Plant Systematics and Evolution

, Volume 222, Issue 1–4, pp 167–185 | Cite as

Abiotic pollen and pollination: Ecological, functional, and evolutionary perspectives

  • J. D. Ackerman


The transport and capture of pollen in ~20% of all angiosperm families occurs in air and water. In other words, pollination is abiotic and occurs via the fluid media, not an animal vector. Whereas some early concepts considered abiotic pollination to be largely a stochastic phenomenon, there is sufficient evidence to indicate that wind pollination (i.e. anemophily) and water pollination (i.e. hydrophily) have deterministic features and are sophisticated fluid dynamic solutions to the problem of pollen release, dispersal, and capture.

An abiotic pollination syndrome is defined in which there is spatial or temporal separation of carpellate and staminate flowers, which are drab, a reduction in perianth parts, stigmas and anthers are exposed to the fluid, and typically unclumped pollen may be produced in large amounts. Separate pollination syndromes are defined for anemophilous (i.e. wind-pollinated), ephydrophilous (i.e. surface-pollinated), and hydrophilous (i.e. submarine-pollinated) plants. Distinctions are based on habitat and physical conditions for pollination, pollen size, shape, and ultrastructure, morphology and ultrastructure of stigmas, and outcrossing rates. For example, anemophilous pollen are spherical and small, ephydrophilous pollen are spherical or reniform and large, while hydrophilous pollen are filiform (i.e. filamentous) or functionally filiform. The pollination mechanisms and mechanics associated with these syndromes reveals a strong evolutionary relationship between plant morphology and fluid dynamics.

Key words

Anemophily hydrophily wind pollination water pollination biomechanics fluid dynamics ephydrophily hyphydrophily dicliny dichogamy autogamy 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ackerman J. D. (1989) Biomechanical aspects of submarine pollination inZostera marina L. Doctoral Dissertation. Cornell University, Ithaca.Google Scholar
  2. Ackerman J. D. (1993) Pollen germination and pollen tube growth in the marine angiosperm,Zostera marina L. Aquat. Bot. 46: 189–202.Google Scholar
  3. Ackerman J. D. (1995) Convergence of filiform pollen morphologies in seagrasses: Functional mechanisms. Evol. Ecol. 9: 139–153.Google Scholar
  4. Ackerman J. D. (1997a) Submarine pollination in the marine angiosperm,Zostera marina: Part I. The influence of floral morphology on fluid flow. Amer. J. Bot. 84: 1099–1109.Google Scholar
  5. Ackerman J. D. (1997b) Submarine pollination in the marine angiosperm,Zostera marina: Part II. Pollen transport in flow fields and capture by stigmas. Amer. J. Bot. 84: 1110–1119.Google Scholar
  6. Ackerman J. D. (1998) Is the limited diversity of higher plants in marine systems due to biophysical limitations for reproduction or evolutionary and physiological constraints? Funct. Ecol. 12: 979–982.Google Scholar
  7. Ackerman J. D., Okubo A. (1993) Reduced mixing in a marine macrophyte canopy. Funct. Ecol. 7: 305–309.Google Scholar
  8. Arber A. (1920) Water Plants, A Study of Aquatic Angiosperms. Cambridge University Press, Cambridge.Google Scholar
  9. Balfour B. (1879) On the genusHalophila. Trans. Bot. Soc. Edin. 13: 290–343 (+5 plates).Google Scholar
  10. Barrett S. C. H., Eckert C. G. (1990) Variation and evolution of mating systems in seed plants. In: Kawano S. (ed.) Biological Approaches and Evolutionary Trend in Plants. Academic Press, New York, pp. 229–254.Google Scholar
  11. Berry P. E., Calvo R. N. (1989) Wind pollination, self-incompatibility, and altitudinal shifts in pollination systems in the high Andean genusEspeletia (Asteraceae). Amer. J. Bot. 76: 1602–1614.Google Scholar
  12. Bornet D. M. (1864) Recherches sur lePhucagrostis major Cavol. Ann. Sci. Nat. Bot (Sr. 5) 1: 5–51 (+11 plates).Google Scholar
  13. Bowman H. H. M. (1922) The distribution and pollination of certain sea-grasses. Mich. Acad. Sci. Papers 22: 3–10 (+4 plates).Google Scholar
  14. Buchmann S. L., O'Rourke M. K., Niklas K. J. (1989) Aerodynamic ofEphedra trifurca. III Selective pollen capture by pollination droplets. Bot. Gaz. 150: 122–131.Google Scholar
  15. Bullock S. H. (1994) Wind pollination of neotropical deciduous trees. Biotropica 26: 172–179.Google Scholar
  16. Burd M. (1994) Bateman's principle and plant reproduction: The role of pollen limitation in fruit and seed set. Bot. Rev. 60: 83–139.Google Scholar
  17. Charlesworth D. (1993) Why are unisexual flowers associated with wind pollination and unspecialized pollinators? Am. Nat. 141: 481–490.Google Scholar
  18. Corbet S. A., Beament L., Eisikowitch D. (1982) Are electrostatic forces involved in pollen transfer? Plant Cell Environ. 5: 125–129.Google Scholar
  19. Cook C. D. K. (1982) Pollination mechanisms in the Hydrocharitaceae. In: Symoens J. J., Hooper S. S., Compère P. (eds.) Studies on Aquatic Vascular Plants. Royal Botanical Society of Belgium, Brussels, pp. 1–15.Google Scholar
  20. Cook C. D. K. (1988) Wind pollination in aquatic angiosperms. Ann. Missouri Bot. Gard. 75: 768–777.Google Scholar
  21. Cook C. D. K. (1996) The Aquatic Plant Book. SPB Academic Publishing, New York.Google Scholar
  22. Cox P. A. (1988) Hydrophilous pollination. Ann. Rev. Ecol. Syst. 19: 261–280.Google Scholar
  23. Cox P. A. (1991) Abiotic pollination: An evolutionary escape for animal pollinated angiosperms. Phil. Trans. R. Soc. Lond. B 333: 217–224.Google Scholar
  24. Crane P. R. (1986) Form and function in wind dispersed pollen. In: Blackmore S., Ferguson I. K. (eds.) Pollen and Spores: Form and Function. Academic, London, pp. 179–202.Google Scholar
  25. Cronquist A. (1988) The Evolution and Classification of Flowering Plants. 2nd edn. New York Botanical Gardens, New York.Google Scholar
  26. Cruden R. W. (2000) Pollen grains: why so many? In: Dafni A., Pacini E., Hesse M. (ed) Pollen and Pollination. Springer, Berlin, pp. 143–165.Google Scholar
  27. Dafni A., Dukas R. (1986) Insect and wind pollination inUrginea martima (Liliaceae). Plant Syst. Evol. 154: 1–10.Google Scholar
  28. Dafni A., Firmage D. (2000) Pollen longevity: Practical, ecological and evolutionary implications. In: Dafni A., Pacini E., Hesse M. (eds.) Pollen and Pollination. Springer, Berlin, pp. 113–132.Google Scholar
  29. DeCock A. W. A. M. (1980) Flowering, pollination and fruiting inZostera marina L. Aquat. Bot. 9: 201–220.Google Scholar
  30. Delpino F., Ascherson P. (1871) Federico Delpino's Eintheilung der Pflanzen nach dem Mechanismus der dichogamischen Befruchtung und Bemerkungen über die Befruchtungs-Vorgänge bei Wasserpflanzen (Aus dessen, Ulteriori osservazioni sulla dicogamia nel regno vegetabile Part II. Fasc. I. [Atti della soc. ital. di sc. nat. XIII, 1870] migetheilt und mit einigen Zusätzen versehen von P. Ascherson. Bot. Zeit. 29: 443–5, 447–59, 463–7.Google Scholar
  31. den Hartog C. (1970) The Sea-Grasses of the World. North Holland Publishing, Amsterdam.Google Scholar
  32. Diez M. J., Talavera S., Garcia-Murillo P. (1988) Contributions to the palynology of hydrophytic, non-entomophilous angiosperms. 1. Studies with LM and SEM. Candollea 43: 147–158.Google Scholar
  33. Ducker S. C., Knox R. B. (1976) Submarine pollination in seagrasses. Nature 263: 705–706.Google Scholar
  34. Ducker S. C., Pettitt J. M., Knox R. B. (1978) Biology of Australian seagrasses: Pollen development and submarine pollination inAmphibolis antarctica andThalassodendron ciliatum (Cymodoceaceae). Aus. J. Bot. 26: 265–85.Google Scholar
  35. Dudley W. R. (1893) The genusPhyllospadix. In The Wilder Quarter-Century Book. Comstock Press, Ithaca, pp. 403–420 + 2 plates.Google Scholar
  36. Erickson E. H., Buchmann S. L. (1983) Electrostatics and pollination. In: Jones C. E., Little R. J. (eds.) Handbook of Experimental Pollination Biology. Van Nostrand Reinhold, New York.Google Scholar
  37. Esau K. (1977) Anatomy of Seed Plants. 2nd edn. J. Wiley and Sons, New York.Google Scholar
  38. Faegri K., van der Pijl L. (1979) The Principles of Pollination Ecology, 3rd edn. Pergamon, Oxford.Google Scholar
  39. Forgacs O. L., Mason S. G. (1958) The flexibility of wood-pulp fibers. TAPPI 41: 695–704.Google Scholar
  40. Gan-Mor S., Schwartz Y., Bechar A., Eisikowitch D., Manor G. (1995) Relevance of electrostatic forces in natural and artificial pollination. Can. Agricult. Engin. 37: 189–194.Google Scholar
  41. Gomez J. M., Zamora R. (1996) Wind pollination in high-mountain populations ofHormathophylla spinosa (Cruciferae). Amer. J. Bot. 83: 580–585.Google Scholar
  42. Goodwillie C. (1999) Wind pollination and reproductive assurance inLinanthus parviflora (Polemoniaceae), a self-incompatible annual. Amer. J. Bot. 86: 948–954.Google Scholar
  43. Grace J. B. (1993) The adaptive significance of clonal reproduction in angiosperms: an aquatic perspective. Aquat. Bot. 44: 159–180.Google Scholar
  44. Guo Y. H., Sperry R., Cook C. D. K., Cox P. A. (1990) The pollination ecology ofZannichelia palustris L. (Zannicheliaceae). Aquat. Bot. 38: 29–45.Google Scholar
  45. Hamrick J. L., Godt M. J. W., Sherman-Broyles S. L. (1995) Gene flow among plant populations: Evidence from genetic markers. In: Hoch P. G., Stevenson A. G. (eds.) Experimental and Molecular Approaches to Plant Biosystematics. Missouri Botanical Garden, St. Louis, pp. 215–232.Google Scholar
  46. Harder L. D. (1998) Pollen-size comparisons among animal-pollinated angiosperms with different pollination characteristics. Biol. J. Linnean Soc. 64: 513–525.Google Scholar
  47. Haynes R. R. (1988) Reproductive biology of selected aquatic plants. Ann. Missouri Bot. Gard. 75: 805–810.Google Scholar
  48. Honig M. A., Linder H. P., Bond W. J. (1992) Efficacy of wind pollination: Pollen load size and natural microgametophyte populations in windpollinatedStaberoha banksii. Amer. J. Bot. 79: 443–448.Google Scholar
  49. Iwanami Y., Sasakuma T., Yamada Y. (1988) Pollen: Illustrations and Scanning Electronmicrographs. Springer, Berlin.Google Scholar
  50. Kausik S. B., Rao P. K. V. (1942) The male gametophyte ofHalophila ovata Gaudich. Halfyrly J. Mys. Univ. 3: 41–49.Google Scholar
  51. Knuth P. (1906) Handbook of Flower Pollination, Based Upon Hermann Müller's Work ‘Fertilisation of Flowers by Insects’. Volume I: Introduction and Literature. Translated by J. R. Ainsworth Davis. Oxford University Press, London.Google Scholar
  52. Koopman B. O. (1956) The theory of search: II Target detection. Oper. Res. 4: 503–531.Google Scholar
  53. Lacroix C. R., Kemp J. R. (1997) Developmental morphology of the androecium ad gynoecium inRuppia maritima L.: Considerations for pollination. Aquat. Bot. 59: 253–262.Google Scholar
  54. Les D. H. (1988) Breeding systems, population structure, and evolution in hydrophilous angiosperms. Ann. Missouri Bot. Gard. 75: 819–835.Google Scholar
  55. Les D. H., Cleland M. A., Waycott M. (1997) Phylogenetic studies in the Alismatidae, II: Evolution of marine angiosperms (seagrasses) and hydrophily. Syst. Bot. 22: 443–463.Google Scholar
  56. Linder H. P., Midgley J. (1996) Anemophilous plants select pollen from their own species from the air. Oecologia 108: 85–87.Google Scholar
  57. Listabarth C. (1992) Insect-induced wind pollination in the palmChamaedorea pinnatifrons and pollination in the relatedWeldlandiella. Biodiv. Conserv. 1: 39–50.Google Scholar
  58. Mahabale T. S. (1968) Spores and pollen grains of water plants and their dispersal. Rev. Palaeobot. Palynol. 7: 285–296.Google Scholar
  59. Martinsson K. (1993) The pollen of SwedishCallitriche (Callitricaceae) — trends towards submergence. Grana 32: 198–193.Google Scholar
  60. Midgley J. J., Bond W. J. (1991a) How important is biotic pollination and dispersal to the success of the angiosperms? Phil. Trans. R. Soc. Lond. B 333: 209–215.Google Scholar
  61. Midgley J. J., Bond W. J. (1991b) Ecological aspects of the rise of angiosperms: A challenge to the reproductive superiority hypothesis. Biol. J. Linn. Aoc. 44: 8–92.Google Scholar
  62. Nicholls M. S., Cook C. D. K. (1986) The function of pollen tetrads inTypha (Typhaphaceae). Verhoff. Geobot. Inst. Zurich 87: 112–119.Google Scholar
  63. Niklas K. J. (1985) The aerodynamics of wind pollination. Bot. Rev. 51: 328–386.Google Scholar
  64. Niklas K. J. (1992) Plant Biomechanics. University of Chicago Press, Chicago.Google Scholar
  65. Niklas K. J. (1997) The Evolutionary Biology of Plants. University of Chicago Press, Chicago.Google Scholar
  66. Niklas K. J., Buchmann S. (1987) The aerodynamics of pollen capture in two sympatricEphedra species. Evol. 41: 104–123.Google Scholar
  67. Niklas K. J., Buchmann S. (1988) Aerobiology and pollen capture in orchard-grownPistacia vera (Anacardiaceae). Amer. J. Bot. 75: 1813–1829.Google Scholar
  68. Niklas K. J., Paw U. K. T. (1983) Conifer ovulate cone morphology: Implications on pollen impaction patterns. Amer. J. Bot. 70: 568–577.Google Scholar
  69. Nixon S. W. (1988) Physical energy inputs and the comparative ecology of lake and marine ecosystems. Limnol. Oceanogr. 33: 1005–1025.Google Scholar
  70. Norstog K. J., Stevenson D. W., Niklas K. J. (1986) The role of beetles in the pollination ofZamia furfuracea L. fil. (Zamiaceae). Biotropica 18: 300–306.Google Scholar
  71. Osborne J. M., Philbrick C. T. (1994) Comparative pollen structure and pollination biology in the Callitrichaceae. Acta. Bot. Gallica 141: 257–266.Google Scholar
  72. Pascasio J. F., Santos J. K. (1930) A critical morphological study ofThalassia hemprichii (Ehrenb.) Aschers. from the Philippines. Nat. Appl. Sci. Bull. Univ. Philipp. 1: 1–19.Google Scholar
  73. Payne W. W. (1981) Structure and function in angiosperm pollen wall evolution. Rev. Palaeobot. Palynol. 35: 35–59.Google Scholar
  74. Perveen A., Qaiser M. (1996) Pollen flora of Pakistan — V. Haloragaceae. Pak. J. Bot. 28: 21–24.Google Scholar
  75. Pettitt J. M. (1976) Pollen wall and stigma surface in the marine angiospermsThalassia andThalassodendron. Micron 7: 21–32.Google Scholar
  76. Pettitt J. M. (1981) Reproduction in seagrasses: Pollen development inThalassia hemprichii, Halophila stipulacea, andThalassodendron ciliatum. Ann. Bot. 48: 609–622.Google Scholar
  77. Pettitt J. M. (1984) Aspects of flowering and pollination in marine angiosperms. Oceanogr. Mar. Biol. Ann. Rev. 22: 315–342.Google Scholar
  78. Pettitt J., Ducker S., Knox B. (1981) Submarine pollination. Sci. Amer. 244: 131–143.Google Scholar
  79. Pettitt J. M., Ducker S. C., Knox R. B. (1978)Amphibolis has no exine. Helobiae Newsletter 2: 19–21.Google Scholar
  80. Pettitt J. M., Jermy A. C. (1975) Pollen in hydrophilous angiosperms. Micron 5: 377–405.Google Scholar
  81. Philbrick C. T. (1984) Pollen tube growth within vegetative tissues ofCallitriche (Callitrichaceae). Amer. J. Bot. 71: 882–886.Google Scholar
  82. Philbrick C. T., Anderson G. J. (1987) Implications of pollen/ovule ratios and pollen size for the reproductive biology ofPotamogeton and autogamy in aquatic angiosperms. Syst. Bot. 12: 98–105.Google Scholar
  83. Philbrick C. T., Bernardello L. M. (1992) Taxonomic and geographic distribution of internal geitonogamy in new worldCallitriche (Callitrichaceae). Amer. J. Bot. 79: 887–890.Google Scholar
  84. Philbrick C. T., Retana A. N. (1998) Flowering phenology, pollen flow, and seed production inMarathrum rubrum (Podostemaceae). Aquat. Bot. 62: 199–206.Google Scholar
  85. Proctor M., Yeo P., Lack A. (1996) Natural History of Pollination. Timber Press, Portland.Google Scholar
  86. Raven P. H., Evert R. F., Eichhorn S. E. (1999) Biology of Plants. 6th edn. W. H. Freeman and Company, New York.Google Scholar
  87. Regal P. J. (1982) Pollination by wind and animals: Ecology and geographic patterns. Ann. Rev. Ecol. Syst. 13: 497–524.Google Scholar
  88. Renner S. S., Ricklefs R. E. (1995) Dioecy and its correlates in the flowering plants. Amer. J. Bot. 82: 596–606.Google Scholar
  89. Rosenberg O. (1901) Ueber die Pollenbildung vonZostera. Meddh. Stockh. Högskolas. Bot. Inst. 4: 3–21.Google Scholar
  90. Ruckleshaus M. H. (1995) Estimation of outcrossing rates and of inbreeding depression in a population of the marine angiosperm,Zostera marina. Mar. Biol. 123: 583–593.Google Scholar
  91. Runions C. J., Rensing K. H., Takaso T., Owens J. N. (1999) Pollination ofPicea orientalis (Pinaceae): Saccus morphology governs pollen buoyancy. Amer. J. Bot. 86: 190–197.Google Scholar
  92. Schemske D. W., Lande R. (1985) The evolution of self-fertilization and inbreeding depression in plants. II Empirical observations. Evol. 39: 41–52.Google Scholar
  93. Schoen D. J., Stewart S. S. (1986) Variation in male reproductive investment and male reproductive success in white spruce. Evol. 40: 1109–1120.Google Scholar
  94. Sculthorpe C. D. (1967) The Biology of Aquatic Vascular Plants. Edward Arnold, London.Google Scholar
  95. Smith J. P. (1977) Vascular Plant Families. Mad River Press, Eureka.Google Scholar
  96. Stelleman P. (1984) Reflections on the transition from wind pollination to ambophily. Acta. Bot. Neerl. 33: 497–508.Google Scholar
  97. Stewart J. G., Rüdenberg L. (1980) Microsporocyte growth and meiosis inPhyllospadix torreyi, a marine monocotyledon. Amer. J. Bot. 67: 949–954.Google Scholar
  98. Sullivan G., Titus J. E. (1996) Physical site characteristics limit pollination and fruit set in the dioecious hydrophilous species,Vallisneria americana. Oecologia 108: 285–292.Google Scholar
  99. Svedelius N. (1932) On the different types of pollination inVallisneria spiralis L. andVallisneria americana Michx. Svensk Bot. Tidskrift 26: 1–12.Google Scholar
  100. Thanikaimoni G. (1986) Pollen apertures: form and function. In: Blackmore S., Ferguson I. K. (eds.) Pollen and Spores: Form and Function. Academic, London, pp. 119–136.Google Scholar
  101. Thorne R. F. (1992) Classification and geography of the flowering plants. Bot. Rev. 58: 225–348.Google Scholar
  102. Tomlinson P. B. (1982) Anatomy of the Monocotyledon: VII Helobiae (Alismatidae). Oxford University Press, New York.Google Scholar
  103. Tomlinson P. B. (1994) Functional morphology of saccate pollen in conifers with special reference to Podocarpaceae. Int. J. Plant. Sci. 155: 699–715.Google Scholar
  104. Vaknin Y., Gan-mor S., Bechar A., Ronen B., Eisikowitch D. (2000) The role of electrostatics forces in pollination. In: Dafni A., Pacini E., Hesse M. (eds.) Pollen and Pollination. Springer, Berlin, pp. 133–142.Google Scholar
  105. Verduin J. J. (1996)In situ submarine pollination in the seagrassAmphibolis antartica (Labill.) Sonderet Aschers.ex Aschers. And its relations to hydrodynamics. In: Kuo J., Phillips R. C., Walker D. I., Kirkman H. (eds.) Seagrass Biology: Proceedings of an International Workshop. University of Western Australia, Nedlands, pp. 123–128.Google Scholar
  106. Verduin J. J., Walker D. I., Kuo J. (1996)In situ submarine pollination in the seagrassAmphibolis antartica: Research notes. Mar. Ecol. Progr. Ser. 133: 307–309.Google Scholar
  107. Vidakovic M. (1991) Conifers: Morphology and Variation. Graficki Zavod Hrvatske, Croatia.Google Scholar
  108. Vogel S. (1994) Life in Moving Fluids, 2nd edn. Princeton University Press, Princeton.Google Scholar
  109. Vroege P. W., Stelleman P. (1990) Insect and wind pollination inSalix repens L. andSalix caprea L. Israel J. Bot. 39: 125–132.Google Scholar
  110. Waycott M., Sampson J. F. (1997) The mating system of an hydrophilous angiospermPosidonia australis (Posidoniaceae). Amer. J. Bot. 84: 621–665.Google Scholar
  111. Whitehead D. R. (1983) Wind Pollination: Some ecological and evolutionary perspectives. In: Real L. (ed.) Pollination Biology. Academic, New York, pp. 97–108.Google Scholar
  112. Yamashita T. (1976) Über die Pollenbildung beiHalodule pinifolia undH. uninervis. Beitr. Biol. Pflanzen 52: 217–226.Google Scholar
  113. Zomlefer W. B. (1994) Guide to Flowering Plant Families. University of North Carolina Press, Chapel Hill.Google Scholar

Copyright information

© Springer-Verlag 2000

Authors and Affiliations

  • J. D. Ackerman
    • 1
  1. 1.Physical Ecology LaboratoryUniversity of Northern British ColumbiaPrince GeorgeCanada

Personalised recommendations