Fisiologia Extinçao Flores

Review
Blackwell Publishing, Ltd.
Tansley review
Form, function and environments of the
early angiosperms: merging extant
phylogeny and ecophysiology with
fossils
Author for correspondence:

Taylor S. Feild
Fax: +1 504 862 8706
Email: acmopyle@hotmail.com
Taylor S. Feild1 and Nan Crystal Arens2
Received: 2 September 2004

Accepted: 8 November 2004
14456, USA
Department of Ecology and Evolutionary Biology, Dinwiddie 310, Tulane University, New Orleans, LA,
701185698, USA; 2Department of Geosciences, Hobart and William Smith Colleges, Geneva, NY
Contents
Summary
383
I.
Introduction
384
II.
Previous images of early angiosperms and their habitats
385
III. Progress in understanding angiosperm phylogeny:

extant basal relations
IV. Early angiosperm ecology: inferences from extant
plants and reflections from the fossil record
V.
The ecology of angiosperm diversification:

gaining a roothold and subsequent diversification
397
VI. The environmental context of early angiosperm

evolution
399
VII. Conclusions
402
386
387
Acknowledgements
402
References
402
Summary
Key words: Amborella, Archaefructus,
angiosperm phylogeny, basal
angiosperms, Chloranthaceae,
diversification, key innovations,
phytochrome function.
The flowering plants angiosperms appeared during the Early Cretaceous period and
within 1030 Myr dominated the species composition of many floras worldwide.
Emerging insights into the phylogenetics of development and discoveries of early
angiosperm fossils are shedding increased light on the patterns and processes of
early angiosperm evolution. However, we also need to integrate ecology, in particular
how early angiosperms established a roothold in pre-existing Mesozoic plant
communities. These events were critical in guiding subsequent waves of angiosperm
diversification during the AptianAlbian. Previous pictures of the early flowering
plant ecology have been diverse, ranging from large tropical rainforest trees, weedy
drought-adapted and colonizing shrubs, disturbance- and sun-loving rhizomatous
herbs, and, more recently, aquatic herbs; however, none of these images were tethered
to a robust hypothesis of angiosperm phylogeny. Here, we synthesize our current
understanding of early angiosperm ecology, focusing on patterns of functional ecology,
by merging recent molecular phylogenetic studies and functional studies on extant basal
angiosperms with the picture of early angiosperm evolution drawn by the fossil record.
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I. Introduction
The flowering plants angiosperms are the most ecologically
diverse and species-dense branch on the green plant tree of
life. With roughly 250 000 extant species (Crane et al., 1995;
Wing & Boucher, 1998; Soltis et al., 2004), angiosperms
have evolved an unparalleled spectrum of growth habits
and ecologies in response to a broad range of habitats
(Stebbins, 1974; Doyle, 1977; Crane et al., 1995; Wing &
Boucher, 1998). Also, angiosperms dominate the composition,
biomass, and biogeochemical functioning of most terrestrial
ecosystems, with the exception of boreal and some
temperate rainforest zones (Bond, 1989; Wing & Boucher,
1998).
In contrast to their prodigious modern presence, the fossil
record reveals that angiosperms and their ecological ascendancy are geologically recent developments. For much of land
plant history, terrestrial vegetation consisted of free-sporing
(e.g. lycopsids, ferns, sphenopsids, mosses) and gymnospermous seed plants (e.g. bennettitaleans, conifers, cycads,
ginkgos, Gnetales and various seed ferns). Despite intriguing
reports of pre-Cretaceous angiosperms (Cornet & Habib,
1992) and suggestive molecular clock analyses (Li et al., 1989;
Martin et al., 1989), distinctive pollen forms of Early Cretaceous age (BerriasianValanginian, Fig. 1) mark the currently
accepted first appearance of flowering plants (Doyle, 1983;

Hughes & McDougall, 1987; Brenner, 1996). By the late
Aptian (112 Ma), flowering plants had diversified significantly and fossils representing a wide range of lineages were
well-differentiated (Doyle, 1969, 1977; Wolfe et al., 1975;
Doyle & Hickey, 1976; Hickey & Doyle, 1977; Muller, 1981;
Upchurch, 1984; Friis et al., 1994, 1999, 2000, 2001; Lupia
et al., 1999). New fossil-calibrated molecular clock studies
also suggest that some of the most speciose lowland tropical
angiosperm clades may have originated during Aptian times
or earlier (Bremer, 2000; Davies et al., 2004).
Ecologically, angiosperms expanded to both poles and
began to dominate the species composition in some lowlatitude floras by Aptian times (Retallack & Dilcher, 1981;
Romero & Archangelsky, 1986; Crane & Lidgard, 1989;
Lidgard & Crane, 1990; Spicer, 1990; Dettmann, 1994;
Cantrill & Nichols, 1996; Wing & Boucher, 1998; Barrett &
Willis, 2001). Many groups of Mesozoic free-sporing and
seed plants became extinct or declined in abundance, as
angiosperms proliferated (Knoll, 1986; Crane & Lidgard,
1989; Lidgard & Crane, 1990; Lupia et al., 1999; McElwain
et al., 2005). Yet other groups pleurocarp mosses, Polypodiaceae ferns and epiphytic lycopods may have diversified
secondarily as broad-leaved angiosperms restructured the
ecology of lowland rain forest plant communities and created
Fig. 1 Major events in the Cretaceous history of flowering plants. Sources for age data and stratigraphic nomenclature are taken from Gradstein
and Ogg (1996), Gradstein et al. (1995) and Berggren et al. (1995), as compiled by A. R. Palmer and J. Geissman for the Geological Society of
America. Global temperature trends (noted by lateral line) are from Frakes (1999), Veizer et al. (2000), and Crowley and Berner (2001). Evidence
for high latitude glaciation is from Frakes and Francis (1988). First appearances of angiosperm pollen are as recorded by Doyle (1983) and
McIntyre and Brideaux (1980). Diversity, relative abundance and geographic distribution data are from Lupia et al. (1999). The age of
Archaefructus is from Swisher et al. (1999). Major intervals of oceanic anoxia events (OAEs) are based on Bralower et al. (2002a,b). In all cases,
an OAE consisted of several brief periods of anoxia distributed through various ocean basins. The level of stratigraphic resolution needed to
present each individual event is outside the scope of this representation. For more detailed stratigraphies, see Heimhofer et al. (2004) and Herle
et al. (2004).
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new environmental opportunities for these lineages during

the Late Cretaceous (Wikstrm & Kenrick, 2001; Shaw et al.,
2003; Schneider et al., 2004).
Although the Cretaceous explosion of angiosperm diversity
is well-documented, the ecological factors underlying this
radiation remain unclear. Most speculation has focused on
the competitive superiority of angiosperms (Stebbins, 1974,
1981; Regal, 1977; Burger, 1981; Bond, 1989). Despite this
emphasis, little attention has been paid either to the actual
ecological strategies used by early angiosperms or to the
environmental context in which the lineage evolved. Recently,
however, new data from several disparate sources are allowing
us to pose and test concrete hypotheses for early angiosperm
ecology. In particular, a spectrum of independent molecular
studies have, for the first time, produced a robust hypothesis
of angiosperm phylogenetic relationships (Mathews &
Donoghue, 1999; Parkinson et al., 1999; Qiu et al., 1999; Soltis
et al., 1999; Doyle & Endress, 2000; Graham & Olmstead,
2000; Zanis et al., 2002), which supplies a framework for
testing ideas about early angiosperm ecology. Also, new data
and analyses from the global Ocean Drilling Project and other
sources have shed new light on global climate and biogeochemical change during the Cretaceous (Fig. 1; e.g. Jahren
et al., 2001; Beerling et al., 2002; Bralower et al., 2002b;
Heimhofer et al., 2004; Herle et al., 2004). These perspectives
provide a context in which to understand the response of early
angiosperms to their changing world.
To begin to connect ecology to the early radiation of angiosperms, we must understand the ecological starting point for
angiosperm evolution. In turn, this may clarify the selective
forces within the environment driving the evolution of
unusual character combinations (e.g. carpels, xylem vessels
and reticulate-veined leaves with freely ending veinlets all on
the same body plan) that may have opened up new ecological
possibilities for Cretaceous angiosperms (Feild, 2004; Feild
et al., 2004). This combination of traits and environment was
critical in initiating waves of angiosperm diversification
during the AptianAlbian, which ultimately drove the development of the modern angiosperm-replete flora. In this review,
we synthesize recent phylogenetic, ecophysiological and
geological discoveries that are pollinating new ideas about
the ecology and environment of early angiosperms.
We will begin by reviewing previous views on early
angiosperm form and function. We will focus specifically on
vegetative functional traits because these have been only
cursorily considered in recent reviews (Crane et al., 1995;
Wing & Boucher, 1998; Feild et al., 2003a; Soltis et al., 2004).
Next, we will synthesize recent empirical and conceptual
advances in the structure of angiosperm phylogeny, and how
these results have, or at least should be, impacting our ability
to pose testable hypotheses about how early angiosperms
functioned within their environments. Through the discussion, we will explore patterns of ecophysiology and vegetative
morphology drawn from living plants and the support for
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these trends in the Early Cretaceous fossil record, while

pointing out areas in the fossil record in need of future
attention. We will finish by discussing the ecology of early
angiosperm diversification and the Cretaceous world into
which the angiosperms debuted and the processes in the
physical and biotic environment that might have allowed
the new lineage to invade, and eventually dominate, the
landscape.
II. Previous images of early angiosperms and

their habitats
1. Ranalian rainforest tree
An early and influential idea about the ecology of the earliest
angiosperms is the woody Ranales or woody magnoliid
hypothesis. This view flowed from a preconception that ancestral
angiosperm flowers were large and consisted of numerous
spirally arranged free perianth parts, stamens and carpels
features that are retained in living Magnoliales and Winteraceae
(Arber & Parkin, 1907; Bews, 1927; Axelrod, 1952; Takhtajan,
1969; Thorne, 1976; Cronquist, 1988; Gottsberger, 1988).
By analogy to these living taxa, the first flowering plants were
portrayed as trees or shrubs that grew and matured slowly
in tropical lowland rainforests or cloud forests. They had
thick, heavy branches plumbed with primitive tracheid-based
xylem. These plants were predicted to have large, simple,
entire-margined leaves that photosynthesized at low rates
(Bews, 1927; Takhtajan, 1969; Cronquist, 1988). Their seedlings
established on undisturbed soil in wet, low-light environments
below the forest canopy. Plants such as Degeneria vitiensis
(Smith, 1949), Galbulimma belgraveana (van Royen, 1962),
Eupomatia, some genera in the Winteraceae (Feild et al.,
2000) and many Magnoliaceae and Myristicaceae species
(Forget, 1991; Kwit et al., 1998; Yasumura et al., 2002)
epitomize the woody Ranalian ecological stereotype. However,
other Magnoliales, such as Annonaceae (126 genera, 1200
species), have diverse growth habits (e.g. vines, shrubs,
and trees) and resist ecological generalization (Berry et al.,
1999; Fisher et al., 2002). A related view reconstructed early
angiosperms as arborescent residents of lowland equable
rainforests. For example, Corner (1949) suggested that the
large-boled tropical durians (Durio, Bombacaceae) were the
least-modified living descendents of the first angiosperms.
2. Weedy xeric shrub
Others suggested that fast-growing, drought-adapted shrubs
from subtropical open, disturbed habitats preceded shadetolerant rainforest trees in angiosperm evolution (Stebbins,
1965, 1974; Axelrod, 1970, 1972). This concept was based
on the belief that seasonal drought would not only favor the
origin of reproductive and vegetative hallmarks of angiospermy,
but would also foster diversification (Stebbins, 1965, 1974).
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Although the woody magnoliids, Magnoliales and Winteraceae

were still viewed as among the most primitive living angiosperms,
Stebbins (1974) concluded that their extant rain forest to
cloud forest ecology was secondarily derived. Stebbins (1974)
pointed out that modern Magnoliaceae and Winteraceae
consist chiefly or entirely of genera with a polyploid origin
(Ehrendorfer & Lambrou, 2000) and that their diploid ancestors
must be extinct, a trend supported by the fossil record of
Magnoliaceae (Masterson, 1994). Over time, Stebbins (1974)
concluded that, polyploidy events, which commonly support
populations invading new environments, allowed the early,
drought-adapted lineages to move into lowland forest museums
where they survived due to perceived low extinction rates.
Meanwhile, other more advanced angiosperm lineages radiated
on a drought-disturbance theme, forcing the early droughtadapted magnoliid forms to extinction.
The arid-origin model conveniently explained the paucity
of early angiosperm fossils because few plant remains can be
preserved over geologic time in dry climates. In fact, no direct
fossil evidence for xerophytic ancestral angiosperms has been
found. However, Doyle and Hickey (Doyle & Hickey, 1976;
Hickey & Doyle, 1977) suggested that the morphology
and sedimentary facies associations of most fossil leaves from
the Early Cretaceous (AptianAlbian) Potomac Group of
eastern North America indirectly supported Stebbins semiarid
hypothesis (Stebbins, 1965, 1974). This was not based on
evidence of aridity in the Potomac area, but rather on the belief
that the disturbed stream margins where fossil angiosperms
leaves were preferentially preserved were the habitats most
likely to be occupied by weedy immigrants from dry regions.
More support for a drought-adapted origin came from the
tropical latitudes of northern Gondwanaland (e.g. Brazil and
West Africa), where a diversity of Early Cretaceous pollen
forms was discovered in association with geologic indicators
of seasonal aridity, such as low abundance of fern spores,
pollen typical of supposedly xerophytic plants (i.e. the extinct
conifer family Cheirolepidiaceae and ephedroid forms linked
to Gnetales) and salt deposits (Doyle & Hickey, 1976; Hickey
& Doyle, 1977; Brenner, 1996). Subsequent studies, however, showed that angiosperm pollen was equally diverse and
abundant in restricted wet areas of Northern Gondwana, such
as northern South America and the Middle East, during the
same timeframe, where there were fewer Cheirolepidiaceae,
more ferns, and deposits of coal (Doyle et al., 1982; Brenner,
1996). Consequently, one climatic regime cannot be favored
over another as the initial one occupied by flowering
plants.
3. Herbaceous weeds
A related view, which emphasized disturbance as a major
catalyst for early angiosperm evolution, proposed that the
first angiosperms were rhizomatous, semiherbaceous weeds
of sunny, unstable stream-sides and flood plains (Taylor &
Hickey, 1992, 1996). In this model, early angiosperms were

rapidly growing pioneers that tolerated disturbance. Their
leaves were toothed with marginal hydathodal glands and
were capable of high photosynthetic rates. This interpretation
was spurred by some early cladistic analyses that placed
herbaceous magnoliids the paleoherbs, which have
variously included Nymphaeales, Piperaceae, Saururaceae,
Lactoris, Aristolochiaceae and Chloranthaceae at the base of
the extant angiosperm tree (Taylor & Hickey, 1992; Doyle
et al., 1994; Nixon et al., 1994). Proponents of a paleoherb
origin also argued that the hypothesis was consistent with
small sizes of angiosperm flowers and seeds, the rarity of
angiosperm wood in Early Cretaceous fossil record, and the
presence of early angiosperm leaf fossils in ephemeral habitats
that were interpreted as sunny (Taylor & Hickey, 1990, 1992,
1996; Wing & Boucher, 1998; Friis et al., 1999, 2000;
Eriksson et al., 2000; but see Feild et al., 2004).
III. Progress in understanding angiosperm

phylogeny: extant basal relations
Whereas the previous descriptions of angiosperm ecology
were consistent with the assumptions based on the data
available at the time, none were explicitly linked to a robust
and independent hypothesis of phylogeny. However, recent
advances in molecular phylogenetics have converged on
similar topologies for extant lineages near the root of the
angiosperm tree (Figs 2 and 3; Mathews & Donoghue, 1999;
Soltis et al., 1999, 2004; Doyle, 2001; Endress, 2001; Zanis
et al., 2002; Feild et al., 2004). This congruence offers a new
tool for exploring early angiosperm ecology.
The first extant basal angiosperms, which are living representatives of lineages that split from the main angiosperm line
relatively early in its history, were recognized using nuclear
rRNA (Hamby & Zimmer, 1992; Doyle et al., 1994) and
chloroplast rDNA ITS sequences (Goremykin et al., 1996).
These analyses submerged the Nymphaeales at the base of the
angiosperm tree. Later studies, incorporating multiple gene
sequence comparisons, retained Nymphaeales near the base,
but placed a suite of several unexpected tropical woody
shrubs, small trees and woody vines around them. In most of
these studies, the first branch was Amborella (1 species), a
vesselless shrub from New Caledonia that had been previously
placed in the Laurales; a second lineage included Nymphaeales; and a third branch (called the Austrobaileyales by some)
consisted of Austrobaileya (1 species), Trimenia (9 species) and
the Illiciales Illicium (40 species, including star anise) and
the Schisandraceae (Kadsura and Schisandra, 40 species). An
alternative topology merged Amborella and Nymphaeales into
a single basal clade (Barkman et al., 2000; Jansen et al., 2004),
but analyses by Zanis et al. (2002) indicated that this union
was not well-supported. Molecular analyses yielding the
present phylogenetic picture incorporated various combinations of all three cellular genomes. These included rbcL and
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atpB from the chloroplast, 18S rDNA from the nucleus, and
five mitochondrial genes (Soltis et al., 1997, 1999; Parkinson
et al., 1999; Qiu et al., 1999; Barkman et al., 2000), duplicated
phytochrome genes (Mathews & Donoghue, 1999; Zanis
et al., 2002), 17 chloroplast genes (Graham & Olmstead,
2000), genes with high substitution rates (i.e. trnL and matK;
Borsch et al., 2003; Hilu et al., 2003), and most recently,
genome-wide analysis of the chloroplast ( Jansen et al.,
2004).
In the current phylogenetic consensus, basal angiosperms
form a grade, referred to as ANITA (for Amborella, Nymphaeales, Illiciales, Trimenia and Austrobaileya) by Qiu et al. (1999).
Above the basal grade, the remaining angiosperms form
eight well-supported monophyletic lineages: Ceratophyllum,
Chloranthaceae, eudicots, Laurales (sans Amborella, Austrobaileya and Trimenia), Magnoliales, monocots, Piperales
(Piperaceae, Saururaceae, Lactoris and Aristolochiaceae) and
Winterales (Canellaceae plus Winteraceae). In contrast to
widespread agreement on the basal grade topology, relations
among these lineages are unresolved. In particular, it remains
unclear which group(s) diverged just above the basal grade.
There are increasing indications, from multigene analyses
(Qiu et al., 1999; Zanis et al., 2002), that the clade including
monocots and Ceratophyllum, forms the next branch above
the ANITA grade, and Chloranthaceae diverge next (Soltis
et al., 2004). The remaining angiosperm lineages aggregate
into a eudicot clade and a eumagnoliid clade, which is
composed of four strongly supported subclades: Magnoliales
and Laurales are sister to Winterales and Piperales (Soltis et al.,
2004). However, these placements are far from concrete.
Other analyses place Ceratophyllum with the eudicots (Hilu
et al., 2003). Chloranthaceae are also sister to monocots in
matK trees (Hilu et al., 2003).
Resolving the positions of Ceratophyllum, Chloranthaceae
and the topology of basal-branches within speciose groups
such as monocots and eudicots remains a significant technical
challenge. Angiosperms above the ANITA grade are highly
variable in morphological and ecological characters, which,
depending on the topology, can influence the interpretation
of ancestral states at the root of the phylogenetic tree. Thus,
we must explore how different phylogenetic hypotheses affect
the patterns of character evolution.
IV. Early angiosperm ecology: inferences from

extant plants and reflections from the fossil
record
Emerging consensus on the phylogeny of living angiosperms
offers a useful approach for elucidating evolutionary patterns
(Soltis et al., 1999, 2004). For instance, the form and
function of basal lineages can be documented and overlaid
onto hypotheses of angiosperm phylogeny to reconstruct
traits of the common ancestor (Forbis et al., 2002; Feild
et al., 2003a, 2004; Soltis et al., 2003, 2004; Kim et al., 2004).
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However, such phylogenetic character mapping has three

important caveats if our goal is to understand the ecology
of Early Cretaceous angiosperms. First, traits reconstructed
as ancestral among living basal angiosperm lineages may
actually reflect a derived condition. This could be true if the
earliest angiosperm lineages and their unique ecologies
went extinct, leaving only later-derived ecologies among the
modern flora. Indeed, the fossil record of early angiosperm
flowers suggests that extensive extinction and turnover
occurred during the Early Cretaceous (BarremianAptian)
when angiosperms were initially diversifying (Friis et al.,
1999, 2000, 2001). Surveys of five Barremian through
Aptian assemblages from Portugal by Friis et al. (1999,
2000, 2001) have identified 150 different angiosperm taxa,
represented by flowers, fruits and seeds, of which most (85%)
were magnoliids (broadly defined to include the ANITA
grade plus eumagnoliids) or monocots. In these floras,
only two of the most basal families (Nymphaeaceae and
Chloranthaceae) have been identified, on the basis of flowers,
fruits and/or dispersed stamens, in the Early Cretaceous (Friis
et al., 1999, 2000, 2001; Eklund et al., 2004). Also, no fossils
can unequivocally place any living genera of basal clades in the
Early Cretaceous, although Asteropollis pollen may be related
to Hedyosmum of the Chloranthaceae (Eklund et al., 2004).
Instead, extant genera of basal lineages, such as Illicium,
Chloranthaceae and Nymphaeales, appear to be the products
of much younger (early to mid-Tertiary) diversification, based
on fossil-calibrated molecular clock phylogenetic studies
(Oh et al., 2003; Zhang & Renner, 2003).
Second, if extant basal lineages identified by molecular
studies truly represent nodes near the start of the angiosperm
radiation, taxa at the tips of the branches, which parameterize
the character data set, may have undergone ecological modification over the last 130 Ma, such that ancestral traits were
lost or significantly modified. For instance, the form and
function of basal lineages could have been re-worked by
changes in climate (e.g. Tertiary cooling), habitat use, or by
shifts in community structure, from fern and gymnospermdominated communities to ones dominated by angiosperms
with possibly different ecosystem-level properties (Knoll &
James, 1987). Evaluating the relative roles of extinction and
ecological modification on patterns of ecological character
evolution will remain unclear until an extensive sample of
Early Cretaceous fossil angiosperms can be added to existing
phylogenies a goal that is significantly beyond current capability and will require renewed attention to morphological
data (Doyle, 2001; Eklund et al., 2004).
A third caveat surrounds the phylogenetic hypothesis
itself. Although todays molecular phylogenies enjoy wide
consensus among a variety of genes and, most unusually,
independent research groups, it is possible that further species
and gene sampling will again rearrange the branching of basal
lineages (Goremykin et al., 2003; but see Soltis & Soltis,
2004).
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Despite these caveats, a character-mapping approach does

allow specific hypotheses to be posed and tested using the fossil
record, a significant advance over previous understanding
(Doyle & Donoghue, 1993; Doyle, 2001; Feild et al., 2003,
2004; Soltis et al., 2004). Although fossils cannot be regreened to exhibit physiology or ecology, they can preserve
ecomorphological, biochemical and/or contextual features
(i.e. types and chemistry of preserving sediments) that are
indicative of past lifestyles (Wing & Boucher, 1998). Thus,
fossils can be applied to test patterns of ecological evolution
deduced from living basal lineages. Most importantly, using
fossil form and function, rather than taxonomic identity, to
test historical hypotheses does not hinge on the unlikely
possibility of finding examples of basal lineages like Amborella
in the Early Cretaceous because ancestral characters suggested
by living plants provide predictions about the ecomorphological
and contextual features of fossils that we should expect to
see if the hypothesis holds. Addressing solely the living end
of this approach, an evolutionary analysis of extant basal
angiosperm ecology, incorporating a variety of eco-functional
traits (e.g. preferred habitats for seedling recruitment, leaf
photosynthetic rate, leaf ecomorphic traits, growth forms)
has revealed two distinct possibilities for the ancestral ecology
of angiosperms: (1) one represented by Amborella and the
terrestrial members of the ANITA grade; and (2) another
represented by the water lilies (Feild et al., 2003, 2004).
In the next section we review the predicted ecological and
functional characters, given these alternatives, and discuss
their relative support by the fossil record and phylogenetic
data.
1. Growth habit and habitat
The first phylogenetic hypothesis predicts woody, tropical
early angiosperms with unusual seeding development (Figs 2
and 3). Amborella and Austrobaileyales pass through a creeping
establishment phase, where seedlings possess a pseudorhizomatous lignotuber and send out multiple scandent
shoots from basal buds before adopting a more typical shrub/
small-tree form (Feild et al., 2004; Fig. 2). Scandent development can also extend to adult plants, as indicated by evolution
of twinning liana habits in Austrobaileya, Schisandraceae and
two Trimenia species (Feild et al., 2003b; Fig. 2). Based on the
phylogenetic distribution of functional characters, ancestral
habitats were reconstructed as moist, low-light understories,
with frequent soil disturbance (Fig. 2; Feild et al., 2004).
Modern examples of these wet, dark and disturbed habitats
include understory stream margins and steep soil washouts
in montane tropical and subtropical cloud forests (Feild
et al., 2004). Multiple shoots and early commitment to
below-ground carbon storage in basal angiosperm seedlings
seem to enable colonization and persistence on unstable
substrates prone to shifting (such as brittle clay and sandy
soils, in between rocks and rotting logs) by increasing whole-
plant anchorage and resilience to traumas that break branches

and roots (Feild et al., 2003a,b, 2004). Yet, to date, no direct
evidence indicates that early Cretaceous angiosperms were
woody or occupied wet, dark, and disturbed zones. Upland
slopes, like those favored by living members of the extant
basal grade, seldom enter the geologic record (Behrensmeyer
et al., 2000). However, stream margins and channels two
disturbed habitats are common terrestrial depositional
settings (Doyle & Hickey, 1976; Hickey & Doyle, 1977;
Behrensmeyer et al., 2000). Thus, re-examination and
discovery of new forested flood plain deposits from the Early
Cretaceous is essential. Examination of these assemblages with
an eye for characters linked to wet, dark and disturbed zones
will allow this hypothesis to be tested. However, simplistic
application of leaf and seed traits to infer growth form is
potentially fraught with error (Feild et al., 2004).
A second image of early angiosperms, represented by the
Nymphaeales, suggests an herbaceous, rhizomatous water plant
with submerged to floating leaves and aerial flowers (an epihydate
habit Cook, 1999). For most water lilies, two dramatically
different light regimes characterize their life history. Most
germinate and develop some leaves under extremely low light
and reduced oxygen tension in undisturbed sediment at the
bottoms of lakes and ponds (Smits et al., 1990). Eventually,
seedlings send up floating leaves capable of tolerating full
sunlight on the water surface (Williamson & Schneider,
1993; Brewer & Smith, 1995). Some tuber-forming water
lilies, such as Barclaya and Ondinea, can establish in more
unstable sediments on the bottoms of clear, slow-moving
streams (Williamson et al., 1989).
An aquatic image for early angiosperms emerged from a
few phylogenies where Nymphaeales emerged as basal (Doyle
et al., 1994; Parkinson et al., 1999; Graham & Olmstead,
2000). However, if either Amborella or Nymphaeales linked
to Amborella (Parkinson et al., 1999; Barkman et al., 2000;
Graham & Olmstead, 2000; Jansen et al., 2004) branch first
from the angiosperm root, then parsimony phylogenetic analysis
reconstructs angiosperms as ancestrally woody and terrestrial
(reconstruction not shown). The latter relation, although
weakly supported by molecular data (Zanis et al., 2002; but
see Jansen et al., 2004), may be substantiated by the presence
of what appear to be vestigial lacunae canals in the protoxylem
of Amborella stems (Bailey & Swamy, 1948; Feild et al.,
2000). Such lacunae, which foster gas exchange in submerged
stems and roots (Dacey, 1980), may be homologous with those
in many Nymphaeales. Under an aquatic origin hypothesis,
angiosperm ancestors may have adopted the submerged
lifestyle to escape competition on land and tap into underexploited freshwater habitats (Sargant, 1908; Arber, 1920;
Sun et al., 2002). Adaptation to seasonally ephemeral pools,
which occurs in most living water lilies (both drytropical and
frozentemperate) (Sculthorpe, 1967; Williams & Schneider,
1993), may have been a ripe environment for the evolution
of rapid growth (via herbaceousness) and accelerated
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Fig. 2 Growth habits among extant basal angiosperms. (a) Twinning, lianaous habit of Austrobaileya scandens, Mt. Bartle Frere, Queensland,
Australia. (b) Seedling of Illicium floridanum, illustrating a pseudo-rhizomatous creeping habit with a central stem axis and an additional shoot
emerging from the base, Apalachicola, Florida, USA. (c) Scandent shrub habit of Amborella trichopoda from Mt. Aoupinie, New Caledonia. Note
the flattened cane-like shoots. (d) Chloranthus henryi herbs regenerating on a collapsed slope from a subtropical evergreen forest, Hunan,
China. (e) Habit of Schisandra glabra, occurring as an understory, scrambling vine, Crowleys Ridge, Arkansas, USA. (f) Sapling of Amborella
trichopoda, note the numerous weeping shoots, that are produced from a lignotuber, from Plateau de Dogny, New Caledonia. (g) Seedling of
Trimenia papuana, Mt. Gumi, Morobe Province, Papua New Guinea. (h) A vine-like sapling of Trimenia papuana, from same locality as (g).
Later in ontogeny, plants become normal-looking multiple stemmed trees. (i) The scrambling vine growth form of Trimenia moorei from
Stockyard Creek, New South Wales, Australia.
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Fig. 4 Stomatal vestibules and striated

abaxial cuticles in extant basal angiosperms.
(a) Austrobaileya scandens; (b) Chloranthus
japonicus; (c) Illicium floridanum; (d)
Trimenia neocaledonica. Bars, 30 m.
reproduction two characteristics thought to underlie

much of the ecological success of angiosperms (Stebbins,
1974, 1981; Burger, 1981; Bond, 1989; Robinson, 1994;
Taylor & Hickey, 1996).
Although most parsimonious character reconstructions
indicate that flowering plants were terrestrial and woody
(Fig. 4, Feild et al. 2004), the fossil record offers some
evidence for early angiosperm aquatics. A recently discovered
fossilized water-lily flower (Friis et al., 2001) showed that the
lineage was present in the Early Cretaceous (Barremian to
early Aptian), but it did not provide direct evidence that the
parent plant was aquatic as are all modern representatives of
the clade. More clearly aquatic forms, resembling water lilies
in having palmately veined nymphaeid (long-petioled, ovalshaped) leaves, are represented by Brasenia-like leaf imprints
from the Kurnub Group (AptianAlbian) (Taylor et al., 2001)

of Jordan and whole plant compression fossils deposited in
a lake environment from the AptianAlbian of Brazil (Mohr
& Friis, 2000). However, none of these fossils preserve
enough detail to associate them unequivocally with the Nymphaeales. Other possible early aquatic angiosperms include
fossil leaves Nelumbites from the Potomac group, which may
be related to water lotus, Nelumbo, a basal aquatic eudicot
(Upchurch et al., 1994).
The discovery of Archaefructus from lake deposits in China
has renewed enthusiasm for the aquatic origin hypothesis
(Sun et al., 1998, 2002; Zhou et al., 2003). Archaefructus
undisputed aquatic habit is based on the character of the
enclosing sediments and fish fossils preserved among the
plants foliage (Sun et al., 2002). Archaefructus is also
Fig. 3 Parsimony distribution of growth habit characters among extant basal angiosperms using MacClade (Madison & Madison, 2000) for
three different phylogenetic hypotheses. Growth habit was treated as an unordered character, and a matrix of character states and coding
decisions is available from the first author on request. Hypothesis (a) is based on the combined molecular/morphology presented by Doyle and
Endress (2000), with the resolution of relations in basal eudicots, Nymphaeales, and monocots based on the molecular studies of Kim et al.
(2004), Les et al. (1999) and Tamura et al. (2004), respectively. Hypothesis (b) is based on the backbone of the matK consensus tree provided
by Hilu et al. (2003) with eudicot, monocot, and Nymphaeales relations expanded as hypothesis (a). Hypothesis (c) is based on the backbone
molecular tree of Zanis et al. (2002).
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exceptional not only for its age (originally dated Late Jurassic;
however, radiometric data supports an Early Cretaceous,
Barremian 124 Ma age, Swisher et al., 1999; Zhou et al.,
2003), but because all parts of the plant are preserved in
organic connection, allowing a complete and accurate reconstruction of the living plant. In the reconstruction of Sun et al.
(2002), flowers and seeds were displayed above the water
surface, leaves were submerged (based on their highly dissected
morphology which suggests they were analogous to the
buoyant filliform leaves of Cabomba, Ceratophyllum, and
some Ranunculus aquatics) (Sculthorpe, 1967), limbs were
partially supported by the water, and roots penetrated lake
sediments. Cladistic analysis by Sun et al. (2002) placed
Archaefructus below the common ancestor of all living
angiosperms. Subsequent studies, based on the assumption
that the outgroup had flowers, have nested Archaefructus at
positions away from the angiosperm root (i.e. as a water lily
or basal eudicot; Friis et al., 2003; M. Bowe, pers. comm.,
2004). Until its relationships are resolved, it will be difficult
to evaluate the ecological significance of Archaefructus.
Furthermore, if species of Archaefructus are correctly dated as
Barremian, then they are too young to represent the earliest
flowering plants because angiosperm radiation was already
well-underway by that time (Friis et al., 1999, 2000, 2001;
Doyle, 2001, fig. 1). In fact, basal-grade eudicots are also
described from the Yixian Formation, which contains Archaefructus (Leng & Friis, 2003).
2. Leaf function: leaf optics and photosynthetic/wateruse physiology
Under the dark-disturbed hypothesis, leaves are functionally
tuned to low-light, wet habitats (Feild et al., 2001, 2003a,b,
2004). Leaf cross-sections of Amborella and the Austrobaileyales
are dominated by spongy parenchyma tissue. The spheroid
shapes of spongy mesophyll create numerous light-reflecting
airwater interfaces, resulting in extensive light-scattering
within the leaf. Consequently, the average path length of
photons moving through the leaf is increased, which can
increase the probability that they are absorbed by chlorophyll
and processed for CO2 reduction. Such extended light paths
are important in light-limited understory habitats, but a
liability in high light environments unless CO2 fixation rate
is correspondingly increased (Smith et al., 1997). Also, the
photosynthetic apparatus of Amborella and most Austrobaileyales
(based on field measurements of 53 species) functions
similarly to that of shade-adapted plants. As shade plants,
Amborella and most Austrobaileyales are characterized by
low, steady-state maximum photosynthetic electron transport
rates and light-saturation points (generally less than 20% full
sunlight), limited ability to adjust leaf physiology to increased
growth irradiances, as well as fruit production under low light
(Feild et al., 2001, 2003b; Griffin et al., 2004). CO2 uptake rates
have not been sampled widely, but reported light-saturated
rates measured under steady-state and physiologically optimal

conditions (i.e. under low leaf water potentials and high
humidity) vary from 4.5 to 12 mol CO2 m2 s1 (Feild et al.,
2003b; Griffin et al., 2004). Low photosynthetic capacity can
be advantageous in shady understory habitats by decreasing
the construction and maintenance respiratory carbon costs
for leaf production (Chazdon et al., 1996). Low photosynthetic
capacity, however, can constrain a plants ability to take advantage
of greater light availability (Smith et al., 1997).
Measurements of dynamic (non-steady-state) photosynthetic responses are more relevant for understanding plant
performance in variably lit understories where transient sunflecks (< 1 min) often dominate the amount of light captured
by leaves (Chazdon et al., 1996). Unfortunately, data are only
available for one basal angiosperm, Austrobaileya scandens
(an understory, subcanopy liana from a few mid-montane
cloud forests of tropical, Queensland, Australia) (Feild et al.,
2003b). Feild et al. found that stomatal conductance of A.
scandens closed very slowly (3 h, compared with 1540 min
in temperate and tropical zone eudicots angiosperms)
(Robinson, 1994; Franks & Farquhar, 1999) when transferred
from a humid to a drier atmosphere. Thus, consistent with its
typically humid/shady habitats, A. scandens appeared unable
to adjust leaf water loss rates fast enough to avoid ensuing low
leaf water potentials and possibly xylem cavitation under the
high and fluctuating humidity conditions of large forest gaps
and exposed canopy habitats. Slow stomatal response to
humidity, however, may be advantageous in understory and
subcanopy environments where A. scandens grows by allowing
time averaging of microenvironmental variation, such as rapid
excursions in humidity, light and leaf temperature during
sunflecks, which could trigger stomatal closure and increase
stomatal limitations on carbon assimilation (Chazdon et al.,
1996).
Robinson (1994) speculated that slow stomatal kinetics
may result from increases in guard cell rigidity induced lignification. Although stomatal lignification was not measured,
stomatal opening kinetics in Austrobaileya were relatively fast
(30 min). Thus, if increased lignification constrains stomatal
aperture then it only seems to impact stomatal closure and not
opening. The slow stomatal response to humidity in Austrobaileya
may be related to the anatomy of the stomatal complex.
Cuticular vestibules, formed from overarching extensions of
the epidermal cells, cover the guard cells of Austrobaileya, resulting in a chamber of still air above the guard cells that may
decouple them from atmospheric humidity (Fig. 4a). Consequently, the guard cells may respond to the locally high water
vapor concentrations within the vestibule that are built-up
when the stomata are open. Slow rates of closure in response
to decreased humidity may reflect slow rates of de-gassing of
the vestibule. Additional functional studies on the regulation
of non-steady-state gas-exchange in more basal angiosperms,
taking into account responses to natural light/humidity
regimes in relation to epidermal anatomy, would be highly
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informative. In applying these physiological responses to early

angiosperms, more work will be needed to understand the
types of light environments that early angiosperms may
have occupied in the Early Cretaceous forests because forest
canopies then were conifer-dominated. Currently, few comparative datasets are available, but light environments from
temperate podocarp forests of New Zealand appear broadly
similar in sunfleck characteristics to angiosperm forests
(McDonald & Norton, 1992).
Water lily leaves, in contrast, are specialized for an amphibious life, with several traits associated with photosynthesis
underwater and opportunistic gas-exchange in floating leaves
exposed to air. Features of water lily leaves increasing aqueous
carbon uptake include finely dissected (Cabomba) and ruffled
leaf blades (e.g. Barclaya, Ondinea, Nuphar), which probably
decrease leaf boundary layer thickness and the widespread
absences of cuticle, stomata and intercellular air-spaces
(Sculthorpe, 1967; Williamson et al., 1989; Williamson &
Schneider, 1993). Photosynthetic physiologies of floating
lily pad and emergent leaves of many Nymphaeales taxa also
differ considerably from terrestrial basal angiosperms, with
evolution of much greater leaf photosynthesis and multistoried palisade mesophyll tissue (Feild et al., 2004). The
development of palisade cells and high photosynthetic rates
may be correlated traits in water lilies because the tubular
shape of palisade cells enhances the penetration efficiency of
direct (collimated) sunlight into the leaf (Smith et al., 1997).
Regulation of stomatal aperture is also different in water lily
leaves compared with terrestrial basal angiosperms (Feild
et al., 2003b). Stomata of Nymphaea and Nuphar were claimed
to remain permanently open, owing to the absence of a
substomatal cavity, which is required to allow subsidiary
cells to bend (Brewer & Smith, 1995). Consistent with leaf
anatomy, Brewer and Smith (1995) found that leaf stomatal
conductances of floating leaves of a temperate water lily,
Nuphar polysepalum, did not respond to diurnal changes in
leaf-to-air vapor pressure deficit, light intensity and temperature responses consistent with occurrence in habitats with
unlimited water (Brewer & Smith, 1995).
At present, the fossil evidence for early angiosperm leaf
function consists mainly of leaf form, cuticular morphology
and stomatal architecture. However, these features have not
yet been extensively analysed for their ecophysiological significance. Nonetheless, it is clear that Early Cretaceous leaves
share a variety of features with living ANITA grade angiosperms.
For example, angiosperm cuticles from zone I of the Potomac
Group (Upchurch, 1984) are typically thick and possess
striated surfaces, highly variable subsidiary cell arrangements,
and large-sized stomata (i.e. stomata longer than 30 m) that
are concealed by cuticular vestibules. All of these features are
observed in Amborella, Austrobaileya, Illicium, Schisandraceae,
Trimenia and some Chloranthaceae cuticles, which suggest
wet understory adaptation (Fig. 4; Bailey & Nast, 1948;
Bailey & Swamy, 1948, 1949; Upchurch, 1984; Kong, 2001;
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Feild et al., 2003b; Oh et al., 2003). Others have interpreted

the stomatal protection and thickened cuticles in zone I
leaves as potentially water-conserving xeromorphic features
(Upchurch, 1984). Yet, paleoclimatic models suggest that the
Potomac Group climate was moist and subtropical (Beerling
& Woodward, 2001), and that thick cuticles are not a secure
indicator of high drought tolerance (Feild et al., 2003b).
Alternatively, these cuticular features may act as compensating
features (by reducing maximum leaf water loss rates) for physiological drought imposed at the leaf level poor hydraulics
of leaf veins/stem xylem in early angiosperms (Doyle et al.,
1982; McElwain et al., 2005). However, this explanation
seems unlikely because xylem hydraulic capacities are not
exceptionally low among extant basal angiosperms that possess
a similar leaf anatomy and occur in wet habitats (Fig. 2) (Feild
et al., 2000, 2001, 2003b).
3. Xylem function
Among the vegetative features of flowering plants, origin of
the angiosperm vessel from single-celled tracheids has long
been viewed as a pivotal innovation (for a review, see Feild,
2004). In terms of xylem conducting efficiency, angiosperm
vessels can dramatically increase the amount of water transported
through a vascular network under a given pressure gradient in
comparison with a similarly sized hydraulic system composed
of tracheids (Sperry, 2003). This is because evolution of
vessels, which are functionally multicellular, allows for the
formation of considerably longer hydraulic compartment lengths
(as short as 1 cm to up to 25 m in length), and therefore less
frequent crossing of resistive pit membranes during water flow
as compared with shorter tracheids (0.10.7 cm long) (Sperry,
2003; Feild, 2004; Sperry & Hacke, 2004). The individual
cells comprising a vessel can be larger in diameter than
tracheids, which greatly increases hydraulic flow (i.e. flow
through ideal capillaries increases to the fourth power of the
radius) (Sperry, 2003; Sperry & Hacke, 2004). Taking greater
hydraulic volume and diameter into account, vessels permit
greater potential hydraulic conductivity per unit conduit area
than a tracheid-based transport system. Indeed, stems of
vessel-bearing angiosperms from a variety of habitats generally
possess greater xylem hydraulic capacity, expressed in terms of
hydraulic flow relative to the amount of cross-sectional area of
xylem invested (sapwood-specific hydraulic conductivity),
than conifers and vesselless angiosperms (Brodribb & Feild,
2000; Sperry, 2003). Although many tracheid-bearing species
are capable of achieving similar or greater stem/root xylem
hydraulic capacities on a leaf area basis (i.e. similar leaf specific
hydraulic conductivities, kL, see Brodribb & Feild, 2000), the
advantage of vessels is in maintaining these conductivities
with less total investment in wood required to support a given
flow rate and leaf stomatal conductance (Sperry, 2003).
Although the xylem of Amborella is composed entirely of
tracheids (Bailey & Swamy, 1948; Feild et al., 2000), it is
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unclear if the first angiosperms were vesselless or vesselbearing because the ancestral state for extant angiosperms as a
whole is uncertain under the three phylogenetic hypotheses
(Fig. 5). An equivocal ancestral state results from the fact that
Nymphaeales, which lack secondary xylem and possess perforated tracheary elements in the primary xylem (thus vessels,
but clearly of a different developmental origin than those of
woody angiosperms), and vessel-bearing Austrobaileyales
diverge immediately above Amborella (Fig. 6). The ancestral
state remains uncertain even if Amborella is linked to Nymphaeales (reconstruction not shown). It also unclear what vascular character state should be used for Archaefructus because
Archaefructus is represented by compression fossils, which
have not yielded cellular details of the vascular system (Sun
et al., 1998, 2002).
Comparative anatomical studies (for a review, see Carlquist
& Schneider, 2002) reveal that the extant basal angiosperm
flora exhibits a continuum of xylem morphologies, from
vesselless to large diameter vessels with simple perforations. For
instance, some vessels in basal angiosperms are relatively wide,
but very short (13 mm long), whereas other can be composed of narrow elements that form long (up to 15 cm) and
potentially wide multicellular hydraulic compartments
(Feild, 2004). Functional studies of basal angiosperm xylem
(Brodribb & Feild, 2000; Feild et al., 2000, 2001, 2003b)
performance show that hydraulic efficiencies range from values
on par with vesselless conifers, such as in Amborella, to capacities on the low end of temperate/tropical eudicot trees and
shrubs (Brodribb & Feild, 2000; Feild et al., 2000, 2003b).
In addition, increasing stem hydraulic efficiency seems to
be associated with tolerance to greater sunlight (Feild, 2004).
This fortunate condition may allow the piecing together of
how different patterns of vessel development specifically
impact functional ability to inhabit different light environments. A blurred distinction between vessels and tracheids in
extant basal angiosperms also suggests that vessel origin does
bring about an immediate dramatic functional shift in
hydraulic efficiency because hydraulic conductivities of some
ANITA grade and Chloranthaceae members are similar to
vesselless Amborella (such as Illicium, Sarcandra, Chloranthus
and a few Ascarina species) (Feild et al., 2000, 2003a).
Instead, vessel origin appears to allow for the exploration of a
new morphospace of xylem hydraulic design, with some of
these experiments associated with the evolution of greater
hydraulic efficiency involving subtle fine-tuning of vessel
structure, including increases in conduit shape as well as
pitting and perforation plate structure.
The xylem hydraulics of the vascular systems of Nymphaeales require future experimental investigation. The high
transpiration rates achieved by floating leaves of Nuphar
(Brewer & Smith, 1995) suggest that high xylem hydraulic
capacity may characterize water lily vascular systems. However, the water-conducting vascular system is dramatically
reduced in many Nymphaeales (Schneider & Williamson,
1993; Williamson & Schneider, 1993) in consisting of

a few protoxylem/metaxylem vascular bundles with small
diameter tracheary elements. The large, mega-porous
canals in the protoxylem of water lily stems and leaves are
likely gas-filled and are involved in the downward transport
of oxygen to the root system and venting of carbon dioxide
and methane (Dacey, 1980). Another possible explanation
for the high transpiration rates of floating leaves is that
water supplies are locally delivered rather than transported
over long distances from root to shoot. For example, petioles
and the lower epidermis of floating leaves of Nymphaea
possess abundant glands (hydopotes) that actively take up
ions from aqueous solutions (Sculthorpe, 1967). Perhaps
these glands act at the primary sources of transpired water in
water lily leaves.
Unfortunately, the Early Cretaceous fossil record is depauperate in angiosperm wood, a pattern that has often been
mentioned as negative evidence for the hypothesis that first
angiosperms were herbaceous (Taylor & Hickey, 1996). Currently, it is unclear if this pattern is real or if it results from a
taphonomic bias in the fossil record (Behrensmeyer et al.,
2000). In this regard, decomposition studies on the wood of
ANITA taxa would be informative since their low density and
lack of resins may decrease their likelihood of preservation.
Until suitable wood fossils can be securely identified as
angiospermous, it will be difficult to test patterns of xylem
structure/function evolution in basal angiosperms using the
fossil record.
4. Photosensory physiology and seed germination
ecology: a common ecophysiological thread?
With respect to optical cues received during seed germination,
the two ecological models for early angiosperms appear to be
similar (Feild et al., 2003b; Mathews et al., 2003). Although
more specific information on seedling light environments is
critically needed, seedling recruitment of most ANITA plants
occurs under low and/or far-red enriched light habitats, such
as in deep water pond sediments or in disturbed soil of
microsites in forest understories (Smits et al., 1990; BarratSegretain, 1996; Feild et al., 2004). Consequently, Mathews
et al. (2003) have suggested that the evolution of traits
enabling seeds to sense and respond to small and transient
variations in light quantity, and to the spectral composition
in a shady environment, may have been crucial for the initial
establishment of angiosperms.
Among the possible features, evolution in the form
and function of phytochromes photoreceptors (which are
chromophore-bearing proteins that transduce variations in
ambient light conditions into a diverse set of physiological
responses) (Smith, 2000) may prove to be a significant piece
of the puzzle. Based on the phylogeny of seed plant phytochromes, there is evidence that both gene and functional
diversification occurred very early in the history of
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Fig. 5 Parsimony distribution of xylem vessel anatomy among extant basal angiosperms. Hypothesis (a) is based on the combined molecular/
morphology presented by Doyle and Endress (2000), with the resolution of relations in basal eudicots, Nymphaeales, and monocots based on
the molecular studies of Kim et al. (2004), Les et al. (1999) and Tamura et al. (2004), respectively. Hypothesis (b) is based on the backbone of
the matK consensus tree provided by Hilu et al. (2003) with eudicot, monocot, and Nymphaeales relations expanded as hypothesis (a).
Hypothesis (c) is based on the backbone molecular tree of Zanis et al. (2002).
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Fig. 6 Parsimony distribution of cambium morphology among extant basal angiosperms. Hypothesis (a) is based on the combined molecular/
morphology presented by Doyle and Endress (2000), with the resolution of relations in basal eudicots, Nymphaeales, and monocots based on
the molecular studies of Kim et al. (2004), Les et al. (1999) and Tamura et al. (2004), respectively. Hypothesis (b) is based on the backbone of
the matK consensus tree provided by Hilu et al. (2003) with eudicot, monocot, and Nymphaeales relations expanded as hypothesis (a).
Hypothesis (c) is based on the backbone molecular tree of Zanis et al. (2002). Extensive cambial development refers to wood production
accruing over several years, as compared to herbs that develop secondary xylem over less than 12 yr.
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angiosperms, involving two phytochromes that play a critical

role in germination and early seedling development under
shade cast by plant canopies. For example, the PHYB lineage,
which encodes the principal mediator of shade avoidance,
split into two lineages some time after the origin of water lilies
but before the origin of Austrobaileyales (S. Mathews, pers.
comm., 2004). Also, the PHYA lineage, which encodes the
principal mediator of very low fluence responses (VLFR) and
responses to far-red light, apparently was subject to an episode
of positive selection (Mathews et al., 2003). Shade avoidance
allows angiosperms to detect and respond to neighboring
vegetation by enhancing elongation growth and accelerating
shoot development. Although shade avoidance is not endemic
to angiosperms (Warrington et al., 1988), its adaptive significance has been tested in angiosperms (Schmitt et al., 1995),
and diversification in the genes acting in shade avoidance may
have been advantageous. Conversely, the VLFR and the farred high irradiance response (FR-HIR) may be important in
allowing shade tolerant angiosperms to germinate and deetiolate in dimly lit environments and to counteract early
shade avoidance responses that could be counterproductive
for young seedlings (Mathews et al., 2003). Outside of
angiosperms, FR-HIRs are rudimentary (Burgin et al., 1999;
Christensen et al., 2002), and VLFRs have not been documented. For this reason, Mathews et al. (2003) suggested that
innovation in phyA, the photoreceptor that mediates these
responses, may have enhanced the ability of early angiosperms
to colonize the forest understory. However, much more work
is needed on seedling responses to basal angiosperms to
controlled light environments to see how they compare to
eudicot and monocot model plant systems (i.e. Arabidopsis
and Oryza) as well as other seed plant lineages (Mathews et al.,
2003).
Little is known about the phylogeny and function of other
photoreceptors that influence seedling development, such as the
blue light receptors, cryptochrome and phototropin, in extant
basal angiosperms. However, two forms of each of these photoreceptors occur in Arabidopsis: one that is responsive to high
light intensity and one that is responsive to low light intensity
(Briggs & Christie, 2002). If this condition originated in the
earliest angiosperms, innovation in the blue light receptors
that play roles in seedling de-etiolation (cryptochrome) and
directional responses to light (phototropin), may also have
contributed to the establishment of early angiosperms in the
forest understory (Liscum et al., 2003).
V. The ecology of angiosperm diversification:

gaining a roothold and subsequent
diversification
When angiosperms first appear in the fossil record during the
Berriasian (i.e. based on pollen) (Doyle, 1983; Hughes &
MacDougall, 1987), they are represented by only a few species
and are of very low abundance. Not until the Aptian and
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Albian, some 30 Myr later, do flowering plants become

significant players in the ecosystems they inhabit (Lupia et al.,
1999). Darwin (1859) blamed this pattern on the paucity of
the fossil record. Today, with intense effort focused on finding
the first fossil angiosperm (e.g. Sun et al., 1998; Friis et al.,
2001) and microfossil as well as macrofossil patterns of their
diversification (Lidgard & Crane, 1990; Lupia et al., 1999),
this argument no longer seems credible. Clearly, the processes
that promoted the origin of the lineage are largely decoupled
from those that allowed early angiosperms to successfully
invade established Mesozoic plant communities and to
speciate. What were these processes and how did they play out
on the Cretaceous stage?
1. Origin, invasion and diversification in three acts
The origin of the flowering plants remains as much an
abominable mystery today as it was when Darwin ruminated
on the topic to his friend J. D. Hooker in July 1879. The fossil
record of the earliest angiosperms is indeed sparse, with the
earliest undisputed records simply a few grains of pollen
(Doyle, 1983). Some pre-Cretaceous macrofossils suggest
angiospermy (e.g. Sanmiguelia from the Triassic) (Cornet
& Habib, 1992), but these are commonly poorly preserved
or can be linked to other Mesozoic seed plant groups (e.g.
Furcula from Triassic) (Scott et al., 1960).
The search for the earliest angiosperm if such a quest can
be undertaken may be complicated by several factors. First,
the environments in which the early flowering plants likely
grew seldom leave a good fossil record. The montane forests
favored by modern ANITA lineages are sites of erosion, not
sedimentary deposition. Forests associated with lowland rivers
can leave excellent records, but few such systems have been
extensively studied from the Jurassic and Cretaceous. Freshwater lakes are one exception. These systems offer excellent
preservations and have been extensively studied because of
their extraordinary vertebrate fossil records (e.g. the Yixian
Formation of China from which the renowned feathered
dinosaurs have been uncovered) (Qiang et al., 1998). Second,
many of the worlds latest Jurassic and Early Cretaceous
terrestrial rocks have yet to be extensively studied. Deposits
in the Middle East, China and New Zealand hold promise
for future fieldwork.
Third, the interpretation of many fossils from this key
interval has been complicated by our preconceptions about
the form of the original angiosperm. We expect the first
angiosperm to have the recognizable constellation of synapomorphies associated with the crown group. This may explain
why pollen has been so useful in documenting the first
appearance of angiosperm. The tectate collumelate form of
the angiosperm pollen wall is a unique trait that appears early
in the history of the lineage. Macrofossils have been more
challenging. In the modern world, flowers are easy to recognize. However, many Mesozoic lineages (e.g. Sanmiguelia,
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Cornet & Habib, 1992; Pentoxylon/Carnoconites, Bose et al.,

1985; Cycadeoidea, Crepet, 1974; Williamsonia/Weltrichia,
Delevoryas, 1991) produced flower-like reproductive structures. Net-veined leaves, another feature of angiospermy, also
appeared in Gnetum and a variety of late Paleozoic seed fern
foliage including Linopteris, Reticulopteris and Lonchopteris
(Taylor & Taylor, 1993). Syndetocheilic stomata (guard and
subsidiary cells originate from one epidermal cell) characterize
angiosperms, but also the Bennettitales and possibly other
Mesozoic seed ferns. Xylem vessels also present problems.
Some basal angiosperms lack vessels (e.g. Amborella), whereas
some nonangiosperm seed plants possess them (i.e. Gnetales,
gigantopterids). However, vessels in nonangiosperm lineages
differ subtly in structure and ontogeny (for a review, see Feild,
2004). Even the hallmarks of flowering plants ovules
surrounded by sporophytic tissue (closed carpel) and
pseudo-double fertilization appear in other lineages (e.g.
Caytoniales, Dilcher, 1979 and Gnetales, Friedman, 1992,
respectively). Such widespread convergence among cooccurring Mesozoic lineages and the early angiosperms that
replaced them likely points toward environmental factors
favoring such traits (Feild, 2004). However, until this record
is reanalysed with an eye toward convergence, and until the
origin of the features can be timed and linked to local
environmental conditions, rather than the unique superiority
of angiosperms, such factors will remain elusive. In the end,
conventional wisdom in paleontology can be shattered with a
single stroke of the rock hammer and a lucky find.
The low species richness and ecological similarity among
extant ANITA lineages, combined with the rarity of
angiosperm fossils before the BarremianAptian, suggest that
the traits promoting angiosperm diversification arose well
after the origin of the lineage. Thus, the dark and disturbed
ecology did not trigger the angiosperms mid-Cretaceous
radiation. Instead, this lifestyle may have been a way for
angiosperms to gain a roothold in well-established Mesozoic
plant communities. Architectural flexibility and dispersion of
meristems may have allowed early angiosperms to flourish in
disturbed understory habitats. Multi-stemmed growth, characterized by large bud banks for shoot iteration following
damage, allows long-term persistence in habitats that experience a wide variety of disturbances. This contrasts with modern understory cycads that recover slowly from disturbance
and are vulnerable to loss of their fewer apical meristems.
With the evolution of vessels, carbon costs for shoot and root
reiteration may have decreased, making early angiosperms
even more efficient in their recovery from disturbance under
low light. In addition, rhizomatous and lianoid habits, and
extensive vegetative propagation increase the discovery and
exploitation of ephemeral, resource-rich patches in the forest
understory. In contrast, the squat, unbranched, sparsely
leaved forms of many Bennettitales (e.g. Cycadeoidea and
Williamsonia) and cycads were probably less able to use patchy
understory resources. If Early Cretaceous forests experienced
significant increases in disturbance frequency or intensity, dark

and disturbed angiosperms may have seized the opportunity
to invade.
If the dark and disturbed ecology did not promote
explosive diversification, what did? Most researchers have
focused on single traits when evaluating the key innovations
commonly associated with spurring increases in speciation
rate (e.g. Sanderson & Donoghue, 1994; Donoghue, 2004).
However, it may be combinations of traits, occurring
together, that spurred angiosperm radiation into a wide range
of new habitats. The combination of vessels, reticulate leaf
venation and a relatively more flexible photosynthetic mechanism needed to handle subcanopy sun flecks rather than
any of these traits alone may have formed the trait complex
that prompted angiosperms to move into new habitats and
diversify. None of these functional traits were necessarily
unique to Mesozoic angiosperms, but their combination was.
Modifications to vessels (e.g. longer functional length
produced by simple perforation plates) increased hydraulic
conductivity. This vascular system, combined with increasing
vein density in leaves, could support the higher transpiration
rates needed to control thermal load in sunny environments,
which, in turn, allowed the evolution of higher photosynthetic rate. Thus, co-occurrence of vessels, reticulate venation
in leaves and high photosynthetic rates may have allowed
Aptian angiosperms to move into sunnier and dryer habitats.
In turn, new habitats exposed angiosperms to novel pollination, predation and dispersal pressures that could set off
explosive diversification. While testable, this hypothesis
awaits a more detailed analysis of relationships among
angiosperms at the cusp of the mid-Cretaceous radiation.
This, in turn, awaits further fossil discoveries and advances in
techniques for analysing morphological data in a phylogenetic
context.
2. Aquatic origin or early aquatic invasion?
Although some phylogenetic studies have suggested an
aquatic ancestor for angiosperms, this seems unlikely from
a variety of ecological and developmental perspectives.
First, once submerged, the angiosperm lineage would have
faced significant barriers to subsequent speciation and
morphological innovation. Fewer than two per cent of
living angiosperm species are aquatic and many of these represent monotypic genera (Cook, 1999). This suggests that
diversification is curtailed in lineages that move from land to
water (Cook, 1999; Donoghue, 2004). This claim requires
additional phylogenetic scrutiny, however, because some
aquatic lineages are more speciose than their terrestrial sistergroups (e.g. Utricularia).
Second, an aquatic lifestyle imposes radically different
biophysical and biomechanical demands on plants compared
with life in air. The diffusivity of O2 and CO2 in water is substantially lower than that in air. A thousand-fold increase in
Tansley review
fluid density also means that aquatic plants operate with

greater diffusion constraints and experience predominantly
tensile forces of waves and currents rather than the compressive effects of gravity (Pedersen, 1993; Niklas, 1997). Whereas
the shift to an aquatic environment would initially favor the
exploration of a new set of vegetative designs in response to a
novel environment, extant angiosperm aquatics show that
these experiments leave little room for morphological diversification. A strong convergence in form and function among
extant aquatic angiosperms from disparate clades suggests that
only a narrow range of solutions to the special problems of
aquatic life is contained within the angiosperm developmental repertoire (Sculthorpe, 1967; Cook, 1999).
Third, once aquatic morphologies are adopted, the lineages
seem unlikely to reinvade land. Out of approximately 200
terrestrial-to-aquatic transitions in flowering plants (Cook,
1999), monocots, which were either ancestrally aquatic or
originated with a high physiological dependence on water as
hyperhydates (i.e. lake-margin plants that grow in watersaturated soils or in the water itself with emergent leaves and
flowers based on Acorus and the Alismatales as early diverging
lines) (Les & Schneider, 1995; Tamura et al., 2004; S. Graham,
pers. comm., 2004), appear to be the only group that reevolved numerous terrestrial forms (Fig. 6; Les & Schneider,
1995). This one-way pattern likely stems from a difficulty in
re-acquiring key traits useful for life on land. For example,
water lilies, and most likely Archaefructus, lack a cambium. An
origin for angiosperms among these lineages would require
three to five re-inventions of the simple bifacial cambium
observed in most lignophytes (i.e. seed plant out-groups) and
many angiosperms (Fig. 6). Considering angiosperms as a
whole, the cambium seems easy to lose but harder (if not
impossible) to re-evolve without a distinctly different structure and function. For instance, monocots have evolved a
novel type of unifacial cambium (etagen cambium) (Tomlinson,
1995). This cambium is situated near the periphery of the
stem, and produces derivatives that differentiate into new
vascular bundles scattered in the stem, each containing both
xylem and phloem (Tomlinson, 1995). To date, no such tell-tale
differences in cambium structure or development have
emerged among the woody basal angiosperms. Further comparative data on the development and genomes of these lineages
might help to close the book on the aquatic origin hypothesis.
If angiosperms did not originate in aquatic habitats, then the
lineage certainly explored wetlands early in its history. Beyond
the all-aquatic Nymphaeales, ancestrally aquatic monocots,
Nelumbo (2 species, sister-group to Platanus), and some Ranunculus are other examples of near-basal aquatic angiosperms.
Ceratophyllum (6 species of rootless submersed herbs), if unrelated to monocots, may represent another aquatic experiment.
What fostered the early aquatic exploration? First, some
early angiosperm lineages may have escaped crowded habitats
on land by evolving toward water. This process has been
suggested as justification for an aquatic origin (Sargant, 1908;
Research
Arber, 1920; Sun et al., 2002). However, it may be more

logical in this context because an early aquatic invasion is consistent with Early Cretaceous diversification among both
terrestrial and aquatic lineages without requiring the reacquisition of traits, such as a bifacial cambium, lost in the transition to a submerged lifestyle. Second, a rich exaptive trait pool
(sensu Gould, 2002, traits that can be co-opted for new functional roles) inherited from ancestors growing in the disturbed
forest understory may have primed lineages for the aquatic
transition. For example, phytochrome mechanisms necessary
for germination in low light and root pressure with hydathodes needed for submerged transpiration (Pedersen, 1993)
were already in place in the common ancestor of extant
angiosperms (Feild et al., 2003a; Mathews et al., 2003).
Third, the aquatic transition may have allowed early lineages
to explore sunny environments without extensive modifications to water-use physiology because they were already accustomed to shady environments where water is not limiting.
Thus, early angiosperms could move to open water by upregulating photosynthesis and losing the cambium.
VI. The environmental context of early

angiosperm evolution
The origin of new traits and unique trait combinations in
newly branched clades have little long-term evolutionary
significance in the absence of environmental circumstances
that allow novel clades to become ecologically important and
diversify (Knoll & Carroll, 1999). Such key environmental
opportunities combine with traits key innovations to give
rise to significant evolutionary radiations (for a recent review,
see Donoghue, 2004). Similarly, environmental opportunities
are essential to allow a new clade, such as the Early Cretaceous
angiosperms, to gain a roothold in established plant
communities of the time (von Hagen & Kadereit, 2003). We
can consider such environmental opportunities at two spatial
and temporal scales. Forces such as tectonics, changes in
atmospheric composition and climate act at regional to global
scales and over intervals of tens of thousands to millions of
years. Such large-scale and long-term changes alter the abiotic
context in which plant communities live. In contrast, a variety
of biotic factors such as pollination, dispersal and disturbance
act at local spatial scales and over very short time spans. Both
small and large-scale environmental changes characterized the
Early Cretaceous and formed the environmental context for
the angiosperm invasion.
1. Large-scale abiotic factors
The world into which angiosperms emerged has traditionally
been assumed to be uniformly warm and equable (Brooks,
1906; Schwarzbach, 1963). However, reports of short-term
global seal-level fluctuations (Abreu et al., 1998), temperature
inference from oxygen isotope data (Hochuli et al., 1999;
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Veizer et al., 2000) and sediments related to glaciation

(Frakes et al., 1992; Alley & Frakes, 2003) suggest that the
Early Cretaceous may have been cooler and more climatically
variable than previously believed. For example, detailed
analyses of phytogeography and the distribution of climate
sensitive sediments show significant spatial and temporal
climate variability (Rees et al., 2002). Rees et al. combined
detailed reconstructions of tectonic plate configurations
with the distribution of climate sensitive sediments (e.g. coal
and evaporates) and fossil floras to reconstruct the global
distribution of ancient climates for the latest Jurassic. During
this interval highlands in equatorial Gondwana, to which
some of the earliest angiosperm pollen fossil have been
linked (Brenner, 1996), experienced cool (Veizer et al., 2000),
summer-wet seasonal (Rees et al., 2002) climates. This
climate mode continued into the Berriasian and Valanginian
(Krassilov, 1973; Allen et al., 1998; Eberth et al., 2001).
Hauterivian time witnessed a brief but dramatic cooling that
is observed in both low and mid latitudes (Price et al., 2000;
Veizer et al., 2000). Another short-lived climate perturbation
coincided with the Early Aptian oceanic anoxic event
(OAE) ( Jenkyns, 1980; Bralower et al., 2002a). OAEs are of
relatively short duration (lasting 0.51 Myr) and produce
major changes in marine faunas (Bralower et al., 2002a).
Calculations by Beerling et al. (2002) suggest that a
substantial release of methane clatharate, likely due to a
changing tectonic regime, resulted in a short-lived global
temperature increase of up to 3C. Methane hydrate occurs
where conditions of temperature and pressure allow methane
produced by sedimentary bacteria to become trapped in the
crystal lattice of ice (Haq, 1998). Once thought to occur only
in deep space, extensive deposits have been found on Earths
continental shelves (Dickens, 2001). When temperature and
pressure conditions change, large reservoirs of gas hydrate can
melt, releasing methane into the water column, where it is
oxidized to produce CO2 (Dickens et al., 1997; Haq, 1998;
Dickens, 2001; Jahren et al., 2001). This sudden release of
CO2 has been linked to rapid climate change (Dickens et al.,
1997; Haq, 1998), periods of ocean anoxia and mass
extinction ( Jahren et al., 2001; de Wit et al., 2002). The
Cretaceous greenhouse began during the late Aptian and
Albian periods and prevailed through the end of the
Cretaceous (Barron, 1983; Frakes & Francis, 1988; Veizer
et al., 2000; Huber et al., 2002). During the greenhouse
interval, global climate varied from warm in the late Albian
through to the late Cenomanian to hot during the latest
Cenomanian through early Campanian, with cooling toward
the end of the period (Huber et al., 2002). Although the
magnitude of climate variation estimated from marine oxygen
isotope data (e.g. Huber et al., 2002) has been questioned
because of uncertainties in paleosalinity and assumptions
about the presence or absence of glacial ice (Fassell &
Bralower, 1999), data from fossil floras have produced similar
patterns (Frakes, 1999), which lends support to the trends.
Proposing a direct link between climate change and either

the origin or early radiation of angiosperms seems premature.
However, it is interesting to note that the initial radiation of
angiosperms occurred during Aptian transition between
icehouse and greenhouse conditions (Jahren et al., 2001). In the
early Aptian, carbon and oxygen isotope data show relatively
low temperatures and high marine productivity, suggesting
humid conditions (Hochuli et al., 1999), although regional
variability in rainfall would be predicted then as today. Warming began in the latest Aptian and continued through the
Albian. Oxygen isotope values in terrestrial calcite cement
show an increase of approximately 10C in the average temperature of rainwater from the mid Aptian to late Albian
at high southern latitudes (Ferguson et al., 1999). Cooling
began following the AlbianCenomanian boundary, with
dramatic warming beginning at CenomanianTuronian boundary
time (Frakes, 1999).
Clearly, we can no longer assume a stable climate during
the interval of angiosperm origin and early radiation. Thus,
we cannot dismiss climate as a player in the angiosperm ecological incursion. However, a mechanistic hypothesis linking
warming and/or fluctuating climate in the mid Cretaceous to
angiosperms infiltration of pre-existing plant communities
has not emerged. Changing climate may have disrupted existing plant communities, perhaps causing extinctions, and
allowing the new lineage to gain a roothold. We know that
plant species associations become flexible and are prone to
change during times of climatic flux (e.g. Coleman et al.,
2003; Mueller et al., 2003; Schonswetter et al., 2003;
McKinnon et al., 2004). However, a tightly coupled record of
mid Cretaceous climate and floristic change would be necessary
to test such a hypothesis.
To complicate the picture further, climate change in the
mid Cretaceous appears to be a consequence of changes
in global tectonics, which had other effects as well. The
Cretaceous warming events described above have been linked
to increased atmospheric CO2 (Arthur et al., 1985; Larson,
1991) produced by elevated rates of seafloor spreading
(Tarduno et al., 1991; Bralower et al., 2002a; Jenkyns, 2003;
Poulsen et al., 2003) beginning in the Aptian. Beyond influencing climate, CO2 flux may have had direct effects on the
biosphere. For example, the Jurassic and Cretaceous are
characterized by at least seven episodes of increased organic
carbon burial in the worlds oceans and widespread dysoxia in
the deep ocean (Jenkyns, 1980; Bralower et al., 2002a). Some
OAEs have been linked to the release and oxidation of
methane hydrate trapped on continental shelves (Beerling
et al., 2002; Jahren et al., 2001 submitted). Others have been
linked directly to volcanic CO2 (Jenkyns, 2003). Whatever
the cause, these events produce rapid and significant (up to
600 ppmv) increases in atmospheric CO2 (Jahren et al., 2001;
Beerling et al., 2002).
In addition to an impact on global climate, changes in
atmospheric composition may have had direct effects on plant
Tansley review
communities. Nonetheless, there is considerable debate over

the effects such changes might have had. Data from modern
plant communities show that significant changes in the
abundance of CO2 alter competitive interactions among cooccurring species and can lead to changes in species competition and relative abundance within communities (Bazzaz &
Miao, 1993). Some experimental results (Bazzaz et al., 1990) and
modeling (Bolker et al., 1995) suggest that angiosperms may
respond more vigorously to increasing CO2 than do conifers,
resulting in changes in forest succession and community
composition over time. If such conclusions can be applied
to the Early Cretaceous, rapid increases in CO2 such as
those observed in association with methane hydrate release
( Jahren et al., 2000) might have facilitated penetration of
angiosperms into established Mesozoic plant communities.
However, all of the experimental studies are based on the
highly derived physiology of modern angiosperms (i.e. exclusively temperate eudicots) and conifers (Pinaceae). More work
on modern nonangiosperm seed plants and a better understanding of the physiology of Cretaceous angiosperms is needed
to further test this hypothesis. Others have suggested that falling atmospheric CO2 levels during the Jurassic and Cretaceous
(Ekart et al., 1999; Berner & Kothavala, 2001; Rothman, 2001)
may have favored angiosperms (McElwain et al., 2005).
McElwain et al. noted a correlation between changes in plant
communities and Early Cretaceous declining CO2, predicted
by global carbon models. They noted that increases in
angiosperm diversity and relative abundance occurred during
fall of CO2 concentrations, and argue that CO2 limitation
would favor more efficient angiosperm physiologies, through
evolution of xylem vessels, net-veined leaves and highly
responsive stomatal opening/closure kinetics, over less
adaptively responsive seed plant and fern lineages. Currently
there is considerable debate in the geologic community over
the quantitative accuracy of the wide range of models and
proxies used to deduce patterns in pCO2 change through time
(e.g. Boucot et al., 2004). Until there is greater agreement on
the patterns and magnitude of pCO2 change during the critical
interval, and until we understand more about the physiological
responses of basal angiosperms and nonangiosperm seed
plants to changing CO2, mechanistic arguments about the
role of atmospheric composition on the early evolution of the
lineage remain unsatisfying
Both of these arguments suggest an underlying physiological superiority of angiosperms compared to the other
Mesozoic seed plant lineages with which they shared the Early
Cretaceous landscape. This assumption has haunted discussions about the early evolution of flowering plants for decades
(Stebbins, 1974, 1981; Regal, 1977; Burger, 1981; Bond,
1989). However, such assumptions are based on modern,
derived physiologies for both angiosperms and conifers. How
relevant were such distinctions in Early Cretaceous communities? Until now, such questions have been unanswerable.
However, the widespread use of carbon isotope discrimina-
Research
tion to infer competitive ability in crop (Read et al., 1991;

Condon et al., 1993) and wild (Toft et al., 1989) opens a new
avenue test the hypothesis of angiosperm competitive superiority. Current agricultural applications use carbon isotope
discrimination to calculate water use efficiency (WUE), which,
in turn, is a proxy for the efficiency of photosynthetic carbon
fixation (Read et al., 1991; Condon et al., 1993). Once the
constraints of diagenetic alteration of the carbon isotopic
signature of fossil plant tissue are understood (Tu et al., 2004.),
such approaches could be applied to seriate the members of
ancient plant communities according to carbon fixation
efficiency. This might allow us to finally determine whether
angiosperm dominance was an inevitable legacy of the
lineages origin.
2. Small-scale biotic factors
Insects, particularly pollinators, have long been recognized as
essential partners in angiosperm evolution (Crepet & Friis,
1987; Crepet, 1996), primarily because differentiation of
pollination syndromes has played such an important role
in the diversification of core angiosperm lineages. Many
basal angiosperms are pollinated primarily by insects (water
lilies, Austrobaileya, Chloranthus, Illicium, Sarcandra) or by
a combination of insects and wind (Amborella, Trimenia,
Hedyosmum), suggesting that an insect or combination
syndrome for ancestral angiosperms (Luo & Li, 1999; Tosaki
et al., 2001; Bernhardt et al., 2003; Thien et al., 2003). Insect
pollination has been inferred for most of the early
angiosperms described to date on the basis of features such as
abundant connective tissue, ethereal oil cells and valvate
anther dehiscence in stamens of Early Cretaceous flowers, as
well as the presence in the Portuguese floras of insect
coprolites consisting exclusively of angiosperm pollen (Friis
et al., 1999, 2000).
Although the radiation of angiosperms and the establishment of discrete pollination syndromes in the early Late
Cretaceous coincides with the first appearance and/or
diversification of many pollinating clades (e.g. lepidopterans,
dipterans and pollinating hymenopterans such as bees)
(Grimaldi, 1999), there is little direct evidence to suggest that
insect diversification played an important role in angiosperm
origin or early evolution (Labandiera & Sepkoski, 1993).
However, insect pollination in the earliest angiosperms may
have permitted outbreeding in isolated individuals or small
populations within Early Cretaceous forest understories.
Dinosaurs have also been promoted as evolutionary partners with angiosperms. Bakker (1978, 1986) suggested that a
transition from canopy-feeding sauropodomorph dinosaurs
(e.g. Diplodocus, Apatosaurus) in the Early Cretaceous to
ground-feeding ornithischian dinosaurs (e.g. Hypsilophodon,
Iguanodon) allowed fast-growing angiosperms to take over
forest understories as slower-growing ferns, cycads and conifers were browsed away. Wing and Tiffney (1987) elaborated
401
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Tansley review
on this idea and further suggested that bulk-feeding dinosaurs

may also have dispersed angiosperm seeds. However, Barrett
and Willis (2001) rejected a strong coevolutionary relationship between angiosperms and dinosaurs because the transition from sauropodomorph to ornithischian dinosaurs did
not match the pattern of angiosperm first appearance and
radiation in either space or time. More importantly, there is
little direct evidence that herbivorous dinosaurs preyed
heavily on angiosperms. The only Early Cretaceous (Albian)
dinosaur gut contents discovered to date are those of an
Australian ankylosaurid, Minmi, whose last meal included
seeds and foliage, some likely of angiosperms (Molnar
& Clifford, 2000). From the Late Cretaceous, suspected
stomach contents from Edmontosaurus (Krusel, 1922) and
Corythosaurus (Currie et al., 1995) suggested a mixed diet
of conifers and angiosperms. Fossil feces from the Late
Cretaceous also suggest a varied diet that included some
angiosperm material (Chin & Brassell, 1994; Rodrguez de
la Rosa et al., 1998). Thus, the limited available evidence
suggests that dinosaurs were generalist feeders, an interaction
too diffuse to produce clear coevolutionary patterns (Barrett
& Willis, 2001).
Most previous discussions of dinosaurangiosperm
interactions have focused on herbivory. However, if early
angiosperms occupied disturbed habitats in the forest understory, they may have taken advantage of habitats created by
foraging dinosaurs (Barrett & Willis, 2001). Hadrosaur footprints among tree trunk casts from the Blackhawk Formation
(Campanian) of Utah, USA (Parker & Balsley, 1980) show
that dinosaurs foraged in the forest understory. More than
simply opening the door to early angiosperm colonization of
Mesozoic plant communities, we suggest that dinosaur disturbance may have helped alter vegetation as angiosperms radiated. In the modern world, large herbivores can transform
plant communities. Forest elephants create and maintain a
distinct forest composition and structure compared to areas of
the same forest not used by the large herbivores (Eggeling,
1947; Jones, 1955; Wing & Buss, 1970; Hft & Hft, 1995;
Struhsaker et al., 1996). Elephants remake forests by creating
gaps, trampling undergrowth and selectively browsing. Seed
dispersal may also be important, but most plants dispersed
by elephants are not dependant upon this mechanism
(Hawthorn & Parren, 2000). Campbell (1991) suggested that
by increasing forest heterogeneity forest elephants may increase
plant species richness in forests; however, this hypothesis has
not been rigorously tested to date. It seems logical to speculate
that under increasing understory disturbance, plants with
abundant vegetative growth, like those of the basal
angiosperms, would be ecologically favored. Thus, disruption
of understory vegetation in the Early Cretaceous may not only
have disrupted populations of previously existing Mesozoic
plants, but may have encouraged the growth of early
angiosperms. Like many such speculations, this idea will be
difficult to test rigorously. However, it bears consideration as
new information on the ecology and timing of the Cretaceous

floral transition comes to light.
VII. Conclusions
The marriage of phylogeny and ecology has offered us a new
and concrete hypothesis on the form and function of early
angiosperms. Although this approach has moved us forward
substantially, allowing testable hypotheses to be posed, the
geologic and fossil record will be the ultimate proving ground
for these ideas. Much work remains to be done. A new,
dark and disturbed image of early angiosperms also poses
ecological questions that can be answered in the forest and
greenhouse. For example, how do living basal angiosperms
and other nonangiosperm seed plants respond to the sorts of
environmental changes proposed for the Early Cretaceous?
How do changes in atmospheric CO2 influence the
competitive interactions of these plants? Still further, can we
find traces of ancient interactions in the carbon isotopic
record of Early Cretaceous plant assemblages? A preliminary
look at the available fossil record suggests that angiosperms
evolutionary success may owe more to the fortuitous
combinations of a large repertoire of traits than to some
intrinsic morphological or physiological superiority, but this
idea awaits further testing.
Acknowledgements
We gratefully thank Michelle Bowe, Charles Davis, Sean
Graham, Sarah Mathews, Jenny McElwain, Doug and Pam
Soltis for sharing in press or submitted manuscripts on
aspects of early angiosperm evolution. We also thank Michael
Donoghue for comments on the manuscript and Sarah
Mathews for insightful discussions on photosensory evolution
in basal angiosperms. Support for this work was provided by
an NSERC operating grant to TSF.
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Author for correspondence:

Taylor S. Feild1 and Nan Crystal Arens2

Received: 2 September 2004

Previous images of early angiosperms and their habitats

III. Progress in understanding angiosperm phylogeny:

The ecology of angiosperm diversification:

VI. The environmental context of early angiosperm

accepted first appearance of flowering plants (Doyle, 1983;

New Phytologist (2005) 166: 383 408

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new environmental opportunities for these lineages during

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these trends in the Early Cretaceous fossil record, while

II. Previous images of early angiosperms and

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Although the woody magnoliids, Magnoliales and Winteraceae

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Hickey, 1992, 1996). In this model, early angiosperms were

III. Progress in understanding angiosperm

www.newphytologist.org New Phytologist (2005)

IV. Early angiosperm ecology: inferences from

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However, such phylogenetic character mapping has three

New Phytologist (2005) 166: 383408

Despite these caveats, a character-mapping approach does

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plant anchorage and resilience to traumas that break branches

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Fig. 4 Stomatal vestibules and striated

reproduction two characteristics thought to underlie

from the Kurnub Group (AptianAlbian) (Taylor et al., 2001)

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rates measured under steady-state and physiologically optimal

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informative. In applying these physiological responses to early

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Feild et al., 2003b; Oh et al., 2003). Others have interpreted

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1993; Williamson & Schneider, 1993) in consisting of

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angiosperms, involving two phytochromes that play a critical

V. The ecology of angiosperm diversification:

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Albian, some 30 Myr later, do flowering plants become

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Cornet & Habib, 1992; Pentoxylon/Carnoconites, Bose et al.,

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significant increases in disturbance frequency or intensity, dark

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fluid density also means that aquatic plants operate with

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