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Systematic comparison and reconstruction of sea urchin (Echinoidea) internal anatomy: a novel approach using magnetic resonance imaging.
Ziegler A
,
Faber C
,
Mueller S
,
Bartolomaeus T
.
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BACKGROUND: Traditional comparative morphological analyses and subsequent three-dimensional reconstructions suffer from a number of drawbacks. This is particularly evident in the case of soft tissue studies that are technically demanding, time-consuming, and often prone to produce artefacts. These problems can partly be overcome by employing non-invasive, destruction-free imaging techniques, in particular micro-computed tomography or magnetic resonance imaging.
RESULTS: Here, we employed high-field magnetic resonance imaging techniques to gather numerous data from members of a major marine invertebrate taxon, the sea urchins (Echinoidea). For this model study, 13 of the 14 currently recognized high-ranking subtaxa (orders) of this group of animals were analyzed. Based on the acquired datasets, interactive three-dimensional models were assembled. Our analyses reveal that selected soft tissue characters can even be used for phylogenetic inferences in sea urchins, as exemplified by differences in the size and shape of the gastric caecum found in the Irregularia.
CONCLUSION: The main focus of our investigation was to explore the possibility to systematically visualize the internal anatomy of echinoids obtained from various museum collections. We show that, in contrast to classical preparative procedures, magnetic resonance imaging can give rapid, destruction-free access to morphological data from numerous specimens, thus extending the range of techniques available for comparative studies of invertebrate morphology.
Figure 1. Establishment of imaging conditions using specimens of Psammechinus miliaris. (A), (B) Comparison of two freshly fixed specimens. Magnetic resonance imaging (MRI) sections at the height of Aristotle's lantern and digestive tract. Resolution: (81 μm)3, no contrast agent added. The two specimens show a high degree of similarity in their overall internal architecture. Arrows indicate paramagnetic gut content. (C), (D) Effects of a contrast agent on image quality. MRI sections at the height of perignathic girdle and lower stomach. Resolution: (81 μm)3. This freshly fixed specimen was scanned (C) before and (D) after the application of a contrast agent, Magnevist. Arrows indicate susceptibility artefacts. (E), (F) Comparison of a freshly fixed and a museum specimen. MRI sections at the height of gonads and upper oesophagus. Resolution: (81 μm)3. The 135-year-old museum specimen (F) gives imaging results comparable to the freshly fixed specimen (E). Both specimens were scanned with contrast agent added. Orientation: ambulacrum II facing upwards. Scale bar: 0.5 cm. ac, axial complex; al, Aristotle's lantern; am, ampulla; es, oesophagus; go, gonad; im, interpyramidal muscle; in, intestine; is, inner marginal sinus; l m, lantern muscle; os, outer marginal sinus; pg, perignathic girdle; re, rectum; si, siphon; st, stomach; to, tooth.
Figure 2. Selected horizontal magnetic resonance imaging sections of different sea urchin species taken from Additional files 3, 4, 5, 6. (A) Eucidaris metularia. Resolution: (81 μm)3. Aristotle's lantern, gonads, Stewart's organs, and stomach can be seen. (B) Psammechinus miliaris. Resolution: (44 μm)3. Aristotle's lantern, lantern muscles, stomach, and ampullae are visible. (C) Echinoneus cyclostomus. Resolution: (86 μm)3. Digestive tract with oesophagus, gastric caecum, stomach, and rectum are shown. (D) Echinocyamus pusillus. Resolution: 20 × 18 × 18 μm3. Aristotle's lantern, gonads, stomach, and rectum are represented. Scale bar: (A)-(C) 0.5 cm; (D): 1 mm. al, Aristotle's lantern; am, ampulla; es, oesophagus; gc, gastric caecum; lm, lantern muscle; re, rectum; so, Stewarts' organ; st, stomach.
Figure 3. Overview chart showing analyzed specimens of 'regular' sea urchins and corresponding 3D reconstructions of selected internal organs. (A) Information on species name, geographic distribution, and systematics. (B) Photograph of scanned specimen, aboral view. (C)-(E) 3D models of reconstructed selected internal organs, stepwise turned by 90°: (C) aboral view (interambulacrum 5 facing upwards); (D) lateral view (interambulacrum 5 at back); (E) oral view (interambulacrum 5 facing downwards). The buccal sacs of Caenopedina mirabilis as well as the siphon of Stomopneustes variolaris could not be seen on the magnetic resonance imaging sections. Scale bar: 1 cm. The colour legend specifies organ designation.
Figure 4. Overview chart showing analyzed specimens of irregular sea urchins and corresponding 3D reconstructions of selected internal organs. (A) Information on species name, geographic distribution, and systematics. (B) Photograph of scanned specimen, aboral view. (C)-(E) 3D models of reconstructed selected internal organs, stepwise turned by 90°: (C) aboral view (ambulacrum III facing to the right); (D) lateral view (ambulacrum III facing to the right); (E) oral view (ambulacrum III facing to the right). Scale bar: 1 cm, except for Echinocyamus pusillus: 1 mm. The colour legend specifies organ designation.
Figure 5. 3D reconstructions of the gastric caecum of selected irregular sea urchin species. The gastric caecum is a translucent body free of sediment and probably constitutes one of the main sites of digestion [38,39]. The upper diagrams show an aboral view, the lower diagrams a lateral view with the anterior side (ambulacrum III) oriented towards the right-hand side. Arrows indicate the position of the junction of the gastric caecum with the stomach. (A) Echinoneus cyclostomus, Echinoneoida. (B) Echinolampas depressa, Cassiduloida. Species of this sea urchin taxon presumably all possess a highly reduced gastric caecum consisting of numerous small blindly ending sacs. (C) Pourtalesia wandeli, Holasteroida. (D) Abatus cavernosus, Spatangoida. Scale bar: 0.5 cm.
Figure 6. Comparison of a digital 3D model with a traditional anatomical sketch. (A)-(C) Eucidaris metularia. Selected views taken from the interactive 3D model: (A) external view; (B) external view with transparent test, internal organs visible; (C) external view with transparent test and all internal organs removed except for Stewart's organs and Aristotle's lantern. (D) Cidaris cidaris (= Dorocidaris papillata). Image taken from [42] and modified. Stewart's organs constitute extensions of the peripharyngeal coelom. Scale bar: 1 cm. The colour legend specifies organ designation. The interactive 3D mode can be accessed by clicking onto Figure 6 in the 3D PDF version of this article: Additional file 7 (Adobe Reader Version 7.1 or higher required).
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