Dark and disturbed: a new image of early angiosperm ecology

Abstract

Better understanding of the functional biology of early angiosperms may clarify eco logical 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 rep resent 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 Chlor anthaceae 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, how ever, 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.

Explosive Radiation of Malpighiales Supports a Mid‐Cretaceous Origin of Modern Tropical Rain Forests

“…We suggest that Malpighiales were among the earliest angiosperm colonizers of the understory in the Cretaceous (Crane 1987), following representatives of the basal ANITA grade, which have been depicted as playing a similar role at the earliest stages of the angiosperm radiation (Feild et al 2004). ANITA-grade plants, some eumagnoliids, and Malpighiales may have successfully competed with existing nonangiospermous plants in the understory, and Malpighiales may have filled a niche that was less occupied by the other new angiosperm groups: the small, subcanopy tree.…”

“…This assumed that larger diaspores help seedlings become established and survive better in heavily shaded environments such as the understory of tropical rain forests. Recent studies (Grubb 1996(Grubb , 1998Grubb and Metcalfe 1996), however, suggest that large diaspores, while an advantage in low-light environments, are not a requirement for successful germination and establishment in the rain forest and may relate more to the ability to germinate on dense leaf litter than to light availability (see also Feild et al 2004). Seeds of contemporary Malpighiales are on average larger than the mean for samples of all angiosperms (A. Moles, personal communication, Seed Information Database, Kew Gardens).…”

“…ANITA-grade plants, some eumagnoliids, and Malpighiales may have successfully competed with existing nonangiospermous plants in the understory, and Malpighiales may have filled a niche that was less occupied by the other new angiosperm groups: the small, subcanopy tree. Modern Malpighiales are often 2-10 m tall, are able to grow and reproduce without direct sunlight, and are more flexible in growth habit than cycad-like seed plants (Crane 1987;Feild et al 2004), that is, like ANITA-grade plants but generally taller. The recently documented (Schneider et al 2004) Late Cretaceous radiation of derived ferns (Polypodiaceae sensu lato) may represent a parallel occupation of forest floor and epiphytic niches.…”

Phylogenetic Analyses of Basal Angiosperms Based on Nine Plastid, Mitochondrial, and Nuclear Genes

“…This set of relationships has been used to formalize a classification system for angiosperms (APG II 2003) and to guide investigation of various aspects of early angiosperm evolution (e.g., Endress and Igersheim 2000;Friis et al 2000;Thien et al 2000;Williams and Friedman 2002;Ronse De Craene et al 2003;Feild et al 2004;Kramer et al 2004). Work is still needed to establish firmly that the current consensus rests on a solid phylogenetic foundation and, more importantly, to resolve the polytomy among Ceratophyllum, Chloranthaceae, monocots, magnoliids, and eudicots.…”

Integrating Early Cretaceous Fossils into the Phylogeny of Living Angiosperms: ANITA Lines and Relatives of Chloranthaceae

“…Because all extant Nymphaeales are aquatic, except for an obvious reversal to wet terrestrial habitats in the well-nested species Barclaya rotundifolia (Schneider and Carlquist 1995;Feild et al 2004), it is most parsimonious to assume that the aquatic habit had originated by the time the crown group evolved. Thus, recognition of crown group fossils in the Aptian-Albian indirectly implies that these were aquatic plants, and this is confirmed by the vegetative morphology of Pluricarpellatia, Scutifolium, and Brasenites (Wang and Dilcher 2006;Taylor et al 2008;Friis et al 2011).…”