Skip to main content
Log in

Acer pseudoplatanus (Sapindaceae): Heterodichogamy and thrips pollination

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

Abstract

One of the pathways to dioecy is via heterodichogamy, a system including protandrous (flowering male first) and protogynous (female first) plants. Using a research crane the reproductive ecology of the heterodichogamous Acer pseudoplatanus was studied in 74 mature trees over 2 years. The synchronized flowering phenology of the trees resulted in reciprocal pollination between the two morphs. Protandrous trees were more numerous (3:1), had more female flowers (2–3:1), had much less pollen on their stigmas (1:15) and had a much lower seed to fruit ratio (1:3–4). The pollinators were probably breeding thrips. The heterodichogamy of A. pseudoplatanus is confirmed and underlined as a functioning ecological system. Depending on the way pollination efficiency changes in time, either of the morphs can be interpreted as “more female” or “more male”. The evolution of heterodichogamy towards dioecy thus depends on more components of the reproductive ecology than have been assumed.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Ananthakrishnan TN (1984) Bioecology of thrips. Indira Publishing House, Michigan

    Google Scholar 

  • Ananthakrishnan TN, Gopinathan K (1998) Nectar utilization and pollination potential of thrips in relation to some Asteraceae. In: Bir B (ed) Nectary biology: structure, function and utilization. Dattsons, Nagpur, pp 163–177

    Google Scholar 

  • Andersen ST (1974) Wind conditions and pollen deposition in a mixed deciduous forest. II. Seasonal and annual pollen deposition 1967–1972. Grana 14:64–77

    Google Scholar 

  • Ashton PS, Givnish TJ, Appanah S (1988) Staggered flowering in the Dipterocarpaceae: new insights into floral induction and the evolution of mast fruiting in the aseasonal tropics. Am Nat 132:44–66

    Article  Google Scholar 

  • Baker JD, Cruden RW (1991) Thrips-mediated self-pollination of two facultatively xenogamous wetland species. Am J Bot 78:959–963

    Article  Google Scholar 

  • Barrett SCH (2002) The evolution of plant sexual diversity. Nat Rev Genetics 3:274–284

    Article  CAS  Google Scholar 

  • Bawa KS (1990) Plant–pollinator interactions in tropical rainforest. Ann Rev Ecol Syst 21:399–399

    Article  Google Scholar 

  • Binggeli, P. 1992. Patterns of invasion of sycamore (Acer pseudoplatanus L.) in relation to species and ecosystem attributes. Ph.D thesis, Ulster. In http://members.lycos.co.uk/woodyplantecology/sycamore. April 2006

  • Buchenau F (1861) Morphologische Bemerkungen über einige Aceraceen. Botanische Zeitung 19:265–286 (three parts)

    Google Scholar 

  • Cornara L, Borghesi B, Caporali E, Casazza G, Roccotiello E, Troiano G, Minuto L (2005) Floral features and reproductive biology in Thymelaea hirsuta (L.) Endl. Plant Syst Evol 250:157–172

    Article  Google Scholar 

  • Dafni A (1992) Pollination ecology--a practical approach. Oxford university press, London

    Google Scholar 

  • Darwin C (1876) The effects of cross and self-fertilisation in the vegetable kingdom. Murray, London

    Google Scholar 

  • Darwin C (1877) The different forms of flowers on plants of the same species. Murray, London

    Google Scholar 

  • De Jong PC (1976) Flowering and sex expression in Acer L.—a biosystematic study. Mededelingen landbouwhogeschool Wageningen, Nederland, pp 76–82

    Google Scholar 

  • De Jong PC (1994) Taxonomy and reproductive biology of maples. In: van Gelderen DM, de Jong PC, Oterdoom HJ (eds) Maples of the world. Timber Press, Cambridge, pp 69–104

    Google Scholar 

  • Dommée B, Bompar JL, Denelle N (1990) Sexual tetramorphism in Thymelaea hirsuta (Thymelaeaceae): evidence of the pathway from heterodichogamy to dioecy at the interspecific level. Am J Bot 77:1449–1462

    Article  Google Scholar 

  • Dufaÿ M, Anstett MC (2003) Conflicts between plants and pollinators that reproduce within inflorescences: evolutionary variations on a theme. Oikos 100:3–14

    Article  Google Scholar 

  • Erbar C, Langlotz M, Leins P (2001) Die Griffel der Bach-Nelkenwurz Geum rivale L. (Rosaceae)--Hakenbildung und Pollenschlauchkonkurrenz. Wulfenia 8:95–109

    Google Scholar 

  • Free JB (1970) Insect pollination of crops. Academic press, Dublin

    Google Scholar 

  • Geber MA, Dawson TE, Delph LF (1999) Gender and sexual dimorphism in flowering plants. Springer, Berlin

    Google Scholar 

  • Gleiser G, Verdú M, Pannell JR (2007) Time-dependent gender specialization and the maintenance of males with protandrous and protogynous hermaphrodites in Acer opalus. Evolution

  • Gottsberger G (1999) Pollination and evolution in neotropical Annonaceae. Plant Species Biol 14:143–152

    Article  Google Scholar 

  • Gross C (2005) Pollination efficiency and pollinator effectiveness. In: Dafni A, Kevan PG, Husband BC (eds) Practical pollination biology. Enviroquest, Cambridge, pp 354–363

    Google Scholar 

  • Grube S (1988) Blütenentwicklung und -biologie der drei einheimischen Ahornarten Acer campestre L., Acer platanoides L. und Acer pseudoplatanus L. Diplomarbeit Heidelberg

  • Haas TP (1933) Untersuchungen an der Gattung Acer. Dissertation München

  • Hesse M (1979) Ultrastruktur und Verteilung des Pollenkitts in der insekten- und windblütigen Gattung Acer (Aceraceae). Plant Syst Evol 131:277–289

    Article  Google Scholar 

  • Hong TD, Ellis RH (1990) A comparison of maturation drying, germination, and desiccation tolerance between developing seeds of Acer pseudoplatanus L. and Acer platanoides L. New Phytologist 116:589–596

    Article  Google Scholar 

  • Howe HF, Westley LC (1997) Ecology of pollination and seed dispersal. In: Crawley MJ (ed) Plant ecology. Blackwell, Oxford, pp 262–283

    Google Scholar 

  • Hyde HA (1950) Studies in atmospheric pollen. IV. Pollen deposition in Great Britain, 1943. Part II. The composition of the pollen catch. New Phytol 49:407–420

    Article  Google Scholar 

  • Kirk WDJ (1996) Thrips. Naturalist’s handbooks 25 Richmond Slough

  • Kirk WDJ (1997) Feeding. In: Lewis T (ed) Thrips as crop pests. CAB International, Walling ford, pp 119–174

    Google Scholar 

  • Knuth P (1898) Handbuch der Blütenbiologie, II Band, I Teil. Leipzig

  • Lloyd DG (1980) Sexual strategies in plants III. A quantitative method for describing the gender of plants. N Z J Bot 18:103–108

    Google Scholar 

  • Lloyd DG, Bawa KS (1984) Modification of the gender of seed plants in varying conditions. Evol Biol 17:255–338

    Google Scholar 

  • Moog U, Fiala B, Federle W, Maschwitz U (2002) Thrips pollination of the dioecious ant plant Macaranga hullettii (Euphorbiaceae) in southeast Asia. Am J Bot 89:50–59

    Article  Google Scholar 

  • Morawetz W, Horchler P (2003) Leipzig canopy crane project (LAK), Germany. In: Basset Y, Horlyck V, Wright SJ (eds) Studying forest canopies from above: the international canopy crane network. Smithsonian tropical research institute and UNEP, pp 79–85

  • Mound L, Terry I (2001) Thrips pollination of the central Australian cycad, Macrozamia macdonnellii (Cycadales). Int J Plant Sci 162:147–154

    Article  Google Scholar 

  • Müller H (1873) Die Befruchtung der Blumen durch Insekten. Leipzig

  • Müller H (1875) Flowering of the Hazel. Nature 12:26

    Article  Google Scholar 

  • Ogata K (1967) A systematic study of the genus Acer. Bull Tokyo Univ For 63:89–206

    Google Scholar 

  • Pendleton RL, Freeman DC, McArthur ED, Sanderson SC (2000) Gender specialization in heterodichogamous Grayia brandegei (Chenopodiaceae): evidence for an alternative pathway to dioecy. Am J Bot 87:508–516

    Article  PubMed  Google Scholar 

  • Pohl F (1937) Die Pollenerzeugung der Windblütler. Beihefte zum botanischen Centralblatt 56:365–470

    Google Scholar 

  • Primack RB (1980) Variation in the phenology of natural populations of montane shrubs in New Zealand. J Ecol 68:849–862

    Article  Google Scholar 

  • Proctor M, Yeo P, Lack A (1996) The natural history of pollination, Timber press, Cambridge

  • Proctor MCF (1978) Insect pollination syndromes in an evolutionary and ecosystematic context. In: Richards AJ (ed) The pollination of flowers by insects. Academic press, London, pp 105–116

    Google Scholar 

  • Rempe H (1938) Untersuchungen über die Verbreitung des Blütenstaubes durch die Luftströmungen. Planta 27:93–147

    Article  Google Scholar 

  • Renner S (2001) How common is heterodichogamy? Trends Ecol Evol 16:595–597

    Article  Google Scholar 

  • Renner SS, Beenken L, Grimm GW, Kocyan A, Ricklefs RE (2007) The evolution of dioecy, heterodichgamy, and labile sex expression in Acer. Evolution 61:2701–2719

    Article  PubMed  CAS  Google Scholar 

  • Sakai S (2002) A review of brood-site pollination mutualism: plants providing breeding site for their pollinators. J Plant Res 115:161–168

    Article  PubMed  Google Scholar 

  • Sakai S, Kato M, Nagamasu H (2000) Artocarpus (Moraceae)--gall midge pollination mutualism mediated by a male-flower parasitic fungus. Am J Bot 87:440–445

    Article  PubMed  Google Scholar 

  • Scholz E (1960) Blütenmorphologische und-biologische Untersuchungen bei Acer pseudoplatanus L. und Acer platanoides L. Der Züchter 30:11–16

    Article  Google Scholar 

  • Seele C (2004) Die Hartholzgesellschaft im Plot des Leipziger Auwaldkrans--Analyse der Bestandsstruktur auf Gemeinschafts- und Artebene. Projektarbeit Leipzig

  • Semm A (1966) Blühen, Früchten und Keimen in der Gattung Acer. Dissertation, München

  • Stout AB (1928) Dichogamy in flowering plants. Bull Torrey Bot Club 55:141–153

    Article  Google Scholar 

  • Tal, O. 2006. Comparative flowering ecology of Fraxinus excelsior, Acer platanoides, Acer pseudoplatanus and Tilia cordata in the canopy of Leipzig’s floodplain forest. Dissertation, Leipzig. Available at http://dol.dl.uni-leipzig.de/receive/DOLDissHabil_disshab_00001013

  • Teulon DAJ, Leskey TC, Cameron EA (1998) Pear thrips Taeniothrips inconsequens (Thysanoptera: Thripidae) life history and population dynamics in sugar maples in Pennsylvania. Bull Entomol Res 88:83–92

    Article  Google Scholar 

  • Verdú M, Gleiser G (2006) Adaptive evolution of reproductive and vegetative traits driven by breeding systems. New Phytologist 169:409–417

    Article  PubMed  Google Scholar 

  • Vogel S (1978) Pilzmückenblumen als Pilzmimeten. Flora 167:329–398

    Google Scholar 

  • Wallander, E (2001) Evolution of wind-pollination in Fraxinus (Oleaceae): an ecophylogenetic approach. P.hD thesis, Göteborg, Sweden

  • Warmke HE (1951) Studies on pollination of Hevea brasiliensis in Puerto Rico. Science 113:646–648

    Article  PubMed  CAS  Google Scholar 

  • Waser NM, Ollerton J (2006) Plant-pollinator interactions: from specialization to generalization, University of Chicago Press, Chicago

  • Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060

    Article  Google Scholar 

  • Webb CJ (1999) Empirical studies: evolution and maintenance of dimorphic breeding systems. In: Geber MA, Dawson TE, Delph LF (eds) Gender and sexual dimorphism in flowering plants. Springer, Berlin, pp 61–69

    Google Scholar 

  • Webber AC, Gottsberger G (1995) Floral biology and pollination of Bocageopsis multiflora and Oxandra euneura in Central Amazonia, with remarks on the evolution of stamens in Annonaceae. Feddes repertorium 106:515–524

    Google Scholar 

  • Weiser F (1973) Beitrag zur Klärung blütenbiologischer Fragen bei Acer pseudoplatanus L. In: Benčať F (ed) International symposium on biology of woody plants. Bratislava, pp 83–86

Download references

Acknowledgment

The author thanks the late Prof. Wilfried Morawetz for his support and kindness, and dedicates this paper to his memory. He further thanks Amots Dafni, Susanne Renner and Avi Shmida for their advice and discussion, Claudia Erbar, Peter Leins and Monika Langlotz for instruction, Martin Unterseher for crane time coordination, Peggy Seltmann for assistance searching literature, and the Minerva foundation for financial support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ophir Tal.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tal, O. Acer pseudoplatanus (Sapindaceae): Heterodichogamy and thrips pollination. Plant Syst Evol 278, 211–221 (2009). https://doi.org/10.1007/s00606-008-0141-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-008-0141-9

Keywords

Navigation