Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
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
.
???displayArticle.abstract???
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).
Attwood,
Microscopy: nanotomography comes of age.
2006, Pubmed
Attwood,
Microscopy: nanotomography comes of age.
2006,
Pubmed
Betz,
Imaging applications of synchrotron X-ray phase-contrast microtomography in biological morphology and biomaterials science. I. General aspects of the technique and its advantages in the analysis of millimetre-sized arthropod structure.
2007,
Pubmed
Bock,
Simultaneous observations of haemolymph flow and ventilation in marine spider crabs at different temperatures: a flow weighted MRI study.
2001,
Pubmed
Brinkley,
Magnetic resonance imaging at 9.4 T as a tool for studying neural anatomy in non-vertebrates.
2005,
Pubmed
Brouwer,
In vivo magnetic resonance imaging of the blue crab, Callinectes sapidus: effect of cadmium accumulation in tissues on proton relaxation properties.
1992,
Pubmed
Burrow,
X-ray microtomography of 410 million-year-old optic capsules from placoderm fishes.
2005,
Pubmed
Davenel,
Noninvasive characterization of gonad maturation and determination of the sex of Pacific oysters by MRI.
2006,
Pubmed
Dunn,
Broad phylogenomic sampling improves resolution of the animal tree of life.
2008,
Pubmed
Gozansky,
Magnetic resonance histology: in situ single cell imaging of receptor cells in an invertebrate (Lolliguncula brevis, Cephalopoda) sense organ.
2003,
Pubmed
Haddad,
NMR imaging of the honeybee brain.
2004,
Pubmed
Hart,
Magnetic resonance imaging in entomology: a critical review.
2003,
Pubmed
Herberholz,
Anatomy of a live invertebrate revealed by manganese-enhanced Magnetic Resonance Imaging.
2004,
Pubmed
Holland,
A comparative study of gut mucous cells in thirty-seven species of the class Echinoidea (Echinodermata).
1970,
Pubmed
,
Echinobase
Hörnschemeyer,
Head structures of Priacma serrata Leconte (Coleptera, Archostemata) inferred from X-ray tomography.
2002,
Pubmed
Huetteroth,
Standard three-dimensional glomeruli of the Manduca sexta antennal lobe: a tool to study both developmental and adult neuronal plasticity.
2005,
Pubmed
Jasanoff,
In vivo magnetic resonance microscopy of brain structure in unanesthetized flies.
2002,
Pubmed
Klaus,
Novel methodology utilizing confocal laser scanning microscopy for systematic analysis in arthropods (Insecta).
2006,
Pubmed
Klaus,
Three-dimensional visualization of insect morphology using confocal laser scanning microscopy.
2003,
Pubmed
Littlewood,
A combined morphological and molecular phylogeny for sea urchins (Echinoidea: Echinodermata).
1995,
Pubmed
,
Echinobase
Mapelli,
Application of NMR microscopy to the morphological study of the silkworm, Bombyx mori, during its metamorphosis.
1997,
Pubmed
Michaelis,
In vivo 3D MRI of insect brain: cerebral development during metamorphosis of Manduca sexta.
2005,
Pubmed
Michels,
Confocal laser scanning microscopy: using cuticular autofluorescence for high resolution morphological imaging in small crustaceans.
2007,
Pubmed
Müller,
Magnetic resonance imaging of the siliceous skeleton of the demosponge Lubomirskia baicalensis.
2006,
Pubmed
Pohlmann,
MRI of tarantulas: morphological and perfusion imaging.
2007,
Pubmed
Ruthensteiner,
Embedding 3D models of biological specimens in PDF publications.
2008,
Pubmed
Shapiro,
Dynamic imaging with MRI contrast agents: quantitative considerations.
2006,
Pubmed
Smith,
Testing the molecular clock: molecular and paleontological estimates of divergence times in the Echinoidea (Echinodermata).
2006,
Pubmed
,
Echinobase
Socha,
Real-time phase-contrast x-ray imaging: a new technique for the study of animal form and function.
2007,
Pubmed
Sodergren,
The genome of the sea urchin Strongylocentrotus purpuratus.
2006,
Pubmed
,
Echinobase
Sutton,
Tomographic techniques for the study of exceptionally preserved fossils.
2008,
Pubmed
Watanabe,
Manganese-enhanced 3D MRI of established and disrupted synaptic activity in the developing insect brain in vivo.
2006,
Pubmed
Wecker,
Investigation of insect morphology by MRI: assessment of spatial and temporal resolution.
2002,
Pubmed
Wirkner,
Improvement of microanatomical research by combining corrosion casts with MicroCT and 3D reconstruction, exemplified in the circulatory organs of the woodlouse.
2004,
Pubmed
Wirkner,
The circulatory system in Mysidacea--implications for the phylogenetic position of Lophogastrida and Mysida (Malacostraca, Crustacea).
2007,
Pubmed
Yushkevich,
User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability.
2006,
Pubmed
