Plant Systematics and Evolution

, Volume 222, Issue 1–4, pp 293–320 | Cite as

Convergent evolution and adaptive radiation of beetle-pollinated angiosperms

  • P. Bernhardt


A literature review of 34 families of flowering plants containing at least one species pollinated primarily by beetles is presented. While the majority of species are represented by magnoliids and basal monocotyledons specialized, beetle-pollinated systems have evolved independently in 14 families of eudicotyldons and six families of petaloid monocots. Four, overlapping modes of floral presentation in plants pollinated exclusively by beetles (Bilabiate, Brush, Chamber Blossom and Painted Bowl) are described. Chamber Blossoms and Painted Bowls are the two most common modes. Chamber Blossoms, found in magnoliids, primitive monocotyledons and in some families of woody eudicots, exploit the greatest diversity of beetle pollinators. Painted Bowls are restricted to petaloid monocots and a few families of eudicots dependent primarily on hairy species of Scarabaeidae as pollen vectors. In contrast, generalist flowers pollinated by a combination of beetles and other animals are recorded in 22 families. Generalist systems are more likely to secrete nectar and exploit four beetle families absent in specialist flowers. Centers of diversity for species with specialized, beetle-pollinated systems are distributed through the wet tropics (centers for Brush and Chamber Blossoms) to warm temperate-Mediterranean zones (centers for Painted Bowls and a few Bilabiate flowers). It is unlikely that beetles were the first pollinators of angiosperms but specialized, beetlepollinated flowers must have evolved by the midlate Cretaceous to join pre-existing guilds of beetlepollinated gymnosperms. The floras of Australia and western North America suggest that mutualistic interactions between beetles and flowers has been a continuous and labile trend in angiosperms with novel interactions evolving through the Tertiary.

Key words

Chamber Blossom chewing mouthparts Coleoptera Cretaceous Painted Bowl magnoliids monocotyledons (basalvs. petaloid) Scarabaeidae 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allen-Wardell G., Bernhardt P., Bitner R., Burquez A., Buchmann S., Cane J., Cox P. A., Feinsinger P., Ingram M., Inouye D., Jones C. E., Kennedy K., Kevan P., Koopowitz H., Medellin-Morales S., Nabhan G. P. (1998) The potential consequences of pollinator declines on the Conservation of biodiversity and stability of food crop yields. Conservation Biology 12: 8–17.Google Scholar
  2. Armstrong J. (1979) Biotic pollination mechanisms in the Australian flora — a review. N. Z. J. Bot. 17: 467–508.Google Scholar
  3. Armstrong J. E. (1986) Floral biology ofMyristica fragrans Houtt. (Myristicaceae), the nutmeg of commerce. Biotropica 18: 32–38.Google Scholar
  4. Armstrong J. E., Irvine A. (1989) Floral biology ofMyristica insipida (Myristicaceae), a distinctive beetle pollination syndrome. Amer. J. Bot. 76: 86–94.Google Scholar
  5. Armstrong J. E., Irvine A. (1990) Functions of staminodia in the beetle-pollinated flowers ofEupomatia laurina. Biotropica 22: 429–431.Google Scholar
  6. Baker H. G., Baker I. (1990) The predictive value of nectar chemistry to the recognition of pollinator types. Israel Journal of Botany 39: 157–166.Google Scholar
  7. Barth F. B. (1985) Insects and Flowers; The Biology of a Partnership. Princeton University Press, New Jersey, USA.Google Scholar
  8. Bawa K. S., Bullock S. H., Perry D. R., Coville R. E., Grayum M. H. (1985) Reproductive biology of tropical lowland rain forest trees. II. Pollination systems. Amer. J. Bot. 72: 346–356.Google Scholar
  9. Bay D. (1995) Thermogenesis in the Aroids. Aroideana 18: 32–39.Google Scholar
  10. Beach J. H. (1982) Beetle pollination ofCyclanthus bipartitus (Cyclanthaceae). Amer. J. Bot. 69: 1074–1081.Google Scholar
  11. Bernhardt P. (1976) The pollination ecology ofHepatica acutiloba DC. (Ranunculaceae). Bulletin of The Torrey Botanical Club 103: 255–258.Google Scholar
  12. Bernhardt P. (1989) The floral ecology of AustralianAcacia. In: Stirton C. H., Zarucchi J. L. (eds.) Advances In Legume Biology. (Monographs in Systematic Botany from the Missouri Botanical Gardens 29) St. Louis, USA, pp. 263–282.Google Scholar
  13. Bernhardt P. (1996) Anther adaptation in animal pollination. In: D'Arcy W. G., Keating R. C. (eds.) The anther: form, function and phylogeny. Cambridge Univ. Press, Great Britain, pp. 192–220.Google Scholar
  14. Bernhardt P. (1999) The rose's kiss; A natural history of flowers. Shearwater Press, Washington, DC.Google Scholar
  15. Bernhardt P., Thien L. B. (1987) Self-isolation and insect pollination in the primitive angiosperms: new evaluations of older hypotheses. Plant Syst. Evol. 156: 159–176.Google Scholar
  16. Bernhardt P., Weston P. (1996) The pollination ecology ofPersoonia (Proteaceae) in eastern Australia. Telopea 6: 775–784.Google Scholar
  17. Bino R. J., Dafni A., Meeuse A. D. J. (1984) Entomophily in the dioecious gymnospermEphedra aphylla Forsk. (C =E. alte C.A. Mey. Mey.) with some notes onE. campylopoda C.A. Mey. I Aspects of the etnomophilous syndrome. Proc. Kopninkle Nederl. Akad. Wetensch. C87: 1–24.Google Scholar
  18. Boror D. J., Triplehorn C. A., Johnson N. (1989) An Introduction to the study of insects. Sixth edition. Saunders College Publishing, Holt, Rinehart and Winston, Inc., Orlando, Florida.Google Scholar
  19. Breckon G., Ortiz W. N. (1983) Pollination ofZamia pumila by fungus gnats. Amer. J. Bot. 70: 106–107.Google Scholar
  20. Chaw S. (1992) Pollination, breeding syndromes, and systematics ofTrochodendron aralioides Sieb. & Zucc. (Trochodendraceae) a relictual species in Eastern Asia. In: Peng C. Phytogeography and Botanical Inventory of Taiwan. (Monograph Series No. 12) Institute of Botany, Academia Sinica, Taipei, pp. 63–77.Google Scholar
  21. Collins B. G., Rebelo T. (1987) Pollination biology of the Proteaceae in Australia and southern Africa. Australian Journal of Ecology 12: 387–421.Google Scholar
  22. Cramer J. M., Meeuse A. D. J., Teunissen P. (1975) A note on the pollination of nocturnally flowering species ofNymphaea. Acta Bot. Neerl. 24: 489–490.Google Scholar
  23. Crepet W. L., Friis E. M. (1987) The evolution of insect pollination in angiosperms. In: Friis E. M., Chaloner W. G., Crane P. R. (eds.) The origins of angiosperms and their biological consequences. Cambridge University Press, England, pp. 181–201.Google Scholar
  24. Cronquist A. (1981) An integrated system of classification of flowering Plants. Columbia University Press, New York, USA.Google Scholar
  25. Dafni A., Bernhardt P., Shmida A., Ivri Y., Greenbaum S., O'Toole C., Losito L. (1990) Red bowl-shaped flowers; convergence for beetle pollination in the Mediterranean region. Israel J. Bot. 39: 81–92.Google Scholar
  26. Dafni A., Bernhardt P., Shmida A., Ivri Y., Greenbaum S., O'Toole C. (1994) Pollination syndromes in the Mediterranean: generalizations and peculiarities. In: Arianoustsou M., Groves R. H. (eds.) Plant-animal interactions in Mediterranean-type ecosystems. Kluwer Academic Publishers, Netherlands, pp. 125–135.Google Scholar
  27. Diels L. (1916) Kaferblumen bei denRanales und ihre Bedeutung fur die Phylogenese der Angiospermen. Ber. Deutsch. Bot. Ges. 34: 758–774.Google Scholar
  28. Dieringer G., Cabrera R. L., Lara M., Loya L., Resyes-Castillo P. (1999) Beetle pollination and floral thermogenicity inMagnolia tamaulipana (Magnoliaceae). Int. J. Plant Sci. 160: 64–71.Google Scholar
  29. Dilcher D. L., Crane P. R. (1984)Archeanthus: An early angiosperm from the Cenomanian of the Western Interior of North America. Annals of the Missouri Botanical Garden 71: 351–383.Google Scholar
  30. Dilley J. D. (1999) The radiation ofCalochortus generalist flowers moving through a mosaic of pollinator assemblages. MSc. Thesis. California State University, Northridge, California.Google Scholar
  31. Eames A. J. (1961) Morphology of the Angiosperms. McGraw-Hill Book Co. Inc, New York.Google Scholar
  32. Endress P. K. (1987) The early evolution of the angiosperm flower. Tree 2: 300–304.Google Scholar
  33. Endress P. K. (1990) Evolution of reproductive structures and functions in primitive angiosperms (Magnoliidae). Memoirs of the New York Botanical Garden 55: 5–34.Google Scholar
  34. Endress P. K. (1994) Diversity and evolutionary biology of tropical flowers. Cambridge Univ. Press, New York, USA.Google Scholar
  35. Englund R. (1993) Movement patterns ofCetonia beetles (Scarabaeidae) among floweringViburnum opulus (Caprifoliaceae): Option for longdistance pollen dispersal in a temperate shrub. Oecologia 94: 295–302.Google Scholar
  36. Essig F. B. (1971) Observations of pollination inBactris. Principes 15: 20–24.Google Scholar
  37. Essig F. B. (1973) Pollination in some New Guinea palms. Principes 17: 75–83.Google Scholar
  38. Faegri K., van der Pijl L. (1979) The Principles of Pollination Ecology. 3rd edn. Pergamon Press, New York.Google Scholar
  39. Farrell B. (1998) “Inordinate Fondness” Explained: Why Are There so many beetles? Science 281: 555–559.Google Scholar
  40. Friis E. M., Crepet W. L. (1987) Time of appearance of floral features. In: Friis E. M., Chaloner W. G., Crane P. R. (eds.) The origins of angiosperms and their biological consequences. Cambridge Univ. Press, Cambridge, England, pp. 145–177.Google Scholar
  41. Futuyma D. J. (1998) Evolutionary Biology. 3rd edn. Sinauer Associates Inc., Sunderland, Massachusetts.Google Scholar
  42. Gibb P. (1977) Floral biology ofTalauma ovata St. Hil. (Magnoliaceae). Ciencia E. Cultura 29: 1437–1441.Google Scholar
  43. Goldblatt P., Bernhardt P. (1999) Pollination ofMoraea species (Iridaceae) with a staminal column. Ann. Missouri Bot. Gard. 86: 47–56.Google Scholar
  44. Goldblatt P., Bernhardt P., Manning J. C. (1998) Pollination of petaloid geophytes by monkey beetles (Scarabaeidae: Rutelinae:Hopliini) in southern Africa. Ann. Missouri Bot. Gard. 85: 215–230.Google Scholar
  45. Gottsberger G. (1977) Some aspects of beetle pollination in the evolution of flowering plants. Plant Syst. Evol. [Suppl.] 1: 211–226.Google Scholar
  46. Gottsberger G. (1988) The reproductive biology of primitive angiosperms. Taxon 37: 630–643.Google Scholar
  47. Gottsberger G. (1989a) Beetle pollination and flowering rhythm ofAnnona spp. (Annonaceae) in Brazil. Plant Syst. Evol. 167: 165–187.Google Scholar
  48. Gottsberger G. (1989b) Comments on flower evolution and beetle pollination in the generaAnnona andRollinia (Annonaceae). Plant Syst. Evol. 167: 189–194.Google Scholar
  49. Gottsberger G., Amaral Jr. A. (1984) Pollination strategies in brazilianPhilodendron species. Ber. Deutsch. Bot. Ges. Bd. 97S: 391–410.Google Scholar
  50. Gottsberger G., Silberbauer-Gottsberger I., Ehrendorfer F. (1980) Reproductive biology in the primitive relic angiospermDrimys brasiliensis (Winteraceae). Plant Syst. Evol. 135: 11–39.Google Scholar
  51. Grant V. (1950) The pollination ofCalycanthus occidentalis. Amer. J. Bot. 37: 294–297.Google Scholar
  52. Grimaldi D. (1999) The co-radiations of pollinating insects and angiosperms in the Cretaceous. Ann. Missouri Bot. Gard. 86: 373–406.Google Scholar
  53. Grimaldi D., Grant K. (1965) Flower pollination in the phlox family. Columbia Univ. Press, New York, NY, USA.Google Scholar
  54. Hawkeswood T. (1980) Jewel beetles as pollinators ofMelaleuca pauperiflora F. Muell. (Myrtaceae) between Eucla (W.A.) and Koonalda (S.A.). Western Australian Naturalist 14: 238–239.Google Scholar
  55. Hawkeswood T. (1981a) Insect pollination ofAngophora woodsiana F. Bail. (Myrtaceae) at Burbank, south-east Queensland. Victorian Naturalist 98: 120–129.Google Scholar
  56. Hawkeswood T. (1981b) Notes on the pollination ofNuytsia floribunda (Labill.) R. Br. (Loranthaceae) and some literature reviewed. Western Australian Naturalist 15: 17–21.Google Scholar
  57. Hawkeswood T. (1982) Notes on insect pollination of two species ofEucalyptus (Myrtaceae) from south-west Western Australia. Victorian Naturalist 99: 28–37.Google Scholar
  58. Hawkeswood T. (1987a) Beetles of Australia. Angus and Robertson, North Ryde, New South Wales, Australia.Google Scholar
  59. Hawkeswood T. (1987b) Pollination ofLeptospermum flavescences SM. (Myrtaceae) by beetles (Coleoptera) in the Blue Mountains, New South Wales, Australia. G. Ital. Entomol. 3: 261–269.Google Scholar
  60. Hawkeswood T. (1987c) Notes on someColeoptera fromBaeckea stenophytlla F. Muell. (Myrtaceae) in New South Wales, Australia. G. Ital. Entomol. 3: 285–290.Google Scholar
  61. Hawkeswood T. (1989) Notes onDiphucephala affinis (Coleoptera: Scarabaeidae) associated with flowers ofHibbertia andAcacia in Western Australia. Plant Syst. Evol. 168: 1–5.Google Scholar
  62. Hawkeswood T. (1990) Insect pollination ofBursaria spinosa (Pittosporaceae) in the Armidale area, New South Wales, Australia. G. Ital. Entomol. 5: 67–87.Google Scholar
  63. Hawkeswood T. (1992)Diphucephala bernhardti sp. Nov. (Coleoptera: Scarabaeidae: Melolonthinae) from heathlands of north-eastern New South Wales, Australia and its association withHibberia flowers (Dilleniaceae). G. it. Ent. 6: 109–117.Google Scholar
  64. Hawkeswood T. (1993) Observations on insect pollination ofMelaleuca lanceolata Otto andVerticordia picta Endl. (Myrtaceae),Leucopogon parviflorus (andr.) Lindl. (Epacridaceae) andEryngium pinnatifidum Bunge (Apiaceae) in Western Australia. G. it. Ent. 6: 239–242.Google Scholar
  65. Henderson A. (1984) Observations on pollination ofChrysophila albida. Principes 28: 120–126.Google Scholar
  66. Irvine A. K., Armstrong J. (1988) Beetle pollination in Australian tropical rainforests. Proc. Ecol. Soc. Aust. 15: 107–113.Google Scholar
  67. Ishida K. (1996) Beetle pollination ofMagnolia praecocissima var.borealis. Plant Species Biol. 11: 198–206.Google Scholar
  68. Johnson L. A. S., Briggs B. G. (1975) On theProteacee — the evolution and classification of a southern family. Bot. J. Linn. Soc. 70: 83–182.Google Scholar
  69. Johnson S. D., Linder H. P., Steiner K. E. (1998) Phylogeny and radiation of pollination systems inDisa (Orchidaceae). Amer. J. Bot. 85: 402–411.Google Scholar
  70. Johnson S. D., Midgley J. J. (1997) Fly pollination ofGorteria diffusa (Asteraceae), and a possible mimetic function for dark spots on the capitululum. Amer. J. Bot. 84: 429–436.Google Scholar
  71. Kato M., Inoue T. (1994) Origin of insect pollination. Science 368: 195.Google Scholar
  72. Knuth P. (1906) Handbook of Flower Pollination Based Upon Hermann Muller's Work The Fertilisation of Flowers By Insects. Oxford at the Clarendon Press, England.Google Scholar
  73. Labandeira C. (1998a) How old is the flower and the fly? Science 280: 57–59.Google Scholar
  74. Labandeira C. (1998b) The role of insects in late Jurassic to Middle Cretaceous ecosystems. In: Lucas S. G., Kirkland J. I., Estep. J. W. (eds.) Lower and Middle Cretaceous terrestrial ecosystems. New Mexico Museum of Natural History and Science. Bull. 14: 105–123.Google Scholar
  75. Lorence D. H. (1980) A systematic and ecoevolutionary study of the Monimiaceae in the Malagasy Region. PhD Thesis, Washington University, St. Louis, Missouri.Google Scholar
  76. Michener C. D. (1979) Biogeography of the bees. Ann. Missouri Bot. Gard. 66: 277–347.Google Scholar
  77. Midgley J. J., Johnson S. D. (1998) Some pollinators do not prefer symmetrically marked or shaped daisy (Asteraceae) flowers. Evolutionary Ecology 12: 123–126.Google Scholar
  78. Momose K., Yumoto T., Teruyoshi N., Kato M., Nagamasu H., Sakai S., Harrison R., Itioka T., Hamid A., Inoue T. (1998) Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. Amer. J. Bot. 85: 1477–1501.Google Scholar
  79. Monteith G. B. (1973) Entomological notes: Dung beetles as pollinators of anArum Lily. News Bull. Entomol. Soc. Queensland 97: 13.Google Scholar
  80. Moore R., Clark W. D., Stearn K. R. (1995) Botany. Wm C. Brown Publishers, USA.Google Scholar
  81. Nagamitsu T., Inoue T. (1997) Cockroach pollination and breeding system ofUvaria elmeri (Annonaceae) in a lowland mixed-dipterocarp forest in Sarawak. Amer. J. Bot. 110: 432–439.Google Scholar
  82. Norman E. M., Clayton D. (1986) Reproductive biology of two Florida pawpaws:Asimina obovata andA. pygmaea. Bulletin of the Torrey Botanical Club 113: 16–22.Google Scholar
  83. Nelson R., Ysaleny B. (1992) Pollination biology in a palm swamp community in the Venezuelan Central plains. Botanical Journal of the Linnean Society 110: 277–302.Google Scholar
  84. Nilsson L. A. (1978) Pollination ecology ofEpipactis palustris (Orchidaceae). Bot. Notiser 131: 355–368.Google Scholar
  85. Norstog K. (1987) Cycads and the origin of insect pollination. American Scientist 75: 270–279.Google Scholar
  86. Northington D. K., Schneider E. L. (1996) The botanical world. Wm, C, Brown Publisers, USA.Google Scholar
  87. Peringuey L. (1902) Descriptive catalogue of theColeoptera of South Africa (Lucanidae and Scarabaeidae). Trans. S. African Phil. Soc. 12: 1–920.Google Scholar
  88. Picker M. D., Midgley J. J. (1996) Pollination by monkey beetles (Coleoptera: Scarabaeidae:Hopliini): flower and colour preferences. African Entomology 4: 7–14.Google Scholar
  89. Piegler R. S. (1988) A review of pollination ofMagnolia by beetles, with a collecting survey made in the Carolinas. Magnolia 45: 1–8.Google Scholar
  90. Prance G. (1980) A note on the pollination ofNymphaea amazonum Mart. & Zucc. (Nymphaeaceae). Brittonia: 505–507.Google Scholar
  91. Prance G., Arias J. (1975) A study of the floral biology ofVictoria amazonica (Poepp.) Sowerby (Nymphaeaceae). Acta Amazonica 6: 163–70.Google Scholar
  92. Primack R. B. (1985) Longevity of individual flowers. In: Johnston R., Frank P. W., Michener C. D. (eds.) Annual Review of Ecology and Systematics 16: pp. 15–38. Palo Alto, California.Google Scholar
  93. Proctor M., Yeo P., Lack A. (1996) The natural history of pollination. Timber Press, Portland, Oregon.Google Scholar
  94. Raven P., Evert R. F., Eichorn S. E. (1999) Biology of Plants. W. H. Freeman and Company, Worth Publishers, New York.Google Scholar
  95. Ren D. (1998) Flower-associated Brachycera flies as fossil evidence for Jurassic angiosperm origins. Science 280: 85–88.Google Scholar
  96. Renner S. S., Johanson K. A. (1995) Breeding system and pollination ofNuphar luteum (L.) Smith (Nymphaeaceae) in Norway. Flora 190: 109–113.Google Scholar
  97. Richards A. J. (1986) Plant Breeding Systems. Allen & Unwin, London, England.Google Scholar
  98. Rodrigues C. M., Teixeira O. W., Pinheiro C. M., Alves De L. M. (1993) Study of the floral biology ofClusia criuva Camb.: A case of mimicry. Bradea 6: 209–220.Google Scholar
  99. Sakai S., Kuniyasu M., Ymoto T., Kato M., Inoue T. (1999) Beetle pollination ofShorea parvifolia (SectionMutica, Dipterocarpaceae) in a general flowering period in Sarawak, Malaysia. Amer. J. Bot. 86: 62–69.Google Scholar
  100. Sakai S., Kuniyasu M., Ymoto T., Kato M., Inoue T. (1999) A new pollination system: Dung-beetle pollination discovered inOrchidantha inouei (Lowiaceae, Zingiberales) in Sarawak, Malaysia. Amer. J. Bot. 86: 56–61.Google Scholar
  101. Samuelson G. A. (1994) Pollen consumption and digestion by leaf beetles. In: Jolivet P. J., Cox M. L., Pettipierre E. (eds.) Novel Aspects of the Biology of Chrysomelidae. Kluwer, Dordrecht, pp. 179–183.Google Scholar
  102. Schneider E. L., Buchanan J. (1980) Morphological studies of the Nymphaeaceae. XI. The floral biology ofNelumbo pentapetala. Amer. J. Bot. 67: 182–193.Google Scholar
  103. Schneider E. L., Buchanan J., Moore L. A. (1977) Morphological studies of the Nymphaeaceae. VII. The floral biology ofNuphar lutea subsp.macrophylla. Britt. 29: 88–99.Google Scholar
  104. Scott Elliot G. (1891) Notes on the fertilisation of South African and Madagascan flowering plants. Ann. Bot. 5: 333–405.Google Scholar
  105. Seres A., Ramirez N. (1995) Biologia floral y polinizacion de algunas monocotiledoneas de un bosquw nublado venezolano. Ann. Missouri Bot. Gard. 82: 61–81.Google Scholar
  106. Seymour R., Schultze-Motel P. (1997) Heat-producing flowers. Endeavour 21: 125–129.Google Scholar
  107. Seymour R., Schultze-Motel P. (1998) Physiological temperature regulation by flowers of the scared lotus. Phil. Trans. R. Soc. Lond. B 353: 935–943.Google Scholar
  108. Schmid R. (1970) Notes on the reproductive biology ofAsterogyne martiana (Palmae). II. Pollination by syrphid flies. Principes 14: 39–49.Google Scholar
  109. Singer R. N., Cocucci A. (1997) Pollination ofPteroglossaspis ruwenzoriensis (Rendle) Role (Orchidaceae) by beetles in Argentina. Bot. Acta 10: 338–342.Google Scholar
  110. Sivadasan M., Sabu T. (1989) Beetle-pollination — cantharophily — inAmorphophallus hohenackeri (Araceae). Aroideana 12: 32–37.Google Scholar
  111. Sohmer S. H., Sefton D. F. (1978) The reproductive biology ofNelumbo pentapetala (Nelumbonaceae) on the upper Mississippi River. II. The insects associated with the transfer of pollen. Britt. 30: 337–354.Google Scholar
  112. Steiner K. (1998a) Beetle pollination of peacock moraeas (Iridaceae) in South Africa. Plant Syst. Evol. 209: 47–65.Google Scholar
  113. Steiner K. (1998b) The evolution of beetle pollination in a South African Orchid. Amer. J. Bot. 85: 1180–1193.Google Scholar
  114. Takhtajan A. (1991) Evolutionary trends in flowering plants. Columbia Univ. Press, New York.Google Scholar
  115. Thien L. B. (1974) Floral biology ofMagnolia. Amer. J. Bot. 61: 1037–1045.Google Scholar
  116. Thien L. B. (1980) Patterns of pollination in the primitive angiosperms. Biotropica 12: 1–13.Google Scholar
  117. Thien L. B., Ellgaard E., Devall M., Ellgaard S., Ramp R. (1999) Population structure and reproductive biology ofSaururus cernuus L. (Saururaceae). Plant Species Biol. 9: 47–55.Google Scholar
  118. Thien L. B., Heimermann W. H., Holman R. T. (1975) Floral odors and quantitative taxonomy ofMagnolia andLiriodendron. Taxon 24: 557–568.Google Scholar
  119. Thien L. B., Kawano S., Latimer S., Devall M., Rosso S., Azumea H., Jobes D. (1995) FluorescentMagnolia flowers. Plant Species Biol. 10: 61–64.Google Scholar
  120. Thien L. B., Pellmyr O., Yatsu L. Y., Berstrom G. (1990) Polysaccharide food-bodies as pollinator rewards inExosperum stipitatum and other members of the Winteraceae. Bull. Mus. Natn., Paris, 4 ser. 12, section B. Adansonia 2: 191–197.Google Scholar
  121. Thien L. B., White D. A., Yatsu L. (1983) The reproductive biology of a relict —Illicium floridanum Ellis. Amer. J. Bot. 70: 719–727.Google Scholar
  122. van der Pijl L., Dodson C. H. (1966) Orchid flowers, their pollination and evolution. University of Miami Press, Coral Gables, Florida.Google Scholar
  123. Vogel S. (1954) Blütenbiologische Typen als Elemente der Sippengliederung. Bot. Stud. 1: 1–338.Google Scholar
  124. Vogel S. (1978) Evolutionary shifts from reward to deception in pollen flowers. In: Richards A. J. (ed.) The Pollination of Flowers by Insects. Linnean Society Symposium Series Number 6. Linnean Society of London, Academic Press, London, pp. 89–96.Google Scholar
  125. Wallace B. J. (1980) Cantharophily and the pollination ofPeristeranthus hillii. The Orchadian 6: 214–215.Google Scholar
  126. Waser N. M., Chittka L., Price M. V., Williams N. M., Ollerton J. (1996) Generalization in pollination systems and why it matters. Ecology 77: 1043–1060.Google Scholar
  127. Whitehead V. B., Giliome J. H., Rebelo A. G. (1987) Insect pollination in the Cape Flora. In: A. G. Rebelo (ed.) A Preliminary synthesis of pollination biology in the Cape Flora. CDIR, Pretoria, South Africa, pp. 52–82.Google Scholar
  128. Yeo P. (1993) Secondary pollen presentation: Form, function and evolution. Springer, Wien New York.Google Scholar
  129. Yo-Bo L., Zhen-Yu L. (1999) Pollination ecology ofChloranthus serratus (Thunb.) Roem. Et Schult. andCh. Fortunei (A. Gray) Solms-Laub. (Chloranthaceae). Annals of Botany 83: 489–499.Google Scholar
  130. Young H. J. (1986) Beetle pollination ofDieffenbachia Longispatha (Araceae). Amer. J. Bot. 73: 931–944.Google Scholar
  131. Zhou S., Hong D., Pan K. (1999) Pollination biology ofPaeonia jishanensis T. Hong & W. Z. Zhao (Paeoniaceae), with special emphasis on pollen and stigma biology. Botanical Journal of the Linnean Society 130: 43–52.Google Scholar

Copyright information

© Springer-Verlag 2000

Authors and Affiliations

  • P. Bernhardt
    • 1
  1. 1.Department of BiologySt. Louis UniversitySt. LouisUSA

Personalised recommendations