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Bark Anatomy of an Early Carboniferous Tree from Australia

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Bark Anatomy of an Early Carboniferous Tree from Australia 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 thick- ness. 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 pos- sible 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 © International Association of Wood Anatomists, 2013 DOI 10.1163/22941932-00000016 Published by Koninklijke Brill NV, Leiden Downloaded from Brill.com10/11/2021 03:31:53AM via free access 184 IAWA Journal 34 (2), 2013 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 second- ary 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 Downloaded from Brill.com10/11/2021 03:31:53AM via free access 186 IAWA Journal 34 (2), 2013 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.
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