The Botanical Review

, Volume 76, Issue 2, pp 220–240 | Cite as

Pollination Syndromes in Mediterranean Orchids—Implications for Speciation, Taxonomy and Conservation

  • Nicolas J. VereeckenEmail author
  • Amots Dafni
  • Salvatore Cozzolino


The Mediterranean flora is spectacularly rich in orchid species that have evolved remarkable adaptations to their environment. Orchids have complex and delicate interactions with their pollinators, which makes them particularly prone to local extinction. Conservation actions should be encouraged for a range of endangered Mediterranean orchid species, but the current taxonomic confusion in several genera and the apparent disagreement among orchid taxonomists make the situation particularly confusing from a conservation perspective. In this review, we document how the different pollination syndromes of Mediterranean orchids (nectar reward, shelter offering, food deception and sexual deception) can have a profound impact on the type of reproductive barriers among species, on floral phenotypic variation as we perceive it, on potentially related processes of species sorting and extinction and, consequently, should have a strong influence on the related conservation management programs. We also highlight that the majority of Mediterranean orchids are pollinated by specialised bees often occupying otherwise narrow ecological niches (e.g. pollen specialisation, brood cell parasites, specific nesting site). This condition makes the orchid-pollinator interactions very fragile and several orchid species prone to local extinction. We illustrate this phenomenon by a selection of case studies that show how the adequate integration of the ecological requirements/traits of the orchids and their associated pollinators into conservation actions could help protect endangered species and ensure the sustainability of the often complex local pollination web.


Mediterranean Orchids Pollination Syndromes Conservation Strategies 



We wish to thank Robert Pemberton, Stella Watts and Hong Liu for their critical reading of the paper and for their constructive comments. NJV thanks Yves Wilcox for providing the photograph of the red helleborine used in Fig. 1, and the FRS-FNRS (Belgium) for financial support via a post-doctoral grant.

Literature Cited

  1. Ackerman, J. D. 1986. Mechanisms and evolution of food-deceptive pollination systems in orchids. Lindleyana 1: 108–113.Google Scholar
  2. ——— & A. M. Montalvo. 1990. Short- and long-term limitation to fruit production in a tropical orchid. Ecology 71: 263–272.Google Scholar
  3. ——— & S. Ward. 1999. Genetic variation in a widespread, epiphytic orchid: Where is the evolutionary potential. Systematic Botany 24: 282–291.Google Scholar
  4. Alcock, J. 2005. An enthusiasm for orchids: Sex and deception in plant evolution. Oxford University Press, Oxford.Google Scholar
  5. Arnold, M. L. 1997. Natural hybridization and evolution. Oxford University Press, Oxford.Google Scholar
  6. Bateman, R. M. 2001. Evolution and classification of European orchids: Insight from molecular and morphological characters. Journal Europäischer Orchideen 33: 33–119.Google Scholar
  7. Bellusci, F., G. Pellegrino & A. M. Palermo. 2008. Phylogenetic relationships in the orchid genus Serapias based on monocoding regions of the chloroplast genome. Molecular Phylogenetics and Evolution 47: 986–991.PubMedGoogle Scholar
  8. Benton, T. 2006. Bumblebees, the natural history and identification of the species found in Britain. Collins, London.Google Scholar
  9. Bidartondo, M. I. & D. J. Read. 2008. Fungal specificity bottlenecks during orchid germination and development. Molecular Ecology 17: 3707–3716.PubMedGoogle Scholar
  10. Biesmeijer, J. C., S. P. M. Roberts, M. Reemer, R. Ohlemueller, M. Edwards, T. Peeters, A. Schaffers, S. G. Potts, R. Kleukers, C. D. Thomas, J. Settele & W. E. Kunin. 2006. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313: 351–354.PubMedGoogle Scholar
  11. Bitsch, J., T. Barbier, S. F. Gayubo, K. Schmidt & M. Ohl. 1997. Hyménoptères Sphecidae d’Europe Occidentale (Vol. 2.). Faune de France 82: 1–427.Google Scholar
  12. Calvo, R. N. 1993. Evolutionary demography of orchids: Intensity and frequency of pollination and the cost of fruiting. Ecology 74: 1033–1042.Google Scholar
  13. Carrière, J. 1995. Généralités, comportement nidificateur et cycle biologique artificiel pour le genre Ceratina (Latreille, 1802) dans l’Hérault (Hymenoptera, Xylocopinae). Lambillionea XCV 2: 244–254.Google Scholar
  14. Chung, M. Y., J. D. Nason & M. G. Chung. 2004. Spatial genetic structure in populations of the terrestrial orchid Cephalanthera longibracteata (Orchidaceae). American Journal of Botany 91: 52–57.Google Scholar
  15. Clausen, C. P. 1940. Entomophagous insects. McGraw-Hill, New York.Google Scholar
  16. Coates, D. J. & K. W. Dixon. 2007. Current perspective in plant conservation biology. Australian Journal of Botany 55: 187–193.Google Scholar
  17. Cozzolino, S. & A. Widmer. 2005. Orchid diversity: An evolutionary consequences of deception? Trends in Ecology and Evolution 20: 487–494.PubMedGoogle Scholar
  18. ———, S. D’Emerico & A. Widmer. 2004. Evidence for reproductive isolate selection in Mediterranean orchids: Karyotype differences compensate for the lack of pollinator specificity. Proceedings of the Royal Society B 271: 259–262.Google Scholar
  19. ———, Cafasso D, Pellegrino G, Musacchio A. & Widmer A. 2003. Fine—scale phylogeographical analysis of Mediterranean Anacamptis palustris (orchidaceae) populations based on chloroplast minisatellite and microsatellite variation. Molecular Ecology 12: 2783–2793.PubMedGoogle Scholar
  20. ———, F. P. Schiestl, A. Müller, O. De Castro, A. M. Nardella & A. Widmer. 2005. Evidence for pollinator sharing in Mediterranean nectar-mimic orchids: Absence of premating barriers. Proceedings of the Royal Society B 272: 1271–1278.PubMedGoogle Scholar
  21. Dafni, A. 1983. Pollination of O. caspia—a nectarless plant which deceives the pollinators of nectariferous species from other plant families. Journal of Ecology 71: 467–474.Google Scholar
  22. ——— 1984. Mimicry and deception in pollination. Annual Review of Ecology and Systematics 15: 259–278.Google Scholar
  23. ——— 1986. Floral mimicry—mutualism and unidirectional exploitation of insects by plants. Pp 81–90. In: T. R. F. Southwood & B. E. Juniper (eds). The plant surface and insects. Arnold, London.Google Scholar
  24. ——— 1987. Pollination in Orchis and related genera: Evolution from reward to deception. Pp 80–104. In: J. Arditti (ed). Orchid biology: Reviews and perspectives IV. Cornell University Press, Ithaca.Google Scholar
  25. ——— & H. Baumann. 1982. Biometrical analysis in populations of Orchis israelitica Baumann and Dafni, O. caspia Trautv and their hybrids. Plant Systematics and Evolution 140: 87–94.Google Scholar
  26. ——— & Y. Ivri. 1979. Pollination ecology of and hybridization between Orchis coriophora L. and O. collina. Sol. ex. Russ (Orchidaceae) in Israel. New Phytologist 83: 181–187.Google Scholar
  27. ——— & ———. 1981. Floral mimicry between Orchis isrealitica Baumann and Dafni (Orchidaceae) and Bellevalia flexuosa Boiss. (Liliaceae). Oecologia 49: 229–232.Google Scholar
  28. ———, ——— & N. B. M. Brantjes. 1981. Pollination of Serapias vomeracea Briq. in Israel by imitation of holes for sleeping solitary male bees (Hym.). Acta Botanica Neerlandica 30: 69–73.Google Scholar
  29. Darwin, C. 1862. The various contrivances by which are fertilized by insects. Murray, London.Google Scholar
  30. Delforge, P. 1994. Guide des Orchide´es d’Europe, d’Afrique du Nord et du Proche-Orient. Delachaux et Niestle, Lausanne.Google Scholar
  31. ——— 2005. Guide des orchidées d’Europe, d’Afrique du Nord et du Proche—Orient. Delachaux & Niestlé, Paris.Google Scholar
  32. ——— 2007. Guide des orchidées de France, de Suisse et du Bénélux. Delachaux & Niestlé, Paris.Google Scholar
  33. Devey, D. S., R. M. Bateman, M. F. Fay & J. A. Hawkins. 2008. Friends or Relatives? Phylogenetics and species delimitation in the controversial European orchid genus Ophrys. Annals of Botany 101: 385–402.PubMedGoogle Scholar
  34. Dötterl, S. & N.J. Vereecken. 2010. The chemical ecology and evolution of bee-flower interactions: A review and perspectives. Canadian Journal of Zoology, in press.Google Scholar
  35. Falk, S. 1991. A review of scarce and threatened bees, wasp and ants of Great Britain. Research and Survey in Nature Conservation 35, Nature Conservancy Council, UK.Google Scholar
  36. Galizia, C. G., J. Kunze, A. Gumbetrt, A.-K. Borg-Karlson, S. Sachs, C. Markl & R. Menzel. 2005. Relationship of visual and olfactory signal parameters in food-deceptive flower mimicry system. Behavioural Ecology 16: 159–168.Google Scholar
  37. Gathmann, A. & T. Tscharntke. 2002. Foraging ranges of solitary bees. Journal of Animal Ecology 71: 757–764.Google Scholar
  38. Gill, D. E. 1989. Fruiting failure, pollination efficiency and speciation in orchids. Pp 458–481. In: D. Otte & J. A. Endlet (eds). Speciation and its consequences. Sinauer, Sundeland.Google Scholar
  39. Gögler, J., J. Stökl, A. Sramkova, R. Twele, W. Francke, S. Cozzolino, P. Cortis, A. Scrugli & M. Ayasse. 2009. Ménage À Trois—Two Endemic species of deceptive orchids and one pollinator species. Evolution 63: 2222–2234.PubMedGoogle Scholar
  40. Goulson, D. 2003. Bumblebees; their behaviour and ecology. Oxford University Press, Oxford.Google Scholar
  41. ——— & P. H. Williams. 2001. Bombus hypnorum (Hymenoptera: Apidae), a new British bumblebee? British Journal of Entomological Natural History 14: 129–131.Google Scholar
  42. Greenleaf, S. S., N. M. Williams, R. Winfree & C. Kremen. 2007. Bee foraging ranges and their relation to body size. Oecologia 153: 589–596.PubMedGoogle Scholar
  43. Greuter, W. 1991. Botanical diversity, endemism, rarity, and extinction in the Mediterranean area: An analysis based on the published volumes of Med-Checklist. Botanical Chronicle 10: 63–79.Google Scholar
  44. Gumbert, A. & J. Kunze. 2001. Colour similarity to rewarding model plants affects pollination in a food deceptive orchid. Biological Journal of the Linnaean Society 72: 419–433.Google Scholar
  45. Hamilton, K. G. A. 1982. Insects and arachnids of Canada Part 10—Homoptera : Cercopidae. Biosystematics Research Institute Publication (Canada Agriculture Canada). PLACEGoogle Scholar
  46. Hedrén, M. 2002. Speciation patterns in Dactylorhiza incarnata/maculata polyploidy complex (Orchidaceae): evidence from molecular markers. Journal Europäischer Orchideen 34: 707–731.Google Scholar
  47. Heywood, V. H. 1995. The Mediterranean flora in the context of world diversity. Ecologia Mediterranea 21: 11–18.Google Scholar
  48. Jacquemyn, H. & R. Brys. 2009. Temporal and spatial variation in flower and fruit production in a food-deceptive orchid: A five-year study. Plant Biology 12(1): 145–153.Google Scholar
  49. Jersáková, J., S. D. Johnson & P. Kindlmann. 2006. Mechanisms and evolution of deceptive pollination in orchids. Biological Reviews 81: 219–235.PubMedGoogle Scholar
  50. ———, ——— & A. Jürgens. 2009. Food deception by plants: From generalized systems to specialized floral mimicry. Pp 223–246. In: F. Baluška (ed). Plant-environment interactions, signaling and communication in plants, from sensory plant biology to active plant behaviour. Springer-Verlag, Berlin Heidelberg.Google Scholar
  51. Kearns, C. A., D. W. Inouye & N. M. Waser. 1998. Endangered mutualisms: The conservation of plant-pollinator interactions. Annual Review of Ecology and Systematics 29: 83–112.Google Scholar
  52. Kosior, A., W. Celary, P. Olejniczak, J. Fijał, W. Król, W. Solarz & P. Płonka. 2007. The decline of the bumble bees and cuckoo bees (Hymenoptera: Apidae: Bombini) of Western and Central Europe. Oryx 41: 79–88.Google Scholar
  53. Kreutz, C. A. J. & H. Dekker. 2000. De orchideeen van Nederland—ecologie, verspreiding, bedreiging, beheer. Uitgave Kreutz and Seckel, Landgraaf & Raalte, The Netherlands.Google Scholar
  54. Kullenberg, B. 1961. Studies in Ophrys pollination. Zoologiska Bidrag Uppsala 34: 1–340.Google Scholar
  55. Lang, D. 2004. Britain’s orchids. WILDguides, English Nature. PLACEGoogle Scholar
  56. Lind, H., M. Frazen, B. Petterson & L. A. Nilsson. 2007. Metapopulation pollination in the deceptive orchid Anacamptis pyramidalis. Nordic Journal of Botany 25: 176–182.Google Scholar
  57. Lucas, G. B. & H. Synge. 1978. The IUCN plant red data book. International Union for Conservation. WWF.UNEP, Paris.Google Scholar
  58. Mace, G. M. & R. Lande. 1991. Assessing extinction threats: Towards a re-evaluation of IUCN threatened species categories. Conservation Biology 5: 148–157.Google Scholar
  59. Mant, J., R. Peakall, F. P. Schiestle & C. F. Williams. 2005. Does selection on floral odor promote differentiation among populations and species of the sexually deceptive orchid genus Ophrys. Evolution 59: 1449–1463.PubMedGoogle Scholar
  60. Michener, C. D. 1974. The social behaviour of bees—a comparative study. Harvard University Press, Cambridge.Google Scholar
  61. ——— 2007. The bees of the world, ed. 2nd. Johns Hopkins University Press, Baltimore.Google Scholar
  62. Montalvo, A. V. & J. D. Ackerman. 1987. Limitations to fruit production in Ionopsis utricularoides (Orchdaceae). Biotropica 19: 24–31.Google Scholar
  63. Murray, T. E., M. Kuhlmann & S. G. Potts. 2009. Conservation ecology of bees: Populations, species and communities. Apidologie 40: 211–236.Google Scholar
  64. Murren, C. J. & A. M. Ellison. 1998. Seed dispersal characteristics of Brassavola nodosa (Orchidaceae). American Journal of Botany 85: 675–680.Google Scholar
  65. Neiland, M. R. M. & C. C. Wilcock. 1998. Fruit set, nectar reward, and rarity in the Orchidaceae. American Journal of Botany 85: 1657–1671.Google Scholar
  66. Nilsson, L. A. 1983. Mimesis of bellflower (Campanula) by the red helleborine orchid Cephalanthera rubra. Nature 305: 799–800.Google Scholar
  67. O’Connell, L. M. & M. O. Johnson. 1998. Male and female pollination success in a deceptive orchid, a selection study. Ecology 79: 1246–1260.Google Scholar
  68. Oertli, S., A. Müller & S. Dorn. 2005. Ecological and seasonal patterns in the diversity of a species-rich bee assemblage (Hymenoptera: Apoidea: Apiformes). European Journal of Entomology 102: 53–63.Google Scholar
  69. Osborne, J. L., S. J. Clark, R. J. Morris, I. H. Williams, J. R. Riley, A. D. Smith, D. R. Reynolds & A. S. Edwards. 1999. A landscape scale study of bumblebee foraging range and constancy, using harmonic radar. Journal of Applied Ecology 36: 519–533.Google Scholar
  70. Pasquet, R. S., A. Peltier, M. B. Hufford, E. Oudin, J. Saulnier, L. Paul, J. T. Knudsen, H. R. Herren & P. Gepts. 2008. Long-distance pollen flow assessment through evaluation of pollinator foraging range suggests transgene escape distances. Proceedings of the National Academy of Sciences of the USA 105: 13456–13461.PubMedGoogle Scholar
  71. Paulus, H. F. & C. Gack. 1995. Zur Pseudokopulation und Bestäubung in der Gattung Ophrys (Orchidaceae) Sardiniens und Korsikas. Jaarbericht Naturwissenschaften Verein. Wuppertal 48: 188–227.Google Scholar
  72. Peakall, R. & F. P. Schiestl. 2004. A mark-recapture study of male Colletes cunicularius bees: Implications for pollination by sexual deception. Behavioural Ecology and Sociobiology 56: 579–584.Google Scholar
  73. Pedersen, H. A. & N. Faurholdt. 2007. The bee orchids of Europe. Kew Publishing, Kew.Google Scholar
  74. Peeters, T. M.J. & M. Reemer. 2003. Bedreigde en verdwenen bijen in Nederland (Apidae s.l.)—Basisrapport met voorstel voor de Rode Lijst. Sichting European Invertebrate Survey—Nederland.Google Scholar
  75. Pilgrim, E. S., M. J. Crawley & K. Dolphin. 2004. Patterns of rarity in the British Flora. Biological Conservation 210: 161–170.Google Scholar
  76. Pillon, Y., M. F. Fay, A. B. Shipunov & M. W. Chase. 2006. Species diversity versus phylogenetic diversity: A practical study in the taxonomically difficult genus Dactylorhiza (Orchidaceae). Biological Conservation 129: 4–13.Google Scholar
  77. ——— & M. W. Chase. 2007. Taxonomic exaggeration and its effect on orchid conservation. Conservation Biology 21: 263–265.PubMedGoogle Scholar
  78. Potts, S. G., B. Vulliamy, S. Roberts, C. O’Toole, A. Dafni, G. Ne’eman & P. Willmer. 2005. Role of nesting resources in organising diverse bee communities in a Mediterranean landscape. Ecological Entomology. 30: 78–85.Google Scholar
  79. Quézel, P. 1985. Definition of the Mediterranean region and the origin of its flora. Pp 9–24. In: C. Gomez-Campo (ed). Plant conservation in the Mediterranean area. W. Junk, Dordrecht.Google Scholar
  80. Rabinowitz, D. 1981. Seven forms of rarity. Pp 205–218. In: H. Synge (ed). The biological aspects of rare plant conservation. Wiley, New York.Google Scholar
  81. Rasmussen, M. N. 2002. Recent development in the study of orchid mycorrhiza. Plant and soil 244: 149–163.Google Scholar
  82. Rhymer, J. M. & D. Simberloff. 1996. Extinction by hybridization and introgression. Annual Rreview of Ecology and Systematics 27: 83–109.Google Scholar
  83. Riley, J. R. 1980. Radar as an aid to the study of insect flight. Pp 131–140. In: C. J. Amlaner, C. J. Amlaner, & D. W. Macdonald (eds). Handbook on biotelemetry and radio tracking. Pergamon, Oxford.Google Scholar
  84. ——— & A. D. Smith. 2002. Design considerations for an harmonic radar to investigate the flight of insects at low altitude. Computers and Electronics in Agriculture 35: 151–169.Google Scholar
  85. Roberts, D. L. 2003. Pollination biology: The role of sexual reproduction in orchid conservation. Pp 113–136. In: K. W. Dixon, S. P. Kell, R. L. Barrett, & P. J. Cribb (eds). Orchid conservation. Natural History Publications, Kota Kinabalu.Google Scholar
  86. Rosenzweig, M. L. 1995. Species diversity in space and time. Cambridge University Press, Cambridge.Google Scholar
  87. Roubik, D. W. 2001. Ups and downs in pollinator populations: When is there a decline? Conservation Ecology 5(1): 2. URL: Scholar
  88. Sabat, A. M. & J. D. Ackerman. 1996. Fruit set in a deceptive orchid: The effect of flowering phenology, display size, and local floral abundance. American Journal of Botany 83: 1181–1186.Google Scholar
  89. Salzmann, C. C., A. M. Nardella & S. Cozzolino. 2007a. Variability in floral scents in rewarding and deceptive orchids: The signature of pollinator-imposed selection? Annals of Botany 100: 757–765.Google Scholar
  90. ———, S. Cozzolino & F. P. Schiestl. 2007b. Floral scent in food-deceptive orchids: Species specificity and source of variability. Plant Biology 9: 270–729.Google Scholar
  91. Sapir, Y., A. Shmida & O. Fragman. 2003. Constructing Red Numbers for endangered plant species—Israeli flora as a test case. Journal for Nature Conservation 11: 91–107.Google Scholar
  92. Schiestl, F. P. & S. Cozzolino. 2008. Evolution of sexual mimicry in the Orchidinae: The role of preadaptations in the attraction of male bees as pollinators. BMC Evolutionary Biology 8: 27.PubMedGoogle Scholar
  93. Scopece, G., A. Musacchio, A. Widmer & S. Cozzolino. 2007. Patterns of isolation in Mediterranean deceptive orchids. Evolution 61: 2623–2642.PubMedGoogle Scholar
  94. Sedivy, C., C. J. Praz, A. Müller, A. Widmer & S. Dorn. 2008. Patterns of host-plant choice in bees of the genus Chelostoma: The constraint hypothesis of host-range evolution in bees. Evolution 62: 2487–2507.PubMedGoogle Scholar
  95. Shepherd, M., S. L. Buchmann, M. Vaughan & S. H. Black. 2003. Pollinator conservation handbook. The Xerces Society, Portland Oregon.Google Scholar
  96. Sladen, F. W. L. 1912. The humble-bee, its life history and how to domesticate it, with descriptions of all the British species of Bombus and Psithyrus. MacMillan, London.Google Scholar
  97. Sosa, V. & T. Platas. 1998. Extinction and persistence of rare orchids in Veracruz, Mexico. Conservation Biology 12: 451–455.Google Scholar
  98. Spaethe, J., W. H. Moser & H. F. Paulus. 2007. Increase of pollinator attraction by means of a visual signal in the sexually deceptive orchid, Ophrys heldreichii (Orchidaceae). Plant Systematics and Evolution 264: 31–40.Google Scholar
  99. Squirrell, S., P. M. Hollingsworth & R. M. Bateman. 2002. Taxonomic complexity and breeding system transitions: Conservation genetics of Epipactis leptochila complex (Orchidaceae). Molecular Ecology 11: 1957–1964.PubMedGoogle Scholar
  100. Stökl, J., P. M. Schluter, T. F. Stuessy, H. F. Paulus & G. Assum. 2008. Scent variation and hybridization cause the displacement of a sexual deceptive orchid species. American Journal of Botany 95: 472–481.Google Scholar
  101. Swartz, N. D. & K. W. Dixon. 2009. Terrestrial orchid conservation in the age of extinction. Annals of Botany 104: 543–556.Google Scholar
  102. Thompson, J. D. 2005. Plant evolution in the Mediterranean. Oxford University Press, Oxford.Google Scholar
  103. Trapnell, D. W., J. L. Hamrick & J. D. Nason. 2004. Three- dimensional fire-scale genetic structure of the neotropical epiphytic orchid Laelia rubescens. Molecular Ecology 13: 1111–1118.PubMedGoogle Scholar
  104. Tremblay, R. L., J. D. Ackerman, J. K. Zimmerman & R. N. Calvo. 2005. Variation in sexual reproduction in orchids and its evolutionary consequences: A spasmodic journey to diversification. Biological Journal of the Linnaean Society 84: 1–54.Google Scholar
  105. Ushimaru, A. & K. Nakata. 2001. Evolution of flower allometry and its significance for pollination success in the deceptive orchid Pogonia japonica. International Journal of Plant Science 162: 1307–1311.Google Scholar
  106. Van der Cingel, N. 1995. An atlas of orchid pollination—European orchid. Balkema, Roterdam.Google Scholar
  107. Van der Pijl, N. & C. H. Dodson. 1966. Orchid flowers: Their pollination and evolution. University of Miami Press, Coral Gables.Google Scholar
  108. Vereecken, N. J. 2009. Deceptive behaviour in plants. I. Pollination by sexual deception in orchids: A host-parasite perspective. In: F. Baluska (ed). 203–222 Plant–Environment Interactions—From Sensory Plant Biology to Active Behaviour. Springer Verlag.Google Scholar
  109. ——— & J. Carrière. 2003. Contribution à l’étude éthologique de la grande scolie à front jaune, Megascolia maculata flavifrons (F., 1775) (Hymenoptera, Scoliidae) en France méditerranéenne. Notes Fauniques de Gembloux 53: 71–80.Google Scholar
  110. ——— & F. P. Schiestl. 2008. The evolution of imperfect floral mimicry. Proceedings of the National Academy of Sciences of the USA 105: 7484–7488.PubMedGoogle Scholar
  111. ——— & ———. 2009. On the roles of colour and scent in a specialized floral mimicry system. Annals of Botany 104(6): 1077–1084.PubMedGoogle Scholar
  112. ———, J. Mant & F. P. Schiestl. 2007. Population differentiation in female sex pheromone and male preferences in a solitary bee. Behavioural Ecology and Sociobiology 61(5): 811–821.Google Scholar
  113. ———, H. Schwenninger, A. Gogala & S. P. M. Roberts. 2009. Mise à jour de la distribution géographique de l’abeille du lierre, Colletes hederae Schmidt & Westrich (Hymenoptera, Colletidae) en Europe. Osmia 3: 2–3.Google Scholar
  114. ———, S. Cozzolino & F. P. Schiestl. 2010. Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids. Editorial Discussion.Google Scholar
  115. Westrich, P. 1989. Die Wildbienen Baden-Württembergs, Teil 1 & 2. Eugen Ulmer, Stuttgart.Google Scholar
  116. ——— 1996. Habitat requirements of central European bees and the problem of partial habitats. Pp 1–16. In: A. Matheson, S. L. Buchmann, C. O’Toole, P. Westrich, & I. H. Williams (eds). The Conservation of Bees. Academic, London.Google Scholar
  117. Wilcock, C. & R. Neiland. 1998. Fruit set, nectar reward, and rarity in the Orchidaceae. American Journal of Botany 85: 1657–1671.Google Scholar
  118. ——— & ———. 2002. Pollination failure in plants: Why it happens and when it matters. Trends in Plant Science 7: 270–277.PubMedGoogle Scholar
  119. Williams, P. H. & J. L. Osborne. 2009. Bumblebee vulnerability and conservation worldwide. Apidologie 40: 367–387.Google Scholar
  120. Wojcik, V. A., G. W. Frankie, R. W. Thorp & J. L. Hernandez. 2008. Seasonality in bees and their floral resource plants at a constructed urban bee habitat in Berkeley, California. Journal of the Kansas Entomological Society 81: 15–28.Google Scholar
  121. Wood, J. J. 1989. British orchids in their European context. Pp 141–145. In: H. Pritchard (ed). Modern methods in orchid conservation: The role of physiology, ecology and management. Cambridge University Press, Cambridge.Google Scholar
  122. Wright, G. A. & F. Schiestl. 2009. The evolution of floral scent: The influence of olfactory learning by insect pollinators on the honest signaling of floral rewards. Functional Ecology 23: 841–851.Google Scholar

Copyright information

© The New York Botanical Garden 2010

Authors and Affiliations

  • Nicolas J. Vereecken
    • 1
    • 2
    Email author
  • Amots Dafni
    • 3
  • Salvatore Cozzolino
    • 4
  1. 1.Evolutionary Ecology & BiologyFree University of Brussels/Université Libre de BruxellesBrusselsBelgium
  2. 2.Institute of Systematic BotanyUniversity of ZürichZürichSwitzerland
  3. 3.Department of Evolutionary and Environmental Biology, Institute of EvolutionHaifa UniversityHaifaIsrael
  4. 4.Department of Structural and Functional BiologyUniversity of Naples “Federico II”NaplesItaly

Personalised recommendations