Skip to main content Accessibility help
  • Print publication year: 2011
  • Online publication date: January 2012

6 - Pollen evidence for the pollination biology of early flowering plants



Angiosperms are the dominant and most diverse plant group living today. They are also found in the greatest number of terrestrial ecosystems on Earth of any group of plants (Judd et al. 2002; Soltis and Soltis 2004). They provide human beings and other terrestrial animals, directly or indirectly, with the majority of their nutrition (e.g. Theissen and Melzer 2007). Much of these foods, such as fruits, nuts, seeds, and grains, are the direct products of flowers, and pollination is an essential step in their formation. Pollination biology has long been an interest of biologists and agricultural scientists (e.g. Faegri and van der Pijl 1979; Proctor et al. 1996; Aizen et al. 2009; Lonsdorf et al. 2009; Mitchell et al. 2009). However, our understanding of the early phases of the evolution of angiosperm pollination is still limited and attempts to reconstruct the history of the interactions between angiosperms and pollinators are challenging (Hu et al. 2008; Taylor and Hu 2010). Evolutionary biologists have attempted to deduce the possible histories of pollination syndromes (summarized in Taylor and Hu, 2010) based upon usually incomplete and limited early angiosperm flower fossil records (e.g. Dilcher 1979; Retallack and Dilcher 1981; Crane et al. 1986; Herendeen et al. 1995; Crepet and Nixon 1996; Friis et al. 1999, 2000, 2006; Crepet 2008), limited insect fossil records(e.g. Grimaldi 1999; Labandeira 2000, 2002; Grimaldi and Engel 2005; Ren et al. 2009), parsimony analysis (e.g. Hu et al. 2008; Friedman and Barrett 2008; Taylor and Hu 2010), investigation on pollination biology of the most basal angiosperms (e.g.Thien et al. 2009), and angiosperm pollen fossil records (e.g. Hu et al. 2008; Taylor and Hu 2010).

Currently there are three hypotheses regarding early angiosperm pollination biology (Taylor and Hu, 2010):

Ancestral angiosperms were insect pollinated (e.g. Crepet and Friis 1987; Wing and Boucher 1998; Friis et al. 1999; Feild and Arens 2005).

During the mid Cretaceous there were increases in advanced pollination syndromes (e.g. Crepet et al. 1991; Crepet 2008; Hu et al. 2008, Taylor and Hu 2010).

Wind pollination (anemophily) is derived (e.g. Culley et al. 2002; Hu et al. 2008, Taylor and Hu 2010).

Ackerman, J. D. 2000 Abiotic pollen and pollination: ecological, functional and evolutionary perspectivesPlant Systematic and Evolution 222 167
Aizen, M. A.Garibaldi, L. A.Cunningham, S. A.Klein, A. M. 2009 How much does agriculture depend on pollinators? Lessons from long-term trends in crop production and diversity deficitsAnnals of Botany 103 1579
Anderson, J. M.Barrett, S. C. H. 1986 Pollen tube growth in tristylous Pontederia cordata (Pontederiaceae)Canadian Journal of Botany 64 2602
APG III 2009 An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IIIBotanical Journal of the Linnean Society 161 105
Archangelsky, S.Gamerro, J. C. 1967 Spore and pollen types of the Lower Cretaceous in Patagonia (Argentina)Review of Palaeobotany and Palynology 1 211
Argue, C. L. 1973 The pollen of Limnocharis flava Buchen., Hydrocleis nymplloides (Willd.) Buchen., and Tenagocltaris latifolia (Don.) Buchen. (Limnocharitaceae)Grana 14 108
Basinger, J. F.Dilcher, D. L. 1984 Ancient bisexual flowersScience 224 511
von Balthazar, M.Pedersen, K. R.Friis, E. M. 2005 Teixeiria lusitanica gen. et nov., a ranunculalean flower from the Early Cretaceous of PortugalPlant Systematics and Evolution 255 5575
Batten, D. J. 1986 Possible functional implications of exine sculpture and architecture in some Late Cretaceous Normapolles pollen. In Pollen and Spores: Form and FunctionLondon, UKAcademic Press
Bernardello, G. 2007 Nectaries and NectarDordrecht, NetherlandsSpringer
Brenner, G. J. 1996 Flowering Plant Origin, Evolution and PhylogenyNew York, NYChapman & Hall
Brenner, G. J.Bickoff, I. 1992 Palynology and age of the Lower Cretaceous basal Kurnub Group from the coastal plain to the northern Negev of IsraelPalynology 16 137
Burger, D. 1990 Early Cretaceous angiosperms from Queensland, AustraliaReview of Palaeobotany and Palynology 65 153
Burger, D. 1993 Early and middle Cretaceous angiosperm pollen grains from AustraliaReview of Palaeobotany and Palynology 78 183
Chaowasku, T.Mols, J.van der Ham, R. W. J. M. 2008 Pollen morphology of Miliusa and relatives (Annonaceae)Grana 47 175
Cox, P. A. 1991 Abiotic pollination: an evolutionary escape for animal-pollinated angiospermsPhilosophical Transactions of the Royal Society London 333 217
Crane, P. R. 1986 Form and function in wind dispersed pollen. In Pollen and Spores: Form and FunctionLondon, UKAcademic Press
Crane, P. R.Friis, E. M.Pedersen, K. R. 1986 Lower Cretaceous angiosperm flowers: fossil evidence on early radiation of DicotyledonsScience 232 852
Crane, P.R.Friis, E. M.Pedersen, K. R. 1989 Reproductive structure and function in Cretaceous ChloranthaceaePlant Systematic and Evolution 165 211
Crepet, W. L. 2008 The fossil record of angiosperms: requiem or renaissance?Annals of the Missouri Botanical Garden 95 3
Crepet, W. L.Friis, E. M. 1987 The Origin of Angiosperms and Their Biological ConsequencesCambridge, UKCambridge University Press
Crepet, W. L.Nixon, K. C. 1996 The Anther: Form, Function and PhylogenyCambridge, UKCambridge University Press
Crepet, W. L.Friis, E. M.Nixon, K. C. 1991 Fossil evidence for the evolution of biotic pollinationPhilosophical Transactions of the Royal Society London 333 187
Culley, T. M.Weller, S. G.Sakai, A. K. 2002 The evolution of wind pollination in angiospermsTrends in Ecology & Evolution 17 361
Dilcher, 1979 Early angiosperm reproduction: an introductory reportReview of Palaeobotany and Palynology 27 291
Dilcher, D. L. 1996 Copnferendias VI Congreso Latinoamericano De Botanica, Mar Del Plata, ArgentiaKew, UKThe Trustees of the Royal Botanical Garden
Dilcher, D. L. 2010 Plants in Mesozoic Time: Morphological Innovations, Phylogeny, EcosystemsBloomington, INIndiana University Press
Dilcher, D.L.Sun, G.Ji, QLi, H. 2007 An early infructescence Hyrcantha decussata (comb. nov.) from the Yixian Formation in northeastern ChinaProceedings of the National Academy of Sciences 104 9370
Doyle, J. A. 1992 Revised palynological correlations of the lower Potomac Group (USA) and the Cocobeach sequence of Gabon (Barremian-Aptian)Cretaceous Research 13 337
Doyle, J. A. 2005 Early evolution of angiosperm pollen as inferred from molecular and morphological phylogenetic analysesGrana 44 227
Doyle, J. A.Hickey, L. J. 1976 Origin and Early Evolution of AngiospermsNew York, NYColumbia University Press
Doyle, J. A.Robbins, E. I. 1977 Angiosperm pollen zonation of the continental Cretaceous of the Atlantic coastal plain and its application to deep wells in the Salisbury EmbaymentPalynology 1 43
Doyle, J. A.Biens, P.Doerenkamp, A.Jardine, S. 1977 Angiosperm pollen from the pre-Albian Lower Cretaceous of equatorial AfricaBulletin des Centres de Recherches Exploration–Production Elf–Aquitaine 1 451
Endress, P. K. 1990 Evolution of reproductive structures and functions in primitive angiosperms (Magnoliidae)Memoirs of the New York Botanical Garden 55 5
Endress, P. K. 1997 Evolution and Diversification of Land PlantsNew York, NYSpringer
Endress, P. K. 2010 The evolution of floral biology in basal angiospermsPhilosophical Transactions of the Royal Society London 365 411
Erdtman, G. 1966 Pollen Morphology and Plant TaxonomyNew York, NYHafner Publishing Company
Faegri, K.van der Pijl, L. 1979 The Principles of Pollination EcologyNew York, NYPergamon Press
Feild, T. S.Arens, N. C. 2005 Form, function and environments of the early angiosperms: merging extant phylogeny and ecophysiology with fossilsNew Phytologist 166 383
Fernandez, V. A.Galetto, L.Astegiano, J. 2009 Influence of flower functionality and pollination system on the pollen size–pistil length relationshipOrganisms Diversity and Evolution 9 75
Friedman, J.Barrett, S. C. H. 2008 A phylogenetic analysis of the evolution of wind pollination in the angiospermsInternational Journal of Plant Sciences 169 49
Friedman, J.Barrett, S. C. H. 2009 Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plantsAnnals of Botany 103 1515
Friis, E. M. 1985 Actinocalyx gen. nov., sympetalous angiosperm flowers from the Upper Cretaceous of southern SwedenReview of Palaeobotany and Palynology 45 171
Friis, E. M.Pedersen, K. R. 1996 Palynology: principles and applicationsCollege Station, TXTexas A&M University
Friis, E. M.Crane, P. R.Pedersen, K. R. 1988 Reproductive structures of Cretaceous PlatanaceaeBiologiska Skrifter K. Danske Videnskabernes Selskab 31 1
Friis, E. M.Pedersen, K. R.Crane, P. R. 1999 Early angiosperm diversification: the diversity of pollen associated with angiosperm reproductive structures in early Cretaceous floras from PortugalAnnals of the Missouri Botanical Garden 86 259
Friis, E. M.Pedersen, K. R.Crane, P. R. 2000 Fossil floral structures of a basal angiosperm with monocolpate, reticulate–acolumellate pollen from the Early Cretaceous of PortugalGrana 39 226
Friis, E. M.Pedersen, K. R.Crane, P. R. 2004 Araceae from the Early Cretaceous of Portugal: Evidence on the emergence of monocotyledonsProceedings of the National Academy of Sciences 101 16565
Friis, E. M.Pedersen, K. R.Crane, P. R. 2006 Cretaceous angiosperm flowers: Innovation and evolution in plant reproductionPalaeogeography, Palaeoclimatology, Palaeoecology 232 251
Furness, C. A.Rudall, P. J. 2004 Pollen aperture evolution: a crucial factor for eudicot success?Trends in Plant Sciences 9 1548
Grimaldi, D. 1999 The coradiations of pollinating insects and angiosperms in the CretaceousAnnals of the Missouri Botanical Garden 86 373
Grimaldi, D.Engel, M. S. 2005 Evolution of the InsectsCambridge, UKCambridge University Press
Halbritter, H.Svojtka, M. 2000
Harder, L. D. 1998 Pollen-size comparisons among animal-pollinated angiosperms with different pollination characteristicsBiological Journal of the Linnean Society 64 513
Heimhofer, U.Hochuli, P. A.Burla, S.Weissert, H. 2007 New records of Early Cretaceous angiosperm pollen from Portuguese coastal deposits: implications for the timing of the early angiosperm radiationReview of Palaeobotany and Palynology 144 39
Herendeen, P. S.Crane, P. R.Drinnan, A. N. 1995 Fagaceous flowers, fruits and cupules from the Campanian (Late Cretaceous) of central Georgia, USAInternational Journal of Plant Sciences 156 93
Hesse, M. 1979 Entwicklungsgeschichte und Ultrastruktur von Pollenkitt und Exine bei nahe verwandten entomophilen und anemophilen Sippen der Oleaceae, Scrophulariaceae, Plantaginaceae und AsteraceaePlant Systematic and Evolution 132 107
Hesse, M. 1979 Ultrastructure and distribution of pollenkitt in the insect- and wind-pollinated genus (Aceraceae)Plant Systematic and Evolution 131 277
Hesse, M. 1981 The fine structure of the exine in relation to the stickiness of angiosperm pollenReview of Palaeobotany and Palynology 35 81
Hesse, M. 1981 Pollenkitt and viscin threads: their role in cementing pollen grainsGrana 20 145
Hesse, M. 2001 Pollen characters of Amborella trichopoda (Amborellaceae): a reinvestigationInternational Journal of Plant Sciences 162 201
Hochuli, P. A.Heimhofer, U.Weissert, H. 2006 Timing of early angiosperm radiation: recalibrating the classical successionJournal of the Geological Society, London 163 587
Hu, S. 2006
Hu, S.Taylor, D. W. 2010
Hu, S.Dilcher, D. L.Jarzen, D. M.Taylor, D. W. 2008 Early steps of angiosperm-pollinator coevolutionProceedings of the National Academy of Sciences 105 240
Hughes, N. F. 1994 The Enigma of Angiosperm OriginCambridge, UKCambridge University Press
Ibrahim, M. I. A. 2002 New angiosperm pollen from the Upper Barremian–Aptian of the western desert, EgyptPalynology 26 107
Ji, Q.Li, H.Bowe, L. M.Liu, Y.Taylor, D. W. 2004 Early Cretaceous Archaefructus eoflora sp. nov. with bisexual flowers from Beipiao, Western Liaoning, ChinaActa Geologica Sinica 78 883
Judd, W. S.Campbell, C. S.Kellogg, E. A.Stevens, P. F.Donoghue, M. J. 2002 Plant Systematics, a Phylogenetic ApproachSunderland, MASinauer Associates, Inc
Labandeira, C. C. 1997 Insect mouthparts: ascertaining the paleobiology of insect feeding strategiesAnnual Review of Ecology, Evolution and Systematic 28 153
Labandeira, C. C. 2000
Labandeira, C. C. 2002 Plant–animal interactions: an evolutionary approachOxford, UKBlackwell Science
Lander, T. A.Harris, S. A.Boshier, D. H. 2009 Flower and fruit production and insect pollination of the endangered Chilean tree, Gomortega keule in native forest, exotic pine plantation and agricultural environmentsRevista Chilena de Historia Natural 82 403
Lazaro, A.Traveset, A. 2005 Spatio–temporal variation in the pollination mode of Buxus balearica (Buxaceae), an ambophilous and sefing species: mainland–island comparisonEcography 28 640
Linder, H. P. 1998 Reproductive BiologyKew, UKThe Royal Botanic Gardens
Linder, H. P. 2000 Pollen and Spores: Morphology and BiologyKew, UKThe Royal Botanic Gardens
Lonsdorf, E.Kremen, C.Ricketts, T. H.Winfree, R.Williams, N. M.Greenleaf, S. S. 2009 Modeling pollination services across agricultural landscapesAnnals of Botany 103 1589
Lupia, R.Herendeen, P. S.Keller, J. A. 2002 A new fossil flower and associated coprolites: evidence for angiosperm–insect interactions in the Santonian (Late Cretaceous) of Georgia, USAInternational Journal of Plant Science 163 675
Maddison, W. P.Maddison, D. R. 1992 MacClade: Analysis of Phylogeny and Character EvolutionSunderland, MASinauer Associates, Inc
Mcconchie, C. A.Knox, R. B.Ducker, S. C.Pettitt, J. M. 1982 Pollen wall structure and cytochemistry in the seagrass Amphibolis griffithii (Cymodoceaceae)Annals of Botany 50 729
Mitchell, R. J.Flanagan, R. J.Brown, B. J.Waser, N. M.Karron, J. D. 2009 New frontiers in competition for pollinationAnnals of Botany 103 1403
Pacini, E. 2000 From anther and pollen ripening to pollen presentationPlant Systematic and Evolution 222 19
Pacini, E.Hesse, M. 2005 Pollenkitt: its composition, forms and functionsFlora 200 399
Pedersen, K.R.Crane, P. R.Drinnan, A. N.Friis, E. M. 1991 Fruits from the mid Cretaceous of North America with pollen grains of the Clavatipollenites typeGrana 30 577
Poinar, G. O.Danforth, B. N. 2006 A fossil bee from Early Cretaceous Burmese amberScience 314 614
Proctor, M.Yeo, P.Lack, A. 1996 The Natural History of PollinationPortland, ORTimber Press
Proctor, M. C. F. 1978 The Pollination of Flowers by InsectsLondonSymposium Series Linnaean Society
Quattrocchio, M. E.Martınez, M. A.Pavisich, A. C.Volkheimer, W. 2006 Early Cretaceous palynostratigraphy, palynofacies and palaeoenvironments of well sections in northeastern Tierra del Fuego, ArgentinaCretaceous Research 27 584
Remizowa, M. V.Sokoloff, D. D.Macfarlane, T. D.Yadav, S. R.Prychid, C. J.Rudall, P. J. 2008 Comparative pollen morphology in the early-divergent angiosperm family Hydatellaceae reveals variation at the infraspecific levelGrana 47 81
Ren, D. 1998 Flower-associated Brachycera flies as fossil evidence for Jurassic angiosperm originsScience 280 85
Ren, D.Labandeira, C. C.Santiago-Blay, J. A.Rasitsyn, A.Shih, C.Bashuev, A.Logan, M. A. V.Hotton, C. L.Dilcher, D. 2009 A probable pollination mode before angiosperms: eurasian, long-proboscid scorpionfliesScience 326 840
Retallack, G.Dilcher, D. L. 1981 Paleobotany, Paleoecology and EvolutionNew York, NYPraeger
Roulston, T. H.Cane, J. H. 2000 Pollen nutritional content and digestibility for animalsPlant Systematic and Evolution 222 187
Rudall, P. J.Remizowa, M. V.Prenner, G.Prychid, C. J.Tuckett, R. E.Sokoloff, D. D. 2009 Non-flowers near the base of extant angiosperms? Spatio–temporal arrangement of organs in reproductive units of Hydatellaceae and its bearing on the origin of the flowerAmerican Journal of Botany 96 67
Sampson, F. B. 2000 Pollen diversity in some modern MagnoliidsInternational Journal of Plant Sciences 161 S193
Sannier, J.Baker, W. J.Anstett, M.-C.Nadot, S. 2009 A comparative analysis of pollinator type and pollen ornamentation in the Araceae and the Arecaceae, two unrelated families of the monocotsBMC Research Notes 2 145
Sargent, R. D.Otto, S. P. 2004 A phylogenetic analysis of pollination mode and the evolution of dichogamy in angiospermsEvolutionary Ecology Research 6 1183
Schrank, E.Mahmoud, M. S. 2002 Barremian angiosperm pollen and associated palynomorphs from the Dakhla oasis area, EgyptPalaeontology 45 33
Smets, E. 1986 Localization and systematic importance of the floral nectaries in the Magnoliatae (Dicotyledons)Bulletin du Jardin botanique national de Belgique 56 51
Soltis, P. S.Soltis, D. E. 2004 The origin and diversification of angiospermsAmerican Journal of Botany 91 1614
Stevens, P. F. 2001
Sun, G.Ji, Q.Dilcher, D. L.Zheng, S.Nixon, K. C.Wang, X. 2002 Archaefructaceae, a new basal angiosperm familyScience 296 899
Tanaka, N.Uehara, K.Murata, J. 2004 Correlation between pollen morphology and pollination mechanisms in the HydrocharitaceaeJournal of Plant Research 117 265
Taylor, D. W. 2010 Plants in Mesozoic Time: Morphological Innovations, Phylogeny, EcosystemsBloomington, INIndiana University Press
Taylor, D. W.Hickey, L. J. 1996 Flowering Plant Origin, Evolution and PhylogenyNew York, NYChapman & Hall
Taylor, D. W.Hu, S. 2010 Coevolution of early angiosperms and their pollinators: Evidence from pollenPalaeontographica, Abteilung B: Palaeobotany –Paleophytology 283 103
Theissen, G.Melzer, R. 2007 Molecular mechanisms underlying origin and diversification of the angiosperm flowerAnnals of Botany 100 603
Thien, L. B.Bernhardt, P.Devall, M. S.Chen, Z. D.Luo, Y. B.Fan, J. H.Yuan, L. C.Williams, J. H. 2009 Pollination biology of basal angiosperms (ANITA grade)American Journal of Botany 96 166
Traverse, A. 2007 PaleopalynologyDordrecht, NetherlandsSpringer
Watson, L.Dallwitz, M. J. 1992
Whitehead, D. R. 1969 Wind pollination in the angiosperms: evolutionary and environmental considerationsEvolution 23 28
Whitehead, D. R. 1983 Pollination BiologyOrlando, FLAcademic Press, Inc.
Wing, S. L.Boucher, L. D. 1998 Ecological aspects of the Cretaceous flowering plant radiationAnnual Review of Earth Planet Science 26 379
Zavada, M. S. 1984 Pollen wall development of Austrobaileya maculataBotanical Gazette 145 11
Zetter, R.Weber, M.Hess, M.Pingen, M. 2002 Pollen, pollenkitt, and orbicules in Craigia bronnii flower buds (Tilioideae, Malvaceae) from the Miocene of Hambach, GermanyInternational Journal of Plant Sciences 163 1067