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Anita Grade) 1 American Journal of Botany 96(1): 1–17. 2009. P OLLINATION BIOLOGY OF BASAL ANGIOSPERMS (ANITA GRADE) 1 Leonard B. Thien, 2,7 Peter Bernhardt, 3 Margaret S. Devall, 4 Zhi-duan Chen, 5 Yi-bo Luo, 5 Jian-Hua Fan, 5 Liang-Chen Yuan, 5 and Joseph H. Williams6 2 Cell and Molecular Biology Department, Tulane University, New Orleans, Louisiana 70118 USA; 3 Department of Biology, Saint Louis University, St. Louis, Missouri 63103 USA; 4 United States Department of Agriculture Forest Service, Center for Bottomland Hardwoods Research, P. O. Box 227, Stoneville, Mississippi 38776 USA; 5 State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, People ’ s Republic of China; and 6 Department of Ecology and Evolution, University of Tennessee, Knoxville, Tennessee 37996 USA The fi rst three branches of the angiosperm phylogenetic tree consist of eight families with ~201 species of plants (the ANITA grade). The oldest fl ower fossil for the group is dated to the Early Cretaceous (115 – 125 Mya) and identifi ed to the Nymphaeales. The fl owers of extant plants in the ANITA grade are small, and pollen is the edible reward (rarely nectar or starch bodies). Unlike many gymnosperms that secrete “ pollination drops, ” ANITA-grade members examined thus far have a dry-type stigma. Copious secretions of stigmatic fl uid are restricted to the Nymphaeales, but this is not nectar. Floral odors, fl oral thermogenesis (a re- source), and colored tepals attract insects in deceit-based pollination syndromes throughout the fi rst three branches of the phylo- genetic tree. Self-incompatibility and an extragynoecial compitum occur in some species in the Austrobaileyales. Flies are primary pollinators in six families (10 genera). Beetles are pollinators in fi ve families varying in importance as primary (exclusive) to secondary vectors of pollen. Bees are major pollinators only in the Nymphaeaceae. It is hypothesized that large fl owers in Nympha- eaceae are the result of the interaction of heat, fl oral odors, and colored tepals to trap insects to increase fi tness. Key words: ANITA grade; basal angiosperms; Coleoptera; Diptera; fl oral deceit; fl oral thermogenesis; Hymenoptera; polli- nation biology. “ Nature will tell you a direct lie if she can. ” — Attributed to laceae and Austrobaileyaceae) contain only a single species Charles Darwin ( Lewis and John, 1963, p. 271). ( Table 1 ). The oldest unequivocal fl oral fossil for the taxa, dated to the Molecular phylogeny now gives biologists the option of Early Cretaceous 115 – 125 Mya, is thought to be related to ex- comparing specifi c lineages of basal angiosperms rather than tant Nymphaeales ( Friis et al., 2001 ). The small fossil fl ower (3 relying on past dogma that insisted a plant was “ primitive ” be- mm long, 2 mm diameter) shrank during fossilization and was cause its fl owers possessed or lacked a particular character or estimated to be about 1 cm in diameter when alive ( Friis et al., suite of characters. 2001 ). Another fossil, Microvictoria (Nymphaeaceae) from the The fi rst three branches of the angiosperm phylogenetic tree, Raritan Formation dated to the Turonian (90 Mya), Upper Cre- constructed with DNA sequences (coding and noncoding), taceous, resembles modern water lilies in the Victoria - Euryale comprise the ANITA grade. This now includes the Hydatel- clade ( Gandolfo et al., 2004 ; Yoo et al., 2005 ). The precise fl o- laceae as the sister group of the Nymphaeales ( Qiu et al., 1999 , ral structure of the fossil fl ower is similar to modern day Victo- 2000 , 2006 ; Soltis et al., 1999 , 2000 ; Barkman et al., 2000 ; Gra- ria Lindley, suggesting entrapment of beetle pollinators, ham and Olmstead, 2000 ; Zanis et al., 2002 ; Borsch et al., 2003 ; indicating that specialized plant – insect associations in the an- Friis and Crane, 2007 ; Saarela et al., 2007 ) . Amborellaceae giosperms were already established at this time ( Gandolfo et forms the fi rst branch, Nymphaeales forms the second, and Aus- al., 2004 ). In a recent study, Ervik and Knudsen (2003) regard trobaileyales is the third and sister to all other fl owering plants pollination of members of the Nymphaeaceae by scarab beetles ( Table 1 ; Fig. 1 ). Therefore, the term “ basal angiosperm ” is to be an ancient mutualistic partnership dating back 100 Mya. used here to refer specifi cally to taxa within the ANITA grade. New data on wind, fl y, and bee pollination in ANITA-grade The ANITA grade, an amalgam of the lineage names, com- plants, however, suggest we reexamine the hypothesis that bee- prises eight families as follows: Amborellaceae, Hydatellaceae, tles pollinated early angiosperms in a “ mess and soil ” system Cabombaceae, Nymphaeaceae, Austrobaileyaceae, Trime- ( Faegri and van der Pijl, 1979 ). niaceae, Schisandraceae, and Illiciaceae ( Table 1 ). The 17 gen- It is also reasonable to hypothesize that specialized pollina- era with ~201 species of fl owering plants are distributed from tion systems between halictid bees, with a lineage extending tropical to cold regions of the world ( Table 1 ). Six of the fami- back 95 – 100 Mya ( Engel, 2001 ), and Nuphar -type fl owers is lies contain only one or two genera, and two families (Amborel- also an old association. These fi ndings suggest insect pollina- tion occurred very early in the fi rst angiosperms. Hu et al. (2008) maintain fossil pollen clumping is evidence for sticky 1 M anuscript received 14 January 2008; revision accepted 17 September pollen and evolved by the mid-Cretaceous, implying an in- 2008. This research was supported by the National Basic Research Program of crease in zoophilous pollination. China (973 program no. 2007CB411600). This paper presents an overview of reproductive systems, 7 A uthor for correspondence (e-mail: [email protected]) pollination syndromes, and new data were added on fl oral thermo- genesis of ANITA grade plants ( Tables 1 – 3 ). The literature was doi:10.3732/ajb.0800016 searched, and a diagram was constructed to show evolutionary 1 2 American Journal of Botany [Vol. 96 Table 1. Reproductive traits of ANITA-grade plants. Taxa No. species Flower size Flower color Sex S/I Reference First branch terrestrial Amborellaceae Amborella 1 3 – 5 mm Cream Unisexual, dioecious Thien et al., 2003 Second branch aquatic Hydatellaceae 7 Hydatella 4 2 – 4 mm Unisexual Saarela et al., 2007 Trithuria 3 2 – 4 mm Unisexual, bisexual Friis and Crane, 2007 Cabombaceae Cabomba 5 2.5 cm White, pink Bisexual, protogynous Schneider and Jeter, 1982 Brasenia 1 2.0 cm Dull purple Bisexual, protogynous Cronquist, 1981 Nymphaeaceae Nuphar 20 2.5 cm Yellow Bisexual, protogynous Lippok and Renner, 1997; Herring, 2003 Barclaya 4 3.0 cm Purplish Bisexual, protogynous Cronquist, 1981 Ondinea 1 3.5 cm Purple-red Bisexual, protogynous Schneider, 1983 Victoria 2 > 50 cm Red-white Bisexual, protogynous Prance and Arias, 1975 Euryale 1 1 – 2.5 cm Blue, violet Bisexual, protogynous Okada, 1930 Nymphaea 50 > 15 cm Blue, white, yellow, red Bisexual, protogynous Meeuse and Schneider, 1979/1980 Third branch terrestrial Austrobaileyaceae Austrobaileya 1 5 cm Red, brown, green Bisexual, protogynous S/I Endress, 1980, 2001 Trimeniaceae Piptocalyx 12 1 – 2 cm White Unisexual, bisexual Endress and Sampson, 1983; Philipson, 1993; Endress 1994 Trimenia 1 1 – 2 cm White Unisexual, bisexual S/I Endress and Sampson, 1983; Endress, 1994; Bernhardt et al., 2003 Schisandraceae Schisandra 25 1 – 2 cm Red, yellow Unisexual, dioecious Saunders, 2000 Kadsura 22 1 – 2 cm Red, yellow Unisexual, monoecious, S/I Saunders, 1998; Lyew et al., 2007 dioecious Illiciaceae Illicium 41 1 – 3 cm Red, white Bisexual, protogynous Smith, 1947; Thien et al., 1983 Notes: S/I = self incompatibility. trends in the fi rst three branches of the angiosperm phyloge- The fi rst topic, fl oral deceit and pollination, examines the netic tree ( Fig. 1 ). Pollen is the primary food resource for role of fl oral resources and the signifi cance of dry and wet stig- visiting insects in the majority of plants (nectar is rare). The dry mas, fl oral heat, and other factors in the types of fl oral deceit in stigmas provide no food (droplets) in the woody plants (fi rst aquatic vs. woody plants. The second topic, fl oral thermogene- and third branches, Tables 1, 3 ; Fig. 1 ). The wet stigmas (sec- sis, examines the roles of fl oral heat in the breeding systems of ond branch, Nymphaeaceae) secrete copious amounts of fl uid large (water lilies) and small fl owers ( Illicium and Kadsura ). A that is not eaten by visiting insects (not a nectar). Floral deceit hypothesis is proposed to explain the large fl owers in many is common throughout all three lineages and is based on various members of the Nymphaeaceae. The role of the extragynoecial fl oral traits, e.g., bright-colored fl owers, fl oral odor, fl oral heat, compitum is also explained in this section. The third topic, pol- host site for egg ovipositing ( Fig. 1 ). linators, is an analysis of the various insect pollinators empha- Most of the plants in the ANITA grade have apocarpous sizing fl ies, beetles, and bees. Generalist vs. specialist modes of fl owers or if syncarpous lack a compitum. In syncarpy (united pollination in the ANITA-grade taxa are presented along with carpels), species of fl owering plants typically have a compitum, switching of pollinators in species of Nuphar . In addition, bee- a zone of tissue in which pollen tubes have the potential to gain tle and bee pollination systems in the ANITA-grade plants are entry to several carpels ( Carr and Carr, 1961 ; Endress, 1994 ; compared with pollination systems in higher taxa. The discus- Sheffi eld et al., 2005 ). In apocarpy (separate carpels), pollen sion presents a broad overview of the pollination and reproduc- tubes are restricted to a single carpel.
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