Virtual taphonomy using synchrotron tomographic microscopy reveals cryptic features and internal structure of modern and fossil plants

Abstract

While more commonly applied in zoology, synchrotron radiation X-ray tomographic microscopy (SRXTM) is well-suited to nondestructive study of the morphology and anatomy of both fossil and modern plants. SRXTM uses hard X-rays and a monochromatic light source to provide high-resolution data with little beam-hardening, resulting in slice data with clear boundaries between materials. Anatomy is readily visualized, including various planes of section from a single specimen, as clear as in traditional histological sectioning at low magnifications. Thus, digital sectioning of rare or difficult material is possible. Differential X-ray attenuation allows visualization of different layers or chemistries to enable virtual 3-dimensional (3D) dissections of material. Virtual potential fossils can be visualized and digital tissue removal reveals cryptic underlying morphology. This is essential for fossil identification and for comparisons between assemblages where fossils are preserved by different means. SRXTM is a powerful approach for botanical studies using morphology and anatomy. The ability to gain search images in both 2D and 3D for potential fossils gives paleobotanists a tool-virtual taphonomy-to improve our understanding of plant evolution and paleobiogeography.anatomy ͉ morphology ͉ palaeobotany ͉ synchrotron radiation X-ray tomographic microscopy V arious methods now exist for visualizing plant material in 3-dimension (3D). Confocal laser-scanning microscopy, electron tomography, and optical coherence microscopy are used for imaging thin (often sectioned) and (semi-)transparent material (1), in conjunction with modern computer programs for 3D reconstruction. Complementing this, other techniques for examining larger specimens or to avoid sectioning ''difficult'' material include neutron imaging, nuclear magnetic resonance (NMR) imaging, X-ray computed tomography (CT), highresolution X-ray computed tomography (HRCT), and synchrotron radiation X-ray tomographic microscopy (SRXTM). Of these, HRCT and SRXTM are the most useful methods to visualize both internal and external morphology and anatomy in a noninvasive and nondestructive manner, and are useable for a range of specimen sizes. HRCT has been used in plant sciences to examine structure and morphology of extant flowers and fruits (1; see also the Digital Morphology digital library of the University of Texas at Austin, www.digimorph.org), density of extant woods (2, 3), spatial distribution of root systems (4-6), and light interception of the tree canopy (7,8). In paleobotany, CT has been used in a few cases to reveal internal structures, including in Paleozoic charophytes (9), silicified Cycadeoidea stems and Araucaria mirabilis cones from the Jurassic (10), an undescribed Cretaceous gymnosperm fructification (11, 12), a Paleogene hymenophyllaceous fern rhizome (13), and Eocene myrtaceous fruits (14).Recently, SRXTM has become increasingly used in biology, especially in paleontology (e.g., 15-20; see ref. 19 for comparative review of the various methods mentioned...

A review of the plants of the Princeton chert (Eocene, British Columbia, Canada)

“…Smith also contributed to the understanding of filicalean fern diversity in the Princeton chert with the description of an extinct fern Trawetsia princetonensis Smith, Stockey, Nishida & Rothwell (Blechnaceae, Smith et al 2006). Smith and colleagues illustrated several Princeton chert plants in more recent discussions of the value of nondestructive computer tomography techniques (Smith et al 2009). Steven J. Karafit completed a M.S.…”

Revision of Icacinaceae from the Early Eocene London Clay flora based on X-ray micro-CT

“…Recent advances in our understanding of angiosperm phylogeny (e.g., Soltis et al 2011) and fruit morphology of selected clades provide an excellent context for re-evaluating the systematics of numerous groups in the London Clay flora. Furthermore, technological advances in the imaging and visualization of fossil material (e.g., X-ray microcomputed tomography, micro-CT) offer a means of nondestructively studying critically important specimens (e.g., holotypes) in high resolution (Smith et al 2009). Collinson et al (2016, this volume) demonstrate the utility and importance of this method for studying the London Clay material.…”

X-ray micro-computed tomography (micro-CT) of pyrite-permineralized fruits and seeds from the London Clay Formation (Ypresian) conserved in silicone oil: a critical evaluation

“…Smith et al (2009a) gave several examples of potential "virtual" fossils. These included: (i) digital endocarps and locule casts produced by digitally removing outer fruit wall and digitally infilling the locule of modern Menispermaceae fruits; and (ii) digital seeds with varying seed coat appearances resulting from sequential virtual removal of seed coat layers from modern seeds.…”

“…Virtual taphonomy (Smith et al 2009a) produces digital fossils for comparison with real fossils to obtain, and explain, the different appearances of the same taxon that may result from variations in fossilization processes. Smith et al (2009a) gave several examples of potential "virtual" fossils.…”

“…Although with far fewer existing instruments compared to micro-CT, synchrotron radiation X-ray tomographic microscopy (SRXTM) is also becoming more widely used for the study of plant fossils (e.g., Smith et al 2008Smith et al , 2009aSmith et al , 2009bSmith et al , 2015Friis et al 2011Friis et al , 2014Friis et al , 2015Collinson et al 2012aCollinson et al , 2012bSteart et al 2014;Moreau et al 2016; and references cited in all of these). Collinson et al (2012b) compared imaging results from micro-CT and SRXTM on an organically preserved fruit from the Eocene of Messel noting that SRXTM provided clearer cellular detail than micro-CT.…”