Interactions between oil-collecting bees and Krameria grandiflora (Krameriaceae) with emphasis on the role of specialized floral traits in the mutual fit

Abstract

Oil-producing flowers have evolved specialized traits along with the ability to secrete oil as reward, leading to the expectation of a narrow relationship between floral architecture and oil-collecting behaviours of pollinators. Krameriaceae flowers have a showy calyx and a less conspicuous dimorphic corolla modified into a pair of elaiophores that secrete the oil, and a group of petaloid petals that, among oil-collecting bees, are used by only Centris (Centridini) during the oil gathering. A manipulative experiment consisted of excising these floral parts to test the prediction that these structures contribute to successful oil gathering by the bees and plant reproduction. We surveyed the oil-collecting bees associated with the Krameria grandiflora A. St.-Hil. across its distribution range and performed the experiment in populations associated with two different oil-collecting bee taxa—Caenonomada (Tapinotaspidini) and Centris, the main pollinators. Although predicted to mediate the floral mechanical fit with Centris, the absence of the petaloid petals had a neutral effect on both oil-gathering behaviour and seed set, when comparing Caenonomada and Centris. A negative effect on these responses was found when the elaiophores were excised, indicating that these glands have greater importance than the petals related to the mutual fit between flowers and pollinators. However, the petaloid petals seemed to function jointly with the sepals in pollinator attraction. When the sepals were excised, only Centris behaviour was affected, but not that of Caenonomada, indicating potentially divergent selective pressures on the calyx. In addition, we provide a novel oil host plant for several oil-collecting bees.

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References

  1. Aguiar AJC, Melo GAR (2009) Notes on oil sources for the bee genus Caenonomada (Hymenoptera, Apidae, Tapinotaspidini). Rev Bras Entomol 53:154–156. https://doi.org/10.1590/S0085-56262009000100033

    Article  Google Scholar 

  2. Alves-dos-Santos I, Machado IC, Gaglianone MC (2007) História natural das abelhas coletoras de óleo. Oecologia Bras 11:544–557. https://doi.org/10.4257/oeco.2007.1104.06

    Article  Google Scholar 

  3. Anderson WR (1979) Floral conservatism in neotropical Malpighiaceae. Biotropica 11:219. https://doi.org/10.2307/2388042

    Article  Google Scholar 

  4. Bronstein JL, Alarcón R, Geber M (2006) The evolution of plant-insect mutualisms. New Phytol 172:412–428. https://doi.org/10.1111/j.1469-8137.2006.01864.x

    Article  PubMed  Google Scholar 

  5. Buchmann SL (1987) The ecology of oil flowers and their bees. Annu Rev Ecol Syst 18:343–369. https://doi.org/10.1146/annurev.es.18.110187.002015

    Article  Google Scholar 

  6. Cane JH (1987) Estimation of bee size using intertegular span (Apoidea). J Kansas Entomol Soc 60:145–147

    Google Scholar 

  7. Capistrano SHB, Loiola MIB (2015) Flora do Ceará. Brasil: Krameriaceae. Rodriguésia 66:905–912. https://doi.org/10.1590/2175-7860201566317

    Article  Google Scholar 

  8. Carlquist S (2005) Wood anatomy of Krameriaceae with comparisons with Zygophyllaceae: phylesis, ecology and systematics. Bot J Linn Soc 149:257–270. https://doi.org/10.1111/j.1095-8339.2005.00451.x

    Article  Google Scholar 

  9. Carneiro LT, Aguiar AJC, Martins CF et al (2015) Krameria tomentosa oil flowers and their pollinators: bees specialized on trichome elaiophores exploit its epithelial oil glands. Flora 215:1–8. https://doi.org/10.1016/j.flora.2015.06.002

    Article  Google Scholar 

  10. Cocucci AA, Sérsic A, Roig-Alsina A (2000) Oil-collecting structures in Tapinotaspidini: their diversity, function and probable origin. Mitteilungen der Münchner Entomol Gesellschaft 90:51–74

    Google Scholar 

  11. Cuartas-Domínguez M, Medel R (2010) Pollinator-mediated selection and experimental manipulation of the flower phenotype in Chloraea bletioides. Funct Ecol 24:1219–1227. https://doi.org/10.1111/j.1365-2435.2010.01737.x

    Article  Google Scholar 

  12. Davis CC, Schaefer H, Xi Z et al (2014) Long-term morphological stasis maintained by a plant-pollinator mutualism. Proc Natl Acad Sci 111:5914–5919. https://doi.org/10.1073/pnas.1403157111

    Article  CAS  PubMed  Google Scholar 

  13. Faegri K, Van der Pijl L (1979) The principles of pollination ecology. Pergamon, Oxford

    Google Scholar 

  14. Fernandes M, Giulietti AM, De Oliveira RP, De Lima CT (2014) Flora da Bahia: Krameriaceae. SITIENTIBUS série Ciências Biológicas 14:1–6. https://doi.org/10.13102/scb199

  15. Ferreira CA, Torezan-Silingardi HM (2013) Implications of the floral herbivory on Malpighiacea plant fitness: visual aspect of the flower affects the attractiveness to pollinators. Sociobiology 60:323–328. https://doi.org/10.13102/sociobiology.v60i3.323-328

    Article  Google Scholar 

  16. Ferreiro G, Baranzelli MC, Sérsic AN, Cocucci AA (2015) Clinal variability of oil and nectar rewards in Monttea aphylla (Plantaginaceae): relationships with pollinators and climatic factors in the Monte Desert. Bot J Linn Soc 178:314–328. https://doi.org/10.1111/boj.12280

    Article  Google Scholar 

  17. Gimenes M, Lobão CDS (2006) A polinização de Krameria bahiana B.B. Simpson (Krameriaceae) por abelhas (Apidae) na restinga, BA. Neotrop Entomol 35:440–445. https://doi.org/10.1590/S1519-566X2006000400003

    Article  PubMed  Google Scholar 

  18. Harder LD, Johnson SD (2009) Darwin’s beautiful contrivances: evolutionary and functional evidence for floral adaptation. New Phytol 183:530–545. https://doi.org/10.1111/j.1469-8137.2009.02914.x

    Article  PubMed  Google Scholar 

  19. Heinze G, Schemper M (2002) A solution to the problem of separation in logistic regression. Stat Med 21:2409–2419. https://doi.org/10.1002/sim.1047

    Article  PubMed  Google Scholar 

  20. Herrera CM (2001) Deconstructing a floral phenotype: do pollinators select for corolla integration in Lavandula latifolia? J Evol Biol 14:574–584. https://doi.org/10.1046/j.1420-9101.2001.00314.x

    Article  Google Scholar 

  21. Herrera CM, Castellanos MC, Medrano M (2006) Geographical context of floral evolution: towards an improved research programme in floral diversification. In: Harder LD, Barrett SCH (eds) Ecology and evolution of flowers. Oxford Univ. Press, Oxford. pp 278–294

    Google Scholar 

  22. Landis JB, Barnett LL, Hileman LC (2012) Evolution of petaloid sepals independent of shifts in B-class MADS box gene expression. Dev Genes Evol 222:19–28. https://doi.org/10.1007/s00427-011-0385-1

    Article  CAS  PubMed  Google Scholar 

  23. Machado IC, Vogel S, Lopes a V (2002) Pollination of Angelonia cornigera Hook. (Scrophulariaceae) by long-legged, oil-collecting bees in NE Brazil. Plant Biol 4:352–359. https://doi.org/10.1055/s-2002-32325

    Article  Google Scholar 

  24. Martins AC, Aguiar AJC, Alves-dos-Santos I (2013) Interaction between oil-collecting bees and seven species of Plantaginaceae. Flora 208:401–411. https://doi.org/10.1016/j.flora.2013.07.001

    Article  Google Scholar 

  25. Martins AC, Melo GAR, Renner SS (2015) Gain and loss of specialization in two oil-bee lineages, Centris and Epicharis (Apidae). Evolution 69:1835–1844. https://doi.org/10.1111/evo.12689

    Article  PubMed  Google Scholar 

  26. Melo GAR, Gaglianone MC (2005) Females of Tapinotaspoides, a genus in the oil-collecting bee tribe Tapinotaspidini, collect secretions from non-floral trichomes (Hymenoptera, Apidae). Rev Bras Entomol 49:167–168. https://doi.org/10.1590/S0085-56262005000100022

    Article  Google Scholar 

  27. Milby TH (1971) Floral anatomy of Krameria lanceolata. Am J Bot 58:569. https://doi.org/10.2307/2441040

    Article  Google Scholar 

  28. Neff JL, Simpson BB (1981) Oil-collecting structures in the Anthophoridae (Hymenoptera): morphology, function, and use in systematics. J Kansas Entomol Soc 54:95–123

    Google Scholar 

  29. Neff JL, Simpson BB (2017) Vogel’s great legacy: the oil flower and oil-collecting bee syndrome. Flora 232:104–116. https://doi.org/10.1016/j.flora.2017.01.003

    Article  Google Scholar 

  30. Possobom CCF, Machado SR (2017) Elaiophores: their taxonomic distribution, morphology and functions. Acta Bot Brasilica 31:503–524. https://doi.org/10.1590/0102-33062017abb0088

    Article  Google Scholar 

  31. Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Timber Press, Portland

    Google Scholar 

  32. Quiñones AE, Wcislo WT (2015) Cryptic extended brood care in the facultatively eusocial sweat bee Megalopta genalis. Insectes Soc 62:307–313. https://doi.org/10.1007/s00040-015-0409-3

    Article  PubMed  PubMed Central  Google Scholar 

  33. R Core Team (2018) R: a language and environment for statistical computing

  34. Rasmussen C, Olesen JM (2000) Oil flowers and oil-collecting bees. Scand Assoc Pollinat Ecol Honours Knut Faegri 39:23–31. https://doi.org/10.1007/s13398-014-0173-7.2

    Article  Google Scholar 

  35. Renner SS, Schaefer H (2010) The evolution and loss of oil-offering flowers: new insights from dated phylogenies for angiosperms and bees. Philos Trans R Soc B Biol Sci 365:423–435. https://doi.org/10.1098/rstb.2009.0229

    Article  CAS  Google Scholar 

  36. Roig-Alsina A (1997) A generic study of the bees of the tribe Tapinotaspidini, with notes on the evolution of their oil-collecting structures (Hymenoptera, Apidae). Mitteilungen der Münchner. Entomol Gesellschaft 87:3–21

    Google Scholar 

  37. Sabino WO, Silva CI, Alves-dos-Santos I (2017) Mating system and sleeping behaviour of the male and female Centris (Paracentris) burgdorfi Friese (Apidae, Centridini). J Insect Behav 30:103–118. https://doi.org/10.1007/s10905-017-9600-x

    Article  Google Scholar 

  38. Sabino WO, Alves-dos-Santos I, da Silva CI (2018) Versatility of the trophic niche of Centris (Paracentris) burgdorfi (Apidae, Centridini). Arthropod Plant Interact. https://doi.org/10.1007/s11829-018-9654-5

    Article  Google Scholar 

  39. Sazima M, Sazima I (1989) Oil-gathering bees visit flowers of eglandular morphs of the oil-producing Malpighiaceae. Bot Acta 102:106–111. https://doi.org/10.1111/j.1438-8677.1989.tb00073.x

    Article  Google Scholar 

  40. Schäffler I, Steiner KE, Haid M et al (2015) Diacetin, a reliable cue and private communication channel in a specialized pollination system. Sci Rep 5:12779. https://doi.org/10.1038/srep12779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Sheahan MC, Chase MW (1996) A phylogenetic analysis of Zygophyllaceae R. Br. based on morphological, anatomical and rbcL DNA sequence data. Bot J Linn Soc 122:279–300. https://doi.org/10.1111/j.1095-8339.1996.tb02077.x

    Article  Google Scholar 

  43. Simpson BB (1982) Krameria (Krameriaceae) flowers: orientation and elaiophore morphology. Taxon 31:517. https://doi.org/10.2307/1220683

    Article  Google Scholar 

  44. Simpson BB (1989) Krameriaceae. Flora Neotrop 49:1–108

    Google Scholar 

  45. Simpson BB, Neff JL (1981) Floral rewards: alternatives to pollen and nectar. Ann Missouri Bot Gard 68:301. https://doi.org/10.2307/2398800

    Article  Google Scholar 

  46. Simpson BB, Weeks A, Helfgott DM, Larkin LL (2004) Species relationships in Krameria (Krameriaceae) based on ITS sequences and morphology: implications for character utility and biogeography. Syst Bot 29:97–108. https://doi.org/10.1600/036364404772974013

    Article  Google Scholar 

  47. Steiner KE, Whitehead VB (1990) Pollinator adaptation to oil-secreting flowers—Rediviva and Diascia. Evolution 44:1701–1707. https://doi.org/10.1111/j.1558-5646.1990.tb03857.x

    Article  PubMed  Google Scholar 

  48. Vogel S (1971) Ölproduzierende Blumen, die durch ölsammelnde Bienen bestäubt werden. Naturwissenschaften 58:58–58. https://doi.org/10.1007/BF00620817

    Article  CAS  Google Scholar 

  49. Vogel S (1974) Olblumen und olsammelnde Bienen. Trop Subtrop Pflwelt 7:1–267

    Google Scholar 

  50. Vogel S (1990) History of the Malpighiaceae in the light of pollination ecology. Mem N Y Bot Gard 55:130–142

    Google Scholar 

  51. Vogel S, Machado IC (1991) Pollination of four sympatric species of Angelonia (Scrophulariaceae) by oil-collecting bees in NE. Brazil. Plant Syst Evol 178:153–178. https://doi.org/10.1007/BF00937962

    Article  Google Scholar 

  52. Von Helversen D, Von Helversen O (1999) Acoustic guide in bat-pollinated flower. Nature 398:759–760. https://doi.org/10.1038/19648

    Article  CAS  Google Scholar 

  53. Werneck FP, Costa GC, Colli GR et al (2011) Revisiting the historical distribution of Seasonally Dry Tropical Forests: new insights based on palaeodistribution modelling and palynological evidencegeb. Glob Ecol Biogeogr 20:272–288. https://doi.org/10.1111/j.1466-8238.2010.00596.x

    Article  Google Scholar 

  54. Zanella FCV (2010) Abelhas e plantas da Caatinga: importância dos visitantes florais na reprodução das plantas herbáceas e da Apis mellifera nas guildas de visitantes florais. In: Anais do IX Encontro sobre Abelhas. Ribeirão Preto, pp 40–43

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Acknowledgements

We thank ICMBio/SISBIO, for allowing us to conduct the study in the Conservation Units, and the Corumbá City Council, for letting us to work at the Piraputangas Park. We also thank Dr. Felipe Vivallo (National Museum/UFRJ, Rio de Janeiro, Brazil), for identifying the specimens of Centridini, Dr. Antônio Aguiar (UnB, Brasília, Brazil), for identifying the specimens of Tapinotaspidini, Dr. Sheina Koffler (IB/USP, São Paulo, Brazil), for the helpful discussions on the research, MSc. Felipe Libran Embid (Georg-August-Universität Göttingen, Göttingen, Germany), for helping with the fieldwork, two anonymous reviewers and the editor, for the constructive criticism and support to the manuscript. We are grateful for the awarded scholarship grants and financial support for LTC and IA by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, 2013/00181-5 and 04/00274-4).

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L.T.C. and I.A. conceived the general outline of the study; L.T.C. designed the methodology, collected the samples with the support of C.B.D.S.A., and led the analysis and writing of the manuscript with substantial contributions by A.T. and I.A. All the authors contributed critically to the drafts and gave final approval for publication.

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Correspondence to Liedson Tavares Carneiro.

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Carneiro, L.T., André, C.B.D.S., Takahasi, A. et al. Interactions between oil-collecting bees and Krameria grandiflora (Krameriaceae) with emphasis on the role of specialized floral traits in the mutual fit. Arthropod-Plant Interactions 13, 213–226 (2019). https://doi.org/10.1007/s11829-019-09689-w

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Keywords

  • Centris
  • Elaiophores
  • Mechanical fit
  • Petaloid
  • Pollinator matching
  • Tapinotaspidini