACETS, 3, 800–817. https://doi.org/10.1139/facets-2017-0116
Ollerton, J., Killich, A., Larborn, E., Watts, S., & Whiston, M. (2007). Multiple meanings and modes: On the many ways to be a generalist flower. Taxon, 56, 717–728. https://doi.org/10.2307/25065856
Palacios, J. A. P., Soteras, F., & Cocucci, A. A. (2019). Mechanical fit between flower and pollinators in relation to realized precision and accuracy in the hummingbird pollinated Dolichandra cynanchoides. Biological Journal of the Linnean Society, 126, 655–665. https://doi.org/10.1093/biolinnean/bly219
Papiorek, S., Junker, R. R., Alves-Dos-Santos, I., Melo, G. A. R., Amaral-Neto, L. P., Sazima, M., Wolowiski, M., Freitas, L., & Lunau, K. (2016). Bees, birds and yellow flowers: Pollinator-dependent convergent evolution of UV patterns. Plant Biology, 18, 46–55. https://doi.org/10.1111/plb.12322
Paterno, G. B., Silveira, C. L., Kollmann, J., Westoby, M., & Fonseca, C. R. (2020). The maleness of larger angiosperm flowers. Proceedings of the National Academy of the Sciences of the United States of America, 117, 10921–10926. https://doi.org/10.1073/pnas.1910631117
Pinheiro, M., Gaglianone, M. C., Nunes, C. E. P., Sigrist, M. R., & Santos, I. A. (2014). Polinização por abelhas. In A. R. Rech, K. Agostini, P. E. A. M. Oliveira, & I. C. S. Machado (Eds.), Biologia da polinização (pp. 205– 233). Rio de Janeiro, Editora Projeto Cultural. https://www.academia.edu/22985605/Biologia_da_Polinização
Portman, Z. M., Orr, K. C., & Griswold, T. (2019). A review and updated classification of pollen gathering behavior in bees (Hymenoptera, Apoidea). Journal of Hymenoptera Research, 71, 171–208. https://doi.org/10.3897/jhr.71.32671
Raine, N. E., & Chittka, L. (2007). The adaptive significance of sensory bias in a foraging context: Floral colour preferences in the bumblebee Bombus terrestris. PLoS ONE, 2, e556. https://doi.org/10.1371/journal.pone.0000556
Ramirez, S., Dressler, R. L., & Ospina, M. (2002). Abejas euglosinas (Hymenoptera: Apidae) de la région neotropical: listado de especies con notas sobre su biología. Biota Colombiana, 3, 7–118. http://revistas.humboldt.org.co/index.php/biota/article/view/108.
Reitan, T., & Nielsen, A. (2016). Do not divide count data with count data: a story from pollination ecology with implications beyond. PLoS ONE, 11, e0149129. https://doi.org/10.1371/journal.pone.0149129.
Rivest, S. A., Austen, E. J., & Forrest, J. R. K. (2017). Foliage affects colour preference in bumblebees (Bombus impatiens): A test in a three dimensional artificial environment. Evolutionary Ecology, 31, 435–446. https://doi.org/10.1007/s10682-017-9893-4
Rodal, M. J. N., Andrade, K. V. A., Vendas, M. F., & Gomes, A. P. S. (1998). Fitossociologia do componente lenhoso de um refúgio vegetacional no município de Buíque, Pernambuco. Revista Brasileira De Biologia, 58, 517–526. https://doi.org/10.1590/S0034-71081998000300017
Sampaio, D. S., Mendes-Rodrigues, C., Engel, T. B. J., Rezende, T. M., Bittencourt, N. S., Jr., & Oliveira, P. E. (2016). Pollination biology and breeding system of syntopic Adenocalymma nodosum and A. peregrinum (Bignonieae, Bignoniaceae) in the Brazilian savanna. Flora, 223, 19–29. https://doi.org/10.1016/j.flora.2016.04.009
Santos, L. L., Santos, L. L., Alves, A. S. A., Oliveira, L. S. D., & Sales, M. F. (2013). Bignoniaceae Juss. no Parque Nacional Vale do Catimbau. Pernambuco. Rodriguésia, 64, 479–494. https://doi.org/10.1590/S2175-78602013000300003
Sérsic, A. N., & Rando, C. (2004). Función mecánica del estaminódio en la polinización de Jacaranda mimosifolia D. Don. In: XXI Reunión Argentina de Ecologia, Mendonza, Argentina.
Shimizu, A., Dohzono, I., Nakaji, M., Roff, D. A., Miller III, D. G., Osato, S., Yajima, T., Niitsu, S., Utsugi, N., Sugawara, T., & Yoshimura, J. (2014). Fine-tuned bee-flower coevolutionary state hidden within multiple pollination interactions. Scientific Reports, 4, 3988. https://doi.org/10.1038/srep03988
Spaethe, J., Tautz, J., & Chittka, L. (2001). Visual constraints in foraging bumblebees: Flower size and color affect search time and flight behavior. Proceedings of the National Academy of Sciences of the United Stated of America, 98, 3898–3903. https://doi.org/10.1073/pnas.071053098
Stebbins, G. L. (1970). Adaptative radiation of reproductive characteristics in angiosperms: I Pollination mechanisms. Annual Review of Ecology and Systematics, 1, 307–326.
Streher, N. S., Bergamo, P. J., Ashman, T. L., Wolowski, M., & Sazima, M. (2020). Effect of heterospecific pollen deposition on pollen tube growth depends on the phylogenetic relatedness between donor and recipient. AoB Plants, 12, plaa016. https://doi.org/10.1093/aobpla/plaa016.
Team, R. C. (2017). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available from: https://www.R-project.org
Theis, N. (2006). Fragrance of Canada thistle (Cirsium arvense) attracts both floral herbivores and pollinators. Journal of Chemical Ecology, 32, 917–927. https://doi.org/10.1007/S10886-006-9051-X
Urban, I. (1883). Monographie der familie der Turneraceen. Jahrbuch Des Königlichen Botanischen Gartens Und Des Botanischen Museums Zu Berlin, 2, 1–152.
Vieira, M. F., Meira, R. M. S. A., Queiroz, L. P., & Meira-Neto, J. A. A. (1992). Polinização e reprodução de Jacaranda caroba (vell.) DC (Bignoniaceae) em área de Cerrado do Sudeste Brasileiro. In Anais VIII Congresso da Sociedade Botânica de São Paulo (13–19).
Walker-Larsen, J., & Harder, L. D. (2000). The evolution of staminodes in angiosperms: Patterns of stamen reduction, loss, and functional re-invention. American Journal of Botany, 87, 1367–1384. https://doi.org/10.2307/2656866
Waser, N. M. (1978). Interspecific pollen transfer and competition between co-occurring plant species. Oecologia, 36, 223–236. https://doi.org/10.1007/BF00349811
Westerkamp, C., & ClaBen-Bockhoff, R. (2007). Bilabiate flowers: The ultimate response to bees? Annals of Botany, 100, 361–74. https://doi.org/10.1093/aob/mcm123
Yanagizawa, Y. A. N. P., & Maimoni-Rodella, R. C. S. (2007). Floral visitors and reproductive strategies in five melittophilous species of Bignoniaceae in Southeastern Brazil. Brazilian Archives of Biology and Technology, 50, 1043–1051. https://doi.org/10.1590/S1516-89132007000700015
Zeileis, A., Kleiber, C., & Jackman, S. (2008). Regression models for count data in R. Journal of Statistical Software, 27, 1–25. https://doi.org/10.18637/jss.v027.i08
Zhang, H. Y., Yan, X. L., Su, S., Zhang, Y. Q., Ren, Y., & Zhang, X. H. (2020). Androecium development and staminode diversity of Cocculus orbiculatus (Menispermaceae). Flora, 265, 151573. https://doi.org/10.1016/j.flora.2020.151573
Zito, P., Tavella, F., Pacifico, D., Campanella, V., Sajeva, M., Carimi, F., Ebmer, A. W., & Dötter, S. (2019). Interspecific variation of inflorescence scents and insect visitors in Allium (Amaryllidaceae: Allioideae). Plant Systematic and Evolution, 305, 727–741. https://doi.org/10.1007/s00606-019-01601-6
Acknowledgements
We thank PELD/CNPq/Catimbau (Long-Term Ecological Research Project) for the permission and logistical support to carry out the project in the Catimbau National Park. To colleagues from the Laboratory of Floral and Reproductive Biology–Polinizar, Botany Department, at UFPE (Federal University of Pernambuco). To Dr. Vinicius L.G. Brito for suggestions in manuscript. To Coordenação de Aperfeiçoamento de Pessoal de Nível Superior–Brasil (CAPES–88882.347732/2019-0 to CASP and Finance Code 001).
Funding
This research was financially supported by the FACEPE (Foundation for the Support of Science and Technology of Pernambuco) (IBPG-1258–2.05/14, IBPG-0550–2.03/14 and BCT-0085–2.03/19) and the CNPq (Proc.n. 311021/2014 and 310508/2019–3).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Pontes, C.A.d., Domingos-Melo, A., Milet-Pinheiro, P. et al. Staminode of Jacaranda rugosa A.H. Gentry (Bignoniaceae) promotes functional specialization by ensuring signaling and mechanical fit to medium-sized bees. Org Divers Evol 22, 527–541 (2022). https://doi.org/10.1007/s13127-022-00558-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13127-022-00558-8