Plant Systematics and Evolution

, Volume 303, Issue 6, pp 709–718 | Cite as

Nectar production, reproductive success and the evolution of generalised pollination within a specialised pollen-rewarding plant family: a case study using Miconia theizans

  • Vinícius L. G. de BritoEmail author
  • André R. Rech
  • Jeff Ollerton
  • Marlies Sazima
Original Article


Generalist plant–pollinator interactions are prevalent in nature. Here, we untangle the role of nectar production in the visitation and pollen release/deposition in Miconia theizans, a nectar-rewarding plant within the specialised pollen-rewarding plant family Melastomataceae. We described the visitation rate, nectar dynamics and pollen release from the poricidal anthers and deposition onto stigmas during flower anthesis. Afterwards, we used a linear mixed model selection approach to understand the relationship between pollen and nectar availability and insect visitation rate and the relationship between visitation rate and reproductive success. Miconia theizans was visited by 86 insect species, including buzzing and non-buzzing bees, wasps, flies, hoverflies, ants, beetles, hemipterans, cockroaches and butterflies. The nectar produced explained the visitation rate, and the pollen release from the anthers was best explained by the visitation rate of pollinivorous species. However, the visitation rates could not predict pollen deposition onto stigmas. Nectar production may explain the high insect diversity and led to an increase in reproductive success, even with unpredictable pollen deposition, indicating the adaptive value of a generalised pollination system.


Generalisation Melastomataceae Miconia theizans Cogn. Nectar dynamics Pollination syndromes Reproductive success 



The authors kindly thank our friends for help in the field and lab: Pedro J. Bergamo, Maraísa Braga, Priscila Vieira, Camila Oliveira, Rafael Pereira and specially Carine Carriere and Cristiano Silva. We thank Fundação de Amparo à Pesquisa do Estado de São Paulo—FAPESP—for funding support to V.L.G.B. (Proc. 2010/51494-5), A.R.R. (Proc. 2009/54491-0), J.O. (Visiting Researcher—Proc. 2013/14442-5) and M.S. (2012/50425-5). MS thanks the funding support from Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq (303084/2011-1).

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

606_2017_1405_MOESM1_ESM.pdf (101 kb)
Supplementary material 1 (PDF 101 kb)
606_2017_1405_MOESM2_ESM.pdf (100 kb)
Supplementary material 2 (PDF 100 kb)
606_2017_1405_MOESM3_ESM.pdf (105 kb)
Supplementary material 3 (PDF 106 kb)
606_2017_1405_MOESM4_ESM.pdf (191 kb)
Supplementary material 4 (PDF 192 kb)
606_2017_1405_MOESM5_ESM.pdf (193 kb)
Supplementary material 5 (PDF 193 kb)


  1. Aguilar R, Martén-Rodriguez S, Avila-Sakar G, Ashworth L, Lopeazaraiza-Mikel M, Quesada M (2015) A global review of pollination syndromes: a response to Ollerton et al. 2015. J Pollinat Ecol 17:126–128Google Scholar
  2. Alarcón R, Waser NM, Ollerton J (2008) Year-to-year variation in the topology of a plant-pollinator interaction network. Oikos 117:1796–1807. doi: 10.1111/j.0030-1299.2008.16987.x CrossRefGoogle Scholar
  3. Albuquerque LB, Aquinol FG, Costa LC, Miranda ZJG, Sousa SR (2013) Melastomataceae Juss. species with potential use in ecological restoration of gallery riparian vegetation of Cerrado/Savanna. Polibotánica 35:1–19Google Scholar
  4. Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G (2013) Köppen´s climate classification map for Brazil. Meteorol Z 22:711–728. doi: 10.1127/0941-2948/2013/0507 CrossRefGoogle Scholar
  5. Amorim FW, Galetto L, Sazima M (2012) Beyond the pollination syndrome: nectar ecology and the role of diurnal and nocturnal pollinators in the reproductive success of Inga sessilis (Fabaceae). Pl Biol 15:317–327. doi: 10.1111/j.1438-8677.2012.00643.x CrossRefGoogle Scholar
  6. Armbruster WS (1988) Multilevel comparative analysis of the morphology, function, and evolution of Dalechampia blossoms. Ecology 69:1746–1761. doi: 10.2307/1941153 CrossRefGoogle Scholar
  7. Armbruster WS, Baldwin BG (1998) Switch from specialized to generalized pollination. Nature 394:632. doi: 10.1038/29210 CrossRefGoogle Scholar
  8. Bartomeus I, Park M, Gibbs J, Danforth B, Lakso A, Winfree R (2013) Biodiversity ensures plant–pollinator phenological synchrony against climate change. Ecol Lett 16:1331–1338. doi: 10.1111/ele.12170 CrossRefPubMedGoogle Scholar
  9. Berger BA, Kriebel R, Spalink D, Sytsma KJ (2016) Divergence times, historical biogeography, and shifts in speciation rates of Myrtales. Molec Phylogen Evol 95:116–136. doi: 10.1016/j.ympev.2015.10.001 CrossRefGoogle Scholar
  10. Borges MR, Melo C (2012) Frugivory and seed dispersal of Miconia theaezans (Bonpl.) Cogniaux (Melastomataceae) by birds in a transition palm swamp: gallery forest in Central Brazil. Brazil J Biol 72:25–31CrossRefGoogle Scholar
  11. Brito VLG, Sazima M (2012) Tibouchina pulchra (Melastomataceae): reproductive biology of a tree species at two sites of an elevational gradient in the Atlantic rainforest in Brazil. Pl Syst Evol 298:1271–1279. doi: 10.1007/s00606-012-0633-5 CrossRefGoogle Scholar
  12. Brito VLG, Fendrich TG, Smidt EC, Varassin IG, Goldenberg R (2016) Shifts from specialised to generalised pollination systems in Miconieae (Melastomataceae) and their relation with anther morphology and seed number. Pl Biol 18:585–593. doi: 10.1111/plb.12432 CrossRefGoogle Scholar
  13. Buchmann SL (1983) Buzz pollination in Angiosperms. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinhold, New York, pp 73–113Google Scholar
  14. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information—theoretic approach. Springer-Verlag, New YorkGoogle Scholar
  15. Busch JW, Delph LF (2012) The relative importance of reproductive assurance and automatic selection as hypotheses for the evolution of self-fertilization. Ann Bot (Oxford) 109:553–562. doi: 10.1093/aob/mcr219 CrossRefGoogle Scholar
  16. Chao A (1987) Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43:783–791. doi: 10.2307/2531532 CrossRefPubMedGoogle Scholar
  17. Chase MW, Hills HG (1992) Orchid phylogeny, flower sexuality and fragrance-seeking. Bioscience 42:43–49. doi: 10.2307/1311627 CrossRefGoogle Scholar
  18. Cheptou PO (2012) Clarifying Baker's Law. Ann Bot (Oxford) 109:633–641. doi: 10.1093/aob/mcr127 CrossRefGoogle Scholar
  19. CPTEC (2010) Centro de previsão de tempo e estudos climáticos. Available at: Accessed 15 Feb 2010
  20. Dafni A, Kevan PG, Husband BC (2005) Practical pollination ecology. Enviroquest, CambridgeGoogle Scholar
  21. Endress PK (1994) Diversity and evolutionary biology of tropical flowers. Cambridge University Press, CambridgeGoogle Scholar
  22. Faegri K, van der Pijl L (1979) The principles of pollination ecology. Pergamon Press, OxfordGoogle Scholar
  23. Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annual Rev Ecol Syst 35:375–403. doi: 10.1146/annurev.ecolsys.34.011802.132347 CrossRefGoogle Scholar
  24. Fracasso CM, Sazima M (2004) Pollination of Cambessedesia hilariana (Kunth) DC. (Melastomataceae): reproductive success versus bee diversity, behaviour and frequency of visits. Brazil J Bot 27:797–804Google Scholar
  25. Franco AM, Goldenberg R, Varassin IG (2011) Pollinator guild organization and its consequences for reproduction in three synchronopatric species of Tibouchina (Melastomataceae). Revista Brasil Entomol 55:381–388CrossRefGoogle Scholar
  26. Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annual Rev Ecol Syst 19:207–233. doi: 10.1146/ CrossRefGoogle Scholar
  27. Galetto L, Bernardello G (2005) Nectar. In: Dafni A, Kevan P, Husband BC (eds) Practical pollination biology. Enviroquest, Ontario, pp 261–313Google Scholar
  28. Goldenberg R, Shepherd GJ (1998) Studies in reproductive biology of Melastomataceae in “cerrado” vegetation. Pl Syst Evol 211:13–29. doi: 10.1007/BF00984909 CrossRefGoogle Scholar
  29. Goldenberg R, Penneys DS, Almeda F, Judd WS, Michelangeli FA (2008) Phylogeny of Miconia (Melastomataceae): patterns of stamen diversification in a megadiverse neotropical genus. Int J Pl Sci 169:963–979. doi: 10.1086/589697 CrossRefGoogle Scholar
  30. Harder LD, Thomson JD (1989) Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. Amer Naturalist 133:323–344CrossRefGoogle Scholar
  31. Hargreaves AL, Harder LD, Johnson SD (2009) Consumptive emasculation: the ecological and evolutionary consequences of pollen theft. Biol Rev 84:259–276. doi: 10.1111/j.1469-185X.2008.00074.x CrossRefPubMedGoogle Scholar
  32. Herrera CM (2005) Plant generalization on pollinators: species property or local phenomenon? Amer J Bot 92:13–20. doi: 10.3732/ajb.92.1.13 CrossRefGoogle Scholar
  33. Kay KM, Reeves PA, Olmstead RG, Schemske DW (2005) Rapid speciation and the evolution of hummingbird pollination in neotropical Costus subgenus Costus (Costaceae): evidence from nrDNA ITS and ETS sequences. Amer J Bot 92:1899–1910. doi: 10.3732/ajb.92.11.1899 CrossRefGoogle Scholar
  34. 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. Meth Ecol Evol 4:811–818. doi: 10.1111/2041-210X.12074 CrossRefGoogle Scholar
  35. Kriebel R, Zumbado MA (2014) New reports of generalist insect visitation to flowers of species of Miconia (Miconieae: melastomataceae) and their evolutionary implications. Brittonia 66:396–404. doi: 10.1007/s12228-014-9337-1 CrossRefGoogle Scholar
  36. Larsson BMH, Barret SCH (1999) The ecology of pollen limitation in buzz-pollinated Rhexia virginica (Melastomataceae). J Ecol 87:371–381. doi: 10.1046/j.1365-2745.1999.00362.x CrossRefGoogle Scholar
  37. Lunau K, Piorek V, Krohn O, Pacini E (2015) Just spines—mechanical defense of malvaceous pollen against collection by corbiculate bees. Apidologie 46:144–149. doi: 10.1007/s13592-014-0310-5 CrossRefGoogle Scholar
  38. Luo Z, Zhang D, Renner SS (2008) Why two kinds of stamens in buzz-pollinated flowers? Experimental support for Darwin’s division-of-labour hypothesis. Funct Ecol 22:794–800. doi: 10.1111/j.1365-2435.2008.01444.x CrossRefGoogle Scholar
  39. Martén-Rodriguez S, Fenster CB, Agnarsson I, Skog LE, Zimmer EA (2010) Evolutionary breakdown of pollination specialization in a Caribbean plant radiation. New Phytol 188:403–417. doi: 10.1111/j.1469-8137.2010.03330.x CrossRefPubMedGoogle Scholar
  40. Melo GF, Machado IC, Luceño M (1999) Reprodución de tres especies de Clidemia (Melastomataceae) en Brasil. Rev Biol Trop 47:359–363Google Scholar
  41. Niemirski R, Zych M (2011) Fly pollination of dichogamous Angelica sylvestris (Apiaceae): how (functionally) specialized can a (morphologically) generalized plant be? Pl Syst Evol 294:147–158. doi: 10.1007/s00606-011-0454-y CrossRefGoogle Scholar
  42. Ollerton J, Killick A, Lamborn E, Watts S, Whiston M (2007) Multiple meanings and modes: on the many ways to a generalist flower. Taxon 56:717–728. doi: 10.2307/25065856 CrossRefGoogle Scholar
  43. Ollerton J, Rech AR, Waser NM, Price MV (2015) Using the literature to test pollination syndromes—some methodological cautions. J Pollinat Ecol 16:101–107Google Scholar
  44. Padgurschi MCG, Pereira LP, Tamashiro JY, Joly CA (2011) Composição e similaridade florística entre duas áreas de Floresta Atlântica Montana, São Paulo, Brasil. Biota Neotrop 11:139–152CrossRefGoogle Scholar
  45. Pannell JR, Auld JR, Brandvain Y, Burd M, Busch JW, Cheptou PO, Conner JK, Goldberg EE, Grant AG, Grossenbacher DL, Hovick SM (2015) The scope of Baker's law. New Phytol 208:656–667. doi: 10.1111/nph.13539 CrossRefPubMedGoogle Scholar
  46. Pereira AC, Silva JB, Goldenberg R, Melo GAR, Varassin IG (2011) Flower color change accelerated by bee pollination in Tibouchina (Melastomataceae). Flora 206:491–497. doi: 10.1016/j.flora.2011.01.004 CrossRefGoogle Scholar
  47. Renner SS (1989) A survey of reproductive biology in Neotropical Melastomataceae and Memecylaceae. Ann Missouri Bot Gard 76:496–518. doi: 10.2307/2399497 CrossRefGoogle Scholar
  48. Rosas-Guerrero V, Aguilar R, Martén-Rodriguez S, Ashworth L, Lopezaraiza-Mikel M, Bastida JM, Quesada M (2014) A quantitative review of pollination syndromes: do floral traits predict effective pollinators? Ecol Lett 17:388–400. doi: 10.1111/ele.12224 CrossRefPubMedGoogle Scholar
  49. Santos APM, Romero R, Oliveira PEAM (2010) Biologia reprodutiva de Miconia angelana (Melastomataceae), endêmica da Serra da Canastra, Minas Gerais. Brazil J Bot 33:333–341CrossRefGoogle Scholar
  50. Schlindwein C, Wittmann D, Martins CF, Hamm A, Siqueira JA, Schiffler D, Machado IC (2005) Pollination of Campanula rapunculus L. (Campanulaceae): how much pollen flows into pollination and into reproduction of oligolectic pollinators? Pl Syst Evol 250:147–156. doi: 10.1007/s00606-004-0246-8 CrossRefGoogle Scholar
  51. Smith SD (2010) Using phylogenetics to detect pollinator-mediated floral evolution. New Phytol 188:354–363. doi: 10.1111/j.1469-8137.2010.03292.x CrossRefPubMedCentralGoogle Scholar
  52. Stebbins GL (1970) Adaptive radiation of reproductive characteristics in Angiosperms, I: pollination mechanisms. Annual Rev Ecol Syst 1:307–326. doi: 10.1146/ CrossRefGoogle Scholar
  53. Tabarelli M, Mantovani W (1999) Woody species richness in the Brazilian Atlantic forest, state of São Paulo (Brazil). Brazil J Bot 59:239–250Google Scholar
  54. Thomson JD, McKenna MA, Cruzan MB (1989) Temporal patterns of nectar and pollen production in Aralia hispida: implications for reproductive success. Ecology 70:1061–1068. doi: 10.2307/1941375 CrossRefGoogle Scholar
  55. Thomson JD, Wilson P, Valenzuela M, Malzone M (2000) Pollen presentation and pollination syndromes, with special reference to Penstemon. Pl Spec Biol 15:11–29. doi: 10.1046/j.1442-1984.2000.00026.x CrossRefGoogle Scholar
  56. Thorp RW (1979) Structural, behavioral, and physiological adaptations of bees (Apoidea) for collecting pollen. Ann Missouri Bot Gard 66:788–812. doi: 10.2307/2398919 CrossRefGoogle Scholar
  57. Tripp EA, Manos PS (2008) Is floral specialization an evolutionary dead-end? Pollination system transitions in Ruellia (Acanthaceae). Evolution 62:1712–1737. doi: 10.1111/j.1558-5646.2008.00398.x CrossRefPubMedGoogle Scholar
  58. Vallejo-Marín M, Manson JS, Thomson JD, Barrett SC (2009) Division of labour within flowers: heteranthery, a floral strategy to reconcile contrasting pollen fates. J Evolution Biol 22:828–839. doi: 10.1111/j.1420-9101.2009.01693.x CrossRefGoogle Scholar
  59. Varassin IG, Penneys DS, Michelangeli FA (2008) Comparative anatomy and morphology of nectar-producing Melastomataceae. Ann Bot (Oxford) 102:899–909. doi: 10.1093/aob/mcn180 CrossRefGoogle Scholar
  60. Waser NM, Ollerton J (2006) Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, ChicagoGoogle Scholar
  61. Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060. doi: 10.2307/2265575 CrossRefGoogle Scholar
  62. Waser NM, Ollerton J, Erhardt A (2011) Typology in pollination biology: lessons from an historical critique. J Pollinat Ecol 3:1–7Google Scholar
  63. Westerkamp C (1996) Pollen in bee-flower relations Some considerations on melittophily. Bot Acta 109:325–332. doi: 10.1111/j.1438-8677.1996.tb00580.x CrossRefGoogle Scholar
  64. Westerkamp C, Claßen-Bockhoff R (2007) Bilabiate flowers—the ultimate response to bees? Ann Bot (Oxford) 100:361–374. doi: 10.1093/aob/mcm123 CrossRefGoogle Scholar
  65. Whitall JB, Hodges SA (2007) Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447:706–709. doi: 10.1038/nature05857 CrossRefGoogle Scholar
  66. Wilson P, Wolfe AD, Armbruster WS, Thomson JD (2007) Constrained lability in floral evolution: counting convergent origins of hummingbird pollination in Penstemon and Keckiella. New Phytol 176:883–890. doi: 10.1111/j.1469-8137.2007.02219.x CrossRefPubMedGoogle Scholar
  67. Zych M, Michalska B, Krasicka-Korczyńska E (2014) Myophily in the critically endangered umbelliferous plant Ostericum palustre Besser (Apiaceae). Pl Syst Evol 300:187–196. doi: 10.1007/s00606-013-0870-2 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2017

Authors and Affiliations

  • Vinícius L. G. de Brito
    • 1
    • 2
    Email author
  • André R. Rech
    • 3
  • Jeff Ollerton
    • 4
  • Marlies Sazima
    • 5
  1. 1.Programa de Pós-Graduação em Biologia Vegetal, Instituto de BiologiaUniversidade Estadual de CampinasCampinasBrazil
  2. 2.Instituto de BiologiaUniversidade Federal de UberlândiaUberlândiaBrazil
  3. 3.Curso de Licenciatura em Educação do Campo, Faculdade Interdisciplinar de HumanidadesUniversidade Federal dos Vales do Jequitinhonha e MucuriDiamantinaBrazil
  4. 4.Landscape and Biodiversity Research Group, School of Science and TechnologyThe University of NorthamptonNorthamptonUK
  5. 5.Departamento de Biologia Vegetal, Instituto de BiologiaUniversidade Estadual de CampinasCampinasBrazil

Personalised recommendations