Plant Systematics and Evolution

, Volume 305, Issue 4, pp 281–291 | Cite as

Study of the reproductive biology of an Amazonian Heterotaxis (Orchidaceae) demonstrates the collection of resin-like material by stingless bees

  • Amauri H. Krahl
  • Ana S. S. de Holanda
  • Dayse R. P. Krahl
  • Maria E. P. Martucci
  • Leonardo Gobbo-Neto
  • Antonio C. Webber
  • Emerson R. PansarinEmail author
Original Article


Tropical and subtropical plants provide to pollinators a range of nutritive and non-nutritive materials as alternative to pollen and nectar, including resins, which are gathered by females of several groups of social and solitary bees. Although resin-like material has previously been recorded in Maxillariinae, these investigations generally did not present data relating to pollinators. In fact, the collection of resins has never been recorded elsewhere in orchids. The aim of this paper was to provide a detailed study of the reproductive biology of an Amazonian Heterotaxis, H. superflua, based on records of flowering phenology, floral morphology, pollinator behavior and breeding system. Heterotaxis superflua offers resin-like material to pollinators and is pollinated by a single species of stingless bee. The resin is a heterogeneous material rich in mucilage, starch and sugars, while lipoidal substances occur as small droplets. Chemical analyses confirm the presence of sugar, which explain the presence of reducing sugars and mucilage detected in the histochemical investigations. Our data also showed the Heterotaxis is self-compatible and pollinator dependent. This study demonstrates for the first time the collection of resin-like material in orchids. The gathering of resin is frequently associated with the nest construction, since this material is considered to be a water-repellent and has anti-pathogen chemical properties. Despite offering of a floral reward, fruit set under natural conditions is lower than for experimental pollinations, suggesting limited pollen flow within the population.


Floral reward Maxillariinae Meliponini bees Reproductive biology Resin Trigona 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. Anderson AB (1981) White-sand vegetation of Brazilian Amazonia. Biotropica 13:99–210CrossRefGoogle Scholar
  2. Armbruster WS (1984) The role of resin in angiosperm pollination: ecological and chemical considerations. Amer J Bot 71:1149–1160CrossRefGoogle Scholar
  3. ArmbrusterWS Webster GL (1981) Sistemas de polinização de duas espécies simpátricas de Dalechampia (Euphorbiaceae) no Amazonas, Brasil. Acta Amazonica 11:13–17CrossRefGoogle Scholar
  4. Baker HG, Baker I (1986) The occurrence and significance of amino-acids in floral nectar. Pl Syst Evol 151:175–186CrossRefGoogle Scholar
  5. Blanco MA, Carnevali G, Whitten WM, Singer RB, Koehler S, Williams NH, Ojeda I, Neubig KM, Endara L (2007) Generic realignments in Maxillariinae (Orchidaceae). Lankesteriana 7:515–537. Google Scholar
  6. Braga PIS (1977) Aspectos biológicos das Orchidaceae de uma campina da Amazônia Central. Acta Amazonica 7:1–89Google Scholar
  7. Clarke AE, Andreson RL, Stone BA (1979) Form and function of arabinogalactans and arabinogalactan-proteins. Phytochemistry 18:521–540CrossRefGoogle Scholar
  8. Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899CrossRefGoogle Scholar
  9. Cushnie TPT, Lamb AJ (2011) Recent advances in understanding the antibacterial properties of flavonoids. Int J Antimicrob Agents 38:99–107. CrossRefGoogle Scholar
  10. Dafni A (1992) Pollination ecology: a practical approach. Oxford University Press, OxfordGoogle Scholar
  11. Davies KL, Stpiczyńska M (2006) Labellar micromorphology of Bifrenariinae Dressler (Orchidaceae). Ann Bot (Oxford) 98:1215–1231. CrossRefGoogle Scholar
  12. Davies KL, Stpiczyńska M (2012) Comparative labellar anatomy of resin-secreting and putative resin-mimic species of Maxillaria s.l. (Orchidaceae: Maxillariinae). Bot J Linn Soc 170:405–435. CrossRefGoogle Scholar
  13. Davies KL, Stpiczyńska M (2017) Comparative floral micromorphology and the ultrastructural basis of fragrance production in pseudocopulatory Mormolyca s.s. and non-pseudocopulatory Maxillaria section Rufescens s.s. (Orchidaceae). Bot J Linn Soc 185:81–112. CrossRefGoogle Scholar
  14. Davies KL, Turner MP (2004) Morphology of Floral Papillae in Maxillaria Ruiz & Pav. (Orchidaceae). Ann Bot (Oxford) 93:75–86CrossRefGoogle Scholar
  15. Davies KL, Roberts DL, Turner MP (2002) Pseudopollen and food-hair diversity in Polystachya Hook. (Orchidaceae). Ann Bot (Oxford) 90:477–484CrossRefGoogle Scholar
  16. Davies KL, Turner MP, Gregg A (2003a) Lipoidal labellar secretions in Maxillaria Ruiz & Pav. (Orchidaceae). Ann Bot (Oxford) 91:439–446CrossRefGoogle Scholar
  17. Davies KL, Turner MP, Gregg A (2003b) Atypical pseudopollen-forming hairs in Maxillaria Ruiz & Pav. (Orchidaceae). Bot J Linn Soc 143:151–158CrossRefGoogle Scholar
  18. de Barros F,Vinhos F, Rodrigues VT, Barberena FFVA, Fraga CN, Pessoa, EM, Forster W, Menini Neto L, Furtado SG, Nardy C, Azevedo CO, Guimarães LRS (2015) Orchidaceae in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. Available at: Accessed 10 Oct 2017
  19. Drescher N, Wallace HM, Katouli M, Massaro CF, Leonhardt SD (2014) Diversity matters: how bees benefit from different resin sources. Oecologia 176:943–953. CrossRefGoogle Scholar
  20. Faegri K, van der Pijl L (1979) The principles of pollination Ecology. Pergamon Press, OxfordGoogle Scholar
  21. Flach A, Dondon RC, Singer RB, Koehler S, Amaral MCE, Marsaioli AJ (2004) The chemistry of pollination in selected Brazilian Maxillariinae orchids: floral rewards and fragrance. J Chem Ecol 30:1045–1056CrossRefGoogle Scholar
  22. Flach A, Marsaioli AJ, Singer RB, Amaral MCE, Menezes C, Ker WE, Batista-Pereira LG, Corrêa AG (2006) Pollination by sexual mimicry in Mormolyca ringens: a floral chemistry that remarkably matches the pheromones of virgin queens of Scaptotrigona sp. J Chem Ecol 32:59–70CrossRefGoogle Scholar
  23. Franz G (1979) Metabolism of reserve polysaccharides in tubers of Orchis morio L. Pl Med 36:68–73CrossRefGoogle Scholar
  24. Gonzáles ML (1999) Polisacáridos. In: Fresno AMV del (ed) Farmacognosia general. Ed. Síntesis, Madrid, pp 335Google Scholar
  25. Gregory M, Baas P (1989) A survey of mucilage cells in vegetative organs of the dicotyledons. Israel J Bot 38:125–174Google Scholar
  26. Hendra R, Ahmad S, Sukari A, Shukor MY, Oskoueian E (2011) Flavonoid analyses and antimicrobial activity of various parts of Phaleria macrocarpa (Scheff.) Boerl fruit. Int J Molec Sci 12:3422–3431. CrossRefGoogle Scholar
  27. Hyde BB (1970) Mucilage-producing cells in the seed coat of Plantago ovata: developmental fine structure. Amer J Bot 57:1197–1206CrossRefGoogle Scholar
  28. Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Co., New YorkGoogle Scholar
  29. Kearns C, Inouye W (1993) Techniques for pollination biologists. University Press of Colorado, NiwotGoogle Scholar
  30. Köppen W (1948) Climatologia: com um estúdio de los climas de la tierra. Fondo de Cultura Econômica, GuadalajaraGoogle Scholar
  31. Krahl AH, Valsko JJ, Trindade DRP, Holanda ASS (2012) Sistema reprodutivo de quatro espécies amazônicas de Orchidaceae e implicações para a orquidofilia. Orquidario 26:63–68Google Scholar
  32. Krahl AH, Holanda ASS, Krahl DRP, Webber AC (2015) Polinização de Camaridium ochroleucum Lindl. (Orchidaceae: Maxillariinae). Biota Amazonica 5:1–7CrossRefGoogle Scholar
  33. Lipp CC, Goldstein G, Meinzer FC, Niemczura W (1994) Freezing tolerance and avoidance in high-elevation Hawaiian plants. Plant Cell Environ 17:1035–1044CrossRefGoogle Scholar
  34. Lokvam J, Braddock JF (1999) Anti-bacterial function in the sexually dimorphic pollinator rewards of Clusia graniflora (Clusiaceae). Oecologia 119:534–540CrossRefGoogle Scholar
  35. Luizão FJ (1995) Ecological studies in contrasting forest types in Central Amazonia. PhD Thesis, University of Stirling, StirlingGoogle Scholar
  36. Mickeliunas L, Pansarin ER, Sazima M (2006) Biologia floral, melitofilia e influência de besouros Curculionidae no sucesso reprodutivo de Grobya amherstiae Lindl. (Orchidaceae: Cyrtopodiinae). Revista Brasil Bot 29:251–258. CrossRefGoogle Scholar
  37. Nayaka HB, Londonkar RL, Umesh MK, Tukappa A (2014) Antibacterial Attributes of Apigenin, Isolated from Portulaca oleracea L. Int J Bacteriol 2014:1–10. CrossRefGoogle Scholar
  38. Ojeda I, Carnevali G, Williams NH, Whitten WM (2003) Phylogeny of the Heterotaxis Lindley complex (Maxillariinae): evolution of the vegetative architecture and pollination syndromes. Lankesteriana 7:45–47Google Scholar
  39. Okada H, Kubo S, Mori Y (1997) Pollination system of Neuwiedia veratrifolia Blume (Orchidaceae, Apostasioideae) in the Malesian wet tropics. Acta Phytotax Geobot 47:173–181Google Scholar
  40. Oliveira DMA, Porto AM, Bittrich V, Venancio I, Marsaioli AJ, Tidsskrift AJ (1996) Floral resins of Clusia spp.: chemical composition and biological function. Tetrahedron Lett 37:6427–6430CrossRefGoogle Scholar
  41. Pansarin ER, Amaral MCE (2006) Biologia reprodutiva e polinização de duas espécies de Polystachya Hook. No Sudeste do Brasil: evidências de pseudoceistogamia em Polystachyeae (Orchidaceae). Revista Brasil Bot 29:423–432CrossRefGoogle Scholar
  42. Pansarin ER, Amaral MCE (2008) Pollen and nectar as a reward in the basal epidendroid Psilochilus modestus (Orchidaceae: Triphoreae): a study of floral morphology, reproductive biology and pollination strategy. Flora 203:474–483. CrossRefGoogle Scholar
  43. Pansarin ER, Maciel AA (2017) Evolution of pollination systems involving edible trichomes in orchids. AoB PLANTS 10:plx033. Google Scholar
  44. Pansarin ER, Pansarin LM (2010) The family Orchidaceae in the Serra do Japi, State of São Paulo, Brazil. Springer, WienGoogle Scholar
  45. Pansarin ER, Pansarin LM (2011) Reproductive biology of Trichocentrum pumilum: an orchid pollinated by oil-collecting bees. Pl Biol (Stuttgart) 13:576–581. CrossRefGoogle Scholar
  46. Pansarin ER, Pedro SRM (2016) Reproductive biology of a hummingbird-pollinated Bilbergia: light influence on pollinator behaviour and specificity in a Brazilian semi-deciduous forest. Pl Biol (Stuttgart) 18:920–927. CrossRefGoogle Scholar
  47. Pansarin ER, Bittrich V, Amaral MCE (2006) At daybreak—reproductive biology and isolating mechanisms of Cirrhaea dependens (Orchidaceae). Pl Biol (Stuttgart) 8:494–502. CrossRefGoogle Scholar
  48. Pansarin LM, de Castro M, Sazima M (2009) Osmophore and elaiophores of Grobya amherstiae (Catasetinae, Orchidaceae) and their relation to pollination. Bot J Linn Soc 159:408–415. CrossRefGoogle Scholar
  49. Parra-Tabla V, Vargas CF, Magaña-Rueda S, Navarro J (2000) Female and male pollination success of Oncidium ascendens Lindley (Orchidaceae) in two contrasting habitat patches: forest vs agricultural field. Biol Conservation 94:335–340CrossRefGoogle Scholar
  50. Pimienta-Barrios E, Nobel PS (1998) Vegetative, reproductive and physiological adaptations to aridity of pitayo (Stenocereus queretaroensis, Cactaceae). Econ Bot 52:401–411CrossRefGoogle Scholar
  51. Pizzolato TD (1977) Staining of Tilia mucilages with Mayer’s tannic acid-ferric chloride. Bull Torrey Bot Club 104:277–279CrossRefGoogle Scholar
  52. Pridgeon AM, Cribb PJ, Chase MW, Rasmussen FN (2009) Genera orchidacearum 5: epidendroideae (part two). Oxford University Press, New YorkGoogle Scholar
  53. Purvis MJ, Collier DC, Walls D (1964) Laboratory techniques in botany. Butterwoths, LondonGoogle Scholar
  54. Robbirt KM, Roberts DL, Hutchings MJ, Davy AJ (2014) Potential disruption of pollination in a sexually deceptive orchid by climatic change. Curr Biol 24:2845–2849. CrossRefGoogle Scholar
  55. Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  56. Sakai WS (1973) Simple method for differential staining of paraffin embedded plant material using toluidine blue o. StainTechnol 43:247–249Google Scholar
  57. Sass JE (1951) Botanical microtechnique, 2nd edn. Iowa State College Press, AmesGoogle Scholar
  58. Schmidt-Adam G, Murray BG (2002) Structure and histochemistry of the stigma and style of Metrosideros excelsa. New Zealand J Bot 40:95–103CrossRefGoogle Scholar
  59. Scogin R, Young DA, Jones CE (1977) Anthochlor pigments and pollination biology: II. The ultraviolet patterns of Coreopsis gigantean (Asteraceae). Bull Torrey Bot Club 104:155–159CrossRefGoogle Scholar
  60. Simpson BB, Neff JL (1981) Floral rewards: alternatives to pollen and nectar. Ann Missouri Bot Gard 68:301–322CrossRefGoogle Scholar
  61. Singer RB (2002) The pollination mechanism in Trigonidium obtusum Lindl (Orchidaceae: Maxillariinae): sexual mimicry and trap-flowers. Ann Bot (Oxford) 89:157–163CrossRefGoogle Scholar
  62. Singer RB, Cocucci AA (1999) Pollination mechanisms in four sympatric Southern Brazilian Epidendroideae orchids. Lindleyana 14:47–56Google Scholar
  63. Singer RB, Koehler S (2004) Pollinarium morphology and floral rewards in Brazilian Maxillariinae (Orchidaceae). Ann Bot (Oxford) 93:39–51CrossRefGoogle Scholar
  64. Singer RB, Flach A, Koehler S, Marsaioli AJ, Amaral MCE (2004) Sexual mimicry in Mormolyca ringens (Lindl.) Schltr. (Orchidaceae: Maxillariinae). Ann Bot (Oxford) 93:755–762CrossRefGoogle Scholar
  65. Singer RB, Marsaioli AJ, Flach A, Reis MG (2006) The ecology and chemistry of pollination in Brazilian orchids: recent advances. Chapter 64. In: da Silva J (ed) Floriculture, ornamental and plant biotechnology, vol. IV. Global Science Books, Middlessex, pp 570–583Google Scholar
  66. Stpiczyńska M, Davies KL (2009) Floral, resin-secreting trichomes in Maxillaria dichroma Rolfe (Orchidaceae: Maxillariinae). Acta Agrobot 62:43–51CrossRefGoogle Scholar
  67. Tremblay RL (1992) Trends in pollination ecology of the Orchidaceae: evolution and systematic. Canad J Bot 70:642–650CrossRefGoogle Scholar
  68. Van der Pijl L, Dodson CH (1966) Orchid flowers: their pollination an evolution. University of Miami Press, Coral GablesGoogle Scholar
  69. Wu T, He M, Zang X, Zhou Y, Qiu T, Pan S, Xu X (2013) A structure-activity relationship study of flavonoids as inhibitors of E. coli by membrane interaction effect. Biochim Biophys Acta 1828:2751–2756. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  • Amauri H. Krahl
    • 1
  • Ana S. S. de Holanda
    • 1
  • Dayse R. P. Krahl
    • 1
  • Maria E. P. Martucci
    • 2
    • 3
  • Leonardo Gobbo-Neto
    • 3
  • Antonio C. Webber
    • 4
  • Emerson R. Pansarin
    • 5
    Email author
  1. 1.Departamento de BotânicaInstituto Nacional de Pesquisas da Amazônia, Programa de Pós-Graduação em BotânicaManausBrazil
  2. 2.Faculdade de Ciências Farmacêuticas de Ribeirão PretoUniversidade de São PauloRibeirão PretoBrazil
  3. 3.Departamento de Farmácia (DEFAR), Escola de FarmáciaUniversidade Federal de Ouro PretoOuro PretoBrazil
  4. 4.Instituto de Ciências BiológicasUniversidade Federal do AmazonasManausBrazil
  5. 5.Department of Biology, Faculty of Philosophy, Sciences and Literature of Ribeirão PretoUniversity of São PauloRibeirão PretoBrazil

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