The Earliest Land Plants

Abstract

Considerable progress has been made in documenting evidence of very early plants starting in the basal Ordovician employing dispersed spore, phytode-bris, and mesofossil data. Macrofossil evidence is sparse until Late Silurian, but recent new data are improving our understanding of aspects of earliest plants. The considerable information about the possible source of cryp-tospores and trilete spores especially from the well-preserved mesofossils of the Late Silurian and Early Devonian is summarized. Promising avenues of research are the study of spore ultrastructure, and neo-paleo compar-isons between newly discovered resistant components of extant bryophytes and fragmentary fossil remains. Recent macrofossil discoveries in the Late Silurian advance our understanding of early events in plant evolution and raise new questions about the timing of evolution or relationships among earliest (mostly vascular) plants.

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ANRV360-ES39-22 ARI 10 October 2008 9:54
The Earliest Land Plants
Patricia G. Gensel
Department of Biology, University of North Carolina, Chapel Hill,
North Carolina 27599-3280; email: pgensel@bio.unc.edu
Annu. Rev. Ecol. Evol. Syst. 2008. 39:459–77
The Annual Review of Ecology, Evolution, and
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Key Words
embryophytes, evolution, dispersed spores, macrofossils, mesofossils
Abstract
Considerable progress has been made in documenting evidence of very early
plants starting in the basal Ordovician employing dispersed spore, phytode-
bris, and mesofossil data. Macrofossil evidence is sparse until Late Silurian,
but recent new data are improving our understanding of aspects of earliest
plants. The considerable information about the possible source of cryp-
tospores and trilete spores especially from the well-preserved mesofossils
of the Late Silurian and Early Devonian is summarized. Promising avenues
of research are the study of spore ultrastructure, and neo-paleo compar-
isons between newly discovered resistant components of extant bryophytes
and fragmentary fossil remains. Recent macrofossil discoveries in the Late
Silurian advance our understanding of early events in plant evolution and
raise new questions about the timing of evolution or relationships among
earliest (mostly vascular) plants.
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INTRODUCTION
The origin and early evolution of plants [Kingdom Plantae or Embryobiota sensu Kenrick & Crane
(1997b)] are believed to have profoundly impacted terrestrial and marine ecosystems, changing
weathering processes, aiding in soil formation, affecting both short- and long-term carbon cycling
(organic carbon burial), and thus influencing atmosphere and climate (Algeo et al. 2001; Beerling
& Berner 2005; Berner 1997, 2001; DiMichele & Hook 1992; Driese & Mora 2001; Graham
et al. 2004a,b).
Kingdom Plantae (embryophytes) includes multicellular photoautotrophs, which possess a
cellulose cell wall. Embryophytes produce a diploid embryo nourished by the parent gametophyte
for some time and resistant-walled (composed of sporopollenin) meiotic products, e.g., spores.
Extant groups of plants include the (a) haploid-dominant, nonvascular (lack lignified tracheids)
bryophytes; (b) diploid-dominant, nonseed-producing vascular plants such as ferns, lycophytes,
and horsetails, and (c) diploid-dominant, seed-bearing vascular plants such as gymnosperms and
angiosperms. Many extinct lineages have been recognized, some of which fall into these categories,
while others form separate clades (Kenrick & Crane 1997b) or are truly of uncertain affinity.
Organisms often included in the term land plant (algae, fungi, lichens) are, by definition, excluded
here, excepting perhaps charophycean green algae.
Background
Phylogenetic analyses have demonstrated monophyly of embryophytes and that charophycean
green algae (possibly Chara or Nitella) are the probable closest sister taxa (Graham 1993; Graham
& Gray 2001; Karol et al. 2001; Kenrick & Crane 1997a,b). Although controversial, liverworts are
argued to be the earliest divergent plants (Goromykin & Hellwig 2005; Kenrick 2000; Kenrick &
Crane 1997b; Nikrent et al. 2000; Qiu et al. 1998, 2006, 2007; Renzaglia et al. 2000). Relationships
of the remaining bryophyte clades are also unsettled; recently Qiu et al. (2006, 2007) conducted
multigene analyses that place hornworts as sister to vascular plants. These phylogenies suggest
that bryophytes existed earlier than vascular plants as well as suggest probable ancestral character
combinations of embryophytes (Mishler & Churchill 1984, Renzaglia et al. 2000) and aid in
considering what entities/clades to which the earliest fragmentary remains might be compared.
However, when drawing comparisons between fossils and extant forms, it is important to recognize
that ca. 470 MY separates earliest plants from their extant relatives, such that many evolutionary
changes or convergences could have occurred.
Based on current knowledge of both micro- and macrofossils, many accept that numerous
organisms occupied subaerial habitats at least since the early Cambrian, the earliest being assem-
blages of microbes, fungi, algae, and probably lichens (some of which may have formed biofilms
or microbial mats) as well as animals (Driese & Mora 2001, Retallack 2000, Shear & Selden 2001),
although additional documentation of such communities is needed. Retallack (2000) and Driese
& Mora (2001) suggest the earliest evidence of life on land is from paleosols with animal-derived,
and possible plant-derived trace fossils in the Late Ordovician. Increasingly, better developed soils
and plant traces including robust rooting structures occur in successively younger strata (Driese
& Mora 2001, Elick et al. 1998). Direct evidence of microbes (cyanobacteria) forming ground
cover is shown by Tomescu et al. (2006) via analyses of carbonized remains in Llandovery fluvial
sediments in Virginia.
The earliest undoubted plant fossils are Late Ordovician (Ashgillian), while polysporangiate
plants appear in mid-late Silurian (ca. 425 Mya) (Figure 1). Vascular plants diversified during the
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Period Epoch Stages M.Y.
Envelope-enclosed cryptospores MDT
Naked cryptospores MDT
Hilate cryptospores
Trilete spores
Tubular elements
Pseudocellular cuticle
Sporangial and probable tracheophyte cuticles
Stomata
Tracheids
Bifurcating axes, tracheophyte type
Rhyniophytoids, Rhyniopsida
Lycopsids (Baragwanathia, etc.)
Zosterophylls
Trimerophytes
Monads, dyads, tetrads
MDT
Banded tubes appear
B
Smooth tubes
S
359.2
374.5
385.3
391.8
397.5
411.2
416.0
428.2
443.7
460.9
471.8
488.3
501.0
513.0
542.0
407.0
Devonian
Ordovician
Silurian
Cambrian
Late
Middle
rian
Llandovery
Middle
Early
Wenlock
Ludlow
Pridoli
Late
Middle
Early
Furongian
Middle
Early
Paibian
Tremadocian
Arenig
Llanvirn
Darriwilian
Caradoc
Ashgill
Lochkovian
Pragian
Emsian
Eifelian
Givetian
Frasnian
Famennian
?
?
?
?
?
?
?
?
??
?
??
SB
?
?
Possible range
?
Major decline in abundance
Known range
Figure 1
Stratigraphic ranges of fossil types used in assessing early plant evolution. (Modified from Edwards 2000, 2003; see also Gensel et al.
1991, Wellman & Gray 2000). Time chart based on International Stratigraphic Chart, ICS from: Gradstein et al. 2004. “A Geological
Time Scale,” Cambridge Univ. Press.
Late Silurian–Early Devonian (ca. 418–407 Mya), via what Bateman et al. (1998) term a novelty
radiation sensu Erwin (1992)—e.g., “rapid highly divergent increases in complexity accompanied
by relatively low speciation rates” (Bateman et al. 1998, p. 283). While true to some extent, this
should be tested further as information accrues.
A long recognized discrepancy exists in the fossil record between the earliest undoubted
megafossil (Cooksonia, Ludlow) and the thirty-million-year-older microfossils representing
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probable embryophyte remains, e.g., spores or fragments of tissues (cuticle, tubes). Several lines
of investigation over the past decade support Gray’s argument (Gray 1985, 1991) that at least
some of the early microfossils represent remains of bryophytes, particularly liverworts. Affinities
of other fossil remains continue to be problematic where synapomorphies of embryophytes are
not discerned. Many diminutive plant fragments (mesofossils) of late Silurian/earliest Devonian
(rhyniophytoids) present interesting combinations of characters that do not fit known plant clades
(Edwards 2000, 2003).
Concerning originations, Heckman et al. (2001) employed molecular clock techniques to deter-
mine the origin of embryophytes and fungi. They used nuclear protein-coding gene sequences and
calibrated with divergence dates from animal phyla and several kingdoms (plant, animal, fungi).
They dated the origin of embryophytes at about 1061 ±109 Mya and the bryophyte-tracheophyte
divergence at 703 ma ±45 Mya. This is much earlier than any fossil data for terrestrial plant
remains. Sanderson (2003) calculated origination of plant groups based on organellar genes, us-
ing different techniques and calibrating with more closely related taxa (earliest seed plants). He
obtained a crown group divergence date of ca. 435 to 480 Mya (origin of vascular plants), which is
more consistent with the fossil record, but does not directly address the origin of embryophytes
as a whole. Such clock calculations remain problematic for many reasons, including rate hetero-
geneity, as summarized by Wellman (2004) and Bateman et al. (1998). Presently the microfossil
record may provide the more accurate minimum origination time for both embryophytes and
tracheophytes.
The various lines of evidence (molecular data, chemistry, ecophysiology, biomechanics, mor-
phology, paleogeography) used to address the possible time of origin, types of early plants and their
relationships, functional aspects, and closest sister group/ancestral group, as well as broader issues
relating to assessing diversity, radiations, homology, taxon recognition, problems of molecular and
morphological phylogenies, and interpreting ecologies are discussed in several recent reviews.
Pertinent ones are by Bateman et al. (1998), Edwards (2000), Edwards & Wellman (2001),
Edwards et al. (1998, 1999), Kenrick & Crane (1997a,b), Steemans (2000), Wellman (1999, 2004),
Wellman & Gray (2000).
This review highlights recent discoveries that have advanced our understanding of early events
in plant evolution and that raise new questions about the timing of evolution or relationships
among earliest (mostly vascular) plants for a broad readership. Existing data are summarized to
provide a background in which to view these discoveries and questions. Advances woven into the
background section include the following:
1. Recentstudies of new spore assemblages suggest factors that influence trilete and cryptospore
distribution;
2. Increased information about possible producers of spores in the Ordovician-Devonian and
about wall ultrastructure of some situ and dispersed spores;
3. Late Ordovician partially preserved sporangia confirm a plant source for certain spore types;
4. Comparisons of extant acid-, heat- and/or decay-resistant bryophyte remains to some cuticle
and tube fragments provide additional support of possible bryophyte affinity for some of the
fossil fragments.
This will be followed by discussion of megafossil discoveries and their implications, in particular
(a) new data on fairly large, complex megafossils from the Late Silurian of Bathurst Island that
suggest earlier tracheophyte diversification than previously known, implying a need to re-evaluate
the composition of late Silurian floras, as well as the timing of lycophyte origination and early
evolution; (b) earlier origin of major plant structures (including rooting structures, leaves, and
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seeds) among tracheophytes that might imply earlier (or more rapid?) diversification than the
record showed originally; much of this also occurs within lycophytes.
WHAT GETS PRESERVED?
Only resistant cells or tissues are likely to survive events during deposition and fossilization, lim-
iting information available about most extinct organisms. An exception might occur in unusual
conditions such as the Early Devonian Rhynie Chert Lagerstaette, where plants (including game-
tophytes), microbes, lichens, algae, fungi, and animals are all preserved, sometimes in life position.
Additionally, which entities are caught in the depositional system, and which ones have actually
been found and studied by paleontologists, affects knowledge about past history of a group or
organism.
Resistant structures likely to remain in plants after fossilization reflect adaptations to withstand
life on land [discussed extensively by Raven & Edwards (2004); Graham & Gray (2001); Van Bergen
et al. (2004)], especially the challenges posed by desiccation or water loss, UV light damage, and
microbe/pathogen attack. Adaptations to these stresses in most living plants include cutin/cutan
and wax-containing cuticles covering the surface of stems, leaves, and reproductive structures,
and lignified cells that provide support or conduct water (fibers, tracheids, and vessel elements)
in many embryophytes. Sporopollenin-coated spores, produced by meiosis in all embryophytes,
are dispersed and thus require protection. The comparable resistant structures in fossil plants are
considered to be of similar chemical composition, but this has been barely tested (Ewbank et al.
1996, Van Bergen et al. 2004). The recent novel finding is that parts of bryophytes, especially liver-
worts long considered to lack resistant structures, actually contain compounds (phenol-derived?)
in cells/cell walls that confer resistance to high temperatures, acid, and decay (Graham & Gray
2001, Graham et al. 2004, Kroken et al. 1996).
The absence of macrofossil remains in the Ordovician/early Silurian has been attributed to
(a) the lack of fossiliferous, terrestrially derived rocks owing to transgressive seas until the
Silurian (Kenrick & Crane 1997a,b; Wellman 2004; Steemans 1999); (b) the fact that the ear-
liest plants lacked resistant cells other than spores (Wellman 2004, but see preceeding); and/or
(c) the idea that early plants may have lived in areas where they were not swept into depositional
basins (Wellman 2004). Probably some early plants did lack resistant structures; these may have
been physiologically tolerant to desiccation and/or had a short vegetative life cycle in order to
survive in subaerial environments (Edwards 2000, Edwards & Richardson 2004, Steemans et al.
2007, Wellman 2004).
Absence of larger parts of plants or whole plants prevents knowing the overall form and size of
the very early plants, and stem group taxa may differ greatly from crown-group (often extant) ones
(Kenrick 2000, Kenrick & Crane 1997b). These researchers present a hypothetical stem group
moss composed of an axial, branched gametophyte with unbranched sporophytes terminating some
axes. If the junction between sporophyte and gametophyte is not visible, these would resemble
some of the early polysporangiophytes (rhyniophytoids) common in late Silurian and earliest
Devonian strata.
By late Silurian time, it is possible to identify cells similar to those in extant plants, namely cuticle
with stomata, trilete spores, and isolated tracheids, as well as a basic body organization comprising
stems, reproductive structures, and, in one instance, leaves, consistent with tracheophytes or
“protracheophytes.” In addition, some of the small mesofossil remains exhibit conducting (and
other) cell types unlike any modern analog, although some are similar to those seen in bryophytes
(Edwards 2000). Small late Silurian/earliest Devonian plants, with branching sporophytes and
apparently lacking tracheids, are termed rhyniophytoids.
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THE RECORD
Major sources of information about earliest plants from the fossil record are (a) microfossils, in-
cluding dispersed spores, cuticle fragments, and tubular structures; and (b) mesofossil and macro-
fossils, for which less and more slowly accruing evidence exists. Figure 1 shows first appearance
and duration of some of these.
Dispersed spores (cryptospores) and phytodebris (cuticles and tubes) occur in continental and
near-shore marine environments, although the majority in older strata are marginal marine and
from several paleocontinents at different latitudes, starting at least by the mid-Ordovician (but see
below) and extending into the Early Devonian. They are preserved because they are produced in
large numbers, composed of resistant materials that can be fossilized, and have the potential for
dispersal by wind and water as a result of their small size (Wellman 2004; Wellman & Gray 2000).
The Record: Dispersed Spores
The earliest accepted occurrences are cryptospore assemblages from the Llanvirn (Strother 2000,
Strother et al. 1996, Wellman 2004, Wellman & Gray 2000). Numerous assemblages occur
fairly widely paleogeographically—with similar taxon composition—for the remainder of the
Ordovician (Gray 1985, Richardson 1996, Steemans et al. 1996, Wellman 1996), suggesting a
long period of evolutionary stasis. Cryptospores (Figure 2a) are alete (lacking a well-defined
aperture), relatively thick-walled sporomorphs (distinguishing them from acritarchs) that occur in
unusual configurations (monads, permanently united dyads or tetrads, thus suggestive of meiosis);
they can be with or without a covering envelope, which itself can be either smooth or ornamented
(Richardson 1996; Steemans 1999, 2000; Strother 2000; Wellman & Gray 2000). Some mon-
ads, probably originally formed as dyads, have a thin area on the proximal surface (termed hilate
cryptospores). Some very early apparently trilete monads are clearly broken-apart components of
obligate tetrads (Steemans 2000). Whole palynomorph assemblage studies initially centered on
Laurussia (Edwards & Richardson 2004, Richardson 1996), but more recent data from Gondwana
and other microcontinents suggest interesting differences in distribution/endemism between cryp-
tospores (more widespread) and trilete spores (some types locally restricted) (Steemans et al.
2007; Wellman 2004).
A major change in the Early Silurian (late Llandovery) involves loss of envelope-covered tetrad
and dyad taxa, continuation of existing naked tetrads and dyads, increase in hilate occurrences
and no new taxon originations (Steemans 2000, Wellman & Gray 2000). Cryptospore diversity
decreases as trilete spore diversity increases through the Silurian, and cryptospores apparently dis-
appear nearly completely by the Early Devonian (Lochkovian). However, this should be confirmed
by additional study of Devonian assemblages to ensure they are not being missed. Steemans (1999,
2000) proposed that the Silurian change in cryptospore/trilete spore diversity resulted from sea-
level rise during the Llandovery that may have reduced habitats in which cryptospore-producing
plants (CSPs) lived. A later regression provided new habitat in which trilete spore-producing
(TSPs) plants may have outcompeted the CSPs; the latter were then restricted to specific habitats
(see also Edwards & Richardson 2004).
Possible Affinities
Cryptospore monads might represent haploid or diploid resistant-walled cells of algae or protists,
or the meiotic spores of plants. Evidence for the latter is increasing. The morphology of some mon-
ads suggests they represent dissociated fragments of particular dyads or tetrads. Non-aperturate
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ab
c
Trilete
spore
Cryptospore types Tubes
Pseudocellular cuticle
Tetrads
Dyads
Monads
Hilate
monad
Naked Membrane-
enclosed
Figure 2
Diagrams of types of fragmentary remains attributed to early plants. (a) Spores, including cryptospore types
and trilete spores. (b) Selected tubular elements. Many other types are known. Far left after Wellman & Gray
(2000); right two after Edwards (2003). (c) Types of pseudocellular cuticles and cuticle from an Upper
Devonian liverwort. Left to right: Silurian cuticle from Banks (1975); Cosmochlaina verruculosus from Lower
Devonian of Wales, after Edwards (1986); Pallavicinia devonicus, after Hueber (1961).
monads and permanent tetrads with envelopes are known among extant bryophytes, particularly
extant sphaerocarpalean liverworts (Edwards et al. 1999; Gray 1985, 1991; Richardson 1996).
Dyads often result from aberrant meiotic events in extant bryophytes or tracheophytes, but fossil
in situ forms are considered a result of normal, perhaps successive, meiosis (Edwards 2000). Ultra-
structure of some dyad spore walls is lamellate and very similar to those in extant liverworts (Taylor
1996). Some cryptospore dyads, hilate monads, and tetrads are found in situ in late Silurian meso-
fossils attributed to rhyniophytoids (Edwards 2000; Edwards et al. 1999; Wellman et al. 1998a,b).
These studies show that similar looking plants can produce either cryptospores or trilete spores
(never both), that different plants can yield spores of similar external morphology but different
ultrastructure, and that some common basic features exist among certain cryptospore and trilete
spore types, hinting at both great diversity and tentative relationships between certain tetrads,
dyads, and monads. Data from in situ and dispersed spores show parallel (convergent) evolutionary
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change from smooth to verrucate/murornate to finely apiculate in both cryptospores and trilete
spores from the Late Silurian to early Devonian (Richardson 1996, 2007; Richardson & Burgess
1999).
These data mostly are from the Late Silurian, when cryptospore diversity and numbers were
declining; these plants, or their spores, may represent relict taxa or show relict features, possibly
indicating what earlier plants were like (Edwards 2000). Finding polysporangiate cryptospore
producers indicates plants beyond a bryophyte grade as currently conceived (Edwards 2000;
Edwards et al. 1998), whereas absence of tracheids precludes positive assignment to tracheophytes.
Might these represent unique protracheophyte clades or are they ancient bryophytes?
Earlier in Time: Late Ordovician Sporangia
Affinities of pre-Silurian cryptospores are often questioned. Wellman et al. (2003) obtained sev-
eral kinds of spore masses with outer sporangial wall fragments from Caradoc nonmarine rocks in
Oman. Preparations were top-sieved to yield these “larger fragments” (ranging from 0.24–0.5 mm).
They contain either naked tetrads, envelope-enclosed tetrads, or naked dyads, thus represent-
ing several different types. These sporangia provide direct evidence that at least some early
cryptospores were meiotic products of embryophytes. Ultrastructure of some spore walls show
numerous lamellae as occurs in liverwort spores.
Possible Earlier Occurrences of Embryophyte-Derived Cryptospores
Permanent tetrads and dyads, and monads (but also polyads) are described from exposures of
Middle Cambrian tidal/estuarine strata in the Bright Angel Shale of the Grand Canyon, Arizona,
and Rogersville Shale, Tennessee, and from cores of the Conasauga Group of eastern Tennessee
(Strother 2000; Strother & Beck 2000; Strother et al. 2004). They are smaller and possibly thin-
ner walled (Wellman 2004), but otherwise strikingly similar to younger counterparts. Wefts of
tubes, some indistinguishable from younger ones comprising the enigmatic organism Nematothal-
lus (increasingly considered fungal or lichen), occur in all localities, and unique, more animal-like
fimbrulate structures occur in the Bright Angel Shale. More problematic are the clusters of rounded
bodies in groups of two to several (polyads), the individual units being very similar to those in
tetrads or dyads. More data are needed; this highlights problems in distinguishing meiotic products
from algal vegetative cells.
The Record: Trilete Spores
The earliest occurrence of trilete spores is latest Ordovician (Ashgillian), in Gondwana (Turkey)
(Steemans et al. 1996), where they are rare. Trilete spores become abundant starting in the mid-
Llandovery, co-occur with cryptospores, and increase in diversity until they dominate most post-
Lochkovian assemblages (Gray 1991; Richardson 1996; Steemans 2000; Wellman & Gray 2000).
Additionally, trends in sculptural patterns can be observed from latest Silurian to early Devonian
(Richardson 1996, 2007; Richardson & Burgess 1999).
Affinity
Trilete spores occur in Cooksonia species, in several rhyniophytoid taxa, and in many early Devonian
vascular plants, as well as in most extant and extinct nonseed producing taxa. They also are known
from some extant hornworts and mosses (Gray 1985, Wellman et al. 1998a).
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Spore Ultrastructure May Aid in Assessing Affinity
To some extent it is possible to examine spore ultrastructure and assess possible affinity, although
much more comparative data are needed to determine the extent of variation within clades. Lim-
itations include (a) determining whether features are due to particular ontogenetic stages, tapho-
nomic effects, preparation techniques, or true variation; and (b) difficulty in assessing homologies
with extant counterparts and recognizing patterns of character distribution. Extensive variation
in both crypto- and trilete spores already is apparent, which will probably be more meaningful as
more data are obtained. Basic patterns include (a) walls homogeneous and single or bi-layered;
(b) walls partly lamellate, partly homogeneous; (c) walls entirely lamellate; (d) walls homogeneous
and spongy; and (e) organization of “envelope” or outer layer.
The Record: Cuticles and Tubes
Fragments of cuticle and isolated or groups of tubular structures occur from the Llanvirn (tubes)
on, especially in the Silurian, but also possibly as early as the Middle Cambrian (tubes) (Figure 2b).
Cuticular fragments appear to be morphologically different from those of vascular plants, are
smooth on one side and have flanges forming cell outlines on the other, and lack evidence of
stomata, but sometimes exhibit circular openings. Tubes are smooth inside and out or ornamented
(either inside or outside), thin to thick walled (either very narrow or much wider), and some
change diameter along their length or branch (summarized in Edwards 2000, Wellman & Gray
2000).
Possible Affinities
Both tubular fragments and cuticles have been allied with the nematophytales (discussed in
Wellman 1995, and references therein). Originally coined by Lang (1937), the term nemato-
phyte referred to associated cuticular and tubular material found in the Welsh borderland; though
their affinity is unknown, these remains were considered vestiges of possible early or basal plants.
Some tubes clearly resemble fungal hyphae (unevenly thickened, branched, with swellings at the
base of the branch), others are of uncertain affinity. Larger-diameter tubes are smooth, or possess
either internal or external thickenings (some referred to as “banded”). It has been suggested that
some could represent early types of conducting tissues of plants, which is supported to a limited
extent by some of the kinds of conducting tissues found in rhyniophytoids (Edwards 2000, 2003).
Other possible sources of tubes and cuticles are discussed below.
Another possibility suggested for both cuticle fragments and some tubes (particularly banded
ones) is that they may represent the acid-hydrolysis- or decay-resistant remains of bryophytes
(Graham & Gray 2001; Graham et al. 2004; Kroken et al. 1996; Kodner et al. 2001). Extant
bryophytes were subjected to treatments designed to simulate aspects of the fossilization pro-
cess, namely acetolysis and burial in soil. Decay and heat- and/or chemical-resistant tissues were
obtained, such as remains of sporangial walls and placentae of some liverworts, including the
early divergent taxon Sphaerocarpos, and the peat moss Sphagnum. Sporangial fragments of the
more derived liverworts Lophocolea and Conocephalum broke apart and, in the latter instance,
released individual or small groups of tubular cells with helical internal thickenings similar to
some banded tubes found in Silurian sediments (Graham & Gray 2001, Graham et al. 2004,
Kroken et al. 1996). Elators from some liverworts also survived treatment. Graham & Gray (2001)
suggest that having acid-resistant walls is a plesiomorphic character of embryophytes and that this
resistance may have been lost in more derived lineages. Graham et al. (2004) studied rotted remains
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of liverworts and found some cuticular fragments, most similar to the Silurian-Devonian fossil
taxon Cosmochlaina (Figure 2c,center), that represent the ventral surface of thallose liverworts with
the distinctive “holes” being similar to openings caused by breaking off of rhizoids in the extant
plant. Additionally, rhizoids from ventral surfaces, as well as basal regions of gametangiophores,
resisted decay and are reminiscent of some tubular structures found as fossils. Chemical studies
are needed to better determine resistant wall compounds, and further investigation of bryophytes
(and perhaps lichens) is needed to determine potentially preservable structures that may expand
such comparisons.
MESO- AND MACROFOSSIL RECORD
Until fairly recently, most of the macrofossil plant remains obtained from late Silurian and earliest
Devonian strata are extremely small and simply organized (Figure 3a), usually consisting of an
unbranched or branched axis (stem) and sporangia (summarized by Edwards 2000; Edwards &
Wellman 2001; Edwards et al. 1998). A few possess tracheids (Lochkovian Cooksonia); others show
differentiation of centrally located conducting cells that in some cases show patterns that approach
those seen in bryophyte conducting cells but of greater variety (Edwards 2000, 2003).
Sporangia, when present, often contain either cryptospores or trilete spores (see above). Vari-
ation in spore morphology (and sometimes other features) occurs within coeval specimens or
species, and specimens/species through time. For example, Pridoli Cooksonia pertoni sporangia pro-
duce different types of trilete spores among different samples, and these differ from Lochkovian
conspecifics (Fanning et al. 1988, Habgood et al. 2002), with each spore type serving as a basis
for subspecific recognition. Cooksonia species also exhibit interspecific differences in spore mor-
phology (Habgood et al. 2002). These findings indicate that external morphology among early
polysporangiophytes may underestimate diversity; variation and evolution occur in less obvious
areas, such as internal organization, sporangium, and spore type. Such rhyniophytoids are most
abundantly preserved in marginal marine sediments in Wales and the Welsh Borderland, but
similar forms have also been found in Bolivia, Argentina, Ireland, New York State, Kazakhstan,
Podolia, Libya, Czechoslovokia, and Shropshire in the United Kingdom.
MORE RECENT DISCOVERIES CHANGE IDEAS ABOUT
COMPOSITION AND LOCAL DISTRIBUTION
OF LATE SILURIAN FLORAS
Although not numerous, new discoveries may alter ideas concerning size and affinity of pre-
Devonian plants and thus both timing and relationships among early forms. Many more such
discoveries are needed.
Complex Late Silurian Plants
Kotyk et al. (2002) report on plants preserved in well-dated Ludlow/Pridoli marine deposits from
Bathurst Island, Arctic Canada (BI), which are larger and more complex than many coeval ones
(Figure 3j–l ), exhibiting pseudomonopodial branching (indeterminate stems), laterally borne
sporangia often aggregated in compact spikes (strobili), and some stems with enations similar to
those in lycopsids. Many strongly resemble zosterophylls found in the Pragian, including Pragian
collections from the same area. Rhyniophytes are rare, and those present are sometimes larger than
coeval rhyniophytoids or cooksonioids, although a few [ Junggaria spinosa (Cooksonella sphaerica)
468 Gensel
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ab c d
efg
hi
jk
l
1 mm 1 mm
1 cm
1 cm
100 µm
500 µm 100 µm
1 cm 1 cm 1 cm
1 cm
1 cm
Figure 3
Selected Late Silurian and earliest Devonian plants, drawn to scale, to show size range from meso- to
macrofossils. e–gare at micrometer scale, others at millimeter to centimeter scale, as indicated. (a)Cooksonia
pertoni, Pridoli, Hereford, England. (b)Cooksonia sp. cf. caledonica, Pridoli, Bolivia. (c)Cooksonia cf.
hemisphaerica, Pridoli, New York State. (d)Cooksonella sphaerica/Junggaria spinosa, Pridoli, NW China.
(e–g) Selected mesofossils from the Lochkovian North Brown Clee Hill locality, Shropshire, UK.
(e)Cullulitheca richardsoni. (f)Fusitheca fanningiae. (g)Grisellatheca salopensis. (h,i) Selected plants from the
Lower Plant Assemblage, Victoria, Australia, Ludlow. (h)Baragwanathia longifolia.(i)Salopella australis.
(j–l ) Selected zosterophylls from Bathurst Island, Arctic Canada, Ludlow. ( j)Zosterophyllum sp. A.
(k)Distichophytum sp. (l)Macivera gracilis.[a,b, and hare redrawn from Edwards & Wellman (2001);
credrawn from Edwards et al. (2004); dredrawn from Cai et al. (1993); e–g redrawn from Edwards (2000);
iredrawn from Tims & Chambers (1984); j–l redrawn from Kotyk et al. (2002).]
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ANRV360-ES39-22 ARI 10 October 2008 9:54
from the Pridoli of northwestern China and Salopella australis from the Ludlow of Australia)
approach their size (Cai et al. 1993, Tims & Chambers 1984).
Other pre-Devonian plant occurrences with stems terminating in sporangia approach this
larger or more complex condition as demonstrated by examples in Figure 3, coming from the
Pridoli of Bolivia and New York State (Edwards et al. 2004), the Lochkovian of Brazil (Gerrienne
et al. 2001), and the Pridoli of Podolia (Ischenko 1975). Though still small, most are larger than
rhyniophytoids or some Cooksonias of any age (also see below). The late Llandovery Pinnati-
ramosus from Fenggang, Guizhou Province, shows considerable morphological and anatomical
complexity; Edwards et al. (2007) interpret it as a rooting system probably from the Permian that
grew into Silurian layers and were fossilized.
The Ludlow “Lower Plant Assemblage” (LPA) of Victoria, Australia (Tims & Chambers 1984)
is less disparate in light of these other occurrences. Current graptolite identifications support a
Ludlow age (Rickards 2000). Rhyniophytes (Salopella, Hedeia), and as yet unnamed zosterophylls
comparable in size to the Arctic specimens, occur. Significantly larger specimens attributed to
the lycophyte Baragwanathia occur; stems are up to 30 cm long, 3 cm wide, and bear leaves. It is
unclear if the Silurian Baragwanathia is the same taxon that occurs in the Upper Plant Assemblage
in Victoria and in the Emsian of Ontario. Implications include the following:
1. Several types of fairly complex plants, mostly allied to Lycophytina, are present ∼6 million
years later than the earliest occurrence of Cooksonia and up to 25 million years earlier than
previous records indicated.
2. These two assemblages suggest relatively little change in morphological complexity of some
species (the BI zosterophylls, possibly Baragwanathia) for as much as 25 million years (late
Ludlow-Pragian).
3. The two assemblages suggest either (a) a very early origin and diversification of the ly-
cophytes (lycopsids, if Baragwanathia is correctly attributed, and zosterophyllopsids). The
undoubted presence of the BI zosterophylls and possible presence of an Australian lycopsid
might indicate that some of the early Silurian trilete spores may have been produced by zos-
terophylls or lycopsids. Though spores are known from several Devonian zosterophylls and
generally are simple retusoid forms, little is known about early lycopsid spores. Thin-walled
scabrate, retusoid trilete spores were obtained from Drepanophycus spinaeformis. There is no
direct match with early-occurring trilete spores, which often have a thickened equatorial
margin, although Taylor (2003) notes that some ultrastructural features of Ambitisporites
compare well with lycophytes (and hornworts). More data are needed, including studies of
ultrastructure; or (b) a very rapid evolution in the lycophyte lineage from the time of first
appearance of vascular plants in the Wenlock.
These occurrences raise major questions about timing, tempo, and possibly mode of early tra-
cheophyte evolution. The latest Ordovician to early Silurian appearance of trilete spores suggests
tracheophyte presence. Implications about phylogenetic relationships and/or earliest appearance
of other clades also should be considered. What is the relationship between lycophytes and other
early plant types if they diverged as early as or even earlier than Cooksonia (considered as a possible
stem group lycophyte, Kenrick & Crane 1997b) or rhyniophytoids or rhyniaceae? A complicating
factor is that quite possibly several taxa are encompassed by Cooksonia-type morphology, some
with tracheids and some so far without. This is also evidenced by differences in sporangial features
and spores across subspecies and species. Did rhyniophytes sensu Kenrick & Crane also diverge
earlier though no record exists? Lastly, spore diversity suggests many plants existed about which
we know nothing.
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Ecological Specialization in Lochkovian Plants
Most late Silurian and earliest Devonian deposits are marginal to fully marine so it is not pos-
sible to assess either diversity within a localized region or exactly where and how these plants
grew. Accumulated data on macrofossils and dispersed spores in well-dated and sedimentologi-
cally studied deposits in the Anglo-Welsh Basin have resulted in some initial hypotheses (Edwards
& Richardson 2004; Richardson 2007; Wellman 2004; Wellman et al. 2007).
Wellman et al. (2000) report the presence of Zosterophyllum in coarse sediments coeval
with rhyniophytoid-rich ones in the Anglo-Welsh basin (earliest Devonian), in contrast to the
Cooksonia/rhyniophytoid-only vegetation previously reported.
Differences also occur in dispersed spore assemblages from the Welsh Borderland (mostly
lowland floodplain sediments) and coeval Scottish localities (intermontane basins), where zos-
terophylls are more common than cooksonias/rhyniophytoids. They suggested rhyniophytoids
were successful in mostly damp environments and adapted via an ephemeral lifestyle to withstand
flooding events, whereas larger tracheophytes such as zosterophylls were more likely to survive
in the comparatively drier intermontane environments. However, Edwards & Richardson (2004)
suggested instead that larger tracheophytes may have inhabited marginal areas where they are
more likely to be caught in depositional events or swept to sea, and rhyniophytoids were more
likely to be near inland bodies of water (lakes, ponds). Co-occurrences were explained as result-
ing from localized environmental differences. Steemans et al. (2007) concurred. More data are
needed; searches in older strata may show the same kind of distribution. It is of interest that
zosterophylls in late Early Devonian strata were regarded as living in physiologically stressful
dysaerobic backswamps and to be marsh dwellers (Hotton et al. 2001).
GAMETOPHYTE/SPOROPHYTE RELATIONSHIPS
AND IMPLICATIONS RELATIVE TO PHYSIOLOGICAL FUNCTIONING
Gametophytes of early plants are only known from the Early Devonian Rhynie Chert and a few
compressions (Sciadophyton, Calyculiphyton), and consist of a basal region (corm) with radiating
axes, each terminated by a cup-shaped structure bearing gametangia. The possibility that a few
mesofossils represent bryophyte gametophytes (Tortilicaulis, Grisellatheca) are inconclusive. From
this, many workers conclude that a basal feature of early plants is having axial gametophytes,
and thus exhibiting an isomorphic alternation of generations (Kenrick & Crane 1997). Gerrienne
et al. (2006) demonstrated a Cooksonia specimen in which five axes attach to a thalloid basal struc-
ture; his favored interpretation of this was that the thalloid structure represented the gametophyte
and the rest the sporophyte. Alternatively the thalloid structure might represent a sporophytic corm
from which stems arose. Gerrienne et al. further argued that a thalloid, not axial, gametophyte
morphology was possible among earliest plants, especially the Rhyniaceae, thus not exhibiting iso-
morphic alternation of generations. Earlier scenarios, and particularly the interpolation theory of
origin of sporophyte, is more readily supportive of a heteromorphic sporophyte and gametophyte
for earliest plants (Mishler & Churchill 1984; Graham 1993).
Inferences of physiological functioning, based on types of cells and tissues present in early
plants, are that all sporophytic remains (axes plus sporangia) and possibly gametophytes were free
living and photosynthetic. Earliest forms may have been poikilohydric, but an early achievement of
homoiohydry (internal conduction of water) is suggested (Raven & Edwards 2004). Alternatively,
Rothwell (1995) and Kenrick & Crane (1997) suggest that some of the earliest plants, like Cooksonia,
may have consisted of branched sporophytes still in attachment to distal parts of a branched, axial
gametophyte.
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Boyce (2008) argues that size is an important consideration in regard to functional constraints
and a potentially useful systematic character in early embryophytes. Analyses of plant size, cell
types, and functional aspects indicate that the less than 1-mm diameter axes of some cooksonioid
Late Silurian plants may lack sufficient area to contain photosynthetic cells in addition to the
clearly established vascular, stereome, and epidermal tissues. Boyce infers that these plants would
have been dependent on a persistent gametophyte for most of their nutrition. Boyce also suggests
that the absence of axial gametophyte structures among these fossils argues for a non-axial early
gametophyte morphology quite different from what is known from the Early Devonian Rhynie
plants, thus indicating that at least some of the earliest forms may have had heteromorphic alter-
nation, with later acquisition of isomorphic gametophytes in certain lineages. Further evidence is
needed to test these intriguing ideas.
EARLIER APPEARANCE OF MAJOR PLANT STRUCTURES
Finally, in mid-Late Silurian/Devonian strata, certain benchmark events in early plant evolution,
such as acquisition of complex form, larger size, rooting structures, leaves, and seeds, are now
known to occur earlier in time than the earlier postulated Middle or Late Devonian. These include
(a) earliest rooting structures in the Pragian, present in zosterophyllopsids and lycopsids (Gensel
et al. 2001); (b) leaves, present in the Ludlow,again in lycopsids if LPA Baragwanathia is Silurian or if
not, then in Pragian lycopsid Drepanophycus and putative euphyllophyte Eophyllophyton; (c) aligned
metaxylem or possible early secondary xylem, Emsian, trimerophytes (Psilophyton, unpublished
taxa); and (d) tree habit, Middle (not Late) Devonian, Eospermatopteris/Wattieza (Stein et al. 2007).
Also, the earliest macrofossil of a liverwort is now Middle, not Late, Devonian, based on a new fossil
metzgerialian liverwort found in New York State (Hernick et al. 2008). Its affinity was realized
after examining the specimens in polarized light.
FUTURE DIRECTIONS
Although the palynological record serves as a good guide to the earliest appearance of plants,
as advocated by Wellman (2004), the macrofossil record is improving. Additional investigation,
preferably using a combination of techniques and approaches from paleobotany, palynology, sed-
imentology, geochemistry, organic chemistry, and neobotany, should yield additional data that, in
turn, will fuel new integration and synthesis of timing and pattern of early plant diversification.
Specifically, detailed sampling of assemblages, with good stratigraphic control and environmental
interpretation, in many geographic regions is needed to address possible sedimentological, preser-
vational, or regional biases to the existing record. Fully marine strata are as likely candidates as
terrestrial for future discoveries. As information about the molecular genetics of plant develop-
ment outside of model organisms increases, integrating with fossil morphologies and occurrences
may aid in assessing homology and in postulating characters of stem group taxa.
SUMMARY POINTS
1. Datafrom macro-, meso-, and microfossils have expanded knowledge of earliest plants ge-
ographically and stratigraphically. Fragmentary sporangial remains from the Ordovician
indicate that at least some very early cryptospores are embryophytic. Similar-appearing
cryptospore-like entities from the Middle Cambrian are intriguing but require additional
study to distinguish from algal remains.
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2. Extensive research by Edwards and colleagues on mesofossils has documented possible
parent plants of cryptospores and some trilete spores. Ultrastructural studies are in early
stages but show great promise in helping determine affinity of dispersed spore types.
3. Experiments on extant bryophytes show that resistant cell walls exist in some parts of both
liverworts and mosses, and some of the remaining fragments generally resemble isolated
or clusters of tubes and cuticles found in Ordovician-Devonian sediments, strengthening
the assertion that bryophytes occurred much earlier than the macrofossil record indicates
(earliest liverwort now Middle Devonian).
4. Several types of comparatively large zosterophylls, relative to contemporaneous plants,
are documented from the Ludlow of Arctic Canada; these along with Baragwanathia
from the Ludlow of Australia suggest an earlier radiation of tracheophytes (at least from
Llandovery). Why are these not seen in other Silurian deposits? This may alter ideas of
relationships of lycophytes relative to other plant groups or mean a search for rhynio-
phytes/rhyniaceans needs to be made.
5. Many plant structures are now documented earlier in time, especially within the Devo-
nian, perhaps also indicating earlier origins or a more rapid radiation.
6. Integration of the megafossil and microfossil, within a well constrained geological con-
text, has great promise of yielding more data about earliest plants.
DISCLOSURE STATEMENT
The author is not aware of any biases that might be perceived as affecting the objectivity of this
review.
ACKNOWLEDGMENTS
The author acknowledges financial support for this work from the P. Mouzon fund of the North
Carolina Botanical Garden and the artwork of Ms. Susan Whitfield.
LITERATURE CITED
Algeo TJ, Scheckler SE, Maynard JB. 2001. Effects of the Middle to Late Devonian spread of vascular land
plants on weathering regimes, marine biotas, and global climate. See Gensel & Edwards 2001, pp. 213–36
Banks HP. 1975. The oldest vascular plants: a note of caution. Rev. Palaeobot. Palynol. 20:13–25
Bateman RM, Crane PR, DiMichele WA, Kenrick PR, Rowe NP, et al. 1998. Early evolution of land plants:
phylogeny, physiology, and ecology of the primary terrestrial radiation. Annu. Rev. Ecol. Syst. 29:263–92
Beerling DJ, Berner R. 2005. Feedbacks and the coevolution of plants and atmospheric CO2.Proc. Natl. Acad.
Sci. USA 102:1302–5
Berner R. 1997. The rise of plants and their effect on weathering and atmospheric CO2.Science 276:544–46
Berner R. 2001. The e ect of the rise of land plants on atmospheric CO2during the Paleozoic. See Gensel &
Edwards 2001, pp. 173–78
Boyce CK. 2008. How green was Cooksonia? The importance of size in understanding the early evolution of
physiology in the vascular plant lineage. Paleobiology 34(2):179–94
Cai CY, Dou YW, Edwards D. 1993. New observations on a Pr´
ıdol´
ı plant assemblage from north Xinjiang,
northwest China, with comments on its evolutionary and palaeogeographical significance. Geol. Mag.
130:155–70
www.annualreviews.org •The Earliest Land Plants 473
Annu. Rev. Ecol. Evol. Syst. 2008.39:459-477. Downloaded from arjournals.annualreviews.org
by Aligarh Muslim University on 08/17/09. For personal use only.

ANRV360-ES39-22 ARI 10 October 2008 9:54
DiMichele WA, Hook RW. 1992. Paleozoic terrestrial ecosystems. In Terrestrial Ecosystems through Time:
Evolutionary Paleoecology of Terrestrial Plants and Animals, ed. AK Behrensmeyer, JD Damuth,
WA DiMichele, R Potts, H-D Sues, SL Wing, pp. 205–35. Chicago: Univ. Chicago Press
Driese SG, Mora C. 2001. Diversification of Siluro-Devonian plant traces in paleosols and influence on
estimates of paleoatmospheric CO2levels. See Gensel & Edwards 2001, pp. 237–53
Edwards D. 1986. Dispersed cuticles of putative nonvascular plants from the Lower Devonian of Britain. Bot.
J. Linn. Soc. 93:250–75
Edwards D. 2000. The role of Mid-Palaeozoic mesofossils in the detection of early bryophytes. Philos. Trans.
R. Soc. London Ser. B 355:733–55
Edwards D. 2003. Xylem in early tracheophytes. Plant Cell Environ. 26:57–72
Edwards D, Banks HP, Ciurca SJ, Laub RS. 2004. New Silurian cooksonias from dolostones of north-eastern
North America. Bot. J. Linn. Soc. 146:399–413
Edwards D, Richardson JB. 2004. Silurian and Lower Devonian plant assemblages from the Anglo-Welsh
Basin: a palaeobotanical and palynological synthesis. Geol. J. 39:375–402
Edwards D, Wang Y, Bassett M, Li C-S. 2007. The earliest vascular plant or a later rooting system? Pinnati-
ramosus qianensis from the marine Lower Silurian Xiushan formation, Guizhou Province, China. Palaios
22(2):155–65
Edwards D, Wellman CH. 2001. Embryophytes on land: The Ordovician to Lochkovian (Lower Devonian)
record. See Gensel & Edwards 2001, pp. 3–28
Edwards D, Wellman CH, Axe L. 1998. The fossil record of early land plants and interrelationships between
primitive embryophytes: too little too late? In Bryology for the 21st century, ed. JW Bates, NW Ashton,
JG Duckett, pp. 15–43. Leeds, UK: Maney Publ. Br. Bryolog. Soc.
Edwards D, Wellman CH, Axe L. 1999. Tetrads in sporangia and spore masses from the Upper Silurian and
Lower Devonian of the Welsh Borderland. Bot. J. Linn. Soc. 130:111–56
Elick JM, Driese SM, Mora CI. 1998. Very large plant and root traces from the Early to Middle Devonian:
implications for early terrestrial ecosystems and atmospheric p(CO2) estimations. Geology 26:143–46
Erwin D. 1992. A preliminary classification of evolutionary radiations. Hist. Biol. 6:133–47
Ewbank G, Edwards D, Abbott GD. 1996. Chemical characterization of Lower Devonian vascular plants.
Org. Geochem. 25:461–73
Fanning U, Richardson JB, Edwards D. 1988. Cryptic evolution in an early land plants. Evol. Trends Plants
2:13–24
Gastaldo RA, DiMichele WA, eds. 2000. Phanerozoic Terrestrial Ecosystems. Tulsa: Paleontol. Soc. Pap. 6
Gensel PG, Edwards D, eds. 2001. Plants Invade the Land: Evolutionary and Environmental Perspectives.New
York: Columbia Univ. Press
Gensel PG, Johnson NG, Strother PK. 1991. Early land plant debris (Hooker’s “Waifs and Strays”?). Palaios
5:520–47
Gensel PG, Kotyk ME, Basinger JF. 2001. Morphology of above- and below-ground structures in Early
Devonian (Pragian-Emsian) plants. See Gensel & Edwards 2001, pp. 83–102
Gerrienne P, Bergamaschi S, Pereira E, Rodrigues M-AC, Steemans P. 2001. An Early Devonian flora,
including Cooksonia, from the Paran´
a Basin (Brazil). Rev. Palaeobot. Palynol. 116:19–38
Gerrienne P, Dilcher DL, Bergamaschi S, Milagres I, Pereira E, et al. 2006. An exceptional specimen of the
early land plant Cooksonia paranensis, and a hypothesis on the life cycle of the earliest eutracheophytes.
Rev. Palaeobot. Palynol. 142(3-4):123–30
Goromykin VV, Hellwig FH. 2005. Evidence for the most basal split in land plants dividing bryophyte and
tracheophyte lineages. Plant Syst. Evol. 254:93–103
Gradstein FM, Ogg JG, Smith AG. 2004. A Geologic Time Scale 2004. Cambridge, UK: Cambridge Univ. Press
Graham LE. 1993. Origin of Land Plants. New York: Wiley. 287 pp.
Graham LE, Gray J. 2001. The origin, morphology and ecophysiology of early embryophytes. See Gensel &
Edwards 2001, pp. 140–58
Graham LE, Kodner RB, Fisher MM, Graham JE, et al. 2004a. Early land plant adaptations to terrestrial
stress: a focus on phenolics. See Hemsley & Poole 2004, pp. 155–69
Graham LE, Wilcox LW, Cook ME, Gensel PG. 2004b. Resistant tissues of modern marchantioid liverworts
resemble enigmatic Early Paleozoic microfossils. Proc. Natl. Acad. Sci. USA 101(30):11025–29
474 Gensel
Annu. Rev. Ecol. Evol. Syst. 2008.39:459-477. Downloaded from arjournals.annualreviews.org
by Aligarh Muslim University on 08/17/09. For personal use only.

ANRV360-ES39-22 ARI 10 October 2008 9:54
Gray J. 1985. The microfossil record of early land plants: advances in understanding of early terrestrialization,
1970–1984. Philos. Trans. R. Soc. London Ser. B 309:167–95
Gray J. 1991. Tetrahedraletes,Nodospora, and the “cross” tetrad: an accretion of myth. In Pollen and Spores,
Patterns of Diversification. Systematics Association Special Volume, ed. S Blackmore, SH Barnes, pp. 49–87.
Oxford: Clarendon Press
Habgood KS, Edwards D, Axe L. 2002. New perspectives on Cooksonia from the Lower Devonian of the Welsh
Borderland. Bot. J. Linn. Soc. 139:339–59
Heckman DS, Geiser DM, Eidell BF, Stauffer RL, Kardos NL, Hedges SB. 2001. Molecular evidence for the
early colonization of land by fungi and plants. Science 293:1129–33
Hemsley AR, Poole I. 2004. The Evolution of Plant Physiology. London: Elsevier
Hernick LV, Landing E, Bartowski K. 2008. Earth’s oldest liverworts—Metzgeriothallus sharonae sp. nov. from
the Middle Devonian (Givetian) of eastern New York, USA. Rev. Palaeobot. Palynol. 148:154–62
Hotton CL, Hueber FM, Griffing DH, Bridge JS. 2001. Early terrestrial plant environments: an example
from the Emsian of Gasp´
e, Canada. See Gensel & Edwards 2001, pp. 179–212
Hueber FM. 1961. Hepaticites devonicus, a new fossil liverwort from the Devonian of New York. Ann. Mo. Bot.
Gard. 48:125–31
Ischenko TA. 1975. The Late Silurian Flora of Podolia 1–180. Kiev: Naukova Dumka
Karol KG, McCourt R, Cimino CT, Delwiche CF. 2001. The closest living relatives of land plants. Science
294:2351–53
Kenrick PR. 2000. The relationships of vascular plants. Philos. Trans. R. Soc. London Ser. B 355:847–55
Kenrick PR, Crane PR. 1997a. The origin and early evolution of plants on land. Nature 389:33–39
Kenrick PR, Crane PR. 1997b. The Origin and Early Diversification of Land Plants. A Cladistic Study. Washington,
DC: Smithson. Inst. Press
Kodner RB, Graham LE. 2001. High-temperature, acid-hydrolyzed remains of Polytrichum (Musci, Poly-
trichaceae) resemble enigmatic Silurian-Devonian tubular microfossils. Am. J. Bot. 88(3):462–66
Kotyk ME, Basinger JF, Gensel PG, deFreitas T. 2002. Morphologically complex plant macrofossils from the
Late Silurian of Arctic Canada. Am. J. Bot. 89(6):1004–13
Kroken SB, Graham LE, Cook ME. 1996. Occurrence and evolutionary significance of resistant cell walls in
charophytes and bryophytes. Am. J. Bot. 83:1241–54
Lang WH. 1937. On the plant-remains from the Downtonian of England and Wales. Philos. Trans. R. Soc.
London Ser. B 227:245–91
Mishler BD, Churchill SP. 1984. A cladistic approach to the phylogeny of the bryophytes. Brittonia 36:406–24
Nikrent DL, Parkinson CL, Palmer JD, Duff RJ. 2000. Multigene phylogeny of land plants: hornworts are
basal and mosses are sister to liverworts. Mol. Biol. Evol. 17:1885–95
Qiu YL, Cho YR, Cox JC, Palmer JD. 1998. The gain of three mitochondrial introns identifies liverworts as
the earliest land plants. Nature 394:671–74
Qiu YL, Li L, WangB, Chen Z, Dombrovska O, et al. 2007. A nonflowering land plant phylogeny inferred from
nucleotide sequences of seven chloroplast, mitochondrial, and nuclear genes. Int. J. Plant Sci. 168(5):691–
708
Qiu YL, Li L, Wang B, Knoop V, Groth-Malonek M, et al. 2006. The deepest divergences in land plants
inferred from phylogenomic evidence. Proc. Natl. Acad. Sci. USA 103:15511–16
Raven JA, Edwards D. 2004. Physiological evolution of lower embryophytes: adaptations to the terrestrial
environment. See Hemsley & Poole 2004, pp. 17–41
Renzaglia KS, Duff RJ, Nikrent DL, Garbary DJ. 2000. Vegetative and reproductive innovations of early land
plants: implications for a unified phylogeny. Philos. Trans. R. Soc. B 355:769–93
Retallack GJ. 2000. Ordovician life on land and early Paleozoic global change. See Gastaldo & DiMichele
2000, pp. 21–45
Richardson JB. 1996. Lower and middle Plaeozoic records of terrestrial palynomorphs. In Palynology: Princi-
ples and Applications, ed. J Jansonius, C McGregor, 2:555–74. College Station, TX: Am. Assoc. Stratigr.
Palynol. Found.
Richardson JB. 2007. Cryptospores and miospores, their distribution patterns in the Lower Old Red Sandstone
of the Anglo-Welsh Basin, and the habitat of their parent plants. Bull. Geosci. 82(4):355–64
www.annualreviews.org •The Earliest Land Plants 475
Annu. Rev. Ecol. Evol. Syst. 2008.39:459-477. Downloaded from arjournals.annualreviews.org
by Aligarh Muslim University on 08/17/09. For personal use only.

ANRV360-ES39-22 ARI 10 October 2008 9:54
Richardson JB, Burgess ND. 1999. Sporomorph evolution in the Anglo-Welsh basin: tempo and parallelism.
In The Evolution of Plant Architecture, ed. MH Kurmann, AR Hemsley, pp. 35–49. Richmond, Surrey, UK:
R. Bot. Gard. Kew
Rickards RB. 2000. The age of the earliest club mosses: the Silurian Baragwanathia flora in Victoria, Australia.
Geol. Mag. 137:207–9
Rothwell G. 1995. The fossil history of branching: implications for the phylogeny of land plants. In Experi-
mental and Molecular Approaches to Plant Biosystematics, ed. PC Hoch, AG Stephenson, pp. 71–86. St. Louis:
Mo. Bot. Gard.
Sanderson MJ. 2003. Molecular data from 27 proteins do not support a Precambrian orgin of land plants. Am.
J. Bot. 90(6):954–56
Shear WA, Selden PA. 2001. Rustling in the undergrowth: animals in early terrestrial ecosystems. See Gensel
& Edwards 2001, pp. 29–51
Steemans P. 1999. Pal´
eodiversification des spores et des cryptospores de l’Ordovicien au D´
evonien inf´
erieur.
Geobios 32(2):341–52
Steemans P. 2000. Miospore evolution from the Ordovician to the Silurian. Rev. Palaeobot. Palynol. 113:189–96
Steemans P, le H´
eriss´
e A, Bozdogan N. 1996. Ordovician and Silurian cryptospores and miospores from
southeastern Turkey. Rev. Palaeobot. Palynol. 93:35–76
Steemans P, Wellman CH, Filatoff J. 2007. Palaeophytogeographical and palaeoecological implications of a
miospore assemblage of earliest Devonian (Lochkovian) age from Saudi Arabia. Palaeogeogr. Palaeoclimatol.
Palaeoecol. 250:237–54
Stein WE, Mannolini F, Hernick LV, Landing E, Berry CM. 2007. Giant cladoxylopsid trees solve the enigma
of the Earth’s earliest forest stumps at Gilboa. Nature 446:904–7
Strother PK. 2000. Cryptospores: The origin and early evolution of the terrestrial flora. See Gastaldo &
DiMichele 2000, pp. 3–20
Strother PK, Al-Hajri SA, Traverse A. 1996. New evidence for land plants from the lower Middle Ordovician
of Saudi Arabia. Geology 24:55–58
Strother PK, Beck JH. 2000. Spore-like microfossils from Middle Cambrian strata: expanding the meaning
of the term cryptospore. In Pollen and Spores: Morphology and Biology, ed. MM Harley, CM Morton,
S Blackmore, pp. 413–424. Richmond, Surrey, UK: R. Bot. Gard. Kew
Strother PK, Wood GD, Taylor WA, Beck JH. 2004. Middle Cambrian cryptospores and the origin of land
plants. Mem. Assoc. Australas. Palaeontol. 29:99–113
Taylor WA. 1996. Ultrastructure of lower Paleozoic dyads from southern Ohio. Rev. Palaeobot. Palynol. 92:269–
79
Taylor WA. 2003. Ultrastructure of selected Silurian trilete spores and the putative Ordovician trilete spore
Virgatisporites.Rev. Palaeobot. Palynol. 126:211–23
Tims JD, Chambers TC. 1984. Rhyniophytina and Trimerophytina from the early land flora of Victoria,
Australia. Palaeontology 27:265–79
Tomescu AMF, Rothwell GW, Honegger R. 2006. Cyanobacterial macrophytes in an Early Silurian
(Llandovery) continental biota: Passage Creek, lower Massanutten Sandstone, Virginia, USA. Lethaia
39:329–38
Van Bergen PF, Blokker P, Collinson ME, Sinninghe Damst´
e JS, de Leeuw JW. 2004. Structural biomacro-
molecules in plants: what can be learnt from the fossil record? In Evolution of Plant Physiology, ed. AR
Hemsley, I Poole, pp. 133–54. London/Amsterdam: Elsevier
Wellman CH. 1995. “Phytodebris” from Scottish Silurian and Lower Devonian continental deposits. Rev.
Palaeobot. Palynol. 84:255–79
Wellman CH. 1996. Cryptospores from the type area of the Caradoc Series in southern Britain. Spec. Pap.
Palaeontol. 55:103–36.
Wellman CH. 1999. Ordovician land plants: evidence and interpretation. Acta Univ. Carol.-Geol. 43:275–77
Wellman CH. 2004. Dating the origin of land plants. In Telling the Evolutionary Time: Molecular Clocks and the
Fossil Record, ed. PJC Donoghue, MP Smith, pp. 119–41. London: Taylor & Francis
Wellman CH, Edwards D, Axe L. 1998a. Permanent dyads in sporangia and spore masses from the Lower
Devonian of the Welsh Borderland. Bot. J. Linn. Soc. 127:117–47
476 Gensel
Annu. Rev. Ecol. Evol. Syst. 2008.39:459-477. Downloaded from arjournals.annualreviews.org
by Aligarh Muslim University on 08/17/09. For personal use only.

ANRV360-ES39-22 ARI 10 October 2008 9:54
Wellman CH, Edwards D, Axe L. 1998b. Ultrastructure of laevigate hilate cryptospores in sporangia and
spore masses from the Upper Silurian and Lower Devonian of the Welsh Borderland. Philos. Trans. R.
Soc. London Ser. B 353:1983–2004
Wellman CH, Gray J. 2000. The microfossil record of early land plants. Philos. Trans. R. Soc. London Ser. B
355:717–32
Wellman CH, Habgood K, Jenkins G, Richardson JB. 2000. A new plant assemblage (microfossil and megafos-
sil) from the Lower Old Red Sandstone of the Anglo-Welsh Basin: Its implications for the palaeoecology
of early terrestrial ecosystems. Rev. Palaeobot. Palynol. 109:161–96
Wellman CH, Osterloff PL, Mohiuddin U. 2003. Fragments of the earliest land plants. Nature 425:282–85
www.annualreviews.org •The Earliest Land Plants 477
Annu. Rev. Ecol. Evol. Syst. 2008.39:459-477. Downloaded from arjournals.annualreviews.org
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Annual Review of
Ecology, Evolution,
and Systematics
Volume 39, 2008
Contents
Top Predators as Conservation Tools: Ecological Rationale,
Assumptions, and Efficacy
Fabrizio Sergio, Tim Caro, Danielle Brown, Barbara Clucas, Jennifer Hunter,
James Ketchum, Katherine McHugh, and Fernando Hiraldo pppppppppppppppppppppppppppppppp1
Revisiting the Impact of Inversions in Evolution: From Population
Genetic Markers to Drivers of Adaptive Shifts and Speciation?
Ary A. Hoffmann and Loren H. Rieseberg ppppppppppppppppppppppppppppppppppppppppppppppppppp21
Radial Symmetry, the Anterior/Posterior Axis, and Echinoderm
Hox Genes
Rich Mooi and Bruno David pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp43
The Great American Schism: Divergence of Marine Organisms After
the Rise of the Central American Isthmus
H.A. Lessios pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp63
The Ecological Performance of Protected Areas
Kevin J. Gaston, Sarah F. Jackson, Lisette Cant ´u-Salazar,
and Gabriela Cruz-Pi ˜n´on ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp93
Morphological Integration and Developmental Modularity
Christian Peter Klingenberg pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp115
Herbivory from Individuals to Ecosystems
Oswald J. Schmitz ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp133
Stoichiometry and Nutrition of Plant Growth in Natural Communities
G¨oran I. ˚
Agren pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp153
Plague Minnow or Mosquito Fish? A Review of the Biology
and Impacts of Introduced Gambusia Species
Graham H. Pyke pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp171
The Impact of Natural Selection on the Genome: Emerging Patterns
in Drosophila and Arabidopsis
Stephen I. Wright and Peter Andolfatto ppppppppppppppppppppppppppppppppppppppppppppppppppp193
v
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Sanctions, Cooperation, and the Stability of Plant-Rhizosphere
Mutualisms
E. Toby Kiers and R. Ford Denison ppppppppppppppppppppppppppppppppppppppppppppppppppppppppp215
Shade Tolerance, a Key Plant Feature of Complex Nature
and Consequences
Fernando Valladares and ¨
Ulo Niinemets ppppppppppppppppppppppppppppppppppppppppppppppppppp237
The Impacts of Fisheries on Marine Ecosystems and the Transition to
Ecosystem-Based Management
Larry B. Crowder, Elliott L. Hazen, Naomi Avissar, Rhema Bjorkland,
Catherine Latanich, and Matthew B. Ogburn ppppppppppppppppppppppppppppppppppppppppppppp259
The Performance of the Endangered Species Act
Mark W. Schwartz pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp279
Phylogenetic Approaches to the Study of Extinction
Andy Purvis pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp301
Adaptation to Marginal Habitats
Tadeusz J. Kawecki pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp321
Conspecific Brood Parasitism in Birds: A Life-History Perspective
Bruce E. Lyon and John McA. Eadie ppppppppppppppppppppppppppppppppppppppppppppppppppppppp343
Stratocladistics: Integrating Temporal Data and Character Data
in Phylogenetic Inference
Daniel C. Fisher ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp365
The Evolution of Animal Weapons
Douglas J. Emlen pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp387
Unpacking β: Within-Host Dynamics and the Evolutionary Ecology
of Pathogen Transmission
Michael F. Antolin ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp415
Evolutionary Ecology of Figs and Their Associates: Recent Progress
and Outstanding Puzzles
Edward Allen Herre, K. Charlotte Jand´er, and Carlos Alberto Machado pppppppppppppppp439
The Earliest Land Plants
Patricia G. Gensel ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp459
Spatial Dynamics of Foodwebs
Priyanga Amarasekare pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp479
Species Selection: Theory and Data
David Jablonski pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp501
vi Contents
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New Answers for Old Questions: The Evolutionary Quantitative
Genetics of Wild Animal Populations
Loeske E.B. Kruuk, Jon Slate, and Alastair J. Wilson pppppppppppppppppppppppppppppppppppp525
Wake Up and Smell the Roses: The Ecology and Evolution
of Floral Scent
Robert A. Raguso pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp549
Ever Since Owen: Changing Perspectives on the Early Evolution
of Tetrapods
Michael I. Coates, Marcello Ruta, and Matt Friedman ppppppppppppppppppppppppppppppppppp571
Pandora’s Box Contained Bait: The Global Problem of Introduced
Earthworms
Paul F. Hendrix, Mac A. Callaham, Jr., John M. Drake, Ching-Yu Huang,
Sam W. James, Bruce A. Snyder, and Weixin Zhang pppppppppppppppppppppppppppppppppppppp593
Trait-Based Community Ecology of Phytoplankton
Elena Litchman and Christopher A. Klausmeier pppppppppppppppppppppppppppppppppppppppppp615
What Limits Trees in C4Grasslands and Savannas?
William J. Bond ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp641
Indexes
Cumulative Index of Contributing Authors, Volumes 35–39 ppppppppppppppppppppppppppp661
Cumulative Index of Chapter Titles, Volumes 35–39 pppppppppppppppppppppppppppppppppppp665
Errata
An online log of corrections to Annual Review of Ecology, Evolution, and Systematics
articles may be found at http://ecolsys.annualreviews.org/errata.shtml
Contents vii
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