Skip to main content
Log in

Convergent evolution and adaptive radiation of beetle-pollinated angiosperms

  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • 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 

  • Armstrong J. (1979) Biotic pollination mechanisms in the Australian flora — a review. N. Z. J. Bot. 17: 467–508.

    Google Scholar 

  • Armstrong J. E. (1986) Floral biology ofMyristica fragrans Houtt. (Myristicaceae), the nutmeg of commerce. Biotropica 18: 32–38.

    Google Scholar 

  • Armstrong J. E., Irvine A. (1989) Floral biology ofMyristica insipida (Myristicaceae), a distinctive beetle pollination syndrome. Amer. J. Bot. 76: 86–94.

    Google Scholar 

  • Armstrong J. E., Irvine A. (1990) Functions of staminodia in the beetle-pollinated flowers ofEupomatia laurina. Biotropica 22: 429–431.

    Google Scholar 

  • 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 

  • Barth F. B. (1985) Insects and Flowers; The Biology of a Partnership. Princeton University Press, New Jersey, USA.

    Google Scholar 

  • 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 

  • Bay D. (1995) Thermogenesis in the Aroids. Aroideana 18: 32–39.

    Google Scholar 

  • Beach J. H. (1982) Beetle pollination ofCyclanthus bipartitus (Cyclanthaceae). Amer. J. Bot. 69: 1074–1081.

    Google Scholar 

  • Bernhardt P. (1976) The pollination ecology ofHepatica acutiloba DC. (Ranunculaceae). Bulletin of The Torrey Botanical Club 103: 255–258.

    Google Scholar 

  • 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.

  • 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 

  • Bernhardt P. (1999) The rose's kiss; A natural history of flowers. Shearwater Press, Washington, DC.

    Google Scholar 

  • 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 

  • Bernhardt P., Weston P. (1996) The pollination ecology ofPersoonia (Proteaceae) in eastern Australia. Telopea 6: 775–784.

    Google Scholar 

  • 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 

  • 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 

  • Breckon G., Ortiz W. N. (1983) Pollination ofZamia pumila by fungus gnats. Amer. J. Bot. 70: 106–107.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • Cronquist A. (1981) An integrated system of classification of flowering Plants. Columbia University Press, New York, USA.

    Google Scholar 

  • 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 

  • 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 

  • Diels L. (1916) Kaferblumen bei denRanales und ihre Bedeutung fur die Phylogenese der Angiospermen. Ber. Deutsch. Bot. Ges. 34: 758–774.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Eames A. J. (1961) Morphology of the Angiosperms. McGraw-Hill Book Co. Inc, New York.

    Google Scholar 

  • Endress P. K. (1987) The early evolution of the angiosperm flower. Tree 2: 300–304.

    Google Scholar 

  • 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 

  • Endress P. K. (1994) Diversity and evolutionary biology of tropical flowers. Cambridge Univ. Press, New York, USA.

    Google Scholar 

  • 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 

  • Essig F. B. (1971) Observations of pollination inBactris. Principes 15: 20–24.

    Google Scholar 

  • Essig F. B. (1973) Pollination in some New Guinea palms. Principes 17: 75–83.

    Google Scholar 

  • Faegri K., van der Pijl L. (1979) The Principles of Pollination Ecology. 3rd edn. Pergamon Press, New York.

    Google Scholar 

  • Farrell B. (1998) “Inordinate Fondness” Explained: Why Are There so many beetles? Science 281: 555–559.

    Google Scholar 

  • 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 

  • Futuyma D. J. (1998) Evolutionary Biology. 3rd edn. Sinauer Associates Inc., Sunderland, Massachusetts.

    Google Scholar 

  • Gibb P. (1977) Floral biology ofTalauma ovata St. Hil. (Magnoliaceae). Ciencia E. Cultura 29: 1437–1441.

    Google Scholar 

  • Goldblatt P., Bernhardt P. (1999) Pollination ofMoraea species (Iridaceae) with a staminal column. Ann. Missouri Bot. Gard. 86: 47–56.

    Google Scholar 

  • 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 

  • Gottsberger G. (1977) Some aspects of beetle pollination in the evolution of flowering plants. Plant Syst. Evol. [Suppl.] 1: 211–226.

    Google Scholar 

  • Gottsberger G. (1988) The reproductive biology of primitive angiosperms. Taxon 37: 630–643.

    Google Scholar 

  • Gottsberger G. (1989a) Beetle pollination and flowering rhythm ofAnnona spp. (Annonaceae) in Brazil. Plant Syst. Evol. 167: 165–187.

    Google Scholar 

  • Gottsberger G. (1989b) Comments on flower evolution and beetle pollination in the generaAnnona andRollinia (Annonaceae). Plant Syst. Evol. 167: 189–194.

    Google Scholar 

  • Gottsberger G., Amaral Jr. A. (1984) Pollination strategies in brazilianPhilodendron species. Ber. Deutsch. Bot. Ges. Bd. 97S: 391–410.

    Google Scholar 

  • 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 

  • Grant V. (1950) The pollination ofCalycanthus occidentalis. Amer. J. Bot. 37: 294–297.

    Google Scholar 

  • Grimaldi D. (1999) The co-radiations of pollinating insects and angiosperms in the Cretaceous. Ann. Missouri Bot. Gard. 86: 373–406.

    Google Scholar 

  • Grimaldi D., Grant K. (1965) Flower pollination in the phlox family. Columbia Univ. Press, New York, NY, USA.

    Google Scholar 

  • 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 

  • Hawkeswood T. (1981a) Insect pollination ofAngophora woodsiana F. Bail. (Myrtaceae) at Burbank, south-east Queensland. Victorian Naturalist 98: 120–129.

    Google Scholar 

  • 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 

  • Hawkeswood T. (1982) Notes on insect pollination of two species ofEucalyptus (Myrtaceae) from south-west Western Australia. Victorian Naturalist 99: 28–37.

    Google Scholar 

  • Hawkeswood T. (1987a) Beetles of Australia. Angus and Robertson, North Ryde, New South Wales, Australia.

    Google Scholar 

  • 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 

  • Hawkeswood T. (1987c) Notes on someColeoptera fromBaeckea stenophytlla F. Muell. (Myrtaceae) in New South Wales, Australia. G. Ital. Entomol. 3: 285–290.

    Google Scholar 

  • Hawkeswood T. (1989) Notes onDiphucephala affinis (Coleoptera: Scarabaeidae) associated with flowers ofHibbertia andAcacia in Western Australia. Plant Syst. Evol. 168: 1–5.

    Google Scholar 

  • Hawkeswood T. (1990) Insect pollination ofBursaria spinosa (Pittosporaceae) in the Armidale area, New South Wales, Australia. G. Ital. Entomol. 5: 67–87.

    Google Scholar 

  • 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 

  • 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 

  • Henderson A. (1984) Observations on pollination ofChrysophila albida. Principes 28: 120–126.

    Google Scholar 

  • Irvine A. K., Armstrong J. (1988) Beetle pollination in Australian tropical rainforests. Proc. Ecol. Soc. Aust. 15: 107–113.

    Google Scholar 

  • Ishida K. (1996) Beetle pollination ofMagnolia praecocissima var.borealis. Plant Species Biol. 11: 198–206.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Kato M., Inoue T. (1994) Origin of insect pollination. Science 368: 195.

    Google Scholar 

  • 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 

  • Labandeira C. (1998a) How old is the flower and the fly? Science 280: 57–59.

    Google Scholar 

  • 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 

  • 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 

  • Michener C. D. (1979) Biogeography of the bees. Ann. Missouri Bot. Gard. 66: 277–347.

    Google Scholar 

  • 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 

  • 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 

  • Monteith G. B. (1973) Entomological notes: Dung beetles as pollinators of anArum Lily. News Bull. Entomol. Soc. Queensland 97: 13.

    Google Scholar 

  • Moore R., Clark W. D., Stearn K. R. (1995) Botany. Wm C. Brown Publishers, USA.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Nilsson L. A. (1978) Pollination ecology ofEpipactis palustris (Orchidaceae). Bot. Notiser 131: 355–368.

    Google Scholar 

  • Norstog K. (1987) Cycads and the origin of insect pollination. American Scientist 75: 270–279.

    Google Scholar 

  • Northington D. K., Schneider E. L. (1996) The botanical world. Wm, C, Brown Publisers, USA.

    Google Scholar 

  • Peringuey L. (1902) Descriptive catalogue of theColeoptera of South Africa (Lucanidae and Scarabaeidae). Trans. S. African Phil. Soc. 12: 1–920.

    Google Scholar 

  • 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 

  • 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 

  • Prance G. (1980) A note on the pollination ofNymphaea amazonum Mart. & Zucc. (Nymphaeaceae). Brittonia: 505–507.

  • Prance G., Arias J. (1975) A study of the floral biology ofVictoria amazonica (Poepp.) Sowerby (Nymphaeaceae). Acta Amazonica 6: 163–70.

    Google Scholar 

  • 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 

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

    Google Scholar 

  • Raven P., Evert R. F., Eichorn S. E. (1999) Biology of Plants. W. H. Freeman and Company, Worth Publishers, New York.

    Google Scholar 

  • Ren D. (1998) Flower-associated Brachycera flies as fossil evidence for Jurassic angiosperm origins. Science 280: 85–88.

    Google Scholar 

  • Renner S. S., Johanson K. A. (1995) Breeding system and pollination ofNuphar luteum (L.) Smith (Nymphaeaceae) in Norway. Flora 190: 109–113.

    Google Scholar 

  • Richards A. J. (1986) Plant Breeding Systems. Allen & Unwin, London, England.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • Scott Elliot G. (1891) Notes on the fertilisation of South African and Madagascan flowering plants. Ann. Bot. 5: 333–405.

    Google Scholar 

  • 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 

  • Seymour R., Schultze-Motel P. (1997) Heat-producing flowers. Endeavour 21: 125–129.

    Google Scholar 

  • 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 

  • Schmid R. (1970) Notes on the reproductive biology ofAsterogyne martiana (Palmae). II. Pollination by syrphid flies. Principes 14: 39–49.

    Google Scholar 

  • Singer R. N., Cocucci A. (1997) Pollination ofPteroglossaspis ruwenzoriensis (Rendle) Role (Orchidaceae) by beetles in Argentina. Bot. Acta 10: 338–342.

    Google Scholar 

  • Sivadasan M., Sabu T. (1989) Beetle-pollination — cantharophily — inAmorphophallus hohenackeri (Araceae). Aroideana 12: 32–37.

    Google Scholar 

  • 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 

  • Steiner K. (1998a) Beetle pollination of peacock moraeas (Iridaceae) in South Africa. Plant Syst. Evol. 209: 47–65.

    Google Scholar 

  • Steiner K. (1998b) The evolution of beetle pollination in a South African Orchid. Amer. J. Bot. 85: 1180–1193.

    Google Scholar 

  • Takhtajan A. (1991) Evolutionary trends in flowering plants. Columbia Univ. Press, New York.

    Google Scholar 

  • Thien L. B. (1974) Floral biology ofMagnolia. Amer. J. Bot. 61: 1037–1045.

    Google Scholar 

  • Thien L. B. (1980) Patterns of pollination in the primitive angiosperms. Biotropica 12: 1–13.

    Google Scholar 

  • 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 

  • Thien L. B., Heimermann W. H., Holman R. T. (1975) Floral odors and quantitative taxonomy ofMagnolia andLiriodendron. Taxon 24: 557–568.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • van der Pijl L., Dodson C. H. (1966) Orchid flowers, their pollination and evolution. University of Miami Press, Coral Gables, Florida.

    Google Scholar 

  • Vogel S. (1954) Blütenbiologische Typen als Elemente der Sippengliederung. Bot. Stud. 1: 1–338.

    Google Scholar 

  • 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 

  • Wallace B. J. (1980) Cantharophily and the pollination ofPeristeranthus hillii. The Orchadian 6: 214–215.

    Google Scholar 

  • 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 

  • 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 

  • Yeo P. (1993) Secondary pollen presentation: Form, function and evolution. Springer, Wien New York.

    Google Scholar 

  • 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 

  • Young H. J. (1986) Beetle pollination ofDieffenbachia Longispatha (Araceae). Amer. J. Bot. 73: 931–944.

    Google Scholar 

  • 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 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bernhardt, P. Convergent evolution and adaptive radiation of beetle-pollinated angiosperms. Pl Syst Evol 222, 293–320 (2000). https://doi.org/10.1007/BF00984108

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00984108

Key words

Navigation