Bark Anatomy of an Early Carboniferous Tree from Australia

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IAWA DecombeixJournal 34 –(2), Fossil 2013: bark 183–196 183

Bark anatomy of an Early Carboniferous tree from Australia

Anne-Laure Decombeix Université Montpellier 2, UMR AMAP, Montpellier, F-34000 France; CNRS, UMR AMAP, Montpellier, F-34000 France E-mail: [email protected]

abstract Our knowledge of the evolution of secondary phloem and periderm anatomy in early lignophytes (progymnosperms and seed plants) is limited by the scarcity of well-preserved fossil bark. Here, I describe the bark of a Mississippian (Early Carboniferous) tree from Australia based on macro- and microscopic observation of two permineralized specimens. The bark tissues are up to 1.5 cm in thickness. The secondary phloem is organized in repeated, multicellular tangential layers of fibers and of thin-walled cells that correspond to axial parenchyma and sieve cells. Fibers are abundant even in the youngest, presumably functional, secondary phloem. Older phloem shows a proliferation of axial parenchyma that further separates the fiber layers. Successive periderm layers originate deep within the phloem and lead to the formation of a rhytidome-type bark, one of the oldest documented in the fossil record. These fossils add to our knowledge of the bark anatomy of Early Carboniferous trees, previously based on a few specimens from slightly younger strata of Western Europe. The complexity of the secondary phloem tissue in Devonian-Carboniferous lignophytes and possible anatomical differences related to growth habit are discussed. Key words: Mississippian, Tournaisian, Queensland, permineralized, lignophyte, secondary phloem, periderm, rhytidome.

INTRODUCTION

Lignophytes are a monophyletic group of plants characterized by the possession of a bifacial vascular cambium that produces both secondary xylem and secondary phloem (Kenrick & Crane 1997). This clade, represented today by the seed plants (gymnosperms and angiosperms), also includes the extinct progymnosperms of the Devonian and Carboniferous, a group that had gymnosperm-type wood and free- sporing reproduction. Lignophytes were one of the three groups of plants in which the tree habit evolved in parallel during the Middle Devonian, about 390 Ma, with the progymnosperm genus Archaeopteris (Meyer-Berthaud et al. 1999; Meyer-Berthaud & Decombeix 2009). After the extinction of Archaeopteris trees around the Devonian- Carboniferous boundary, several new arborescent taxa assigned to the progymnosperm Protopitys and to the first arborescent seed plants appeared (Galtier & Meyer-Berthaud

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2006; Decombeix et al. 2011a). In order to better understand the early evolution of the tree-habit within the lignophytes, it is necessary to understand the evolution of not only their wood, which provides both mechanical support and hydraulic conduction, but also their bark. The latter indeed contains the secondary phloem, necessary for the active conduction of hormones, photosynthates, and other assimilates through the plant (Beck 2005). Also important is the presence of secondary cortical tissues (periderm) that reflect the possibility for the plant to increase in diameter well beyond the limits of its primary body. Because of their peripheral position, bark tissues can potentially also have an important role in stem stiffness and/or elasticity (Niklas 1999), as well as in protection against herbivores, pathogens, fire, etc. However, while the secondary xylem anatomy of the early members of the lignophytes has been relatively well documented, less is known about the anatomy of the secondary tissues of their bark, i. e., secondary phloem and periderm (see for example Taylor 1990). This is due to two factors. First, the tissues located outside the vascular cambium tend to separate from the rest of the axis (decortication) before fossilization. Second, phloem tissues contain unlignified conducting cells that degrade much more easily than those of the xylem. Thus, phloem is less often preserved in the fossil record. As a result, our knowledge of the early evolution of secondary phloem and periderm during the Devonian and Carboniferous remains patchy. Here, I describe the bark of an Early Carboniferous tree from Queensland, Australia, that contains well-preserved secondary phloem and periderm and adds to our knowledge of bark anatomy in early arborescent lignophytes. These new specimens represent some of the oldest examples of a rhytidome-type bark in the fossil record. The complexity of the secondary phloem tissue in Devonian-Carboniferous lignophytes is discussed, as well as possible anatomical differences related to growth habit.

MATERIAL AND METHODS

This study is based on fossil material collected by Francis M. Hueber at the locality of “Dotswood”, on the north face of Mt. St. Michael, in the Burdekin Basin, NE Queens- land. The horizon yielding plants at this locality belongs to a non-marine formation, the Percy Creek Volcanics. The plants are preserved in volcaniclastic sediments, perhaps following a catastrophic burial. Their inferred age is Tournaisian (Early Mississippian, 359–347 Ma). More details on the locality can be found in Hueber and Galtier (2002) and Decombeix et al. (2011b). The Dotswood locality has yielded numerous heavily silicified trunks, including a tree fern (Hueber & Galtier 2002) and two types of lignophytes with very distinct types of secondary xylem (Decombeix et al. 2011b). The first one corresponds to the putative heterosporous progymnosperm Protopitys buchiana, with wood that is recognizable by its small uniseriate rays and uniseriate, transversely elongated pits on the radial walls of tracheids. The second type has wood with multiseriate rays and araucarioid type of radial pitting. It is similar in these characters to the putative arborescent seed plants genera Pitus and Eristophyton from the Early Carboniferous of Western Europe, but differs from them in characters of the primary body (Decombeix et al. 2011b). During

Downloaded from Brill.com10/11/2021 03:31:53AM via free access Decombeix – Fossil bark 185 an examination of F. Hueber material kept at the National Museum of Natural History, Smithsonian Institution, Washington D.C., in 2007, two slices of large (> 20 cm in diameter) trunks with preserved bark were identified. Both belong to the second wood type previously described, but unnamed. Their stele is too compressed to yield good anatomical details. A first specimen had already been partly sectioned into 8 small blocks (USNM553730, A–H) containing the outermost part of the secondary xylem and the bark. Several thin sections had been made, but only one of them was found in the collections. The second specimen (USNM553727) was a slice of trunk with about 13 cm of secondary xylem on its best preserved side (Fig. 1A, B). A block of this trunk including a well-preserved part of the bark and some secondary xylem (item 4) was cut at the Smithsonian. Both specimens were loaned for preparation and study. Seventeen wafers and thin-sections of the secondary xylem and bark in the transverse, tangential and radial planes were made at UMR AMAP, Montpellier, following the standard method (Hass & Rowe 1999). Observation and photography were conducted using Sony XCD-U100CR digital cameras attached to an Olympus SZX12 stereomi- croscope and to an Olympus BX51 compound microscope. Images were captured using Archimed software (Microvision Instruments) and plates were composed with Adobe Photoshop CS5 version 12.0 (Adobe Systems Inc.). Transformations made to the images in Photoshop include cropping, rotation, adjustment of contrast, and con- version to grayscale. Cell and tissue measurements were made with ImageJ version 1.45 (Rasband 1997–2012). The specimens are part of the collections of the National Museum of Natural History, Smithsonian Institution, Washington, and have received the numbers USNM553727 and USNM553730 .

RESULTS Secondary xylem (Fig. 1C–E) The secondary xylem anatomy of the trunks is succinctly mentioned here in order to compare it to the structure of the secondary phloem. A more thorough description is provided in Decombeix et al. (2011b, p. 53). The secondary xylem is composed exclusively of tracheids and parenchymatous rays. Only a small portion of the secondary xylem of specimen USNM553730 was sampled; it does not show any growth rings. The other specimen, USNM553727, is a large trunk that did not show any distinct growth rings either. In the outer part of the specimens, the tracheids are polygonal to rounded. They range from 20–74 µm in radial diameter (average 53 µm, standard deviation: 9, n =100) and 23–68 µm in tangential diameter (average 45 µm, standard deviation: 10, n =100) (Fig. 1C). Rays are very long in transverse section (several centimeters) and separate 1–8 files of secondary xylem tracheids. They are uni- to triseriate and up to 50 cells high in tangential section (Fig. 1D). The radial wall of the secondary xylem tracheids bears multiseriate crowded, alternate pits with an oblique aperture (Fig. 1E). Cross-field pitting was not seen.

Macroscopic features of the bark (Fig. 1A, B; 2A, E) The maximum preserved thickness of the bark is 1–1.5 cm (Fig. 1A, B). The outer part of the specimens locally shows vertical ridges. Transverse sections show that these

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Figure 1. Early Carboniferous tree from Australia: general aspect (A, B) and secondary xylem anatomy (C–E). – A: Transverse section of a trunk with preserved bark, specimen USNM553727. – B: Detail of the bark in specimen USNM553727. – C: Secondary xylem in transverse section. – D: Secondary xylem in tangential section showing multiseriate and high rays. – E: Secondary xylem in radial section showing biseriate pits. — Slide numbers: C: USNM553730-A-CT1; D, E: USNM553727-A-CL1α. — Scale bars of A: 5 cm; B: 1 cm; C: 250 µm; D: 100 µm; E: 50 µm. ridges are formed by the unequal thickness of the bark (Fig. 1A, B); the secondary xylem cylinder in contrast has a very smooth outline. The secondary phloem is layered, with alternating light and dark bands of tissue. The inner part is mostly composed of dark layers while towards the outside of the bark the light layers are much larger and represent most of the tissue. The secondary phloem is divided into concentric zones 2–3 mm thick (e.g., zones 1–4 in Fig. 2A) by successive layers of periderm that form a rhytidome.

Secondary phloem anatomy (Fig. 2, 3) The secondary phloem is a complex tissue composed of several types of cells that are regularly organized in multicellular tangential layers corresponding to the dark and light layers observed with the naked eye. The light bands are formed by thin-walled cells that are interpreted as axial parenchyma and conducting cells. The dark bands are formed by thick-walled cells that are elongated in longitudinal section and interpreted

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Figure 2. Early Carboniferous tree from Australia: general bark anatomy and inner secondary phloem (secondary xylem is towards the bottom on transverse sections, towards the left on longitudinal sections). – A: General view of the bark in transverse section showing successive zones of secondary phloem (1–4) separated by periderm layers. – B: Inner secondary phloem in transverse section. – C: Detail of secondary xylem, cambium zone and innermost secondary phloem (zone 1 of photo A) in transverse section. – D: Detail of innermost secondary phloem anatomy in transverse section. – E: General view in longitudinal section showing successive zones of secondary phloem (1–3) separated by periderm layers. – F: Detail of inner part of secondary phloem in longitudinal section showing groups of fibers, rays and elongated thin-walled cells (arrows). — Ph2: secondary phloem; X2: secondary xylem; c: cambium; P: periderm; f: fiber; r: ray. — Slide numbers: A & B: USNM553730-H-CT2; C & D: USNM553730-A-CT1; E & F: USNM553727-A-CL1β. — Scale bars of A: 2 mm; B: 500 µm; C, D, F: 100 µm; E: 1 mm.

Downloaded from Brill.com10/11/2021 03:31:53AM via free access 188 IAWA Journal 34 (2), 2013 as fibers. Both types of layers are crossed by parenchymatous rays that are uniseriate to biseriate, occasionally triseriate in the older phloem.

Cambium zone and inner phloem (Fig. 2) The region of the cambium is usually not well preserved and contains only crushed cells (Fig. 2C). The innermost (youngest) part of the secondary phloem (zone 1 in Fig. 2A and 2E; Fig. 2B–D), limited on the outside by the innermost periderm, is about 2 mm in thickness in both specimens. It comprises conspicuous multicellular layers composed of fibers and ranging from 110–340 µm in radial thickness (average 220 µm, standard deviation 80 µm, n = 8). In between the layers of fibers are multicellular layers of less well-preserved cells with thin walls that have a comparable thickness (110–280 µm, average 220 µm, standard deviation 60 µm, n = 8). The radial number of fibers in a layer is variable, both between successive layers in a same region of the bark and in different parts of a same layer within the bark. Some layers have a relatively high number of fibers, with up to 8 or 9 radial rows, while other are only 1–3 rows thick. The groups of fibers are separated tangentially by conspicuous parenchymatous rays that are uni- to triseriate (Fig. 2B, D). In addition, a few isolated fibers sometimes occur between the layers (Fig. 2D, arrow). The fibers are rectangular to square, more rarely hexagonal, in transverse section. They range from 29–62 µm in radial diameter (average 45 µm, standard deviation: 6, n = 100) and 18–58 µm in tangential diameter (average 38 µm, standard deviation: 9, n =100). The walls are 9–26 µm in thickness (average 15 µm, standard deviation: 4, n = 50). The lumina is limited in most cases to a small oval opening less than 10 µm in diameter; in the fibers with the thickest walls, there is only a central slit-like region with no real lumina. The length of the fibers could not be determined properly on the longitudinal sections, but they appear to be very long (Fig. 2E, F). In between the layers of fibers, layers of thin-walled cells are present but often crushed (Fig. 2D). Rays are indistinguishable in these layers. In longitudinal section, these zones contains some cells that are very long (Fig. 2F) and that we interpret as sieve cells, although no distinct sieve areas could be observed, probably due to the preservation. This inner part of the secondary phloem is delimited radially by a layer of periderm 400–500 µm in thickness (Fig. 2A, E).

Older phloem (Fig. 3) Beyond the innermost periderm, the phloem is characterized by a much higher pro- portion of thin-walled cells, probably due to a combination of better preservation and a proliferation of axial parenchyma cells (zone 2–4 in Fig. 2A & E; 3A–D). The layers of fibers have a comparable thickness to those in the inner phloem (120–280µ m, average 200 µm, standard deviation 60 µm, n = 8). The layers of thin-walled cells, on the other hand, range from 470–810 µm in thickness (average 590 µm, standard deviation 110 µm, n= 8). Thus, while in the inner zone the average ratio of thin-walled-cell layer thickness to fiber layer thickness was around 1 : 1, in the older phloem the average ratio is close to 3 :1. This gives a very different, more parenchymatous, aspect to the tissue.

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Figure 3. Early Carboniferous tree from Australia: older secondary phloem (secondary xylem is towards the bottom on transverse sections, towards the left on longitudinal sections). – A, B: Transverse sections of older secondary phloem corresponding respectively to zone 2 and 3 of Fig 2A. – C: Detail of secondary phloem in transverse section. – D: Longitudinal section through zones 2 and 3 of Fig. 2A showing group of fibers and a periderm layer. – E: Radial section showing a group of fibers, a ray and axial parenchyma cells (p). – F: Radial sections showing a group of fibers, parenchyma and possible compressed sieve elements (s, arrow). — X2: secondary xylem; P: periderm; Ph2: secondary phloem; f: fiber; r: ray. — Slide numbers: A & B: USNM553730- H-CT2; C & D: USNM553730-A-CT1; E: USNM553727-A-CL1β' F: USNM553730-G-CL2. — Scale bars of A, B: 1 mm; C: 500 µm; D: 250 µm; E, F: 50 µm.

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Figure 4. Early Carboniferous tree from Australia: periderm in (A) transverse and (B) longitudinal section – Slide numbers: A: USNM553730-A-CT1; B: USNM553727-A-CL1β. — Scale bars: 200 µm.

It also increases the conspicuousness of the isolated fibers noticed in the innerphloem (Fig. 2D, arrow), which appear as uni- to bilayered tangential layers (Fig. 3C). The radial arrangement of the tissue is still visible and the rays can be followed across both fiber layers and thin-walled cells layers. Rays are uni- to triseriate and their cells are a little enlarged tangentially in transverse section (Fig. 3C). In radial section, ray cells are longer than high (Fig. 3E). The thin-walled cells are the dominant cell type in this part of the phloem (Fig. 3C). They are 31–93 µm in diameter (average 53 µm, standard deviation = 15 µm, n = 50). In longitudinal section, most of the thin-walled cells are isodiametric to a little radially elongated (Fig. 3D, E) and we thus interpret them as axial parenchyma cells. Their heights range from 31–94 µm (average 54 µm, standard deviation = 14 µm, n = 50). In radial section, their rounded outline distinguishes them from ray cells which are rectangular (Fig. 3E). A few thin, longitudinally elongated cells are occasionally present within this parenchyma (Fig. 3F) and are tentatively interpreted as sieve cells.

Periderm (Fig. 2A, 4) At least four successive layers of periderm have been observed on the largest preserved portion of bark (Fig. 2A). The layers range from 400–800 µm in thickness. The thickest appear to be double in some zones and some layers anastomose (Fig. 4A). Each periderm layer is composed of cells that are rectangular and radially flattened in transverse section and appear higher than wide in longitudinal section (Fig. 4B).

DISCUSSION

The trunks with preserved bark from Dotswood are a rare example of good anatomical preservation of bark tissue in a Paleozoic lignophyte tree. Among the progymnosperms, a small amount of secondary phloem was described in Middle Devonian progymnosperms belonging to the aneurophytales (Beck 1957; Scheckler & Banks 1971a; Stein & Beck

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1983), and in the arborescent genus Archaeopteris (Archaeopteridales; Arnold 1930; Lemoigne et al. 1983; Meyer-Berthaud et al. 2013). Secondary phloem in these plants was composed of several types of cells including fibers. A zone of tangentially flattened cells arranged in radial rows and interpreted as a periderm was documented in several Aneurophytales and possibly in a branch of Archaeopteris (Scheckler 1978). Among the earliest seed plants, secondary phloem anatomy was documented in arborescent taxa of Mississippian (Early Carboniferous) age (Galtier & Meyer-Berthaud 2006 and references therein). This tissue contained different types of cells, including fibers. Periderm has been reported in several taxa and is usually of the rhytidome type, with the exception of the genus Pitus. In contrast, non-arborescent gymnosperms of the same period such as Calamopitys apparently lacked fibers in the secondary phloem and did not possess a periderm (Galtier & Hébant 1973). The new specimens described in this paper bring additional information on the bark anatomy of Early Carboniferous lignophyte trees and highlight some trends in the evolution of secondary phloem.

Rhytidome A prominent characteristic of the Australian specimens reported in this paper is the presence of a rhytidome-type bark with sequent periderms. Detailed reports of sequent periderms in Mississippian plants before the present work are restricted to the descriptions of two putative arborescent seed plants: 1) Endoxylon from the Middle and Late Mississippian of Scotland (Scott 1924) and, 2) Stanwoodia from the Middle Mississippian of Scotland (Galtier & Scott 1991). Given their Early Mississippian age (middle Tournaisian, Tn2), the Australian specimens now represent the oldest occur- rence of this type of bark in the fossil record. The position of the layers of periderm within the secondary phloem indicates a deep origin, similar to the situation reported in the slightly younger arborescent taxa Endoxylon (Scott 1924), Stanwoodia (Galtier & Scott 1991), Eristophyton (Scott 1902; Galtier et al. 1993; Galtier & Scott 1994), and possibly Bilignea (Galtier et al. 1993).

Phloem organization The Australian trees show a complex secondary phloem with an organization in alternating tangential bands of thin-walled cells and fibers, comparable to that seen in some geologically younger fossils and extant taxa. Den Outer (1967) considered one of the major trends in the evolution of gymnosperm phloem through time to be an increase in the organization of phloem in repeating tangential bands. However, his work was based on extant taxa only, and studies of fossil secondary phloem have shown that this regular arrangement was already present in the Carboniferous (e.g., Taylor 1990). This has been well-demonstrated in the Late Carboniferous Callistophyton, Heterangium, Medullosa, and Cordaixylon (Smoot 1984a, 1984b; Taylor 1988). A rhythmic production of the secondary phloem cell types is also documented in all the Early Carboniferous seed plants or putative seed plants taxa in which this tissue is known (Galtier & Hébant 1973; Galtier & Meyer-Berthaud 2006). There are no data on the secondary phloem of the earliest seed plants of Late Devonian age, because of their small size and lack of preservation of this tissue (e.g., Elkinsia, Serbet & Rothwell 1992).

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Among progymnosperms, the Early Carboniferous species Protopitys buchiana, the other arborescent lignophyte taxa found at the Dotswood locality, was interpreted by Walton (1969) as having a simple, parenchymatous secondary phloem. In contrast, Solms-Laubach (1893), in a previous description of that species, reported a piece of bark composed of alternating layers of “stone cells”, i.e., sclereids, and crushed tissue containing elongated cells that he interpreted as sieve cells. His observation suggests that in Protopitys too the secondary phloem might have produced different types of cells rhythmically and formed concentric layers. As noted by Solms-Laubach, the presence of stone cells in the place of fibers in this tissue is unusual. This, and the conflicting observation of this tissue later made by Walton, calls for further clarifications of the secondary phloem anatomy in this widespread but scantily known Early Carboniferous tree (Decombeix et al. 2011a). No distinct organization has been detected in the secondary phloem found in roots of the Devonian progymnosperm tree Archaeopteris (Arnold 1930; Meyer-Berthaud et al. 2013). However, the observation of a small trunk from Morocco shows that the fibers are preferentially arranged in tangential bands (Scheckler et al. 2001). The dif- ference with previously described specimens could be due either to the different nature of the observed organs (root vs. stem) or to a different systematic affinity. In any case, there is evidence for a rhythmic secondary phloem differentiation in at least the stem of some archaeopteridalean progymnosperms, which pushes the appearance of this complex organization back to the Late Devonian. Finally there is no good evidence of such a rhythmic differentiation in the secondary phloem of aneurophytalean progymnosperms. In this group the only organization that appears is that of the fibers in small radially oriented rows e.g.( , Beck 1957; Scheckler & Banks 1971a, b; Stein & Beck 1983). This combined information indicates that a rhythmic development was already present in the phloem of several taxa during the Late Devonian and Early Carboniferous. Because this patterning has not been observed in the aneurophytalean progymnosperms, it might be a shared character between Archaeopteris, possibly Protopitys, and the seed plants. Smoot (1984a) suggested that this organization was linked to the necessity for a close spatial relationship between the conducting elements and the parenchyma. This physiological requirement might explain the early appearance of this type of secondary phloem anatomy in lignophyte evolution.

Phloem fibers Esau et al. (1953) distinguish two types of phloem fibers: 1) those that differentiate close to the cambium and are part of the functional secondary phloem and, 2) those that differentiate in the outer part of the phloem as part of the ageing process of some other cell types. The presence of fibers in the functional phloem has been closely examined in previous anatomical studies of Paleozoic lignophytes. This is because fibers are present in the functional phloem of the aneurophytalean progymnosperms, the oldest lignophytes and putative ancestors of the seed plants (e.g., Rothwell & Erwin 1987). The presence of fibers in the inner, presumably functional, part of the phloem is also documented in the arborescent progymnosperm Archaeopteris (Meyer-Berthaud et al. 2013). Among

Downloaded from Brill.com10/11/2021 03:31:53AM via free access Decombeix – Fossil bark 193 putative arborescent seed plants of Mississippian age, secondary phloem containing fibers has been described in detail and illustrated in late Visean (Middle Mississippian) specimens of Stanwoodia kirktonense (Galtier & Scott 1991) and Eristophyton fasciculare (Galtier et al. 1993; Galtier & Scott 1994). In Eristophyton fasciculare, fibers appear to be rare or absent in the innermost part of the secondary phloem (Galtier & Scott 1994). In Stanwoodia on the other hand, they are undoubtedly present close to the cambium (Galtier & Scott 1991). A similar situation occurs in an unnamed stem from the late Tournaisian of Algeria (“taxon 3” of Galtier & Meyer-Berthaud 2006). These specimens and the ones described in the present paper show that fibers were undoubtedly present in the functional secondary phloem of some arborescent Missis- sippian lignophytes, a trait that they thus share with the Devonian progymnosperms. An interesting point is that fibers are absent in the secondary phloem of the Early Carboniferous taxon Calamopitys (Galtier & Hébant 1973) and in most Late Carbonifer- ous taxa in which this tissue have been studied in detail. This includes Callistophyton, Lyginopteris, Heterangium, and the cordaitalean axes Amyelon (roots), Cordaixylon and Mesoxylon (stems) (Williamson & Scott 1895; Hall 1952; Russin 1981; Smoot 1984a, 1984b; Taylor 1988). Studies of extant plants show that the presence and arrangement of fibers in the secondary phloem can have a taxonomic value (e.g., Chang 1954). It is, however, interesting to note that within some groups the abundance of secondary phloem fibers has been suggested to be linked to growth habit. This trend is observed in extant cycads, where fibers are much more abundant in large arborescent species than in smaller species (Miller 1919; Greguss 1968; see also discussion in Ryberg et al. 2007). In the genus Bauhinia (Fabaceae), the four shrubby and arborescent species have secondary phloem fibers while the two lianescent species lack fibers (Ewers & Fisher 1991). The Carboniferous seed plants Lyginopteris, Calamopitys, Heterangium and Callistophyton, which all lack fibers in the functional secondary phloem, have been reconstructed as plants of a relatively small size. Lyginopteris has been interpreted as having a vine-like habit based on its long internodes and adventitious roots (see Dunn 2006 and references therein) and on a biomechanical analysis of its stems (Masselter et al. 2007). Calamopitys also has stems with long internodes and biomechanical anal- yses shows that it was a semi-self-supporting or leaning plant (e.g., Rowe et al. 1993). Callistophyton has been reconstructed as having a scrambling, shrub-like habit (Roth- well 1975). Finally, at least some species of Heterangium probably were also vine-like (Pigg et al. 1987). Thus all of these Carboniferous taxa that lack secondary phloem fibers appear to have been small, non- or semi-self-supporting plants. In contrast, the Devonian arborescent progymnosperm Archaeopteris and Early Carboniferous arborescent seed plants had fibers in their phloem. The situation is more complex among other Carboniferous taxa. The habit within the genus Medullosa is thought to have ranged from vine-like to shrubby to arborescent, with a majority of non self-supporting species (Dunn 2006 and references therein). Medullosa steinii, which has been reconstructed as a vine, does not have secondary phloem fibers (Dunn et al. 2003). However, the four species of Medullosa studied by Smoot (1984a) all show fibers in the functional phloem. It is not completely clear wheth- er this different anatomy can be directly related to growth habit. A similar situation

Downloaded from Brill.com10/11/2021 03:31:53AM via free access 194 IAWA Journal 34 (2), 2013 occurs among the cordaites. Plants within this group showed a wide range of habit, from prostrate stems with adventitious roots, to shrubs, to large trees (Stewart & Rothwell 1993; Taylor et al. 2009). The stems of two genera (Mesoxylon and cf. Cordaixylon) studied by Taylor (1988) lack fibers in the secondary phloem, while other taxa apparently possessed distinct tangential bands of fibers (e.g., Shanxioxylon, Wang et al. 2003). Finally, it must be noted that at least some of the aneurophytalean progymnosperms of the Devonian, which all possess fibers in their secondary phloem, were most likely not fully self-supporting (Speck & Rowe 2003; Stein et al. 2012). It can, however, be argued in this case that the distribution of fibers in aneurophytaleans differs from that of later taxa in which fibers are organized in tangential bands (see above) and these differences may confer different mechanical properties. Further work on permineralized Devonian and Carboniferous specimens such as the trunks studied in this paper will hopefully allow us to test the possible relationships between bark anatomy and growth habit, and between bark anatomy and systematic affinities among early lignophytes at a larger scale.

ACKNOWLEDGEMENTS

Francis Hueber is gratefully thanked for providing access to the specimens and for his kind welcome during a visit to the Smithsonian in 2007. W. DiMichele and J. Wingerath (Smithsonian Institution, Washington) helped with the preparation and loan of the specimens. Thanks also to Brigitte Meyer- Berthaud (UMR AMAP, France) for offering valuable comments on a first draft of the manuscript, and to Edith Taylor and an anonymous reviewer for their thorough and helpful reviews. 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/.

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