(2007) - the ecophysiology of early angiosperms

The ecophysiology of early angiosperms TAYLOR S. FEILD 1 & NAN CRYSTAL ARENS 2 1 Department of Ecology and Evolution, University of Tenness ee, Knoxville , TN, USA and 2 Department of Geosciences, Hobart and William Smith Colleges, Geneva, NY, USA ABSTRACT Angiosperms first appeared during the Early Cretaceous, and within 30 million years they reigned over many floras wo rld wi de . Associ at ed wi th this ri se to prominence, angiosperms produced a spectrum of reproductive and veg- etative innovations, which produced a cascade of ecological consequences that altered the ecology and biogeochemistry of the planet. The pace, pat tern and phylogenetic systemat- ics of the Cretaceous angiosperm diversification are broadly sketched out. Howev er, the ecophy siolog y and envir on- menta l interactions that energized the early angiosperm radiat ion remai n unres olved . This constr ains our abilit y to diagnose the select ive pressures and habita t conte xts responsible for the evolution of fundamental angiosperm features, such as flowers, rapid growth, xylem vessels and net-veined leaves, which in association with environmental opportunities, drove waves of phylogenetic and ecological diversification. Here, we consider our current understand- ing of earl y angi osp erm ecophysi ol ogy . We focus on comparative patterns of ecophysiological evolution, empha- siz ing car bon- and wat er -us e tra its , by mer gin g recent molecular phylogenetic studies with physiological studies focused on e xtant basal angio sperms. In doing so, we discuss how earl y angiosp erms est abl ishe d a root hol d in pre - existing Mesozoic plant communities, and how these events canalized subsequent bursts of angiosperm diversification during the Aptian–Albian. Key-words: Amborella; angiosperm diversification; aquatic origin; Chloranthaceae; ecological stasis; xylem vessels. INTRODUCTION The flowering plants, or angiosperms, are the most species- dense and ecologically diverse branch on the green plant tree of life (Soltis et al . 2005). In addition to impressive diversity (~ 250 000 species), angiosperms have evolved an unpar allel ed bread th of ecophysiological perfo rmanc e, underpinned by high-capacity and flexible metabolisms and extreme structural diversity (Bond 1989; Sperry 2003). In metabolic perfo rmanc e, angiosper ms range from deep- shade rain forest herbs growing at the limits of land pl ant autotr ophy to sun- lovi ng weeds boundi ng the ot her extreme wi th the hi ghest CO2 assimi latio n, O2 evolut ion and water los s rates kno wn. Ass oci ated wit h broad metabolic performance, angiosperms exhibit corre- spond ing diver se whol e-plan t vascular plumbi ng design s and ecomorphological variation. Beyond impressive diversity, angiosperms are the modern vegetational dominants. Angiosperm ecophysiologies dictate present-day terrestrial water, nutrient and carbon cycles, as well as feedback on community disturbance and regeneration dynamics (Knoll & J ames 1987; V olk 1989; Ber ner & Ko tha val a 200 1). Finally, angiosperm ecophysiological and structural diver- sit y is fou ndational in the genera tion and mai nte nance of terrestrial biodiversity by providing diverse resources for polli nator s, dispers ers and herbi vores (F arrell 1998; Grimaldi 1999). Angio sperm diversity and ecolog ical domin ance , how- ever , arose relatively recent ly. Unlik e other major land plant lineage s (i.e . ‘bryo phyte s’, lycoph ytes , ferns and other see d plants ), which extend into the Pal eoz oic, the first unequivocal angiosperm fossils appear nearly 100 Ma later in low paleolatitudes of southern Laurasia and northern Gondwana (~ 135 Ma; Knoll , 1986; Crane, Fr iis & Peder sen 1995; Brenner 1996; Lupia, L idgard & Crane 1999). Within ~ 15 Ma, angiosperms radiated into a riot of u nprecedented variation in foliar, reproductive and pollen morphological diver sity (Hicke y & Doyle 1977; Upchur ch 1984; Lidga rd & Crane 1990; Fri is , Peder sen & Cra ne 1999, 2000; Lupia et al . 1999; Crepe t, Nixon & Gan dolfo 2004; Hochul i, Heimh ofer & Weissert 2006). The interpretation of these fossils and molecular clock analyses of divergence times within the clade demonstrate that most of the major angiosperm lin- eages appeared during a relatively short (10–15 Ma) geo- logica l wind ow (Cra ne et al . 1995; Friis et al . 1999, 2000; Bremer 2000; Magallón & Sanderson 2001, 2005; Crepet et al . 2004; Davies et al . 2004; Bell, Soltis & Soltis 2005). Angiosperm diversification produced a cascade of conse- quence s for Meso zoic plant commun ities . Angiospe rms adv anc ed to the pol es of bot h hemisp her es and began dominating a few low-latitude communities by the Aptian times (~ 112 Ma; Romero & Arc hangel sky 1986; Wing , Hickey & Swisher 1993; Lupia et al . 1999; Hochuli et al . 2006). Alth ough they accounte d for by far the largest pro- por tion of spe cie s, ang ios per ms did not domina te the maj or - ity of ecosystems, even in the Latest Cretaceous (Wing et al . 199 3). How eve r, by the Late Cre tac eous, many pla nt commu nities were transitioning into angios perm- reple te one s as fer ns , lyc oph yte s and other see d pla nt lin eag es declin ed in abundance. Several ancient groups such as the Correspondence: T aylor S. Feild. E-mail: [email protected] Plant, Cell and Environment (2007) 30 , 291–309 doi: 10.1 1 1 1/j.1365-3040.2006.01625.x © 2007 The Authors Journal compilation © 2007 Blackwell Publishing Ltd 291

(2007) - the ecophysiology of early angiosperms

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