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.
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References
Ananthakrishnan TN (1984) Bioecology of thrips. Indira Publishing House, Michigan
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
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
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
Baker JD, Cruden RW (1991) Thrips-mediated self-pollination of two facultatively xenogamous wetland species. Am J Bot 78:959–963
Barrett SCH (2002) The evolution of plant sexual diversity. Nat Rev Genetics 3:274–284
Bawa KS (1990) Plant–pollinator interactions in tropical rainforest. Ann Rev Ecol Syst 21:399–399
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)
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
Dafni A (1992) Pollination ecology--a practical approach. Oxford university press, London
Darwin C (1876) The effects of cross and self-fertilisation in the vegetable kingdom. Murray, London
Darwin C (1877) The different forms of flowers on plants of the same species. Murray, London
De Jong PC (1976) Flowering and sex expression in Acer L.—a biosystematic study. Mededelingen landbouwhogeschool Wageningen, Nederland, pp 76–82
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
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
Dufaÿ M, Anstett MC (2003) Conflicts between plants and pollinators that reproduce within inflorescences: evolutionary variations on a theme. Oikos 100:3–14
Erbar C, Langlotz M, Leins P (2001) Die Griffel der Bach-Nelkenwurz Geum rivale L. (Rosaceae)--Hakenbildung und Pollenschlauchkonkurrenz. Wulfenia 8:95–109
Free JB (1970) Insect pollination of crops. Academic press, Dublin
Geber MA, Dawson TE, Delph LF (1999) Gender and sexual dimorphism in flowering plants. Springer, Berlin
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
Gross C (2005) Pollination efficiency and pollinator effectiveness. In: Dafni A, Kevan PG, Husband BC (eds) Practical pollination biology. Enviroquest, Cambridge, pp 354–363
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
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
Howe HF, Westley LC (1997) Ecology of pollination and seed dispersal. In: Crawley MJ (ed) Plant ecology. Blackwell, Oxford, pp 262–283
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
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
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
Lloyd DG, Bawa KS (1984) Modification of the gender of seed plants in varying conditions. Evol Biol 17:255–338
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
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
Müller H (1873) Die Befruchtung der Blumen durch Insekten. Leipzig
Müller H (1875) Flowering of the Hazel. Nature 12:26
Ogata K (1967) A systematic study of the genus Acer. Bull Tokyo Univ For 63:89–206
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
Pohl F (1937) Die Pollenerzeugung der Windblütler. Beihefte zum botanischen Centralblatt 56:365–470
Primack RB (1980) Variation in the phenology of natural populations of montane shrubs in New Zealand. J Ecol 68:849–862
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
Rempe H (1938) Untersuchungen über die Verbreitung des Blütenstaubes durch die Luftströmungen. Planta 27:93–147
Renner S (2001) How common is heterodichogamy? Trends Ecol Evol 16:595–597
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
Sakai S (2002) A review of brood-site pollination mutualism: plants providing breeding site for their pollinators. J Plant Res 115:161–168
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
Scholz E (1960) Blütenmorphologische und-biologische Untersuchungen bei Acer pseudoplatanus L. und Acer platanoides L. Der Züchter 30:11–16
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
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
Verdú M, Gleiser G (2006) Adaptive evolution of reproductive and vegetative traits driven by breeding systems. New Phytologist 169:409–417
Vogel S (1978) Pilzmückenblumen als Pilzmimeten. Flora 167:329–398
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
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
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
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
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
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.
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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
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DOI: https://doi.org/10.1007/s00606-008-0141-9