Arthropod-Plant Interactions

, Volume 5, Issue 4, pp 279–285 | Cite as

Floral epidermal structure and flower orientation: getting to grips with awkward flowers

  • Sean A. Rands
  • Beverley J. Glover
  • Heather M. Whitney
Original Paper


The petal epidermis has been found to be important in mediating flower-pollinator interactions. Structures produced on the petal surface, in particular cone-shaped papillate (or conical) cells, have been shown to enhance bumblebee preference for flowers. One reason for this increase in preference is that the conical cells facilitate efficient handling of flowers. This is particularly clear when flower architecture requires bees to land on a vertical surface. We therefore tested the hypothesis that flowers that are held vertically show a greater tendency to produce conical cells. Analysis of 183 species finds that there is no significant relationship between the structures on the petal surface and flower orientation. We discuss the multifunctional properties of conical cells and other floral surface structures that may mean that other factors are of equal or greater importance in the relationship between pollinators and petal epidermal form.


Tactile structures Grip Floral orientation Plant surface Conical cell Pairwise comparisons 



Heather M. Whitney is supported by an ERC starting grant (#260920). Two anonymous reviewers are gratefully thanked for their comments.

Supplementary material

11829_2011_9146_MOESM1_ESM.txt (6 kb)
Additional file 1: Data used for comparative study. This file (a comma-delimited text file) presents the character states of the 183 species used in the analysis. The top line of the file details the character type. For each species on subsequent lines, the first six characters are the character states found in Table 2 of Kay et al. (1981) where ‘0’ denotes the absence and ‘1’ denotes the presence of the relevant epidermal structures. The final column for each species presents the orientation data collected as is described in the methods: ‘0’ denotes upward and ‘1’ denotes not-upward flowers. (TXT 5 kb) (122 kb)
Additional file 2: Phylogeny used for the comparative analyses. Drawn using Treeview X (Page 1996). (PS 121 kb)


  1. Aizen MA (2003) Down-facing flowers, hummingbirds and rain. Taxon 52:675–680CrossRefGoogle Scholar
  2. Albach DC, Chase MW (2001) Paraphyly of Veronica (Veroniceae; Scrophulariaceae): evidence from the internal transcribed spacer (ITS) sequences of nuclear ribosomal DNA. J Plant Res 114:9–18. doi: 10.1007/PL00013971 CrossRefGoogle Scholar
  3. Al-Shehbaz IA, Beilstein MA, Kellogg EA (2006) Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview. Plant System Evol 259:89–120. doi: 10.1007/s00606-006-0415-z CrossRefGoogle Scholar
  4. Anderberg AA, Trift I, Källersjö M (2000) Phylogeny of Cyclamen L. (Primulaceae): evidence from morphology and sequence data from the internal transcribed spacers of nuclear ribosomal DNA. Plant System Evol 220:147–160. doi: 10.1007/BF00985043 CrossRefGoogle Scholar
  5. Baumann K, Perez-Rodriguez M, Bradley D, Venail J, Bailey P, Jin H, Koes R, Roberts K, Martin C (2007) Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development 134:1691–1701. doi: 10.1242/dev.02836 PubMedCrossRefGoogle Scholar
  6. Bayer RJ, Starr JR (1998) Tribal phylogeny of the Asteraceae based on two non-coding chloroplast sequences, the trnL intron and trnL/trnF intergenic spacer. Ann Mo Bot Gard 85:242–256CrossRefGoogle Scholar
  7. Beilstein MA, Al-Shehbaz IA, Kellogg EA (2006) Brassicaceae phylogeny and trichome evolution. Am J Bot 93:607–619PubMedCrossRefGoogle Scholar
  8. Charlton NL, Houston AI (2010) What currency do bumble bees maximize? PLoS One 5:e12186. doi: 10.1371/journal.pone.0012186 PubMedCrossRefGoogle Scholar
  9. Chittka L, Menzel R (1992) The evolutionary adaptation of flower colours and the insect pollinators’ colour vision. J Comp Physiol A 171:171–181. doi: 10.1007/BF00188925 CrossRefGoogle Scholar
  10. Dafni A, Potts SG (2004) The role of flower inclination, depth, and height in the preferences of a pollinating beetle (Coleoptera: Glaphyridae). J Insect Behav 17:823–834. doi: 10.1023/B:JOIR.0000048991.45453.73 CrossRefGoogle Scholar
  11. Desfeux C, Maurice S, Henry J-P, Lejeune B, Gouyon P-H (1996) Evolution of reproductive systems in the genus Silene. Proc R Soc B 263:409–414. doi: 10.1098/rspb.1996.0062 PubMedCrossRefGoogle Scholar
  12. Donoghue MJ, Olmstead RG, Smith JF, Palmer JD (1992) Phylogenetic relationships of Dipsacales based in rbcL sequences. Ann Mo Bot Gard 79:333–345CrossRefGoogle Scholar
  13. Downie SR, Katz-Downie DS, Spalik K (2000) A phylogeny of Apiaceae tribe Scandiceae: evidence from nuclear ribosomal DNA internal transcribed spacer sequences. Am J Bot 87:76–95PubMedCrossRefGoogle Scholar
  14. Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L (2006) Bees associate warmth with floral colour. Nature 442:525. doi: 10.1038/442525a PubMedCrossRefGoogle Scholar
  15. Erber J, Kierzak S, Sander E, Grandy K (1998) Tactile learning in the honeybee. J Comp Physiol A 183:737–744. doi: 10.1007/s003590050296 CrossRefGoogle Scholar
  16. Fenster CB, Armbruster WS, Dudash MR (2009) Specialization of flowers: is floral orientation an overlooked first step? New Phytol 183:502–506. doi: 10.1111/j.1469-8137.2009.02852.x PubMedCrossRefGoogle Scholar
  17. Fior S, Karis PO (2007) Phylogeny, evolution and systematics of Moehringia (Caryophyllaceae) as inferred from molecular and morphological data: a case of homology reassessment. Cladistics 23:362–372. doi: 10.1111/j.1096-0031.2007.00150.x CrossRefGoogle Scholar
  18. Fior S, Karis PO, Casazza G, Minuto L, Sala F (2006) Molecular phylogeny of the Caryophyllaceae (Caryophyllales) inferred from chloroplast matK and nuclear rDNA ITS sequences. Am J Bot 93:399–411PubMedCrossRefGoogle Scholar
  19. Giurfa M, Dafni A, Neal PR (1999) Floral symmetry and its role in plant-pollinator systems. Int J Plant Sci 160:S41–S50. doi: 10.1086/314214 PubMedCrossRefGoogle Scholar
  20. Goertzen LR, Cannone JJ, Gutell RR, Jansen RK (2003) ITS secondary structure derived from comparative analysis: implications for sequence alignment and phylogeny of the Asteraceae. Mol Phylog Evol 29:216–234. doi: 10.1016/S1055-7903(03)00094-0 CrossRefGoogle Scholar
  21. Goldblatt P (1990) Phylogeny and classification of the Iridaceae. Ann Mo Bot Gard 77:607–627CrossRefGoogle Scholar
  22. Goyret J, Raguso RA (2006) The role of mechanosensory input in flower handling efficiency and learning by Manduca sexta. J Exp Biol 209:1585–1593. doi: 10.1242/jeb.02169 PubMedCrossRefGoogle Scholar
  23. Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, OxfordGoogle Scholar
  24. Hoch PC, Crisci JV, Tobe H, Berry PE (1993) A cladistic analysis of the plant family Onagraceae. System Bot 18:31–47CrossRefGoogle Scholar
  25. Hong D-Y, Zhou S-L (2003) Paeonia (Paeoniaceae) in the Caucasus. Bot J Linn Soc 143:135–150. doi: 10.1046/j.1095-8339.2003.00173.x CrossRefGoogle Scholar
  26. Imamura A, Ushimaru A (2007) Flower orientation on slopes in the myco-heterotrophic species Monotropastrum globosum. Plant Sp Biol 22:161–166. doi: 10.1111/j.1442-1984.2007.00188.x CrossRefGoogle Scholar
  27. Jansen RK, Michaels HJ, Palmer JD (1991) Phylogeny and character evolution in the Asteraceae based on chloroplast DNA restriction site mapping. System Bot 16:98–115CrossRefGoogle Scholar
  28. Kay QON, Daoud HS, Stirton CH (1981) Pigment distribution, light reflection and cell structure in petals. Bot J Linn Soc 83:57–84. doi: 10.1111/j.1095-8339.1981.tb00129.x CrossRefGoogle Scholar
  29. Kevan PG (1975) Sun-tracking solar furnaces in high arctic flowers: significance for pollination and insects. Science 189:723–726. doi: 10.1126/science.189.4204.723 PubMedCrossRefGoogle Scholar
  30. Kevan PG, Lane MA (1985) Flower petal microtexture is a tactile cue for bees. Proc Natl Acad Sci USA 82:4750–4752PubMedCrossRefGoogle Scholar
  31. Kudo G (1995) Ecological significance of flower heliotropism in the spring ephemeral Adonis ramosa (Ranunculaceae). Oikos 72:14–20CrossRefGoogle Scholar
  32. Lamb JM, Wells H (1995) Honey bee (Apis mellifera) use of flower form in making foraging choices. J Kansas Entomol Soc 68:388–398Google Scholar
  33. Långström E, Chase MW (2002) Tribes of Boraginoideae (Boraginaceae) and placement of Antiphytum, Echiochilon, Ogastemma and Sericostoma: a phylogenetic analysis based on atpB plastid DNA sequence data. Plant System Evol 234:137–153. doi: 10.1007/s00606-002-0195-z CrossRefGoogle Scholar
  34. Leonard AS, Dornhaus A, Papaj DR (2011) Flowers help bees cope with uncertainty: signal detection and the function of floral complexity. J Exp Biol 214:113–121. doi: 10.1242/jeb.047407 PubMedCrossRefGoogle Scholar
  35. Levin RA, Wagner WL, Hoch PC, Nepokroeff M, Pires JC, Zimmer EA, Sytsma KJ (2003) Family-level relationships of Onagraceae based on chloroplast rbcL and ndhF data. Am J Bot 90:107–115PubMedCrossRefGoogle Scholar
  36. Maddison WP (2000) Testing character correlation using pairwise comparisons on a phylogeny. J Theor Biol 202:195–204. doi: 10.1006/jtbi.1999.1050 PubMedCrossRefGoogle Scholar
  37. Maddison WP (2006) Pairwise comparisons package for Mesquite, version 1.1 []
  38. Maddison WP, Maddison DR (2006) Mesquite: a modular system for evolutionary analysis. Version 1.12. []
  39. Martins EP (1996) Phylogenies and the comparative method in animal behavior. Oxford University Press, New YorkGoogle Scholar
  40. Martins L, Oberprieler C, Hellwig FH (2003) A phylogenetic analysis of Primulaceae s.l. based on internal transcribed spacer (ITS) DNA sequence data. Plant System Evol 237:75–85. doi: 10.1007/s00606-002-0258-1
  41. Morgan DR, Soltis DE, Robertson KR (1994) Systematic and evolutionary implications of rbcL sequence variation in Rosaeae. Am J Bot 81:890–903CrossRefGoogle Scholar
  42. Natali A, Manen J-F, Ehrendorfer F (1995) Phylogeny of the Rubiaceae-Rubioideae, in particular the tribe Rubieae: evidence from a non-coding chloroplast DNA sequence. Ann Mo Bot Gard 82:428–439CrossRefGoogle Scholar
  43. Nee S, Read AF, Harvey PH (1996) Why phylogenies are necessary for comparative analysis. In: Martins EP (ed) Phylogenies and the comparative method in animal behavior. Oxford University Press, New York, pp 399–411Google Scholar
  44. Noda K, Glover BJ, Linstead P, Martin C (1994) Flower colour intensity depends on specialized cell shape controlled by a Myb-related transcription factor. Nature 369:661–664. doi: 10.1038/369661a0 PubMedCrossRefGoogle Scholar
  45. Oberprieler C, Vogt R (2000) The position of Castrilanthemum Vogt and Oberprieler and the phylogeny of Mediterranean Anthemidae (Compositae) as inferred from nrDNA ITS and spDNA trnL/trnF IGS sequence variation. Plant System Evol 225:145–170. doi: 10.1007/BF00985465 CrossRefGoogle Scholar
  46. Ollerton J, Alarcón R, Waser NM, Price MV, Watts S, Cranmer L, Hingston A, Peter CI, Rotenberry J (2009) A global test of the pollination syndrome hypothesis. Ann Bot 103:1471–1480. doi: 10.1093/aob/mcp031 PubMedCrossRefGoogle Scholar
  47. Olmstead RG, dePamphilis CW, Wolfe AD, Young ND, Elisons WJ, Reeves PA (2001) Disintegration of the Scrophulariaceae. Am J Bot 88:348–361Google Scholar
  48. Oxelman B, Lidén M, Berglund D (1997) Chloroplast rps16 intron phylogeny of the tribe Sileneae (Caryophyllaceae). Plant System Evol 206:393–410. doi: 10.1007/BF00987959 CrossRefGoogle Scholar
  49. Oxelman B, Kornhall P, Olmstead RG, Bremer B (2005) Further disintegration of Scrophulariaceae. Taxon 54:411–425CrossRefGoogle Scholar
  50. Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedGoogle Scholar
  51. Pagel M (2000) Statistical analysis of comparative data. Trends Ecol Evol 15:418. doi: 10.1016/S0169-5347(00)01952-2 CrossRefGoogle Scholar
  52. Parkinson CL, Mower JP, Qiu Y-L, Shirk AJ, Song K, Young ND, dePamphilis CW, Palmer JD (2005) Multiple major increases and decreases in mitochondrial substitution rates in the plant family Geraniaceae. BMC Evol Biol 5:73. doi: 10.1186/1471-2148-5-73 PubMedCrossRefGoogle Scholar
  53. Patiño S, Jeffree C, Grace J (2002) The ecological role of orientation in tropical convolvulaceous flowers. Oecologia 130:373–379. doi: 10.1007/s00442-001-0824-1 CrossRefGoogle Scholar
  54. Pfosser M, Speta F (1999) Phylogenetics of Hyacinthaceae based on plastid DNA sequences. Ann Mo Bot Gard 86:852–875CrossRefGoogle Scholar
  55. Rands SA, Whitney HM (2008) Floral temperature and optimal foraging: is heat a feasible floral reward for pollinators? PLoS One 3:e2007. doi: 10.1371/journal.pone.0002007 PubMedCrossRefGoogle Scholar
  56. Rands SA, Whitney HM (2010) Effects of pollinator density-dependent preferences on field margin pollination in the midst of agricultural monocultures: a modelling approach. Ecol Model 221:1310–1316. doi: 10.1016/j.ecolmodel.2010.01.014 CrossRefGoogle Scholar
  57. Read AF, Nee S (1995) Inference from binary comparative data. J Theor Biol 173:99–108. doi: 10.1006/jtbi.1995.0047 CrossRefGoogle Scholar
  58. Reeves G, Chase MW, Goldblatt P, Rudall P, Fay MF, Cox AV, Lejeune B, Souza-Chies T (2001) Molecular systematics of Iridaceae: evidence from four plastid DNA regions. Am J Bot 88:2074–2087PubMedCrossRefGoogle Scholar
  59. Ridley M, Grafen A (1996) How to study discrete comparative methods. In: Martins EP (ed) Phylogenies and the comparative method in animal behavior. Oxford University Press, New York, pp 76–103Google Scholar
  60. Ro K-E, Keener CS, McPheron BA (1997) Molecular phylogenetic study of the Ranunculaceae: utility of the nuclear 26S ribosomal DNA in inferring intrafamilial relationships. Mol Phylog Evol 8:117–127. doi: 10.1006/mpev.1997.0413 CrossRefGoogle Scholar
  61. Scheiner R, Erber J, Page RE Jr (1999) Tactile learning and the individual evaluation of the reward in honey bees (Apis mellifera L.). J Comp Physiol A 185:1–10. doi: 10.1007/s003590050360
  62. Scheiner R, Page RE Jr, Erber J (2001) The effects of genotpye, foraging role and sucrose responsiveness on the tactile learning performance of honey bees (Apis mellifera L.). Neurobiol Learn Mem 76:138–150. doi: 10.1006/nlme.2000.3996 PubMedCrossRefGoogle Scholar
  63. Simone-Finstrom M, Gardner J, Spivak M (2010) Tactile learning in resin foraging honeybees. Behav Ecol Sociobiol 64:1609–1617. doi: 10.1007/s00265-010-0974-4 CrossRefGoogle Scholar
  64. Spalik K, Downie SR (2001) The utility of morphological characters for inferring phylogeny in Scandiceae subtribe Scandicinae (Apiaceae). Ann Mo Bot Gard 88:270–310CrossRefGoogle Scholar
  65. Speta F (1971) Beitrag zur Systematik von Scilla L. subgen. Scilla (inklusive Chionodoxa Boiss.). Öst Bot Z 119:6–18. doi: 10.1007/BF01373105 CrossRefGoogle Scholar
  66. Stevens PF (2007) Angiosperm phylogeny website. Version 8, June 2007. []
  67. Tadey M, Aizen MA (2001) Why do flowers of a hummingbird-pollinated mistletoe face down? Funct Ecol 15:782–790. doi: 10.1046/j.0269-8463.2001.00580.x CrossRefGoogle Scholar
  68. Ushimaru A, Hyodo F (2005) Why do bilaterally symmetrical flowers orient vertically? Flower orientation influences pollinator landing behaviour. Evol Ecol Res 7:151–160Google Scholar
  69. Ushimaru A, Kawase D, Imamura A (2006) Flowers adaptively face down-slope in 10 forest-floor herbs. Funct Ecol 20:585–591. doi: 10.1111/j.1365-2435.2006.01153.x CrossRefGoogle Scholar
  70. Ushimaru A, Dohzono I, Takami Y, Hyodo F (2009) Flower orientation enhances pollen transfer in bilaterally symmetrical flowers. Oecologia 160:667–674. doi: 10.1007/s00442-009-1334-9 PubMedCrossRefGoogle Scholar
  71. Vargas P, Morton CM, Jury SL (1999) Biogeographic patterns in Mediterranean and Macaronesian species of Saxifraga (Saxifragaceae) inferred from phylogenetic analyses of ITS sequences. Am J Bot 86:724–734PubMedCrossRefGoogle Scholar
  72. Vargas P, Roselló JA, Oyama R, Güemes J (2004) Molecular evidence for naturalness of genera in the tribe Antirrhineae (Scrophulariaceae) and three independent evolutionary lineages from the New World and the Old. Plant System Evol 249:151–172. doi: 10.1007/s00606-004-0216-1 CrossRefGoogle Scholar
  73. Wagstaff SJ, Olmstead RG, Cantino PD (1995) Parsimony analysis of cpDNA restriction site variation in subfamily Nepetoideae (Labiatae). Am J Bot 82:886–892CrossRefGoogle Scholar
  74. Warren J, James P (2008) Do flowers wave to attract pollinators? A case study with Silene maritima. J Evol Biol 21:1024–1029. doi: 10.1111/j.1420-9101.2008.01543.x PubMedCrossRefGoogle Scholar
  75. Warwick SI, Sauder CA (2007) Phylogeny of tribe Brassiceae (Brassicaceae) based on chloroplast restriction site polymorphisms and nuclear ribosomal internal transcribed spacer and chloroplast trnL intron sequences. Can J Bot 83:467–483. doi: 10.1139/B05-021 CrossRefGoogle Scholar
  76. Watson LE, Evans TM, Boluarte T (2000) Molecular phylogeny and biogeography of the Tribe Anthemideae (Asteraceae), based on chloroplast gene ndhF. Mol Phylog Evol 15:59–69. doi: 10.1006/mpev.1999.0714 CrossRefGoogle Scholar
  77. Whitney HM, Dyer A, Chittka L, Rands SA, Glover BJ (2008) The interaction of temperature and sucrose concentration on foraging preferences in bumblebees. Naturwissenschaften 95:845–850. doi: 10.1007/s00114-008-0393-9 PubMedCrossRefGoogle Scholar
  78. Whitney HM, Chittka L, Bruce TJA, Glover BJ (2009a) Conical epidermal cells allow bees to grip flowers and increase foraging efficiency. Curr Biol 19:948–953. doi: 10.1016/j.cub.2009.04.051 PubMedCrossRefGoogle Scholar
  79. Whitney HM, Federle W, Glover BJ (2009b) Grip and slip: mechanical interactions between insects and the epidermis of flowers and flower stalks. Commun Integr Biol 2:505–508. doi: 10.4161/cib.2.6.9479 PubMedCrossRefGoogle Scholar
  80. Whitney HM, Kolle M, Alvarez-Fernandez R, Steiner U, Glover BJ (2009c) Contributions of iridescence to floral patterning. Commun Integr Biol 2:230–232PubMedCrossRefGoogle Scholar
  81. Whitney HM, Kolle M, Andrew P, Chittka L, Steiner U, Glover BJ (2009d) Floral iridescence, produced by diffractive optics, acts as a cue for animal pollinators. Science 323:130–133. doi: 10.1126/science.1166256 PubMedCrossRefGoogle Scholar
  82. Whitney HM, Bennett KMV, Dorling M, Sandbach L, Prince D, Chittka L, Glover BJ (in press) Why do so many petals have conical epidermal cells? Ann Bot. doi: 10.1093/aob/mcr065
  83. Wojciechowski MF (2003) Reconstructing the phylogeny of legumes (Leguminosae): an early 21st century perspective. In: Klitgaard BB, Bruneau A (eds) Advances in legume systematics, part 10: higher level systematics. Royal Botanic Gardens, Kew, London, pp 5–35Google Scholar
  84. Wortley AH, Rudall PJ, Harris DJ, Scotland RW (2005) How much data are needed to resolve a difficult phylogeny? Case study in Lamiales. System Biol 54:697–709. doi: 10.1080/10635150500221028 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Sean A. Rands
    • 1
  • Beverley J. Glover
    • 2
  • Heather M. Whitney
    • 3
  1. 1.Centre for Behavioural Biology, School of Veterinary ScienceUniversity of BristolLangford, BristolUK
  2. 2.Department of Plant SciencesUniversity of CambridgeCambridgeUK
  3. 3.School of Biological SciencesUniversity of BristolBristolUK

Personalised recommendations