Before the debut of angiosperms, a diverse assemblage of seed plants (Bennettitales, cycads, numerous conifers and the enigmatic group Czekanowskiales) and ferns filledterrestrial communities (Rees, Ziegler & Valdes 2000). Thus, it is clear that angiosperms did not begin their rise by simply shifting into the ecological space emptied out by a mass extinction event – a ‘victors by default’ process (Lupia et al. 1999). Instead, we know that the processes determining the ways in which fundamental resources were processed by light-, water- and carbon-use mechanisms played important roles in enabling angiosperms to intercalate themselves into intact communities and radiate. We are left with three key questions. What functional features contributed to angiosperms' initial invasiveness? What role did the environment play? And how did early evolutionary events canalize later directions of functional innovation?
A major hypothesis to account for the rise of angiosperm dominance is the competitive superiority hypothesis. This hypothesis views the earliest angiosperms as highly competitive, functioning with well-honed ecophysiological performances and therefore growing much faster, cheaper and therefore better than co-occurring Cretaceous gymnosperms and ferns (Stebbins 1965, 1974; Hickey & Doyle 1977, Doyle & Donoghue 1986; Bond 1989). Suggested key ecophysiological enablers of early angiosperm invasion include innovations in leaves and wood, such as xylem vessels and reticulate-veined leaves with freely ending veinlets and herbaceousness – all traits appearing with the origin of the clade and predicted to immediately imbue the clade with high opportunistic performance and rapid speciation potential (Stebbins 1974; Doyle & Donoghue 1986, 1993; Bond 1989; Taylor & Hickey 1996). Previous whole-plant images of early angiosperms cultivated this concept. Early angiosperms were imaged as ruderal, drought-tolerant and sun-loving shrubs (Stebbins 1974), aquatic herbs (Burger 1981; Sun et al. 2002; Ji et al. 2004) and high-light-tolerant floodplain/riparian herbs or shrubs with high photosynthetic and transpiration rates (Hickey & Doyle 1977; Taylor & Hickey 1996). These views motivated numerous studies aimed at discovering the floral and vegetative ‘key innovations’– intrinsic organismic traits catalysing ecological, morphological and/or species diversification – of early angiosperm success (Stebbins 1974, 1981; Carlquist 1975; Burger 1981; Doyle & Donoghue 1986, 1993; Friedman 1998; Gorelick 2001).
However, the notion that angiosperms sprinted out of the evolutionary blocks propelled by functionally superior traits is due for reconsideration (Sanderson & Donoghue 1994; Magallón & Sanderson 2001). Firstly, the bulk of angiosperm diversity (represented by orchids, grasses, rosiids and asterids; Stebbins 1974, 1981) did not arise near the base of the angiosperm tree. Instead, basal angiosperm lineages are relatively species poor (Magallón & Sanderson 2001). Secondly, many of the oft-mentioned angiosperm innovations, such as simple pitted xylem vessels, flowers, out-crossing mechanisms, insect associations and double fertilization, assembled within angiosperm lineages that have low diversity today (Carlquist & Schneider 2002a; Williams & Friedman 2002; Friedman & Williams 2004; Bateman et al. 2006; Friedman 2006). Thirdly, many of the so-called innovations themselves appear to have evolved through a series of intermediates with modest functional capabilities (e.g. vessels; Hacke et al. 2006). While many angiosperm stem lineages have been lost to extinction (Friis et al. 2000, Friis, Pedersen & Crane 2001), it seems clear that the overwhelming modern diversity of angiosperms cannot be explained by the evolution of a single character or even a discrete complex of characters acquired at the origin of the clade (Magallón & Sanderson 2001).
Moreover, an exclusive focus on the origin of key innovations obscures the co-ordinate role of environment – the key opportunity – under which new traits found utility and were refined by natural selection (de Queiroz 2002; Donoghue 2005). We suggest that the damp, dark and disturbed ancestral habitat of angiosperms allowed the origin and refinement of ecophysiological traits – such as vessels and broad, net-veined leaves – that permitted the new lineage to gain a roothold in the Mesozoic understorey (Boyce 2005; Feild & Arens 2005). These traits were later co-opted or modified as the lineage broke out into more demanding environments and began its meteoric rise (Lupia et al. 1999) to vegetation dominance.
Ecophysiology of the initial roothold
By analogy with modern basal angiosperms, early vessels were relatively small in diameter for a given length, present in low density and probably retained pit membrane remnants (Carlquist & Schneider 2002a; Hacke et al. 2006). Consistent with their anatomy, these early vessels probably did not confer a major advantage in hydraulic capacity to their bearers (Hacke et al. 2006). In fact, one might argue that early vessels were initially disadvantageous to the plants that produced them because of an increased risk of drought embolism. However, improved hydraulic capacity to support high transpiration and greater drought resilience were not necessary for success in the damp, shady understorey. Here, high humidity and wet soils minimized transpirational demand and enabled high leaf water potentials – conditions that lower the risk of embolism. Frequent and reliable root pressure generation in the wet understorey also ensured that hydraulic embolism, when it occurred, did not last long (Feild et al. 2005). Instead, vessels may have offered relatively similar hydraulic capacity as tracheids but with lower carbon investment, an advantage in a light-limited habitat and where frequent disturbance by understorey foragers damaged or destroyed shoots (Feild 2005).
Similarly, the ancestral leaf of angiosperms – broad and net-veined, with large stomata, complex subsidiary cell network, low photosynthetic rates per unit area and high optical efficiency (via uniform ‘spongy’ mesophyll cells and an internally reflective lower epidermis) – offers little functional advantage outside heavily shaded and humid microsites (DeLucia et al. 1991, 1996; Smith et al. 1997). Yet under the canopy, where light is a limiting resource, leaves that function in these ways are advantageous in carbon-use efficiency. Thus, the competitive advantages conferred by early vessels and shade-adapted leaves were not of globally superior function or drivers of rapid speciation, but more modest accommodation to the rigours of a specific ancestral habitat – the damp, Mesozoic forest understorey. What habitats did early angiosperm shift to next, and how did an ancestral ecophysiology as wet- and shade-adapted canalize these shifts?
Early breakout habitats and ecophysiologies
Angiosperms explored sunny, aquatic zones early in their evolution (Feild et al. 2004). Beyond the all-aquatic basal lineages Nymphaeales and Hydatellaceae, other early aquatic experiments include several basal monocots (Acorus, Alismatales; Les & Schneider 1995), basal eudicot lineages (i.e. Nelumbo, some Ranunculus species) and the phylogenetic vagabond lineage Ceratophyllum (see Soltis et al. 2005). Traits that evolved in the damp, shady understorey seem to have primed early angiosperms for aquatic exploration. For example, root pressure and hydathodes present in the common ancestor of extant angiosperms (Feild et al. 2003a) could by co-opted for the long-distance transport of ions and water for submersed ‘transpiration’ (Sculthorpe 1967; Pedersen & Sand-Jensen 1997). Early angiosperms also exploited the open water by losing the vascular cambium and up-regulating leaf photosynthesis via large increases in leaf thickness (i.e. multiple-palisade layers), increases in stomatal densities and loss of stomatal control of leaf gas exchange (Brewer & Smith 1995; Feild et al. 2004). However, aquatic shifts and the suite of physiological modifications wrapped around them did not set the stage for later diversification on land (see further discussion).
To break into brighter and more evaporative terrestrial habitats, several ecophysiological modifications to whole-plant function are involved as lineages transitioned from light-limited to more water-limited environments. In addition to metabolic up-regulation and allocation, leaves must evolve palisade mesophyll and amphistomy to process collimated light and increase photosynthetic rate per unit area to take advantage of greater sunlight (Smith et al. 1997). Furthermore, evolution of smaller stomata, finer guard cell regulation and better control of gas exchange across the leaf may increase water-use efficiency (Sack et al. 2003). Changes in leaf gas exchange function were probably coupled with increased density and regularization of the leaf vein network, and perhaps the evolution of xylem vessels in the venation to minimize pressure drops within the leaf under high transpiration (Zwieniecki et al. 2002; Sack et al. 2003; Arens 2006).
Modifications to secondary xylem vessels in the wood were also probably associated with movement out of the shade. To accommodate greater transpirational demand, evolution of greater sapwood hydraulic efficiencies can cut the hydraulic costs of transpiration (Sperry 2003). Here, vessels changed in a number of ways, including the evolution of simple perforation plates, increase in vessel densities, as well as lengthening and widening of individual vessels (Hacke et al. 2006). Finally, dependence on root pressure for growth and embolism refilling would be expected to decline as angiosperms branched out into brighter and drier habitats or as plant size increased. This is because opportunities to generate root pressure drop off as rainfall and humidity decline. The unyoking of root pressure ‘addiction’ likely involved the increases in xylem cavitation resistance, rapid stomatal control to humidity and leaf water potential, as well as evolution of physiological mechanisms of osmotic adjustment to maintain turgor and embolism refilling under tension (Stahlberg & Cosgrove 1997; Sperry 2003).
A preliminary look at early-derived ecologies among the extant basal flora indicates that angiosperms gradually entered more exposed and increasingly disturbed habitats, but these zones were very wet (i.e. wet, montane cloud forests; Feild et al. 2004). Specific habitats include as colonizers of steep landslips, along forest margins and in large forest-light gaps (Sugden, Tanner & Kapos 1985; Todzia 1988; Wagner & Lorence 1999; Feild et al. 2004; Martin & Ogden 2005). Ascarina, Hedyosmum and Trimenia represent independent lines that evolved greater leaf photosynthetic performances and abilities to recruit seedlings in brighter, more large-scale disturbed habitats. Consistent with greater ecological amplitude, Ascarina- and Hedyosmum-like chloranths, represented by fossil pollen and flowers, appear to lead the initial waves of angiosperm invasion into high-latitude Northern and Southern Hemisphere communities during the Early Cretaceous (Romero & Archangelsky 1986; Eklund et al. 2004; Feild et al. 2004). Trimenia, however, lack a Mesozoic fossil record. Among basal angiosperms, the initial transitions to higher-light environments are characterized by a high degree of lineage-dependent, functional experimentation, in which fine-tuned performances were assembled piece-by-piece. Gap-establishing Chloranthaceae and Trimenia species, for example, evolved high leaf photosynthetic rates, but maintained a lack of palisade cells, leaf teeth and, therefore, reliance on root pressure and large stomata at low density. Similarly, other taxa that stay in the understorey, such as several Illicium species, evolved a single palisade layer and lost leaf teeth, but leaf photosynthetic rates remain low and leaf epidermises stayed tuned to low evaporative demand (Feild et al. 2004).
Hydraulically, stem xylem vessels of Ascarina, Hedyosmum and Trimenia seem to remain functionally undifferentiated from understorey-dwelling basal groups, with no major divergences in hydraulic resistance or vulnerability to cavitation (Hacke et al. 2006). Xylem venation of patterns of angiosperm leaves exhibit a similar pattern. When the architectural variability of basal angiosperm venation was quantified and compared with that of magnoliids and eudicots, basal angiosperms emerged as significantly more variable than later diverging clades (Arens 2006). This suggests that early in angiosperm history, the lineage honed its leaf vein architecture towards greater efficiency, perhaps minimizing pressure drops through the leaf system (Zwieniecki et al. 2002; Sack et al. 2003) in supplying water to the lamina's photosynthetic cells. These functional patterns in basal angiosperms suggest that functional experimentation for higher-light use occurs first in the optical- and CO2-processing traits of leaves, while xylem modifications for intrinsic hydraulic efficiency are slower to evolve. Such experimentation was only possible under the relatively low evaporative demands (as compared with a lowland tropical rain forest) and high water availabilities characterizing the sorts of large-scale disturbed habitats that Chloranthaceae and Trimenia recruit in.
The evolution of lianous habits represents another track for exploring different environments in early angiosperms. Basal angiosperm lianas typically establish in the damp, dark understorey, but later climb into more well-lit and drier environments as they climb up their hosts into the forest subcanopy. Associated with the evolution of climbing, the traits related to vessel hydraulic efficiencies ramp up considerably (Carlquist 1984, 1999, 2001b), but leaf photosynthetic capacities and the ability to process collimated light remain low (Feild et al. 2003b, 2004).
Much more detailed work is needed to piece together the nature of ecophysiological transitions promoting breakthroughs in higher light tolerance and emerging out of the clouds by increasing tolerance to greater evaporative demand. Interestingly, the observation that independent forays out of the shade as wet, gap-colonists and subcanopy vines did not entrain considerable species diversification (Magallón & Sanderson 2001) suggests that co-ordinated shifts in hydraulic and photosynthetic performances of hydraulic efficiency are necessary to make a substantial movement out of wet habitats. In the later phases of early angiosperm history, we predict that the forms and functions refined in the understorey and along the wet forest edge are co-opted for evolution of high productivity in unstable habitats with fluctuating resource availabilities – an ability so emblematic of highly successful eudicot and monocot lineages (Stebbins 1974, 1981; Bond 1989; Taylor & Hickey 1996; Brodribb et al. 2005). From this point, the uniquely invasive features and high physiological performance of angiosperms promotes further biogeographic, ecological and taxonomic expansion with significant consequences for the lineages with whom they share the biosphere (Schneider et al. 2004).