Skip to main content
SpringerLink
Log in

Phenology, reproductive biology and diversity of buzzing bees of sympatric Dichorisandra species (Commelinaceae): breeding system and performance of pollinators

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

This paper reports on phenology, breeding system and dependence on pollinators of two sympatric Dichorisandra species. Dichorisandra incurva is a chamaephyte with continuous growth and precocious flowering, whereas D. hexandra is a geophyte with seasonal growth and delayed flowering. Flowering and fruiting occur mainly in the wet season; thus moisture can be important for both species. Besides moisture, photoperiod seems also to be related to the flowering only of D. incurva. Flowers of both species are poricidal, oligandrous, zygomorphic and buzz-pollinated by Apidae and/or Halictidae bees. Dichorisandra incurva is self-compatible, while D. hexandra shows a late-acting self-incompatible system. Moreover, herkogamy and poricidal anthers prevent spontaneous self-pollination in D. incurva. Therefore, medium- to large-sized Apidae are the most suitable pollinators as they make regular contact with anthers and stigmas and are further known to perform trapline foraging. This behaviour is particularly important for D. hexandra where Halictidae are considered pollen robbers, thus wasting pollen which, consequently, causes low reproductive efficacy in this species. Nevertheless, bee diversity is probably advantageous for the reproductive success of both Dichorisandra species. While the efficiency of each bee species is not known, further studies will show whether additional benefits are gained from the maintenance of these interactions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alexander MP (1980) A versatile stain for pollen, fungi, yeast and bacteria. Stain Technol 55:13–18

    CAS  PubMed  Google Scholar 

  • Ando T, Nomura M, Tsukahara J, Watanabe H, Kokubun H, Tsukamoto T, Hashimoto G, Marchesi E, Kitching IJ (2001) Reproductive isolation in a native population of Petunia sensu Jussieu (Solanaceae). Ann Bot (Oxford) 88:403–413

    Article  Google Scholar 

  • Aona LYS, Amaral MCE (2009) Flora da Serra do Cipó, Minas Gerais: Commelinaceae. Bol Bot Univ São Paulo 27:253–258

    Google Scholar 

  • Aona LYS; Pellegrini MOO (2014). Commelinaceae. In: Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB6924. Accessed 28 June 2014

  • Aona LYS, Faden RB, Amaral MCE (2011) Five new species of Dichorisandra J. C. Mikan (Commelinaceae) from Bahia State Brazil. Kew Bull 66:479–491

    Article  Google Scholar 

  • Aona-Pinheiro LYS, Amaral MCE (2012) Four new species of Dichorisandra J.C. Mikan (Commelinaceae) from Southeast Brazil. Phytotaxa 48:7–22

    Google Scholar 

  • Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell D, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421

    Article  Google Scholar 

  • Batalha MA, Martins FR (2004) Reproductive phenology of the Cerrado plant community in Emas National Park (central Brazil). Austral J Bot 52:149–161

    Article  Google Scholar 

  • Benavides AN, Wolf JHD, Duivenvoorden JF (2006) Recovery and succession of epiphytes in upper Amazonian fallows. J Trop Ecol 22:705–717

    Article  Google Scholar 

  • Boaventura YMS, Mathes LAF (1987) Aspectos da biologia da reprodução em plantas ornamentais cultivadas no estado de São Paulo: i – Dichorisandra thyrsiflora Mikan (Commelinaceae). Acta Bot Brasil 1:189–199

    Article  Google Scholar 

  • Buchmann SL (1983) Buzz pollination in Angiosperms. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinhold Inc., New York, pp 73–113

    Google Scholar 

  • Charlesworth B, Charlesworth D (2000) Reproductive isolation: natural selection at work. Curr Biol 10:R68–R70

    Article  CAS  PubMed  Google Scholar 

  • Coleman JR, Coleman MA (1982) Reproductive biology of an andromonoecious Solanum (S. palinacanthum Dunal). Biotropica 14:69–75

    Article  Google Scholar 

  • Cuevas J, Polito VS (2004) The role of staminate flowers in the breeding system of Olea europaea (Oleaceae): an andromonoecious, wind-pollinated taxon. Ann Bot (Oxford) 93:547–553

    Article  Google Scholar 

  • Dafni A (1992) Pollination ecology: a practical approach. Oxford University Press, Oxford

    Google Scholar 

  • Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analysing ecological networks. R News 8:8–11

    Google Scholar 

  • Faden RB (1983) Isolating mechanisms among five sympatric species of Aneilema R.Br. (Commelinaceae) in Kenya. Bothalia 14:997–1002

    Google Scholar 

  • Faden RB, Hunt DR (1991) The classification of the Commelinaceae. Taxon 40:19–31

    Article  Google Scholar 

  • Frankie GW, Haber WA, Opler PA, Bawa KS (1983) Characteristics and organization of the large bee pollination system in the Costa Rican dry forest. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinhold Inc., New York, pp 411–447

    Google Scholar 

  • Gardner M, Macnair M (2000) Factors affecting the co-existence of the serpentine endemic Mimulus nudatus Curran and its presumed progenitor, Mimulus guttatus Fischer ex DC. Biol J Linn Soc 69:443–459

    Article  Google Scholar 

  • Gotelli NJ, Entsminger GL (2000) EcoSiM: Null models software for ecology. Version 7 Acquired Intelligence Inc. & Kesey-Bear, Jericho VT. 05465. http://garyentsminger.com/ecosim/index.htm. Accessed 04 July 2013

  • Grossman GD (1986) Food resources partitioning in a rocky intertidal fish assemblage. J Zool 1:317–355

    Article  Google Scholar 

  • Hardy CR, Stevenson DW, Kiss HG (2000) Development of the gametophytes, flower, and floral vasculature in Dichorisandra thyrsiflora (Commelinaceae). Amer J Bot 87:1228–1239

    Article  CAS  Google Scholar 

  • Hopkins MJG, Hopkins HCF, Sothers CA (2000) Nocturnal pollination of Parkia velutina by Megalopta bees in Amazonia and its possible significance in the evolution of chiropterophily. J Trop Ecol 16:733–746

    Article  Google Scholar 

  • Hrycan WC, Davis AR (2005) Comparative structure and pollen production of the stamens and pollinator-deceptive staminodes of Commelina coelestis and C. dianthifolia (Commelinaceae). Ann Bot (Oxford) 95:1113–1130

    Article  Google Scholar 

  • Janzen DH (1971) Euglossine bees as long-distance pollinators of tropical plants. Science 171:203–205

    Article  CAS  PubMed  Google Scholar 

  • Johnson J, Omland K (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108

    Article  PubMed  Google Scholar 

  • Kaul V, Koul AK (2008) Floral phenology in relation to pollination and reproductive output in Commelina caroliniana (Commelinaceae). Austral J Bot 56:59–66

    Article  Google Scholar 

  • Kaul V, Koul AK (2009) Sex expression and breeding strategy in Commelina benghalensis L. J Biosci 34:977–990

    Article  PubMed  Google Scholar 

  • Kawai Y, Kudo G (2009) Effectiveness of buzz pollination in Pedicularis chamissonis: significance of multiple visits by bumblebees. Ecol Res 24:215–223

    Article  Google Scholar 

  • Kouonon LC, Jacquemart AL, Bi AIZ, Bertin P, Baudoin JP, Dje Y (2009) Reproductive biology of the andromonoecious Cucumis melo subsp. agrestis (Cucurbitaceae). Ann Bot 104:1129–1139

    Article  PubMed Central  PubMed  Google Scholar 

  • Kovach W (2004) Oriana Version 2.0 for Windows. Kovach Computing Services, Anglesey,Wales

  • Larson BMH, Barret SCH (2000) A comparative analysis of pollen limitation in flowering plants. Biol J Linn Soc 69:503–520

    Article  Google Scholar 

  • Lloyd DG, Webb CJ, Dulberger R (1990) Heterostyly in species of Narcissus (Amaryllidaceae) and Hugonia (Linaceae) and other disputed cases. P1 Syst Evol 172:215–227

    Article  Google Scholar 

  • Maia DC (2006) Estudo taxonômico dos gêneros Commelina L. e Dichorisandra J.C. Mikan (Commelinaceae), no estado do Paraná, Brasil. Dissertation. Federal University of Paraná

  • Marques MCM, Roper JJ, Salvalaggio APB (2004) Phenological patterns among plant life-forms in a subtropical forest in southern Brazil. Pl Ecol 173:203–213

    Article  Google Scholar 

  • Martin FW (1959) Staining and observing pollen tubes in the style by means of fluorescence. Stain Technol 34:125–128

    CAS  PubMed  Google Scholar 

  • Mikich SB, Silva SM (2001) Composição florística e fenologia das espécies zoocóricas de remanescentes de floresta estacional semidecidual no Centro-Oeste do Paraná Brasil. Acta Bot Brasil 15:89–113

    Article  Google Scholar 

  • Monasterio M, Sarmiento G (1976) Phenological strategies of plant species in the tropical savannah and the semi-deciduous forest of the Venezuelan Llanos. J Biogeogr 3:325–355

    Article  Google Scholar 

  • Morellato PC (1995) As estações do ano na floresta. In: Leitão Filho HF, Morellato LP (eds) Ecologia e preservação de uma floresta tropical urbana – reserva de Santa Genebra. Editora da Unicamp, Campinas. pp 37–41

  • Morellato LPC, Leitão Filho HF (1996) Reproductive phenology of climbers in a southeastern Brazilian forest. Biotropica 28:180–191

    Article  Google Scholar 

  • Morellato LPC, Alberti LF, Hudson IL (2010) Applications of circular statistics in plant phenology: a case studies approach. In: Hudson IL, Keatley MR (eds) Phenological Research: methods for environmental and climate change analysis. Springer, London, pp 339–359

    Chapter  Google Scholar 

  • Neal PR, Anderson GJ (2005) Are ‘mating systems’ ‘breeding systems’ of inconsistent and confusing terminology in plant reproductive biology? or is it the other way around? Pl Syst Evol 250:173–185

    Article  Google Scholar 

  • Newstrom LE, Frankie GW, Baker HG (1994) A new classification for plant phenology based on flowering patterns in lowland tropical rain forest tress at La Selva, Costa Rica. Biotropica 26:41–159

    Article  Google Scholar 

  • Ohashi K, Thomson JD (2009) Trapline foraging by pollinators: its ontogeny, economics and possible consequences for plants. Ann Bot (Oxford) 103:1365–1378

    Article  Google Scholar 

  • Oliveira PE (2008) Fenologia e biologia reprodutiva das espécies de Cerrado. In: Sano SM, Almeida SP, Ribeiro JF (eds) Cerrado: ecologia e flora, vol 1. EMBRAPA Cerrados, Brasília, pp 274–290

    Google Scholar 

  • Owens SJ (1981) Self-incompatibility in the Commelinaceae. Ann Bot (Oxford) 47:567–581

    Google Scholar 

  • Pianka ER (1973) The structure of lizard communities. Annual Rev Ecol Syst 4:53–74

    Article  Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing, R Foundation for Statistical Computing. Vienna, Austria. http://www.R-project.org Accessed 03 July 2013

  • Radford AE, Dickinson WC, Massey JR, Bell CR (1974) Vascular plant systematics. Harper & Row Publishers, New York

    Google Scholar 

  • Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Annual Rev Ecol Syst 16:179–214

    Article  Google Scholar 

  • Rocha-Filho LC, Krug C, Silva CI, Garófalo CA (2012) Floral resources used by Euglossini bees (Hymenoptera: apidae) in coastal ecosystems of the Atlantic Forest. Psyche 2012:1–13

    Article  Google Scholar 

  • Sarmiento G, Monasterio M (1983) Life forms and phenology. In: Bouliere F (ed) Ecosystems of the world: tropical savannas. Elsevier Science, Amsterdan, pp 79–108

    Google Scholar 

  • Seavey SR, Bawa K (1986) Late-acting self-incompatibility in Angiosperms. Bot Rev 52:195–219

    Article  Google Scholar 

  • Snow AA, Spira TP, Simpson R, Klips RA (1996) The ecology of geitonogamous pollination. In: Lloyd DG, Barrett SCH (eds) Floral biology: studies on floral evolution in animal-pollinated plants. Chapman Hall, New York, pp 191–216

    Chapter  Google Scholar 

  • Solomon BP (1986) Sexual allocation and andromonoecy: resource investment in male and hermaphrodite flowers of Solanum carolinense (Solanaceae). Amer J Bot 73:1215–1221

    Article  Google Scholar 

  • Steiner J, Zillikens A, Kamke R, Feja EP, Falkenberg DB (2010) Bees and melittophilous plants of secondary Atlantic forest habitats at Santa Catarina island, southern Brazil. Oecologia Austral 14:16–39

    Article  Google Scholar 

  • Ushimaru A, Itagaki T, Ishii HS (2003) Floral correlations in an andromonoecious species, Commelina communis (Commelinaceae). Pl Spec Biol 18:103–106

    Article  Google Scholar 

  • van Schaik CP, Terborgh JW, Wright SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annual Rev Ecol Syst 24:353–377

    Article  Google Scholar 

  • Vogel S (1978) Evolutionary shifts from reward to deception in pollen flowers. In: Richards AJ (ed) The pollination of flowers by insects. Academic Press, London, pp 89–96

    Google Scholar 

  • Wcislo WT, Arneson L, Roesch K, Gonzalez V, Smith A, Fernández H (2004) The evolution of nocturnal behaviour in sweat bees, Megalopta genalis and M. ecuadoria (Hymenoptera: halictidae): an escape from competitors and enemies? Biol J Linn Soc 83:377–387

    Article  Google Scholar 

  • Whalen MD, Costich DE (1986) Andromonoecy in Solanum. In: D’Arcy WG (ed) Solanaceae. Columbia University Press, New York, Biology and Systematics, pp 284–302

    Google Scholar 

  • Yang C, Gituru RW, Guo Y (2007) Reproductive isolation of two sympatric louseworts, Pedicularis rhinanthoides and Pedicularis longiflora (Orobanchaceae): how does the same pollinator type avoid interspecific pollen transfer? Biol J Linn Soc 90:37–48

    Article  Google Scholar 

  • Zapata TR, Arroyo MTK (1978) Plant reproductive ecology of a secondary deciduous tropical forest in Venezuela. Biotropica 10:221–230

    Article  Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th edn. Pearson Prentice-Hall, New Jersey

    Google Scholar 

Download references

Acknowledgments

We thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for financial support to MRS and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) to MS. We are also grateful to anonymous reviewers for valuable comments, the Fundação José Pedro de Oliveira for permission to work at Santa Genebra Reserve, S.R. de M. Pedro, for bee identification; Luciano Paganucci Queiroz for pollen tube studies; Camila Aoki and Luis Fernando Alberti for phenological analysis; and Augusto Cesar de Aquino Ribas for the visiting bee species graph by R.

Author information

Authors and Affiliations

  1. Laboratório de Botânica, Centro de Ciências Biológicas e da Saúde, Caixa Postal 549, Universidade Federal de Mato Grosso do Sul, 79070-900, Campo Grande, Mato Grosso do Sul, Brazil

    Maria Rosângela Sigrist

  2. Departamento de Biologia Vegetal, Caixa Postal 6109, Universidade Estadual de Campinas, 13083-970, Campinas, São Paulo, Brazil

    Marlies Sazima

Authors
  1. Maria Rosângela Sigrist
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marlies Sazima
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria Rosângela Sigrist.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sigrist, M.R., Sazima, M. Phenology, reproductive biology and diversity of buzzing bees of sympatric Dichorisandra species (Commelinaceae): breeding system and performance of pollinators. Plant Syst Evol 301, 1005–1015 (2015). https://doi.org/10.1007/s00606-014-1131-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-014-1131-8

Keywords

Search

Navigation