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Comparative morphological and structural analysis of selected cidaroid and camarodont sea urchin spines

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Abstract

The external and internal morphologies of cidaroid and camarodont sea urchin primary spines are investigated giving an overview of the internal microstructure and structural properties. The investigated species comprise the cidaroids Eucidaris metularia, Phyllacanthus imperialis, Plococidaris verticillata and Prionocidaris baculosa as well as the camarodont Heterocentrotus mammillatus (Echinodermata: Class Echinoidea), and morphological descriptions are based on scanning electron microscopy and micro-computed tomography. Stereom types and densities are differentiated using pore and trabecular diameter measurements. Structural analysis was performed using three point bending tests resulting in the calculation of force, deflection and stress, strain relationships. All studied species possess primary spines with a medulla consisting of laminar stereom regardless of the age and position of the spine on the tests. Differences in stereom morphology occur in the radiating layer and the surface of the spines. Material densities and stereom types differ with respect to growth lines when present and the radiating layer. The primary spines also show large differences in their outer morphologies ranging from smooth, striated to tuberculate. H. mammillatus spines are shown to bear more stress resistance than those of the cidaroids. Differences in spine morphologies and reaction to stress are interpreted with respect to functional morphological response, to ambient environmental parameters and their strategies between and within evolutionary stages.

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Acknowledgments

The work was part of a dissertation in the interdisciplinary project “New materials for light, permeable impact protective systems: sea urchins as a model” funded by the “Stiftung Baden-Württemberg”. Special thanks go to Hartmut Schulz and Peter Fittkau for helping with the SEM, to Sebastian Schmelzle for managing the 3D images and to Hema-CT for the CT-images and Wolfgang Gerber for total spine images. Achim Vohrer is thanked for the lively discussion during bending tests at the ITV Denkendorf.

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Authors and Affiliations

  1. University of Bonn, Meckenheimer Allee 169, 53115, Bonn, Germany

    Jan Nils Grossmann

  2. University of Tübingen, Sigwartstr. 10, 72071, Tübingen, Germany

    James H. Nebelsick

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  1. Jan Nils Grossmann
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Correspondence to Jan Nils Grossmann.

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Communicated by A. Schmidt-Rhaesa.

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Supplementary 1: Mathematical equations and formulae for the bending tests (XLSX 24 kb)

435_2013_192_MOESM2_ESM.tif

Supplementary 2 Plococidaris verticillata spine: a) medulla and radiating layer at the base; b) laminar medulla, galleried radiating layer and cortex in detail; c) medulla in the shaft; d) tip of a spine including medulla, radiating layer and cortex; e) galleried radiating layer of a whorl; f) whorl in detail, including radiating layer and cortex. The galleries are inclined with reference to the medulla at ca. 45° from central long axis of the spine. The thickness of the cortex ranges from ca. 80 µm at the base, 60 to 70 µm at the flanks, to ca. 80 µm at the tip (scale bars = 100 µm except for e = 50 µm) (after Grossmann and Nebelsick 2013) (TIFF 16602 kb)

435_2013_192_MOESM3_ESM.tif

Supplementary 3 Eucidaris metularia spine in longitudinal direction: a) medulla (middle), radiating layer and cortex near the milled ring; b) galleried radiating layer; c) the shaft; d); microperforated cortex; e) radiating layer and cortex; f) medulla in the upper spine part. The cortex thickness has a mean value of around 150 µm (Fig. 5C and E). From the base to the tip it thickens from around 128 µm to 152 µm (scale bars = 100 µm, except for d = 10 µm) (TIFF 16342 kb)

435_2013_192_MOESM4_ESM.docx

Supplementary 4 Larger aboral spines of Phyllacanthus imperialis: Medulla: Box-plot and histogram (a and b) of the pore diameter and (c and d) the trabeculae diameter; Radiating layer: Box-plot and histogram (e and f) of the pore diameter and (g and h) the trabeculae diameter. Box plots include median, minimum and maximum values of the investigated data and the outliers, as well as the area where 25 % and 75 % of the values are lying. The histogram includes the frequencies, and the distribution curve (dark line vertical to the x-axis), as well as the mean value. Spine images in the box plots show the approximate position of the investigated area (DOCX 332 kb)

435_2013_192_MOESM5_ESM.docx

Supplementary 5: Larger fully grown spines of Heterocentrotus mammillatus: Medulla: Box-plot and histogram (a and b) of the pore diameter and (c and d) the trabeculae diameter; Radiating layer: Box-plot and histogram (e and f) of the pore diameter and (g and h) the trabeculae diameter. Box plots include median, minimum and maximum values of the investigated data and the outliers, as well as the area where 25 % and 75 % of the values are lying. The histogram includes the frequencies, and the distribution curve value (dark line vertical to the x-axis) as well as the mean. Spine images in the box plots show the investigated area position approximately (DOCX 380 kb)

435_2013_192_MOESM6_ESM.tif

Supplementary 6 Oral spine of Heterocentrotus mammillatus in different views: two-dimensional longitudinal view (a) and cross-sections of the tip (b), middle shaft (c) and the base (d). The spine from the centre to the outside is separated into medulla, disrupting growth rings and the radiating layer. The outside of the spine is covered by an epidermis (scale bars = 5 mm) (TIFF 3427 kb)

435_2013_192_MOESM7_ESM.xlsx

Supplementary 7 a Force-deflection and b stress-strain diagram of juvenile Heterocentrotus mammillatus spines: The numbers in the legend are the spine samples. After the highest force loading the spines broke (XLSX 86 kb)

435_2013_192_MOESM8_ESM.xlsx

Supplementary 8 a Force-deflection and b stress-strain diagram of fully grown Heterocentrotus mammillatus spines: The numbers in the legend are the spine samples. After the highest force loading the spines broke. The values of the sample B9 are not shown due to structural failure after measurement start (XLSX 600 kb)

435_2013_192_MOESM9_ESM.xlsx

Supplementary 9 a Force-deflection and b stress-strain diagram of juvenile Phyllacanthus imperialis spines: The numbers in the legend are the spine samples. After the highest force loading the spines broke (XLSX 66 kb)

435_2013_192_MOESM10_ESM.xlsx

Supplementary 10 a Force-deflection and b stress-strain diagram of fully grown Phyllacanthus imperialis spines. The numbers in the legend are the spine samples. After the highest force loading the spines broke (XLSX 102 kb)

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Grossmann, J.N., Nebelsick, J.H. Comparative morphological and structural analysis of selected cidaroid and camarodont sea urchin spines. Zoomorphology 132, 301–315 (2013). https://doi.org/10.1007/s00435-013-0192-5

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