Structure of the Earliest Leaves: Adaptations to High Concentrations of Atmospheric CO

2
Author(s): HaoShougang, CharlesB.Beck, and WangDeming
Source: International Journal of Plant Sciences, Vol. 164, No. 1 (January 2003), pp. 71-75
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71
Int. J. Plant Sci. 164(1):7175. 2003.
2003 by The University of Chicago. All rights reserved.
1058-5893/2003/16401-0008$15.00
STRUCTURE OF THE EARLIEST LEAVES: ADAPTATIONS TO HIGH
CONCENTRATIONS OF ATMOSPHERIC CO
2
Hao Shougang,
1,
* Charles B. Beck,
2,
and Wang Deming*
*Department of Geology, Peking University, Beijing 100871, Peoples Republic of China; and Museum of Paleontology,
University of Michigan, Ann Arbor, Michigan 48109, U.S.A.
New fossils of the early Devonian plant Eophyllophyton bellum provide morphological and anatomical
information that contributes to an understanding of the origin and early evolution of the megaphyll. These
earliest leaves are characterized by leaf divisions, apparently arranged in several planes, that possess branching
venation and a mesophyll of longitudinally elongate cells lacking differentiation into palisade and spongy
layers. These features support the hypothesis that the megaphyll was derived from an axial branching system.
The small size and deeply incised margin of these leaves indicate an adaptation to an environment of heat
stress and high concentration of atmospheric CO
2
. Whereas the available evidence indicates that the megaphyll
evolved during the early Devonian, a period of harsh environmental conditions, the evolution and radiation
of larger megaphylls was apparently correlated with a massive drop in atmospheric CO
2
during the late
Devonian and early Carboniferous.
Keywords: Early Devonian, Eophyllophyton bellum, megaphyll, structure, atmospheric CO
2
.
Introduction
The origin and evolution of the leaf was an important evo-
lutionary event affecting all terrestrial life on Earth. Jefferey
(1917) categorized leaves as microphylls and megaphylls and
emphasized the evolutionary signicance of this division.
Among vascular cryptogams (nonseed plants), microphylls are
usually small leaves, each with a single vein that is the exten-
sion of a leaf trace from the vascular column of the stem into
the leaf. Megaphylls, in contrast, are usually larger leaves char-
acterized by multiple veins that diverge as one or more leaf
traces from the stem vascular system. Immediately above the
level of departure of the leaf traces, there is usually a region
of parenchyma in the vascular cylinder called a leaf gap.
As noted by Foster and Gifford (1974), although micro-
phylls are usually small, size is not the signicant feature in
the recognition of this leaf type but rather its distinctive vas-
culature. They point out that within the Lycopsida, Selaginella
has very small leaves, but those of Isoetes are much larger, in
one species attaining a length of up to 50 cm. Each leaf, how-
ever, is characterized by a single vein and is, thus, a microphyll.
Among extinct plants with microphylls, even large plants such
as Lepidodendron bore leaves sometimes reaching lengths of
as much as 78 cm but vascularized by only a single vein (Stew-
art and Rothwell 1993).
The most signicant character of a megaphyll is also the
vasculature of the leaf, not its size. Whereas in most plants
with megaphylls the departure from the stem of the leaf vas-
culature is associated with a leaf gap, some extant ferns have
solid vascular columns (protosteles) and, thus, no leaf gaps
1
E-mail sghao@pku.edu.cn.
2
E-mail chbeck@umich.edu.
Manuscript received March 2002; revised manuscript received August 2002.
(Foster and Gifford 1974). We can conclude, therefore, that
among vascular cryptogams, the distinctive feature of a mi-
crophyll is the presence of a single vein and of a megaphyll
the presence of several to many veins, often branched, in each
leaf.
Bower (1935) postulated that microphylls and megaphylls
represent two separate evolutionary pathways. Among the sev-
eral competing hypotheses of the origin of microphylls,
Bowers enation hypothesis is the most plausible. According
to Bower, an enation is an outgrowth froma stemthat, through
time, in a series of related taxa becomes vascularized. This
hypothesis is supported by an evolutionary series of related
Devonian taxa, Sawdonia (and Discalis), Asteroxylon, and
Drepanophycus. Sawdonia produced spinelike, unvascularized
appendages (enations). In Asteroxylon, a single trace extended
to the base of the enations, and in Drepanophycus it extended
into the spinelike leaf (Banks 1968, 1975; Gensel et al. 1975;
Gensel 1984; Hao 1989; Niklas and Banks 1990). Megaphylls
are thought to have evolved fromsmall, photosynthetic, lateral
branch systems in a manner proposed by Zimmermann (1952).
According to Zimmermanns telome theory, the following
transformations took place in leaess, dichotomous plants dur-
ing the evolution of the megaphyll, beginning with overtop-
ping, i.e., the establishment of unequal dichotomy resulting
in a main axis bearing lateral dichotomous branch systems.
This was followed by planation (i.e., attening) and ultimately
webbing (production of lamina) of dichotomous lateral branch
systems. Although this is a widely accepted concept of the
evolution of megaphylls, Beck (1970) pointed out that the
telome theory is not supported by a single, well-dened evo-
lutionary series of related fossil taxa. We may ask, therefore,
when and how did the megaphyll evolve from leaess axes,
and what was the relationship to the environment of this sig-
nicant development? Although these issues have been exten-
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72 INTERNATIONAL JOURNAL OF PLANT SCIENCES
Table 1
Morphological and Quantitative Data for Leaves in Transverse Sections
Character
Petiole
(BUPB1-8-5;
g. 3d)
Basal region of leaf
(BH-04;
g. 3c)
Basal region of leaf
(BH-02;
g. 3b)
Distal segment
(BUHB1-8-3;
g. 3a)
Shape of division or distal segment Solid, elliptic Planate, multiramous Planate, trichotomous Planate
Width (mm) 250 # 120 1210 1200 1130
Thickness (thinnest # thickest region) (mm) 40 # 200 45 # 180 20 # 100
Diameter of vein (mm) 58 # 94 78 # 110 42 # 55
Number of tracheids visible in vein 17 18 11
Diameter of tracheids in vein (mm) 826 7.528 7.516
Order of maturation of primary xylem in vein Centrarch (?) Centrarch
Diameter of mesophyll cells (mm) 2055 1845 2050
sively discussed, based on discoveries in the fossil record (Gen-
sel and Andrews 1984; Stewart and Rothwell 1993), there are
still no denitive answers.
The fossil record shows that the megaphyll did not become
widespread until the end of the Devonian period, ca. 360 mil-
lion years ago, nearly 40 million years after the evolution of
the earliest vascular plants. Recently, Beerling et al. (2001)
proposed an explanation for the long delay in the evolution
of the megaphyll. They observe that the occurrence of mega-
phylls in the late Devonian is correlated with a massive drop
in atmospheric CO
2
during the Devonian period, some
410363 million years ago. They suggest that leaess plants
of the early Devonian, which inhabited a high CO
2
environ-
ment, would not have needed megaphylls with broad lamina
and many stomata and, further, that broadly laminate mega-
phylls would have suffered lethal overheating in such an en-
vironment because of their greater interception of solar energy
and low rate of transpiration.
In this article, we reinvestigate the leaves of Eophyllophyton
bellumand provide evidence for the viewpoint that these leaves
were, in fact, megaphylls. We suggest, further, that their struc-
tural characteristicssmall size, incised margins, and undif-
ferentiated mesophyllwere adaptations to an environment
of heat stress and high CO
2
concentration. This coevolutionary
relationship between megaphylls and environment probably
resulted in a gradual change in size and complexity of the
anatomy and morphology of leaves as the concentration of
atmospheric CO
2
diminished during the Devonian.
Material and Methods
The new specimens that we report on here are from a col-
lection in the Department of Geology, Peking University, from
the same outcrops as the type specimens of Eophyllophyton
bellum established by Hao and Beck (1993). These specimens
were collected from the second and third lithological units, of
Pragian age (Hao and Gensel 2001), in the Posongchong For-
mation near Zhichang village in the Wenshan district, south-
eastern Yunnan, China. Most of the leaf compressions are
converted into charcoal, but some parts of a few specimens
are permineralized. When subjected to a bulk maceration in
hydrochloric and hydrouoric acids, they fall apart into thin
pieces, thus negating any possibility of determining accurately
their three-dimensional form. Consequently, several leaves
were transferred from the matrix using Waltons transfer tech-
nique (Walton 1953) and were then observed by scanning elec-
tron microscopy (SEM). In order to observe internal structure,
64 thin sections of ve partially permineralized specimens were
prepared according to the technique of Stein et al. (1982). The
thin sections were prepared along leaves, from the petiole to
the lamina of the most distal division. Selected sections are
illustrated in gure 3a3d, and dimensions are provided in
table 1.
Results
The leaves of Eophyllophyton bellum were borne laterally
or terminally on the axis. They are small and fan shaped, with
the laminae highly dissected; are either vegetative or fertile;
and range in width from 1.7 to 4.8 mm, in length from 2.2
to 5.0 mm, and in thickness from 40 to 200 mm. They seem
to occur in clusters at the ends of small lateral branches. Their
dichotomous pattern of division reects an isotomous or an-
isotomous venation, with each subdivision of the lamina served
by a single vein. In some instances, the pattern of division of
the lamina is almost pinnate (g. 1).
We believe that one cluster, consisting of two leaves curved
inward toward each other (g. 2a), might be fertile, although
we have no denitive evidence to support this view. Each leaf
is ca. 1.6 mm wide and 2.3 mm long. The lower leaf shows
inner divisions at or near the base, exposed because the outer
division (arrow S) is missing.
A few ridges (g. 2a, 2b, arrows) parallel to the long axis
of the leaves appear to represent leaf divisions that had broken
off in the matrix. This indicates that the subdivisions of the
leaf were not held strictly in a single plane. This view is sup-
ported by evidence in the thin sections (g. 3b, 3c), in which
transverse segments of different leaf divisions occur in several
planes. The margins of the laminate divisions are deeply in-
cised, almost laciniate (gs. 1, 2b). Unfortunately, we have not
observed any preserved epidermis in the SEM photographs;
thus, we do not knowthe frequency or distribution of stomata.
Only a very short, poorly preserved segment of the single-
layered epidermis has been observed in a thin section (g. 3e,
arrow).
The leaf lamina is comprised of a uniform mesophyll four
to six cell layers thick. Mesophyll cells, which appear to be
randomly arranged, are polygonal or hexagonal in transverse
view (g. 3f ), elongate with oblique end walls in longitudinal
view (g. 3h), and 1550 mm in width and 120240 mm in
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HAO ET AL.STRUCTURE OF THE EARLIEST LEAVES 73
Fig. 1 Leaves of Eophyllophyton bellum (scale bar p 0.5 mm)
showing leaf laminae, pattern of dissection, bifurcating venation (ar-
rows), and pinnately divided leaf (BUPB 144-2, BUPB 188, BUPB 144-
6). a, b, Vegetative leaves. c, Fertile leaves.
Fig. 2 SEM photographs of leaves of Eophyllophyton bellum. a,
Possible fertile cluster consisting of two leaves, with evidence of at-
tachment sites of missing divisions (arrows), and a missing distal seg-
ment (arrowS) (scale bar p0.5 mm; specimen HS 05). b, Leaf showing
position of attachment of a missing division (arrow) (scale bar p0.5
mm; HS 12). c, Leaf lamina; note overlapping divisions (scale bar p
100 mm; HS 06).
length. The mesophyll is structurally similar to that of a mod-
ern isobilateral leaf without differentiation into layers of pal-
isade and spongy parenchyma but differs in its lack of a con-
spicuous system of intercellular air channels. At high
magnication, the appearance of closely spaced pits in the
walls of the mesophyll cells (g. 3g, 3h) is probably the result
of degradation or the presence in the cells of small mineral
octahedra, which create a false impression.
A main vein in the petiole, or near the base of the leaf, is
relatively thick, containing more than 10 tracheids (g. 3b,
3d, 3e; table 1). It is characterized by a centrarch primary
xylem strand like that of the axis. We have not observed
second-order veins in lateral divisions of the structurally pre-
served laminae that also contain main veins, but we have seen
such veins in the compression specimens (g. 1a1c, arrows).
Presumed second- (or third-?) order veins that we have ob-
served in some sections of distal laminar segments are very
small and contain only one or, at most, several tracheids, as
seen in transverse and longitudinal sections (g. 3a, 3h). The
tracheids exhibit a helically sculptured pattern with small pits
in the wall between the secondary thickenings, like those of
the vascular column of the plant axis.
Discussion
The evidence presented above corroborates our earlier con-
clusion that the early Devonian (Pragian, ca. 400 million years
ago) plant Eophyllophyton bellum bore megaphyllous leaves,
i.e., laminate leaves with a branching system of veins. Fur-
thermore, the megaphyll of Eophyllophyton exhibits charac-
teristics that we interpret to have been derived from an axial
branching system. That the laminar divisions appear not to
have been held in one plane might indicate that the process of
planation was incomplete and that webbing of the divisions
occurred prior to planation in these leaves. However, the ap-
parent disposition of the subdivisions of the leaves could be
an artifact of preservation. The longitudinally elongate meso-
phyll cells, the similarity of the tracheary elements in the plant
axes and in the leaf veins, the homogeneous nature of the leaf
mesophyll, and the fact that the leaves lack a well-developed
systemof intercellular air channels all indicate that these mega-
phylls evolved from an axial branch system.
Beerling et al. (2001) suggested that the evolution of broadly
laminate megaphylls, which appear rst in late Devonian
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74 INTERNATIONAL JOURNAL OF PLANT SCIENCES
Fig. 3 Leaf sections of Eophyllophyton bellum. ad, Transverse sections through a petiole (d), basal region of leaves (b, c), and distal segment
(a) showing veins (i.e., primary xylem of vascular bundles; arrows) (scale bar p100 mm; BUPB 1-8-3, BH-02, BH-04, BUPB 1-8-5). e, Enlarged
view of b showing a centrarch primary xylem strand and a few epidermal cells of a single layer (arrow) (scale bar p 50 mm). f, g, Enlargement
of mesophyll showing cell shapes in transverse view and abundant pyrite octahedra within cell lumina (see discussion in text) (scale bar p 15
mm; BUPB 1-8-12, BUPB 1-8-6). h, Longitudinal section through vein showing one or two tracheids with helically sculptured walls and longi-
tudinally elongate mesophyll cells parallel to leaf surface (scale bar p 20 mm; BUPB 1-9-12).
strata, was correlated with a drop in atmospheric CO
2
and
establishment of more moderate climatic conditions. The fos-
sils of Eophyllophyton, however, were collected from south-
eastern Yunnan located during the early Devonian in an equa-
torial zone at ca. 0 latitude (Fang et al. 1989; Hao and Gensel
1998). Consequently, we conclude that the evolution of the
rst megaphylls, as demonstrated by the leaves of E. bellum,
occurred during a period of high atmospheric concentration
of CO
2
.
The leaves of Eophyllophyton are characterized by several
features that we believe were structural adaptations for sur-
vival of a plant with laminate, megaphyllous leaves in an atmo-
sphere of high CO
2
concentration such as that of the early
Devonian (Berner 1994). Their small size and, especially, their
high degree of dissection would have minimized the problem
of heating by solar radiation even if the rate of transpiration
were low (Kenrick 2001). Although we have no knowledge of
the frequency of stomata in the epidermis of Eophyllophyton
leaves, in an atmosphere of high CO
2
concentration one would
assume that the frequency would be low (Edwards et al. 1993;
Edwards 1998). Plants such as Adoketophyton subverticilla-
tum (Li and Edwards 1992) and Celatheca beckii (Hao and
Gensel 1995), contemporaries of Eophyllophyton, also bore
planate leaike organs that were small or highly dissected,
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HAO ET AL.STRUCTURE OF THE EARLIEST LEAVES 75
characteristics similar to those of Eophyllophyton, which
probably compensated for the harsh environmental conditions
and facilitated the evolution of laminate megaphylls in plants
of the early Devonian. It is probable that the presence of mega-
phylls such as those of Eophyllophyton contributed to the
increase of O
2
and the decrease of CO
2
in the early Devonian
atmosphere (Berner 1997, 2001), thus contributing to more
favorable conditions under which large megaphylls had
evolved by the late Devonian.
Acknowledgments
We thank D.-B. Ni, C.-Y. Zhou, and Q.-Y. Jia for help with
fossil preparation. This study was supported by the National
Natural Science Foundation of China (40232019), the Major
Research Projects of the Ministry of Science and Technology,
China (G2000077700), and the Chinese Stratigraphy Project
of the Ministry of Science and Technology, China (2001 DEA
20020-5).
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