American Journal of Botany 100(11): 2219–2230. 2013.
A CALLIXYLON (ARCHAEOPTERIDALES,
PROGYMNOSPERMOPSIDA) TRUNK WITH PRESERVED SECONDARY
PHLOEM FROM THE LATE DEVONIAN OF MOROCCO1
ANNE-LAURE DECOMBEIX2 AND BRIGITTE MEYER-BERTHAUD
Université Montpellier 2 and CNRS, UMR AMAP, Montpellier, F-34000 France
• Premise of the study: During the Devonian, the evolution of secondary phloem produced by a bifacial vascular cambium was
a key innovation that increased the ability of plants within the lignophyte clade to redistribute photosynthates and other organic
compounds throughout their body. Unraveling the secondary phloem anatomy of the first arborescent lignophytes is crucial to
understand the evolution of this tissue and the physiology of early trees.
• Methods: A 10 cm wide stem of Callixylon with preserved secondary phloem from the Famennian of Morocco is described
using thin-sections.
• Key results: The secondary phloem of this Callixylon zalesskyi-type of stem is composed of fibers, sclereids, rays, axial parenchyma, and putative sieve cells. Fibers differentiate early and are relatively abundant in the inner phloem. In the older phloem,
fibers are arranged in tangential bands alternating with extensive layers of axial parenchyma. Changes between the young and
old phloem involve the periclinal division and radial elongation of the axial parenchyma cells. The presence of fibers in the
inner, presumably functional phloem, combined with evidence for rhythmicity in the production of different phloem cell types
are documented for the first time in detail in an archaeopteridalean progymnosperm. No periderm was observed within the
preserved seven millimeters of bark tissues.
• Conclusions: The secondary phloem anatomy supports a close affinity of archaeopteridalean progymnosperms with both aneurophytalean progymnosperms and seed plants. The production of secondary phloem might have provided an advantage to these
first arborescent lignophytes over other types of Devonian early trees, especially in dry conditions.
Key words: Callixylon; cambium; Devonian; lignophytes; Morocco; progymnosperms; secondary phloem.
One of the keystones of Devonian paleobotany was the description by C. B. Beck in 1960 of the anatomical connection
between Archaeopteris fern-like foliage and a branch with
Callixylon conifer-like wood (Beck, 1960a, b). This discovery
led to the recognition of a new group of Devonian-Carboniferous
plants characterized by a gymnospermous vegetative body and
reproduction by spores, the progymnosperms (Beck, 1960b).
Today, the progymnosperms include three orders, the Aneurophytales (Mid-Late Devonian), the Archaeopteridales (Mid-Late
Devonian), and the Protopityales (Early Carboniferous) (Beck,
1976; Taylor et al., 2009). While the relationships among these
three taxa are still unresolved, the progymnosperms yield a fundamental position in plant phylogeny because they include the
ancestor of the seed plants (e.g., see Rothwell & Serbet, 1994;
Crane et al., 2004; Hilton and Bateman, 2006). Together, the
progymnosperms and the spermatophytes form the lignophyte
clade (Kenrick and Crane, 1997), the major synapomorphy of
1 Manuscript received 7 May 2013; revision accepted 15 July 2013.
The authors thank the Services Géologiques du Maroc (Rabat, Morocco)
for issuing work permits and exporting samples, and J. Wendt, B. Kaufmann,
and S. E. Scheckler for their help in the field. Comments on the manuscript
by Edith Taylor and an anonymous reviewer are gratefully acknowledged.
This work is partly funded by the French National Agency for Research,
project ANR TERRES 2010 BLAN 607 02. AMAP (Botany and Computational Plant Architecture) is a joint research unit which associates
CIRAD (UMR51), CNRS (UMR5120), INRA (UMR931), IRD (R123),
and Montpellier 2 University (UM2); http://amap.cirad.fr/.
2 Author for correspondence (e-mail: [email protected])
doi:10.3732/ajb.1300167
which is the possession of a bifacial vascular cambium, i.e., a
lateral meristem that produces both secondary xylem and secondary phloem. This is in contrast with the unifacial vascular cambium that evolved in other extinct and extant groups of plants
and which only produces secondary xylem (Eggert and Gaunt,
1973; Eggert and Kanemoto, 1977; Cichan, 1985a, b, 1986).
Among the progymnosperms, the Archaeopteridales are of
particular interest because they are among the oldest plants
to have reached the tree habit during the Middle Devonian (e.g.,
see Meyer-Berthaud and Decombeix, 2007; Meyer-Berthaud
et al., 2010; Cornet et al., 2012). From an ecological point of
view, the abundance and worldwide distribution of archaeopteridalean fossils during the Late Devonian indicate that this
group was a major component of ecosystems worldwide until
their extinction around the Devonian/Carboniferous boundary
(Beerbower et al., 1992). Paleosol studies show that they were
able to grow in better drained soils than contemporaneous trees,
forming dense stands that provided the humidity necessary for
their free-sporing (heterosporous) reproduction (Beck, 1964;
Driese et al., 1997; Mintz et al., 2010).
From an evolutionary point of view, anatomical studies have
highlighted several “modern” characters of Archaeopteridales
vegetative body. They were the first plants to combine the possession of true leaves, a deep root system, and a eustelic vascular
organization (Beck, 1981; Beck and Wight, 1988). Architectural
analyses of their aerial and underground parts have revealed a
lateral branching syndrome comparable to the axillary branching of seed plants (Meyer-Berthaud et al., 1999), the presence
of latent meristems capable of producing adventitious shoots
or roots for crown repair or vegetative reproduction (Trivett,
1993; Meyer-Berthaud et al., 1999), and the production of large
American Journal of Botany 100(11): 2219–2230, 2013; http://www.amjbot.org/ © 2013 Botanical Society of America
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lateral roots of endogeneous origin (Meyer-Berthaud et al.,
2013). The presence of a circular-patterned secondary xylem at
branch junctions indicates the existence in Archaeopteridales of
a mechanism of polar auxin flow comparable to that of extant
seed plants (Rothwell and Lev-Yadun, 2005).
Despite this wealth of information, several questions about
the biology of the Archaeopteridales remain to be solved. One
of them concerns the anatomy of their secondary phloem, the tissue responsible for the active conduction of hormones, photosynthates, and other assimilates throughout these early trees that
have been estimated to reach up to 30 m in height (Mosbrugger,
1990). Most studies of the vegetative anatomy of Archaeopteridales are indeed based either on small branches or on pieces of
trunks that are decorticated, i.e., with no tissues preserved outside
the secondary xylem. As a result, there is little information about
the secondary phloem anatomy of Archaeopteridales, usually described as simple and parenchymatous (Arnold, 1930a, 1930b;
Lemoigne et al., 1983).
Here we describe a new trunk with Callixylon wood from
the Late Devonian of Morocco with several millimeters of preserved secondary phloem. This specimen allows us to study in
detail the anatomy of this tissue and to analyze the anatomical
changes linked to maturation. We show that archaeopteridalean
trees had a complex secondary phloem containing fibers, comparable to that of the aneurophytalean progymnosperms and of
some Early Carboniferous seed plants. These results provide
new anatomical characters that support the affinities of the Archaeopteridales with the Aneurophytales and with the seed
plants, and fill a gap in our understanding of phloem evolution
in early lignophytes. They also open the door to further studies
on the physiology of the first trees.
MATERIALS AND METHODS
The specimen under study is an 11 cm long and 10 cm wide portion of trunk
preserved in calcite. It was collected in 1998 by B. Meyer-Berthaud and S. E.
Scheckler on the northwest slope of Jebel El Mrakib in the eastern Anti-Atlas
mountain range, Morocco. The locality also contains other remains of Archaeopteridales (Meyer-Berthaud et al., 1999, 2000, 2013), cladoxylopsids (Soria et al.,
2001), and a few lycopsid axes. The plants occur in a marine horizon that corresponds to a basinal deposit probably close to an island bordering the West
African craton. Its early Famennian age is indicated by the associated marine
fauna (see details in Meyer-Berthaud et al., 1997).
Due to the lack of good preservation of organic matter, the trunk was studied
using thin-sections (Hass and Rowe, 1999) in transverse (5 sections), radial (9), and
tangential (5) planes. Observation and photography were conducted using Sony
XCD-U100CR digital cameras attached to an Olympus SZX12 stereomicroscope
and to an Olympus BX51 compound microscope. Images were captured using
Archimed software (Microvision Instruments, Evry, France) and plates were
composed with Adobe Photoshop CS5 version 12.0 (Adobe Systems, San José,
California, USA). Transformations made to the images in Photoshop include
cropping, rotation, and adjustment of contrast. Means are given for at least 50
measurements, unless otherwise stated in the text. The specimen and corresponding slides are kept in the Collections de Paléobotanique de l’Université
Montpellier 2 under the accession number MD22.
RESULTS
General aspect (Fig. 1A)— The trunk is 9 × 11 cm in diameter. Its center contains a large primary body with parenchymatous pith over 1 cm in diameter surrounded by numerous
primary vascular strands. There are about 4.3-4.5 cm of wood
with apparent growth layers. A large portion of the outer surface of the trunk is covered with a layer of secondary phloem up
to 7 mm thick. There is no evidence of periderm.
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Stele and vascular traces (Figs. 1B, 2A-F)— The primary
vascular system of the trunk has a eustelic organization (Figs. 1, 2A).
The pith is 1.2 cm wide and composed of parenchymatous cells
48-175 µm (mean: 109 µm) in diameter. The cells are polygonal
and isodiametric in the central part of the pith. They tend to
be stretched radially close to the margin. Cells with black content are scattered throughout the pith (e.g., see Fig. 2A, E).
Transverse sections also show groups of cells showing darker,
sometimes patterned, walls. Longitudinal sections, however, indicate that neither sclereids, nor fibers, nor tracheids occur in
the pith and that the supposedly thick walls of such cells are
artifactual.
A total of 25 primary vascular strands can be observed on a
transverse section (Fig. 1B). The majority of them are located
in contact with the secondary xylem, a few might be separated
from it by a single layer of parenchyma (Figs. 1B, 2A-D). The
strands range from 150 to 500 µm in diameter. The largest ones,
which are presumably close to the level of production of a vascular trace, have a mesarch maturation (Fig. 2A, B). The smallest look almost endarch (Fig. 2C) or do not even show any clear
conspicuous protoxylem strand in transverse section (Fig. 2D).
Metaxylem tracheids range from 16 to 62 µm in diameter and
protoxylem tracheids, 7 to 12 µm (n = 30).
Vascular traces are produced by the division of a caulinar
strand, with the latter strand lying in a radial plane to the departing trace (Figs. 1B, 2E). Two departing traces can be seen on a
single transverse section (Fig. 1B). A relatively large trace is
visible within the wood cylinder (Fig. 2F).
Secondary xylem anatomy (Figs. 1, 2G-J)— The secondary
xylem is up to 4.5 cm in thickness (Fig. 1A). It is composed of
tracheids and rays containing parenchymatous cells and occasional ray tracheids (Fig. 2G-J). At least 14 distinct rings are
present (Fig. 1A). These rings are continuous around the trunk
and are marked by the presence of 1-3 rows of tracheids with a
reduced radial diameter (Fig. 2G). Measurements show that
these zones correspond to latewood according to Mork’s first
formula (Mork, 1928; Denne, 1989), i.e., the thickness of the
tracheid walls is larger than the diameter of the lumen.
The secondary xylem tracheids are rectangular to slightly
rounded or polygonal in transverse section (Fig. 2G, H). Their
radial diameter ranges from 20 to 53 µm (mean: 34 µm) in the
first centimeter of the wood and 20 to 59 µm (mean: 38 µm) in
the outermost part. The radial walls of the tracheids bear multiseriate bordered pits that are arranged in groups separated
by unpitted areas (Fig. 2J). The pits are 7-14 µm in diameter
(n = 30) and have an oval oblique aperture. Groups are composed of 8-12 pits and unpitted areas range from 15-30 µm. No
pitting was observed on tangential walls.
Rays are uniseriate to partly biseriate (Fig. 2I). In the outermost
part of the wood, they range from 2 to11 cells in height (mean: 4.7),
with 95% of them being 2 to 7 cells high. Ray tracheids may be
locally abundant. The parenchymatous cells that compose the majority of the rays are 19 to 33 µm (mean: 26 µm) wide and 16 to 55
µm (mean: 36 µm) high in tangential section. In radial section they
are procumbent, 64 to 169 µm (mean: 121 µm) long. Cross-field
pitting consists of several crowded oval pits (Fig. 2J).
Secondary phloem anatomy (Figs. 1A, 3, 4, and 5)— The
cambial zone is not well-preserved. Its position is marked by a
brown zone with a minimum thickness of 100-150 µm where
cellular detail is missing (Figs. 3A-C, 4A). The maximum
amount of preserved secondary phloem is 7 mm (Fig. 1A).
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DECOMBEIX AND MEYER-BERTHAUD—SECONDARY PHLOEM OF CALLIXYLON
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Fig. 1. Callixylon zalesskyi-type trunk with phloem from the Devonian of Morocco: General anatomy of specimen MD22. (A) Representative transverse section showing the central stele, wood, a large trace (T), and the position of the preserved secondary phloem (Ph2, dark gray); light gray represents
nonpreserved areas; camera lucida drawing of slide MD22-AbcS.1; scale bar = 1 cm. (B) Detail of the eustele showing the position of the primary xylem
strands and departing leaf traces (LT); camera lucida drawing of slide MD22-AbcS.1; scale bar = 2 mm.
Three types of cells can be identified in transverse sections
of the secondary phloem: (1) radially elongated thin-walled
cells corresponding to ray cells; (2) more or less isodiametric
thin-walled cells corresponding to axial parenchyma and putative sieve cells; and (3) thick-walled cells (Figs. 3, 5). In longitudinal section, the thick-walled cells appear to be of two
types: (1) long cells interpreted as fibers (Fig. 4A-D) and (2) short
cells, often in vertical rows, interpreted as sclereids (Fig. 4F).
The respective proportion of the different cell types varies
between the inner (younger) and the outer (older) phloem
(Figs. 3A, 4A, B).
conspicuous. Rare, unusual, elongated cells with irregular thick
walls in the outer part of the phloem might correspond to sclerified sieve cells (Fig. 4E).
Axial parenchyma—Axial parenchyma is the most abundant
cell type in the secondary phloem (Figs. 3A, 4B). It is composed
of large thin-walled cells that are isodiametric to higher than
wide in longitudinal section (e.g., see Fig. 4D). Most are empty
but some show a dark content (Figs. 3D, E, 4D). In cross sections
of the innermost (youngest) phloem, axial parenchyma cells are
rarely well-preserved (Figs. 3D, E, 5A). They are isodiametric
and measure 23-68 µm (mean: 45 µm) in diameter. In the older
phloem, parenchyma cells are well-preserved and abundant
(Figs. 3A, 5B, C). Their tangential diameter remains comparable (mean 47 µm) but their radial diameter increases to 50-122 µm
(mean: 76 µm) (Fig. 5B, C). In longitudinal sections, the parenchyma cells are 55-161 µm (mean: 97 µm) high (Fig. 4D, E).
Fibers—Fibers, i.e., thick-walled cells that are elongated in
longitudinal section, are very conspicuous in both the inner,
presumably functional, phloem and in the outer phloem (Figs.3,
4, 5). In transverse section, they are square to slightly rounded
(Figs. 3D, E, 5A-C) and measure 19-67 µm (mean: 38 µm) in
tangential diameter and 19-56 µm (mean: 33 µm) radially. Some
show a small oval to circular lumen, while others are totally
occluded by the secondary wall. In longitudinal section, the fibers are straight to slightly curved and very long, up to 9-12 mm
(Fig. 4A-D). The bending of some fiber ends along rays is suggestive of their intrusive growth (Fig. 4B).
Phloem rays—Although the cambial zone is not well-preserved there are some indications that the phloem rays are continuous with those of the secondary xylem. They are comparable
to them in height and width. Secondary phloem rays separate
2-10 rows of cells in transverse section (e.g., see Fig. 5B). They
are uniseriate, rarely partly biseriate, and 1-14 cells high with
95% of the rays 2-7 cells high, as in the secondary xylem
(Figs. 3A, D, 4A, B, 5B). These dimensions do not change
toward the outside of the phloem. Ray cells are slightly larger
than in the xylem. They range from 16 to 67 µm (mean: 35 µm)
µm wide and 15 to 78 µm (mean: 35µm) high in tangential section. They are longer than high in radial section (Fig. 4A, B, E),
with a length of 33-187 µm (mean: 104 µm).
Sieve cells—Although elongated, thin-walled cells are occasionally observed in longitudinal section, no undisputable sieve
cell has been observed. This is probably due in a large part to
the bad preservation of thin-walled cells in the inner part of the
phloem where sieve cells would be expected to be the most
Sclereids—Some sclereids occur in the secondary phloem
(Fig. 4F), either isolated or in short vertical rows. They can be
found either close to groups of fibers or isolated in the axial
parenchyma. They are present in both the old and young phloem
and are thus interpreted as being part of the functional phloem.
This does not exclude the possibility that some may result from
the late differentiation of axial parenchyma cells.
Anatomy of the inner phloem vs. outer phloem—While the
same cell types are present throughout the thickness of the secondary phloem, their respective proportion varies significantly
(Figs. 3A, 4A, B). This gives a very different aspect to the inner
(e.g., see Figs. 3C-E, 4A, C) and outer (e.g., see Figs. 4B, D, E,
5 B-D) regions of the tissue.
The younger part of the phloem (Ph2i in Figs. 3-5) is about
200-400 µm in thickness. In both transverse and longitudinal
sections, it has a compact aspect due to an apparent dominance
of the thick-walled cells (fibers and sclereids) (Figs. 3, 4A, B).
At low resolution, the thin-walled cells (axial parenchyma and
sieve cells) which are not well-preserved seem much less abundant. Radial sections observed at higher resolution, however,
show a regular alternation between thin- and thick-walled cells
resulting in a comparable number of each cell type in this part
of the phloem (Fig. 4C).
The older phloem exceeds 6 mm in thickness. In this part, the
proportion of thick-walled cells is significantly lower (Figs. 3A,
4B, D, E, 5B, C). For example, in a typical 250 µm × 250 µm
zone of the inner phloem there are 58 thick-walled cells, while
there are only 12 in a similar surface area in the outer phloem.
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Fig. 2. Callixylon zalesskyi-type trunk with phloem from the Devonian of Morocco: Primary vascular system (A-F) and secondary xylem anatomy
(G-J). (A) Detail of the stele showing the pith, two mesarch primary xylem strands and the inner secondary xylem; slide MD22-AbcS.1; scale bar = 200
µm. (B) Typical mesarch primary xylem strand; slide MD22-AbcS.1; scale bar = 200 µm. (C) Small, almost endarch primary xylem strand; slide MD22AbcS.1 ; scale bar = 100 µm. (D) Small group of primary xylem tracheids with no distinct protoxylem; slide MD22-AbcS.1; scale bar = 100 µm. (E)
Departing leaf trace (LT) with cauline primary vascular strand (arrow) laying in a radial plane to the trace; slide MD22-AbcS.1; scale bar = 200 µm. (F)
Radial section showing part of the pith (P) and secondary xylem (2×) and a large vascular trace (T) crossing the wood with parenchyma on its adaxial side
(arrow); slide MD22-Ca1R.1; scale bar = 1 mm. (G) Transverse section of the secondary xylem showing a layer of tracheids with reduced radial diameter;
slide MD22-AbcS.1; scale bar = 100 µm. (H) Transverse section of the secondary xylem in a region containing ray tracheids; slide MD22-AbcS.1; scale
bar = 50 µm. (I) Longitudinal section of the secondary xylem with low uniseriate rays; slide MD22-AaL1; scale bar = 100 µm. (J) Radial section of the
secondary xylem showing the grouped pits on the radial walls of the tracheids and rays (R) with cross-field areas containing several oval pits; slide MD22CbR1; scale bar = 40 µm.
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DECOMBEIX AND MEYER-BERTHAUD—SECONDARY PHLOEM OF CALLIXYLON
This gives a more parenchymatous aspect to the older phloem.
This change in the relative abundance of cell types between the
inner and outer parts of the phloem is rather abrupt (Figs. 3A, 4B).
Radial sections of the outer phloem show that the number of
thin-walled cells separating the fibers is higher, commonly
ranging from 2 to 5 (Fig. 4B, D, E), and that some vertical rows
are composed of very wide parenchyma cells (Fig. 4D). In addition, transverse sections show that the thick-walled cells are
arranged in tangential bands in the outer phloem, a pattern that
is not obvious in the inner part (Figs. 3A, 5B). The tangential
bands of fibers in the older phloem are usually 2 to 10 cells wide
tangentially and one cell thick, with occasionally two cells radially. Transverse sections also show that divisions of parenchyma
cells are exclusively periclinal. The number of parenchyma cells
varies not only between successive bands of fibers (Fig. 5B),
but also between two adjacent radial rows of parenchyma cells
(e.g., see Fig. 5C). The development of neighboring cells between tangential bands of fibers is highly coordinated with the
nondividing cells enlarging radially while the dividing cells
retain a small radial diameter. Interestingly, rays remain wellpreserved and straight in the outer part of the phloem (Figs.
4A, 5B), which suggests that the oldest portion of this tissue
may still have been functional.
DISCUSSION
Affinities of the trunk—The trunk with preserved phloem
possesses a eustele with mesarch primary xylem strands and secondary xylem tracheids that bear pits in groups separated by
unpitted areas. This is characteristic of stems of the archaeopteridalean genus Callixylon (Zalessky, 1911). To be able to
compare phloem anatomy among different species of Archaeopteridales in the future, it is necessary to consider the specific
affinities of the Moroccan trunk.
The taxonomy of Callixylon axes is based on characters
of the primary vascular system and wood anatomy. Recently,
Orlova and Jurina (2011) summarized known information about
the different species described to date and proposed four morphological groups: Trifilievii, Erianum, Newberryi, and Arnoldii.
The new specimen from Morocco can be clearly distinguished
from the two latter groups. The Arnoldii group, which includes
only C. arnoldii C.B. Beck (Beck, 1962), is characterized by a
radial pitting of the tracheids that is uniseriate and composed of
pits each with a circular aperture. This is in contrast with the
new specimen in which radial pits are multiseriate and have
oval apertures.
The new trunk also differs from taxa of the Newberryi group
by the lack of multiseriate rays. In this group, Callixylon newberryi (Dawson) Elkins & Wieland is the only taxon for which
the primary vascular anatomy is known (Arnold, 1931). Axes of
C. newberryi with a stele of comparable size to that of the Moroccan specimen have most of their primary xylem strands separated
from the secondary xylem by parenchyma, while this is not or
rarely the case in the new specimen.
The Trifilievii and Erianum groups include taxa with multiseriate radial pits showing an oblique apertures, and uni- to biseriate rays of various heights. The Trifilievii group lacks ray
tracheids, while they are present in the Erianum group, which is
thus the one most similar to the Moroccan trunk. Within this
Erianum group, Orlova and Jurina (2011) distinguish between
taxa that have abundant or more occasional ray tracheids. Species with occasional ray tracheids, similar to the situation in the
2223
new specimen, include Callixylon zalesskyi Arnold and C. petryi
C.B. Beck. The latter is known to correspond to a root and
can be recognized by the presence of pits with horizontal apertures. It is, however, unclear at the present whether this is a true
taxonomic character or a characteristic of all Callixylon roots,
since it is found in roots with various types of wood anatomy
(Meyer-Berthaud et al., 2013). The closest species to the Moroccan trunk is thus C. zalesskyi. We should note here that in a
previous revision of the genus Callixylon, Lemoigne et al. (1983)
considered that C. zalesskyi and C. trifilievii Zalessky had only
minimal differences and could be considered synonyms. However, subsequent papers by Beck and Wight (1988) and Orlova
and Jurina (2011) showed that there is no convincing evidence
of ray tracheids in C. trifilievii while they are undoubtedly present in C. zalesskyi. We thus choose here to follow the classification system proposed by Orlova and Jurina, according to which
the new specimen belongs to the Erianum group and is most
similar to C. zalesskyi. This species was first described by
Arnold (1930a) from the Genundewa limestone (early Frasnian),
in New York State, USA. It is based on three stems a few
centimeters in diameter that have a 0.8-1 cm wide pith with up
to 20 primary vascular strands. These are in contact with the
wood or occasionally separated by 1-2 parenchyma cells. Thus
the primary vascular system anatomy of C. zalesskyi is also
consistent with that of the new trunk from Morocco. A small
possible difference is the ray height that is slightly higher in the
US specimens (3-25 cells high vs. 2-11 cells).
Possible mechanism underlying the changes between inner
and outer phloem— In the secondary phloem of the Callixylon
zalesskyi-type of stem from Morocco, the dimensions of the
fibers and sclereids do not change significantly across the
phloem, nor does ray size in number of cells. Average ray height
is 4 cells in both the inner and outer phloem. There is a moderate increase in ray cell width from 32 µm in the youngest phloem
(range 18-56 µm) to 39 µm in the oldest (range 25 to 67 µm).
Most of the changes, however, come from the axial parenchyma
cells through two processes: (1) a substantial enlargement of
individual cell radial diameter and (2) an increase in the number
of cells by periclinal division (proliferation) (Fig. 5A, C). Both
can be observed within the same tangential band of parenchyma
(Fig. 5C). This increase in the size and number of the axial parenchyma cells is interpreted as the main cause for the changes
observed between the inner and outer part of the phloem, by
increasing the distance between thick-walled cells and separating them into isolated tangential bands (Fig. 5A). The model
proposed in Fig. 6 illustrates these processes. It shows how
the fiber arrangement in tangential bands that characterizes
the old phloem of the C. zalesskyi-type stem from Morocco
derives from an apparently less organized arrangement of the
elements of the young phloem. It also emphasizes the early
differentiation of the thick-walled cells (fibers and sclereids)
in the secondary phloem of this stem. The functional sieve
cells in the Moroccan stem occurred in the young phloem
where they were intercalated between the axial parenchyma
cells. We presume that the sieve cells collapsed early. They
are not represented in the model which, admittedly, overestimates the surface area occupied by the axial parenchyma cells
in the inner phloem.
Comparison with previous description of archaeopteridalean secondary phloem— The first description of secondary
phloem in a Callixylon axis was that by Arnold (1930a) who
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Fig. 3. Callixylon zalesskyi-type trunk with phloem from the Devonian of Morocco: General aspect of the secondary phloem (A) and details of the
cambium zone and inner secondary phloem (B-E) in transverse section. Cambium is toward the bottom on all photos. (A) General view showing the cambial zone (C), and the inner (Ph2i) and outer (Ph2o) parts of the secondary phloem (see text for details); slide MD22-Aes.1; scale bar = 200 µm. (B, C)
Region of the cambium (nonpreserved, C) and innermost preserved phloem (Ph2); slides MD22-AcS.1 (B) and MD22-AbcS.1 (C); scale bars = 100 µm.
(D, E) Details of the anatomy of the inner part of the phloem (Ph2i of Fig. 3A) showing the presence of uniseriate rays (R), fibers (F), and thin-walled cells
(*), including some with dark content (arrows); slides MD22-AeS.1 (D) and MD22-AcS.1 (E); scale bars = 50 µm.
reported this tissue in one of the three original specimens of
C. zalesskyi, a 3.5 cm wide stem from New York. He described
it as consisting of alternating layers of empty cells and cells
with dark content. The empty cells were radially elongated and
interspersed with possible resin containing cells. Interestingly,
the cells with dark content were described by Arnold as “about the
same size and shape as the [secondary xylem] tracheids.” In a
subsequent paper that focused on the bark anatomy of Callixylon,
Arnold (1930b) compared the secondary phloem of the stem
just mentioned and that of a 9 mm wide root. The secondary
phloem of both axes was described as composed of empty thinwalled cells and “tannin cells.” No precision was given on the wall
November 2013]
DECOMBEIX AND MEYER-BERTHAUD—SECONDARY PHLOEM OF CALLIXYLON
2225
Fig. 4. Callixylon zalesskyi-type trunk with phloem from the Devonian of Morocco: Anatomy of the secondary phloem in longitudinal section. Cambium is on the left on all the photos. (A) Outermost secondary xylem (2×), cambium zone (C), inner part (Ph2i), and outer part (Ph2o) of the secondary
phloem; slide MD22-AaR.1; scale bar = 200 µm. (B) General view of the secondary phloem illustrating the difference in thickness and in anatomy between
the inner part (Ph2i) and more parenchymatous outer part (Ph2o). Note the rays (R), and some fibers with a curved end (arrows); slide MD22-AaR.1; scale
bar = 200 µm. (C) Detail of the inner part of the secondary phloem showing an alternation of fibers (F) and thin-walled cells (*); slide MD22-AaR.1; scale
bar = 100 µm. (D) Detail of the outer part of the secondary phloem showing several rows of axial parenchyma cells (P) between the rows of fibers (F); slide
MD22-AeRa.1; scale bar = 100 µm. (E) Section in the outer part of the phloem with rays (R), fibers (F), axial parenchyma (P), and one elongated thickwalled cell (arrow) that differs from the fibers and is interpreted as a possible sclerified sieve cell; slide MD22-AeRa1; scale bar = 100 µm. (F) Section in
the outer part of the phloem showing a sclereid (arrow); slide MD22-Aat4; scale bar = 100 µm.
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AMERICAN JOURNAL OF BOTANY
[Vol. 100
Fig. 5. Callixylon zalesskyi-type trunk with phloem from the Devonian of Morocco: Outer part of the secondary phloem in transverse section. Cambium is toward the bottom on all photos. (A) Transition between the inner part of the phloem (Ph2i) and the outer, more parenchymatous, part (Ph2o); slide
MD22-AcS.1; scale bar = 50 µm. (B) General view of the outer part of the phloem showing rays (R) and alternating tangential bands of fibers and parenchyma; slide MD22-AbcS.1; scale bar = 100 µm. (C) Detail of the outer part of the phloem. The radial number of cells varies from one band of parenchyma
to the other and even within a single band (arrow); slide MD22-AeS.1; scale bar = 50 µm. (D) General view of the outermost preserved part of the phloem.
Some arrangement in tangential bands is still visible for example on the left side, no periderm tissue present; slide MD22-AcS.2; scale bar = 200 µm.
thickness of the latter which were described as longitudinally
elongated with oblique end walls. In the root, the phloem
contained mostly thin-walled cells of two sizes and infrequent
clusters of “tannin cells.” In the stem, the “tannin cells” were
organized in bands 2-5 cells thick alternating with bands of
thin-walled cells. The presence of secondary phloem was then
mentioned by Beck (1953) in a C. petryi root but not described
nor illustrated. In their review of the genus Callixylon, Lemoigne
et al. (1983) provided a short description of the secondary phloem
of two stems of unknown diameter, one assigned to C. trifilievii
from the Donetz basin in Ukraine, the other referred to as
Callixylon sp. from Gaspé (Canada). They noted that the anatomy was comparable to that found in C. zalesskyi by Arnold
and stated that all elements, with and without content, were
thin-walled. Following the work of Arnold (1930a, b) and
Lemoigne et al. (1983), it was thus considered that the secondary phloem of the Archaeopteridales was simple and parenchymatous, lacked fibers, and contained so-called tannin-cells that
were arranged in tangential layers in stems, and in irregularly
distributed clusters in roots.
November 2013]
DECOMBEIX AND MEYER-BERTHAUD—SECONDARY PHLOEM OF CALLIXYLON
2227
In the specimens referred to as Callixylon sp. and C. trifilievii
by Lemoigne et al. (1983), the secondary phloem is organized in
alternating bands composed of (a) 2-8 layers of isodiametric thinwalled cells and (b) 1-3 layers of radially elongated thin-walled
cells in transverse section. We interpret the second type of elements as corresponding to the enlarged axial parenchyma cells
found in the Moroccan specimen. The first type may correspond,
at least in part, to undifferentiated fibers and sclereids.
Fig. 6. Callixylon zalesskyi-type trunk with phloem from the Devonian
of Morocco: Model of secondary phloem development in transverse section.
Sieve cells are not represented. Young phloem characterized by early differentiation of thick-walled cells, and radial alternation of thick-walled and
thin-walled cells, in a 1:1 or 1:2 ratio. Old phloem characterized by arrangement of thick-walled cells in discontinuous tangential bands alternating with
bands of axial parenchyma cells, this pattern resulting from coordinated periclinal division and radial enlargement of axial parenchyma cells.
More recently, the investigation of large Callixylon roots
from Morocco (Meyer-Berthaud et al., 2013) demonstrated that
the phloem of Callixylon was more complex than previously
thought and contained fibers. The new trunk described in this
paper provides additional proof of the presence of fibers in the
secondary phloem of Callixylon. It also supports previous observation of a difference in organization between the phloem
of the roots and of the stems. The distribution of fibers in the
trunk presented in this paper and in the roots described by
Meyer-Berthaud et al. (2013) is similar to that of the so-called
tannin cells of Arnold, i.e., organized in repeated tangential layers in the stem and less conspicuously organized in the root.
Considering that both Arnold’s stem and the Moroccan specimen
belong to the same zalesskyi-type of Callixylon, this suggests
that Arnold’s “tannin cells” correspond to poorly sclerified or
undifferentiated fibers and sclereids. Given the small diameter
of Arnold’s specimens, it is possible that the differentiation of
the sclerified elements was not uniform in the secondary phloem
of archaeopteridaleans. It may have been related to the size of
the stems/branches/roots or, within a single individual, to the
architectural status of the axis, i.e., to its stage of differentiation
in relation to its position (i.e., proximal/distal) within the tree.
Implications for secondary phloem evolution in progymnosperms and early seed plants— It is now possible to compare
more accurately the anatomy and organization of secondary
phloem in Archaeopteridales with that of other progymnosperms and of early seed plants of Late Devonian–Mississippian age. The presence of fibers in the secondary phloem of
Archaeopteridales, including in the inner, supposedly functional, part is important to understand the evolution of this tissue in early lignophytes. The presence of fibers in the functional
secondary phloem has been demonstrated in all genera of aneurophytalean progymnosperms in which this tissue is known
(e.g., see Beck, 1957; Scheckler and Banks, 1971a, b; Stein and
Beck, 1983). Because the Aneurophytales are the oldest known
lignophytes, the presence of fibers can be considered plesiomorphic. The presence of fibers in the earliest seed plants of Late
Devonian age such as Elkinsia (Serbet and Rothwell, 1992) is
unknown due to their small development of secondary tissue
and lack of preservation of the phloem. Among Carboniferous
taxa, fibers are undoubtedly present in the secondary phloem of
several taxa of Mississippian trees of putative seed plant affinities
(Galtier and Meyer-Berthaud, 2006) and in some Pennsylvanian
seed plants such as the Medullosales (Smoot, 1984a) and some
but not all Cordaitales (Taylor, 1988; Wang et al., 2003). In
other Carboniferous seed plants, such as the nonarborescent
Calamopitys, Lyginopitys, Heterangium, and Callistophyton,
the phloem lacks fibers (Williamson and Scott, 1895; Hall,
1952; Galtier and Hébant, 1973; Russin, 1981; Smoot, 1984b).
It is unknown at present whether this difference observed among
Carboniferous seed plants can be linked to taxonomic affinities
and/or plant habit (Decombeix, 2013).
Our new data on the secondary phloem anatomy of Archaeopteridales demonstrates a very strong similarity with that of
the Aneurophytales. Indeed, the innermost phloem of the Moroccan trunk shows the same organization as that of Proteokalon, Tetraxylopteris, and Triloboxylon, with abundant fibers,
some cells with dark content, and thin-walled cells (e.g., see
Beck, 1957; Scheckler and Banks, 1971a, b; Stein and Beck,
1983). The organization of the older phloem in Callixylon, with
distinct tangential layers of thick-walled cells alternating with
layers of thin-walled cells, can appear superficially different.
However, we showed that this appearance results from the enlargement and proliferation of the parenchyma cells located between the fibers to adjust to the increase in size of the trunk, a
process less important or absent in Aneurophytales which had
smaller stems. Thus this difference could simply represent the
adaptation to an increase in plant stature of a phloem tissue with
a comparable original organization.
A comparable situation is observed in the putative arborescent
seed plants of Mississippian age in which secondary phloem
anatomy is known. In Stanwoodia kirktonense Galtier & Scott
from the Viséan of Scotland (Galtier and Scott, 1991), the secondary phloem reaches a maximum thickness of 1.5 mm. It contains several types of thin-walled cells and fibers. As in the
Callixylon trunk from Morocco, a radial arrangement of the
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AMERICAN JOURNAL OF BOTANY
fibers is obvious close to the cambium (Galtier and Scott, 1991,
Fig. 6b), but in slightly older phloem it is the organization in alternating tangential bands that is the most conspicuous. Putative
arborescent seed plants from the Mississippian of Australia
(Decombeix, 2013) and Algeria (‘taxon 3’ of Galtier and MeyerBerthaud, 2006) also show secondary phloem organized in
alternating tangential bands of fibers and thin-walled cells. A
comparable phloem organization is seen in Eristophyton fasciculare Scott, another putative arborescent seed plant (Galtier and
Scott, 1993). However, a difference with the Callixylon trunk described in this paper and with the other Mississippian taxa is the
rarity of fibers close to the cambial zone in Eristophyton.
In both Archaeopteridales and Mississippian trees, the proliferation of parenchyma cells as the secondary phloem ages highlights the fact that layers of thick- and thin-walled cells tended
to be produced rhythmically by the vascular cambium of the
stem. A similar rhythmic production of different types of phloem
cells is also observed in Carboniferous seed plants that lack
phloem fibers (such as Calamopitys and Callistophyton, Galtier
and Hébant, 1973; Smoot, 1984b). In those cases, layers of
sieve cells alternate with layers of axial parenchyma. Thus the
secondary phloem of archaeopteridalean progymnosperms shows
similarities with other Devonian-Carboniferous lignophytes not
only by their cellular composition but also by the rhythmic organization of different cell types within the tissue. It is necessary to mention that in the third order of progymnosperms, the
Mississippian Protopityales, the anatomy of the secondary
phloem remains uncertain and contradictory. The arborescent
species of the order, Protopitys buchiana Goeppert, was interpreted by Walton (1969) as having a simple, parenchymatous
secondary phloem, while Solms-Laubach (1893) reported the
presence of alternating layers of “stone cells” (i.e., sclereids)
separated by thin-walled cells.
It is interesting that tangential layers of fibers do not appear
as clearly in roots of Erianum-type Callixylon (Meyer-Berthaud
et al., 2013) as they do in the new trunk, which appears to belong to the same group. This is apparently due to the production
of a smaller proportion of fibers in the secondary phloem of the
roots compared to the stems. As a result, only small groups of a
few fibers can be seen in the older root phloem instead of bands.
This is consistent with observations of extant seed plants, in
which there are usually more living cells and fewer fibers in the
bark of the roots compared to stems of the same taxon (Esau,
1965, p. 523).
The new Callixylon trunk from Morocco, which possesses
the largest amount of secondary phloem reported to date within
the Archaeopteridales, does not show any evidence of a periderm within the 7 mm wide preserved part of its bark. If this
specimen had a periderm, this tissue was peripheral and unlike
the rhytidome-type of bark found in Stanwoodia (Galtier and
Scott, 1991) or in a recently described Tournaisian trunk from
Australia (Decombeix, 2013). Localized zones of tangentially
flattened cells arranged in radial rows and interpreted as a periderm have been documented in small, penultimate branches of
Archaeopteris (Scheckler, 1978) but no evidence of this tissue
exists in other axes. The nature of the outermost bark tissue of
the Archaeopteridales (old secondary phloem or cork) thus remains unknown.
Physiology—Increased hydraulic conduction and mechanical
support by secondary xylem tissue produced by a vascular cambium evolved in several plant groups, either with a unifacial cambium or, in the case of the lignophytes, with a bifacial vascular
[Vol. 100
cambium. Both types of cambium could produce a significant
amount of wood that allowed these plants to reach a certain height
starting in the Middle and Late Devonian (e.g., see Mosbrugger,
1990). However the presence in lignophytes of secondary phloem
that increased the ability to distribute photosynthates throughout
the plant appears as a key innovation (Donoghue, 2005). The
regular production of new phloem cells all through the life of the
plant also allowed compensation for tissue loss due to senescence
or environmental reasons, unlike in taxa with a unifacial cambium that only had primary phloem. This would be particularly
important in large, long-lived plants.
From a physiological point of view, there is a remarkable
feature in the phloem of the Moroccan stem, i.e., the significant
increase in the amount of axial parenchyma and the probability
that rays remained functional in the old phloem. These observations suggest that the entire phloem of this Callixylon zalesskyitype of stem can actually be regarded as functional, the inner
part dedicated to transport and the outer part to storage. The
possibility of accumulating a large amount of photosynthates
and other types of molecules in aerial stems, outside the root
system, may have not only increased the capacity of storage of
the tree but may have also facilitated its ability to mobilize food
and other compounds closer to the aerial sites of growth and
reproduction.
Archaeopteridales grew in poorly- to well-drained soils, and
can be found in more upland environments than other Devonian
trees (Mintz et al., 2010). Since all these taxa had a free-sporing
reproduction, it is probable that the archaeopteridalean ability
to adapt to drier conditions is linked to their important investment in the production of secondary vascular tissues, in opposition to the contemporaneous cladoxylopsid and lycopsid trees
(Meyer-Berthaud and Decombeix, 2009; Meyer-Berthaud et al.,
2010). The production of significant amounts of both secondary
xylem and secondary phloem gave them the possibility to
develop large roots capable of exploring soils more extensively to get water, and a large surface of conducting tissues
to transport this water and redistribute throughout the tree the
carbohydrates produced in their leaves, the first megaphylls
(Galtier, 2010). Studies of extant lignophytes have shown a
functional coupling between secondary xylem and phloem
(e.g., see Zwieniecki et al., 2004 and references therein). In particular, it is interesting to note that secondary phloem can allow
a faster return to normal hydraulic conditions in the secondary
xylem after embolism, through an active transport of solutes
between the two tissues via the rays (e.g., see Salleo et al.,
1996). The presence of secondary phloem in the Archaeopteridales would then provide another advantage over other types of
Devonian trees in dry conditions.
Conclusions—Detailed studies of the anatomy of fossil taxa are
essential to the understanding of plant evolution at several levels.
One is to solve phylogenetic relationships and understand how and
in what conditions the structures observed today evolved. In that
regard, this paper provides new information on the secondary
phloem of archaeopteridalean progymnosperms that links them to
the aneurophytalean progymnosperms and early seed plants.
Knowledge of fossil plant anatomy is also a prerequisite for
studies of plant-environment interactions in the past. The development of the Archaeopteridales in the Middle Devonian and
the ensuing formation of widespread forests in the Late Devonian has been hypothesized to have impacted the carbon cycle
and caused the environmental changes at the end of the Devonian
(Algeo et al., 2001; Le Hir et al., 2011). To test this hypothesis
November 2013]
DECOMBEIX AND MEYER-BERTHAUD—SECONDARY PHLOEM OF CALLIXYLON
it is necessary to understand the biology of these plants compared to other contemporaneous taxa. In this regard, the study of
archaeopteridalean secondary phloem tissue presented in this
paper is an important milestone in the gathering of information
required for future modeling of the physiology of early trees.
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