Overcoming the fragility – X-ray computed micro-tomography elucidates brachiopod endoskeletons
© Seidel and Lüter; licensee BioMed Central. 2014
Received: 26 February 2014
Accepted: 6 August 2014
Published: 27 September 2014
The calcareous shells of brachiopods offer a wealth of informative characters for taxonomic and phylogenetic investigations. In particular scanning electron microscopy (SEM) has been used for decades to visualise internal structures of the shell. However, to produce informative SEM data, brachiopod shells need to be opened after chemical removal of the soft tissue. This preparation occasionally damages the shell. Additionally, skeletal elements of taxonomic/systematic interest such as calcareous spicules which are loosely embedded in the lophophore and mantle connective tissue become disintegrated during the preparation process.
Using a nondestructive micro-computed tomography (μCT) approach, the entire fragile endoskeleton of brachiopods is documented for the first time. New insights on the structure and position of tissue-bound skeletal elements (spicules) are given as add ons to existing descriptions of brachiopod shell anatomy, thereby enhancing the quality and quantity of informative characters needed for both taxonomic and phylogenetic studies. Here, we present five modern, articulated brachiopods (Rectocalathis schemmgregoryi n. gen., n. sp., Eucalathis sp., Gryphus vitreus, Liothyrella neozelanica and Terebratulina retusa) that were X-rayed using a Phoenix Nanotom XS 180 NF. We provide links to download 3D models of these species, and additional five species with spicules can be accessed in the Supplemental Material. In total, 17 brachiopod genera covering all modern articulated subgroups and 2 inarticulated genera were X-rayed for morphological analysis. Rectocalathis schemmgregoryi n. gen., n. sp. is fully described.
Micro-CT is an excellent non-destructive tool for investigating calcified structures in the exo- and endoskeletons of brachiopods. With high quality images and interactive 3D models, this study provides a comprehensive description of the profound differences in shell anatomy, facilitates the detection of new delicate morphological characters of the endoskeleton and gives new insights into the body plan of modern brachiopods.
A true spicular endoskeleton is found only in articulated brachiopods where it is strongly developed in all species of the Terebratulidae, Platidiidae and Kraussinidae. In the families Megathyrididae, Dallinidae, Laqueidae and Thecideidae it is only developed in some species, and it does not occur at all in the Terebratellidae . Spicules were first described in detail by Hancock  in Terebratulina retusa (Linnaeus, 1758), by Lacaze-Duthiers  in Lacazella mediterranea (Risso 1826) and extensively by Eudes-Deslongchamps  in T. retusa (Figure 1E), Kraussina rubra (Pallas, 1766), Gryphus vitreus (Born, 1778), Megerlia truncata (Linnaeus, 1767) and Platidia anomioides (Scacchi & Philippi in Philippi, 1844). Based on comprehensive investigations of the material obtained from the Valdivia- (1898-1899) and Gauß-Expeditions (1901-1903), F. Blochmann , tested the usefulness of the calcareous bodies for species diagnostics when other shell characters fail (Figure 1F, G). Despite existing illustrations of minute single spicules  (Figure 1H), the fragility of the endoskeleton limits the ability to visualise and therefore understand the anatomy of the endoskeleton as a whole. However, understanding the anatomy of the endoskeleton is essential for taxonomic and systematic analyses, as well as for any hypotheses on the functional properties of the endoskeleton of brachiopods.
Scanning electron microscopy (SEM) has been used for decades to visualise biological structures of interest in brachiopod shells, such as muscle scars, punctae, teeth, crura and the brachidium , and references therein. However, this method is limited by the fact that it is only surface-sensitive. Studying hard tissue of modern brachiopods with SEM requires treatment with chemical dissolvers to remove the soft tissue, which can lead to the damage of the shell. Additionally, endoskeletal elements such as calcareous spicules which are loosely embedded within the lophophore and mantle connective tissue disintegrate during the preparation process. Despite exhaustive research on hard tissue of brachiopods using high resolution SEM-imaging, a pictured overview of the occurrence, abundance and exact spatial distribution of endoskeletal spicules within the soft body has been lacking – until now.
In order to understand the inner shell morphology of either fossil and modern brachiopod shells X-ray radiographs of animals have been used since the 1970’s -. Hagadorn  was the first to use micro-computed tomography (μCT) and reconstructed 3D models to visualise the coiled lophophore support structures inside pyritized steinkerns of the Silica Shale brachiopod Paraspirifer bownockeri (Stewart, 1927). With increasing resolution and practicability of X-ray devices within the last decade computed tomography has become a valuable adjunct technique. A few studies have been carried out since on brachiopod shell morphology using micro-computed tomography (- as well as synchrotron radiation X − ray tomographic microscopy (SRXTM), which provides an even higher image fidelity ,.
The majority of analyses of fossil brachiopods using a microtomograph were carried out by Pakhnevich -. In 2010 he included 6 modern species in his investigations showing developmental series of the brachidium of Macandrevia cranium (Müller, 1776), the spiculation of the mantle connective tissue of the ventral valve of T. retusa and scans of Eucalathis murrayi (Davidson, 1878). Unfortunately, details of the scanning parameters and the scanning set up are missing (e.g. scans performed wet or dry, in ddH2O or EtOH). The presented images do not include all the information μCT scans actually are able to provide. For instance, data on spiculation within the lophophore and mantle of T. retusa or E. murrayi is limited, although micro computed tomography appears highly applicable for such tasks.
By using the non-invasive μCT approach, we were able to document the internal shell anatomy and to visualise the shells of modern brachiopods. We added structural and positional data on tissue-bound skeletal elements (e.g. spicules) to existing descriptions of brachiopod shell anatomy. We scanned long-term preserved specimens from the historical wet collection of the Museum für Naturkunde Berlin, Germany as well as recently collected samples which represent 19 brachiopod genera covering all articulated subgroups and two genera of (inarticulated) craniids. Here, we illustrate whole mount scans of five representative species to underline the capability of the non-invasive μCT approach for visualising hard tissue of brachiopods and present new characters of the endoskeleton with a SEM-comparable resolution of approximately 10 μm. Comprehensive descriptions of the spicule arrangements within the brachiopod soft tissue are given in the results chapter (for results on the remaining 5 species with spicules see Supplemental Material). One of the five species illustrated in detail was found during the deep-sea expedition SO 205 “Mangan” on manganese nodules in the Central East Pacific and is described as a new species Rectocalathis schemmgregoryi n. gen., n. sp.
Species presented within this article
R. schemmgregoryi n. gen., n. sp.
SO205/St. 40, NE Pacific
P. Martinez Arbizu
RV MSM19/1076-1, S-Atlantic, SW of Africa
Naples, Italy, Mediterranean Sea
Doubtful Sound, Bauza Island, NZ
Volume analyses and morphometric measurements using VG Studio Max 2.1
Vol. Spic Loph.
Vol. Spic. DV
Vol. Spic VV
R. schemmgregoryi n. gen., n. sp.
Terebratulina retusa(Cancellothyrididae) – ZMB Bra 2253
Rectocalathis schemmgregoryin. gen., n. sp. (Chlidonophoridae) – ZMB Bra 2254
Phylum BRACHIOPODA Duméril, 1806
Subphylum RHYNCHONELLIFORMEA Williams & others, 1996
Class RHYNCHONELLATA Williams & others, 1996
Order TEREBRATULIDA Waagen, 1883
Suborder TEREBRATULIDINA Waagen, 1883
Superfamily CANCELLOTHYRIDOIDEA Thomson, 1926
Family CHLIDONOPHORIDAE Muir-Wood, 1959
Subfamily EUCALATHINAE Muir-Wood, 1965
Genus Rectocalathis n. gen.
Type species - Rectocalathis schemmgregoryi n. sp.
Etymology - Genus named after its anatomically correct orientation (from Latin: rectus = upright, straight) when attached to its natural substrate due to the unusual position of the foramen.
Diagnosis - Small eucalathine brachiopod with a smooth to faintly costate shell and an extreme form of epithyrid (subumbonal) pedicle opening towards the ventral side of the animal.
Species Rectocalathis schemmgregoryi n. sp.
Type material - Holotype: ZMB Bra 2254, Paratypes: ZMB Bra 2350, 2352 (total: 3 specimens).
Type locality - NE Pacific, Clipperton Region, 11°47′56″N 116°49′85″W, Cruise SO 205 MANGAN, Station EBS 40, depth: 3954 m, May 5th 2010.
Etymology - Species named after the late brachiopod researcher Mena-Daniela Schemm-Gregory, who unexpectedly died in July 2013, much too early in her promising career.
Distribution - So far only known from the type locality.
Diagnosis - Punctate and small, subcircular to pentagonal shell with complete oval foramen perforating the ventral valve. Dorsal valve with long, slightly medially incurved, thick crura with blunt crural processes, no loop. Heavy spiculation within the lophophore and tentacles, and fragile median spiculation in the dorsal mantle.
Dorsal valve interior (Figure 3A, C). – Hinge line almost straight and wide (0.57 × valve width), sockets large and both ridges almost parallel to hinge line. Outer socket ridges long, narrow, submarginal, inner socket ridges minute, fused with large cardinal flange. Dorsal umbo projects beyond the hinge line, cardinal process large, anteroaxially labiate, laterally fused with cardinal flange. Crura bases broad, crura thick, straight or slightly convergent to the front, from ventral view axes of crural processes slightly rotated from the axis of the crura and descending braches. Surface with punctae, no tubercles, faint median septum in the posterior half, and faint depression posterior of the centre of the valve where the dorsal mantle spiculation is located.
Inside of ventral valve (Figure 3B). – Deltidial plates conjoint, no conjunction line, symphytium abruptly curved posteriorly. Hinge teeth with elongate base, almost parallel to the hinge line, with outer, lateral base submarginal, inner base elongated towards the foramen, distal ends pointed. Surface with punctae, no tubercles. Symmetrical muscle scars within depressed area of the keel between foramen and a thick median groove (mg) within the middle of the posterior half.
Spiculation - Spicules develop within the lophophore, the tentacles and the dorsal mantle (Figure 3C). The spiculation within the schizolophous lophophore is strong, and takes up almost the entire volume of the mantle cavity (Figure 3F, G). It consists of a smaller, centred, radiating network of thick and multibranched spicules and two outer “rings” which support the lophophore with its two arms bearing the strongly spiculated tentacles (Figure 3D). The radiating structure is positioned in between the lophophoral arms as a symmetrical web of spicules supporting all parts of the arms of the lophophore. On the anterior side, the arms of the lophophore are curled ventrally and separated. Posteriorly, they are fused leaving a large opening for the mouth. The spicules of the tentacles are half-cylinder shaped. The lophophoral endoskeleton is positioned on the anterior third of the ventral side of the crura. Posteriorly, two excrescences of the endoskeleton extend next to the broad crural processes to support the endoskeleton’s orientation (Figure 3D). The dorsal mantle exhibits only a faint but distinct spiculation, which is positioned medially just below the tips of the crura, and slopes anteriorly (Figure 3G). The spicules are slender and delicate, and too fragile to support the loop holding the weight of the lophophoral endoskeleton. In contrast to the spiculation in Eucalathis sp., these spicules show a distinct morphology composed of two parts (Figure 3G1 and G2). The anterior part is in one plane with the anterior body wall and the posterior part is oriented dorsoventrally, reaching axially into the visceral cavity. While the spicules of the anterior part are short and form a dense network, the spicules of the posterior part are rather long and less branched. The mantle spiculation is not connected to the floor of the valve or to the lophophoral endoskeleton.
Remarks - The spiculation pattern of Rectocalathis schemmgregoryi n. gen, n. sp. easily identifies it as a member of Eucalathinae. Especially the spicules of the dorsal mantle epithelium, which are not connected to any other spicules of the internal skeleton, are a characteristic of this group (see also Eucalathis sp.). Within Eucalathinae, four genera Eucalathis Fischer & Oehlert, 1890, Bathynanus Foster, 1974, Notozyga Cooper, 1977, and Nanacalathis Zezina, 1981, are described . All species within these genera have disjunct deltidial plates resulting in a hypothyrid foramen, except Nanacalathis which has conjunct deltidial plates forming a mesothyrid foramen. Rectocalathis schemmgregoryi n. gen, n. sp. also has conjunct deltidial plates, but an extreme form of an epithyrid foramen with the pedicle opening lying in a subumbonal position on the ventral side of the animal. Comparable to Nanacalathis spp., Rectocalathis schemmgregoryi n. gen., n. sp. lacks a brachidial loop, but it clearly differs from Nanacalathis through its nearly smooth shell. So far, Rectocalathis schemmgregoryi n. gen., n. sp. has only been found in the deep sea at a single station during the MANGAN-Expedition of the German research vessel SONNE (SO 205). Same as Bathynanus and Nanacalathis, it is expected that Rectocalathis n. gen. is also restricted to deep water.
Eucalathissp. (Chlidonophoridae) – ZMB Bra 2351
Gryphus vitreus(Terebratulidae) – ZMB Bra 2261
Liothyrella neozelanica(Terebratulidae) – ZMB Bra 2255
Full data sets and additional material
Figures and interactive 3D models of additional 5 species with spicules (Laqueus rubellus (Sowerby, 1846) – Additional files 8 and 9, M. truncata – Additional files 10 and 11, P. anomioides – Additional files 12 and 13, Pumilus antiquatus Atkins, 1958 – Additional files 14 and 15, P. atlantica – Additional files 16 and 17) can be accessed as Online Supplemental Material, as well as a phylogenetic tree and tables concerning the scan parameters and morphometric analyses of all species of the initial study.
Applicability of micro-computed tomography for the study of modern brachiopods
Scanning modern brachiopods with an X-ray micro-computed tomograph (μCT) creates naturally aligned virtual sections (2D) and interactive 3D models. μCT is a unique tool for obtaining and visualising structural and positional data of the spiculation and the inner shell morphology of modern brachiopods. The present μCT data visualises the endoskeleton and the shell with high accuracy and natural orientation. In a short period of time, the endoskeletal spiculation in 10 out of 19 investigated genera was detected by analyzing stacks of 2 dimensional images. The scanning and reconstruction is a clean and quick procedure, whereas the subsequent virtual sectioning and colouration necessary to create 3D models is much more time consuming, but is particularly important for understanding the three dimensional architecture of structures, linking colours to regions of interest and it results in an unlimited set of views. Hard parts of the animals can be easily defined and marked, whereas soft tissue visualization needs staining.
With the achieved resolution of 10 microns the anatomy of single spicules and differences in the surface texture (e.g. muscle scars) can be visualised. However, the quality of images depends significantly on the rendering algorithm that is applied, which is in turn linked to the computing power and total operation time. In this study the volume renderer PHONG and an isosurface renderer were used. The latter does not affect the CPU as much as the volume render and yields good results for simulating transparency. The chosen scan parameters represent appropriate balances between so called “fast scans” (~15 minutes) and scans of longer duration (>50 minutes) which resulted in data of more than 20 GB / file). The presence of minute structures such as spicules and punctae canals could easily be detected with the scan parameters that were applied, in whole mount scans of any specimen size.
μCT (Phoenix Nanotom XS 180 NF) produces high resolution images of brachiopods visualising their mineralized exo- and endoskeleton and allows rotational analysis of the specimen. Depending on the condition of the animal and the scan duration (scan parameters, such as number of images, timing, “average and skip”) μCT images are comparable to SEM images by showing the full set of informative characters of the shell, e.g. muscle scars, punctae, growth lines, costae, tubercles, septae, spicules, teeth and sockets, crura and brachidium. However, in regard to the resolution it is less effective than scanning electron microscopy (SEM), hence SEM would be the first method of choice for surface-sensitive investigations, especially when resolutions of only a few microns or less are needed. None of the specimens investigated in this study were physically damaged through μCT scanning. As a result, after being scanned the specimen of Eucalathis sp. was successfully included in a DNA sequencing analysis which underlines the compatibility of μCT and molecular analyses. However, there is no certainty about a maximum radiation dose for successful post-scan DNA sequencing and therefore, rather short scans and immediate DNA amplification are recommended.
What is the function of a brachiopod’s endoskeleton?
Speculation about the function of spiculation has been fuelled by a general debate concerning the vulnerability of brachiopods . Their generally poor soft tissue yield results in little predation pressure, especially when the tissue contains spicules or toxins ,. However, it is known that modern echinoderms, gastropods and crabs certainly penetrate the shell and do feed on brachiopods , and references therein]. The strength of the brachiopod shell is more affected by the thickness and ribbing, rather than by the biconvexity or presence of punctae . However, organic matter is inaccessible to predators when placed within the punctae and similarly the internal tissue is not palatable when containing high amounts of inorganic spicules. Analyses of tissue of modern brachiopods and their value to predators revealed a higher inorganic content in the tissue of punctate than the impunctate brachiopods , which is in accordance with the observations in this study. Therefore, the co-occurence of spiculation and punctation may be referred to as non-chemical responses to predatory pressure.
Another criterion is the mechanical support for the soft tissue, especially of the lophophore. Mechanical tests with Terebratulina unguicula (Carpenter, 1864) revealed that a mean elastic modulus for spiculated tissues is more than three times greater than for artificially decalcified tissues . In this study, all of the “short looped” specimens with little exoskeletal support of the lophophore (brachidium) exhibit spicules within the lophophore. Certain load-bearing features of the endoskeleton can be identified. The design of these structures suggests a perfect cooperation with the brachidium to maintain function and orientation of the lophophore with its protruding arms, as observed in the posterior excrescences of the endoskeleton in Eucalathis sp. and Rectocalathis schemmgregoryi n. gen., n. sp. or in the distinct thick and plate-shaped structures for load-bearing in G. vitreus and L. neozelanica. The conspicuous load-bearing structure of G. vitreus and L. neozelanica can be addressed as an additional synapomorphic character of the family Terebratulidae (see Additional file 18: Figure S6. Phylogeny), identified due to this nondestructive μCT approach. A massive, area-wide spiculation within soft parts offers either mechanical support or fulfils a potent anti-predator function, or both. It is questionable whether the weak spiculation in the dorsal body wall of Eucalathis sp. and Rectocalathis schemmgregoryi n. gen., n. sp. serves as mechanical support. The anatomy suggests a regulation of the coelomic cavity pressure in interaction with muscles. Nonetheless, the weak spiculation in the dorsal body wall as well as in the specialized lophophoral endoskeleton indicates the close phylogenetic relationship of both species (see Additional file 16: Figure S6. Phylogeny)
The aim of this μCT study was to depict the profound differences of the hard parts and shell anatomy of modern brachiopods and to establish μCT scan and subsequent data processing protocols suitable for specimens preserved in alcohol. Micro-CT is an excellent non-destructive tool for visualizing the calcified exo- and endoskeleton of brachiopods. Acquired data on spiculation delivers a substantial contribution to formerly available documentations of brachiopod hard parts (endoskeleton) due to its visualization in its entirety. The phylogenetic relevance of spiculation has been indicated, with promising new informative characters. However extensive sampling is necessary to verify these findings and to discover intra-specific variability of spiculation.
Materials and methods
Representatives of 17 brachiopod genera covering all modern articulated subgroups and two representatives of inarticulated craniids were scanned for morphological analysis. The results from specimens with spicules are shown in this paper or can be accessed in the Supplemental Material. All specimens were selected from either the historical wet collection of the Museum für Naturkunde Berlin, Germany or from recently collected samples. For specimens used in this study see Table 1 and Additional file 1: Table S1. All specimens were stored in 75 - 80% ethanol (EtOH). For scanning, the specimen’s valves were slightly opened with a needle and transferred gradually to distilled water. The scanning was performed dry to prevent soft tissue from moving, especially of the lophophore and the tentacles. For scanning the calcareous shell, it made no difference whether the prefixation was performed in alcohol, formaldehyde or Bouin’s solution.
Scan parameters used in this study
Timing value (ms)
Averaging & Skip
Scan Time ~ (min)
2 – 1
R. schemmgregoryi n. gen., n. sp.
2 – 1
2 – 1
2 – 1
2 – 1
Image processing of the initial 3D reconstruction with earmarking of the “regions of interests”, cleaning of the volume, specimen analyses and morphometries was carried out on a Dell Workstation (Dell Precision T7500, Intel Xeon E5530, 2.4 GHz; graphics card: NVIDIA GeForce GTX 285; operating system: Microsoft Windows XP Professional x64 Edition) using the software “Volume Graphics Studio Max 2.1” (Volume Graphics GmbH, Heidelberg, Germany, http://www.volumegraphics.com). The reconstructions were virtually sectioned to illustrate key features. Images (also 360° full HD (1920×1080) movie clips, data not shown, for details please contact the authors) were obtained using an isosurface or volume (PHONG) rendering algorithm. To illustrate the natural position of the spiculation and internal shell features the isosurface render algorithm was used to simulate transparency of the shell.
For subsequent data processing mostly open source software was used. As for the 3D interactive models, the open source software “MeshLab 1.3.2” (MeshLab, Visual Computing Lab – ISTI – CNR; http://meshlab.sourceforge.net/) for cleaning and down sampling the meshes and “DAZ Studio 22.214.171.124 Standart”(DAZ Productions, Inc., dba DAZ 3D; 224 South 200 West #250, Salt Lake City, UT 84101 USA; http://www.daz3d.com/) for creating the u3d file format were used. The final 3D interactive pdf file was created using the commercial software Adobe Acrobat 8 Professional 8.1.0. (Adobe® Systems Incorporated, San José, CA).
Thanks are due to Johannes Müller and Christy Hipsley (both Museum für Naturkunde, Berlin) for their support and invaluable help with setting up the μCT to optimize the results. We are indebted to the crews, the scientific leaders (namely Pedro Martinez Arbizu, Kaj Hörnle, Reinhard Werner, and Gert Wörheide) and the shipboard scientific parties of several deep-sea expeditions (SO 205 “Mangan”, SO 208 “Plumeflux”, MSM 19-3, LU 839/2 and WO 896/7 “DeepDownunder”) for providing material for this study. We also thank Jana Hoffmann, Bernard L. Cohen, Georg Maghon, Claudia Wolter, Paul Meredith, Sally Carson, Jim Fyfe, Nina Furchheim, and Peter Wirtz for collecting and providing additional specimens of different species. Collection campaigns and expeditions were financially supported within several projects funded by the German Research Foundation (DFG) and the German Ministry of Education and Research (BMBF).
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