Dark and disturbed: a new image of early angiosperm ecology

Paleobiology, Winter 2004 by Feild, Taylor S, Arens, Nan Crystal, Doyle, James A, Dawson, Todd E, Donoghue, Michael J

Abstract.-Better understanding of the functional biology of early angiosperms may clarify ecological factors surrounding their origin and early radiation. Phylogenetic studies identify Amborella, Nymphaeales (water lilies), Austrobaileyales, and Chloranthaceae as extant lineages that branched before the radiation of core angiosperms. Among living plants, these lineages may represent the best models for the ecology and physiology of early angiosperms. Here we combine phylogenetic reconstruction with new data on the morphology and ecophysiology of these plants to infer early angiosperm function. With few exceptions, Amborella, Austrobaileyales, and Chloranthaceae share ecophysiological traits associated with shady, disturbed, and wet habitats. These features include low and easily light-saturated photosynthetic rates, leaf anatomy related to the capture of understory light, small seed size, and clonal reproduction. Some Chloranthaceae, however, possess higher photosynthetic capacities and seedlings that recruit in canopy gaps and other sunny, disturbed habitats, which may have allowed Cretaceous Chloranthaceae to expand into more diverse environments. In contrast, water lilies possess ecophysiological features linked to aquatic, sunny habitats, such as absence of a vascular cambium, ventilating stems and roots, and floating leaves tuned for high photosynthetic rates in full sun. Nymphaeales may represent an early radiation into such aquatic environments. We hypothesize that the earliest angiosperms were woody plants that grew in dimly lit, disturbed forest understory habitats and/or shady streamside settings. This ecology may have restricted the diversity of pre-Aptian angiosperms and living basal lineages. The vegetative flexibility that evolved in the understory, however, may have been a key factor in their diversification in other habitats. Our inferences based on living plants are consistent with many aspects of the Early Cretaceous fossil record and can be tested with further study of the anatomy, chemistry, and sedimentological context of Early Cretaceous angiosperm fossils.

Introduction

Flowering plants-angiosperrns-today include more than 257,000 species and have dominated most terrestrial ecosystems since the Late Cretaceous (Crane 1987; Crane and Lidgard 1989; Crane et al. 1995; Wing and Boucher 1998; Lupia et al. 1999). Much discussion has focused on the ecology of the earliest angiosperms. What sorts of habitats did they occupy? How did they function? Answers remain elusive, owing in part to disparate views on the ecological starting point for flowering plant evolution (Doyle and Donoghue 1993; Sanderson and Donoghue 1994).

Previous Interpretations of Early Angiosperm Ecology.-The traditional representation of early angiosperms is that of woody magnoliids, with large bisexual flowers consisting of numerous free perianth parts, stamens, and carpels, as in extant Magnoliales and Winteraceae (e.g., Arber and Parkin 1907; Takhtajan 1969; Thorne 1976; Cronquist 1988; Gottsberger 1988). By analogy with these living taxa, the first flowering plants would be slowly growing and maturing trees or shrubs with large leaves that photosynthesized at low rates. These plants would have established in wet, low-light environments below the forest canopy (Table 1) (Bews 1927; Axelrod 1952; Takhtajan 1969; Thorne 1976; Cronquist 1988).

In contrast, others suggested that the first angiosperms were weedy, drought-tolerant shrubs that lived in open, disturbed habitats of semi-arid tropical to subtropical regions (Table 1) (Stebbins 1965, 1974; Axelrod 1970). From there, other authors suggested that angiosperms moved into disturbed streamside habitats in mesic environments (Doyle and Hickey 1976; Hickey and Doyle 1977). These suggestions built on arguments that variable conditions might have favored the evolution of the reproductive and vegetative hallmarks of angiosperms, such as short generation time, the closed carpel, reduction of ovules and gametophytes, double fertilization and endosperm, and flexible seedling growth (Stebbins 1965, 1974), and on paleoecological inferences from the diversity of Early Cretaceous angiosperm pollen in the Northern Gondwana tropics, associated with indicators of aridity, and the morphology and sedimentary associations of Early Cretaceous angiosperm leaves (Brenner 1976; Doyle and Hickey 1976; Hickey and Doyle 1977). Subsequent studies, however, showed that angiosperm pollen was equally diverse in parts of Northern Gondwana that show evidence for wetter climates (Doyle et al. 1982; Brenner 1996).

A related view reconstructed the first angiosperms as fast-growing, rhizomatous, and semiherbaceous plants of sunny, unstable streamsides (Table 1). This interpretation arose from early phylogenetic analyses that rooted the angiosperms among the "paleoherbs," variously including Nymphaeales, Piperaceae, Saururaceae, Lactoris, Aristolochiaceae, and Chloranthaceae (Donoghue and Doyle 1989; Taylor and Hickey 1992). The paleoherb hypothesis was argued to be consistent with small angiosperm seed sizes and the paucity of angiosperm wood in Early Cretaceous floras (Taylor and Hickey 1990, 1992, 1996; Doyle et al. 1994; Nixon et al. 1994; Wing and Boucher 1998; Eriksson et al. 2000). In this scenario, early angiosperms tolerated disturbance and had high leaf photosynthetic capacity and short generation times (Taylor and Hickey 1992, 1996; Wing and Boucher 1998).