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Bee pollination and evidence of substitutive nectary in Anadenanthera colubrina (Leguminosae-Mimosoideae)

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Abstract

Anadenanthera colubrina (Vell.) Brenan (Leguminosae-Mimosoideae) is a widely-distributed tree in seasonally dry tropical forests of South America that was classified previously as lacking nectaries. However, some studies have stated that its flowers produce nectar, while others analyzed the composition of unifloral honey produced from A. colubrina flowers, raising the question about nectar production in the species. We studied the pollination and reproductive biology of A. colubrina var. cebil (Griseb.) Altschul in a natural population in the Caatinga, northeastern Brazil. Reproductive phenology, sexual system, floral biology, resource, and pollinators were investigated. We analyzed the breeding system through controlled pollinations for addressing its dependence on pollen vectors for reproduction. Anadenanthera colubrina flowered in the dry season, flower heads are heteromorphic, with staminate flowers at the base and perfect flowers at the apex of the inflorescence, characterizing andromonoecy. Anthesis is diurnal. We observed small drops of nectar at the apex of the petals of some flowers per inflorescence. Together with observations on flower visitor behavior and histochemical tests, we propose that A. colubrina produces floral nectar at the apex of the corolla, characterizing a substitutive nectary (sensu Vogel). This is the first record of substitutive nectary in the Mimosoideae and the first record of andromonoecy in the genus. Bees were the main pollinators (higher frequency), although other insects such as wasps, butterflies, and small beetles were also observed collecting nectar and/or pollen. The species is self-incompatible, thus depending on insect pollen vectors, mainly bees, for reproduction.

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References

  • Altschul SR (1964) A taxonomic study of the genus Anadenanthera. Contrib Gray Herb Harvard Univ 193:1–65

    Google Scholar 

  • Ancibor E (1969) Los nectarios florales en Leguminosas-Mimosóideas. Darwiniana 15:128–142

    Google Scholar 

  • Araújo ED, Costa M, Chaud-Netto J, Fowler HG (2004) Body size and flight distance in stingless bees (Hymenoptera: Meliponini): inference of flight range and possible ecological implications. Braz J Biol 64:563–568

    Article  PubMed  Google Scholar 

  • Arroyo MTK (1981) Breeding systems and pollination biology in Leguminosae. In: Polhill RM, Raven PH (eds) Advances in Legume Systematics, Part 2. Royal Botanic Gardens, Kew, London, pp 723–769

    Google Scholar 

  • Avila R Jr, Pinheiro M, Sazima M (2015) The generalist Inga subnuda subsp. luschnathiana (Fabaceae): negative effect of floral visitors on reproductive success? Plant Biol 17:728–733

    Article  PubMed  Google Scholar 

  • Bawa KS, Beach JH (1981) Evolution of sexual systems in flowering plants. Ann Mo Bot Gard 68:254–274

    Article  Google Scholar 

  • Bawa KS, Webb CJ (1984) Flower, fruit and seed abortion in tropical forest trees: implications for the evolution of paternal and maternal reproductive patterns. Am J Bot 71:736–751

    Article  Google Scholar 

  • Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796

    Article  CAS  PubMed  Google Scholar 

  • Costa RB, Kageyama PY, Mariano G (1992) Estudo do sistema de cruzamento de Anadenanthera falcata Benth., Vochysia tucanorum Mart. e Xylopia aromatica Baill., em área de cerrado. Rev Bras Sementes 14:93–96

    Article  Google Scholar 

  • Costa RB, Contini AZ, Melo ESP (2003) Sistema reprodutivo de Anadenanthera peregrina (L.) Speg e Vochysia haenkiana (Spreng.) Mart. em fragmento de cerrado na Chapada dos Guimarães—MT. Cienc Rural 33:305–310

    Article  Google Scholar 

  • Da Costa Leite JM, Trugo LC, Costa LSM, Quinteiro LMC, Barth OM, Dutra VML, Maria CAB (2000) Determination of oligosaccharides in Brazilian honeys of different botanical origin. Food Chem 70:93–98

    Article  Google Scholar 

  • Endress PK (1994) Diversity and evolutionary biology of tropical flowers. Cambridge tropical biology series. Cambridge University Press, Cambridge

    Google Scholar 

  • Faegri K, Pijl L (1979) The principles of pollination ecology. Pergamon Press, London

    Google Scholar 

  • Ferraz EMN, Rodal MJN, Sampaio EVSB (2003) Physiognomy and structure of vegetation along an altitudinal gradient in the semi-arid region of northeastern Brazil. Phytocoenologia 33:71–92

    Article  Google Scholar 

  • Kenrick J (2003) Review of pollen-pistil interactions and their relevance to the reproductive biology of Acacia. Aust Syst Bot 16:119–130

    Article  Google Scholar 

  • Koptur S (1983) Flowering phenology and floral biology of Inga (Fabaceae: Mimosoideae). Syst Bot 8:354–368

    Article  Google Scholar 

  • Kraus JE, Arduin M (1997) Manual Básico de Métodos em Morfologia Vegetal. Editora Universidade Rural Seropédica, Rio de Janeiro

    Google Scholar 

  • Lewis GP, Elias TS (1981) Tribe 3. Mimoseae Bronn (1822). In: Polhill RM, Raven PH (eds) Advances in legume systematics, Part 1. Royal Botanic Gardens, Kew, London, pp 155–168

    Google Scholar 

  • Lewis GP, Schrire B, Mackinder B, Lock M (2005) Legumes of the world. Royal Botanic Gardens, Kew, London

    Google Scholar 

  • Linares-Palomino R, Oliveira-Filho AT, Pennington RT (2011) Neotropical seasonally dry forests: diversity, endemism, and biogeography of woody plants. In: Dirzo R, Young HS, Mooney HA, Ceballos G (eds) seasonally dry tropical forests—Ecology and conservation. Island Press, Washington, pp 3–21

    Chapter  Google Scholar 

  • Lopez-Portillo J, Eguiarte LE, Montana C (1993) Nectarless honey mesquites. Funct Ecol 7:452–461

    Article  Google Scholar 

  • Luckow M (2005) Tribe Mimoseae. In: Lewis GP, Schrire B, MacKinder B, Lock M (eds) Legumes of the world. Royal Botanic Gardens, Kew, London, pp 163–183

    Google Scholar 

  • Machado ICS, Barros LM, Sampaio EVSB (1997) Phenology of caatinga species at Serra Talhada, PE, Northeastern Brazil. Biotropica 29:57–68

    Article  Google Scholar 

  • Maia-Silva C, Silva CI, Hrncir M, Queiroz RT, Imperatriz-Fonseca VL (2012) Guia de plantas visitadas por abelhas na Caatinga. Editora Fundação Brasil Cidadão, Fortaleza

    Google Scholar 

  • Marinho CR, Souza CD, Barros TC, Teixeira SP (2014) Scent glands in legume flowers. Plant Biol 16:215–226

    Article  CAS  PubMed  Google Scholar 

  • Miller JS, Diggle PK (2007) Correlated evolution of fruit size and sexual expression in andromonoecious Solanum sections Acanthophora and Lasiocarpa (Solanaceae). Am J Bot 94:1706–1715

    Article  PubMed  Google Scholar 

  • Ortiz PL, Arista M, Oliveira PE, Talavera S (2003) Pattern of flower and fruit production in Stryphnodendron adstringens, an Andromonoecious legume tree of Central Brazil. Plant Biol 5:592–599

    Article  Google Scholar 

  • Pereira FM, Freitas BM, Alves JE, Camargo RCR, Lopes MTR, Vieira-Neto JM, Rocha RS (2004) Flora Apícola do Nordeste. Embrapa Meio-Norte, Teresina

    Google Scholar 

  • Pires JPA, Freitas L (2008) Reproductive biology of two tree species of Leguminosae in a montane rain forest in southeastern Brazil. Flora 203:491–498

    Article  Google Scholar 

  • Prado DE, Gibbs PE (1993) Patterns of species distributions in the dry seasonal forests of South America. Ann Mo Bot Gard 80:902–927

    Article  Google Scholar 

  • Queiroz LP (2009) Leguminosas da caatinga. Universidade Estadual de Feira de Santana, Feira de Santana

    Google Scholar 

  • Santos A, Moreira RFA, Maria CAB (2015) Study of the principal constituents of tropical angico (Anadenanthera sp.) honey from the atlantic forest. Food Chem 171:421–425

    Article  CAS  PubMed  Google Scholar 

  • Schrire BD, Lewis GP, Lavin M (2005) Biogeography of the Leguminosae. In: Lewis GP, Schrire B, MacKinder B, Lock M (eds) Legumes of the world. Royal Botanic Gardens, Kew, London, pp 21–54

    Google Scholar 

  • Sedgley M, Harbard J, Smith R-MM, Wickneswari R, Griffin AR (1992) Reproductive biology and interspecific hibridisation of Acacia mangium and Acacia auriculiformis A. Cunn. Ex Benth. (Leguminosae: Mimosoideae). Aust J Bot 40:37–48

    Article  Google Scholar 

  • Silva LMB, Barbosa DCA (2000) Crescimento e sobrevivência de Anadenanthera macrocarpa (Benth.) Brenan (Leguminosae), em uma área de Caatinga, Alagoinha, PE. Acta Bot Bras 14:251–261

    Article  Google Scholar 

  • Stone GN, Raine NE, Prescott M, Willmer PG (2003) Pollination ecology of Acacias (Fabaceae, Mimosoideae). Aust Syst Bot 16:103–118

    Article  Google Scholar 

  • Torres C, Eynard MC, Aizen MA, Galetto L (2002) Selective fruit maturation and seedling performance in Acacia caven (Fabaceae). Int J Plant Sci 163:809–813

    Article  Google Scholar 

  • Tybirk K (1993) Pollination, breeding system and seed abortion in some African Acacia species. Bot J Linn Soc 112:107–137

    Article  Google Scholar 

  • Vallejo-Marín M, Rausher MD (2007) Selection through female fitness helps to explain the maintenance of male flowers. Am Nat 169:563–568

    Article  PubMed  Google Scholar 

  • Vogel S (1990) Radiación adaptativa del síndrome floral em las familias neotropicales. Bol Acad Nac Cienc Córdoba 59:5–30

    Google Scholar 

  • Vogel S (1997) Remarkable nectaries: structure, ecology, organophyletic perspectives. I. Substitutives nectaries. Flora 192:305–333

    Article  Google Scholar 

  • Vogel S, Lopes AV, Machado IC (2005) Bat pollination in the NE Brazilian endemic Mimosa lewisii: an unusual case and first report for the genus. Taxon 54:693–700

    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 

Download references

Acknowledgements

The authors thank the Instituto Agronômico de Pernambuco (IPA) for the permission to study on lands of the Estação Experimental de Serra Talhada; Gilcean Jones and Thamires Campos for help in field work; Carlos Eduardo Nobre for identifying the butterfly and Gisele Azevedo for identifying the wasp; Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for funding through a PhD Fellowship to L. A. Borges; a Research Grant to I. C. Machado and A. V. Lopes, and financial support to A. V. Lopes (CNPq Grant Numbers 567739/2008-2; 307209/2010-5 and 308832/2014-0).

Funding

Funding was provided by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) through a PhD Fellowship to L. A. Borges, a Research Grant to I. C. Machado and A. V. Lopes, and financial support to A. V. Lopes (CNPq Grant Numbers 567739/2008-2; 307209/2010-5 and 308832/2014-0).

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Correspondence to Ariadna Valentina Lopes.

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Borges, L.A., Machado, I.C. & Lopes, A.V. Bee pollination and evidence of substitutive nectary in Anadenanthera colubrina (Leguminosae-Mimosoideae). Arthropod-Plant Interactions 11, 263–271 (2017). https://doi.org/10.1007/s11829-017-9514-8

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