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Comparative morphology and phylogenetic significance of Gregory’s diverticulum in sand dollars (Echinoidea: Clypeasteroida)

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Abstract

Several derived sand dollar (Echinoidea: Clypeasteroida) families are characterized by the presence of Gregory’s diverticulum, an accessory organ of the digestive tract. This soft tissue structure is composed of a central tubular cecum that gives off multiple lobes into the periphery of the test. Most notable are the organ’s capacity to selectively store sand grains that the animal has taken up from the surrounding sediment as well as the gradual reduction of Gregory’s diverticulum during ontogeny. Several aspects of the biology of this structure have remained unexplored, including the organ’s precise morphology and structural diversity. In order to provide a concise basis for future histological, physiological, and functional analyses, a comprehensive comparative morphological and phylogenetic study across numerous taxa was undertaken. Taxon sampling comprised over 100 clypeasteroid species, including various fossil taxa. This extensive dataset permits establishing a concise terminology that incorporates all of the organ’s substructures. In addition, three-dimensional models of Gregory’s diverticulum are presented that provide an improved spatial understanding of the organ’s morphology in situ. The combined data from dissection, X-ray imaging, microcomputed tomography, and magnetic resonance imaging reveal a previously unknown variability of the structure, which also yields several phylogenetically informative morphological characters. Among those sand dollar families that possess Gregory’s diverticulum, the organ is present in two distinct shapes, which can be distinguished by the number, shape, and location of substructures. In addition, the data provide unequivocal evidence that Gregory’s diverticulum is absent in the extant taxa Rotulidae and Astriclypeidae, but also in the enigmatic Marginoproctus.

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Abbreviations

μCT:

Microcomputed tomography

2D:

Two-dimensional

3D:

Three-dimensional

Amb:

Ambulacrum

BMNH:

British Museum of Natural History, London, UK

BPBM:

Bernice P. Bishop Museum, Honolulu, HI, USA

CASG:

California Academy of Sciences Geology, San Francisco, CA, USA

CASIZ:

California Academy of Sciences Invertebrate Zoology, San Francisco, CA, USA

CT:

Computed tomography

FDNR:

Florida Department of Natural Resources, St. Petersburg, FL, USA

IAmb:

Interambulacrum

MCZ:

Museum of Comparative Zoology, Cambridge, MA, USA

MMBS:

Misaki Marine Biological Station, Misaki, Japan

MNHN:

Muséum national d'Histoire naturelle, Paris, France

MRI:

Magnetic resonance imaging

Mya:

Million years ago

NMNS:

National Museum of Natural Science, Taipei, Taiwan

SIO:

Scripps Institution of Oceanography, San Diego, CA, USA

UB:

Université de Bourgogne, Dijon, France

UCMP:

Museum of Paleontology, University of California, Berkeley, CA, USA

UNEFM:

Museo de la Universidad Nacional Experimental Francisco de Miranda, Falcón, Venezuela

USNM:

United States National Museum, Washington, DC, USA

UT:

University of Texas at Austin, Austin, TX, USA

UTO:

University of Toronto, Ontario, Canada

WAM:

Western Australian Museum, Perth, Western Australia, Australia

ZMB:

Museum für Naturkunde, Berlin, Germany

ZMH:

Zoologisches Museum Hamburg, Hamburg, Germany

ZMK:

Zoologisk Museum København, Copenhagen, Denmark

ZSM:

Zoologische Staatssammlung München, Munich, Germany

References

  • Agassiz, L. R. (1841). Des Scutelles. In L. R. Agassiz (Ed.), Monographies d'Échinodermes vivans et fossiles. Neuchâtel: Petitpierre. 151 pp.

    Google Scholar 

  • Agassiz, A. E. (1872–74). Revision of the Echini. The University Press, Cambridge. 762 pp.

  • Anisimov, A. P. (1982). Morphological and cytochemical characteristics of the alimentary canal epithelium of the sand dollar Scaphechinus griseus (Mortensen) (Echinodermata: Echinoidea: Clypeasteroida). Biologya Morya, 1, 28–34 [in Russian].

    Google Scholar 

  • Borzone, C. A., Tavares, Y. A. G., & Soares, C. R. (1997). Adaptação morfológica de Mellita quinquiesperforata (Clypeasteroida, Mellitidae) para explorar ambientes com alto hidrodinamismo. Iheringia, Série Zoologia, 82, 33–42.

    Google Scholar 

  • Burke, R. D. (1982). Echinoid metamorphosis: retraction and resorption of larval tissues. In J. M. Lawrence (Ed.), International Echinoderms Conference, Tampa Bay (pp. 513–518). Rotterdam: AA Balkema.

    Google Scholar 

  • Burke, R. D. (1983). Neural control of metamorphosis in Dendraster excentricus. Biological Bulletin, 164, 176–188.

    Article  Google Scholar 

  • Caso, M. E. (1980). The echinoids of the Pacific coast of Mexico. Third part—Order Clypeasteroida. Publicaciones Especiales Centro de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México 4: 1–252.

  • Chen, C. P., & Chen, B. Y. (1994). Diverticulum sand in a miniature sand dollar Sinaechinocyamus mai (Echinodermata: Echinoidea). Marine Biology, 119, 605–609.

    Article  Google Scholar 

  • Chia, F. S. (1969). Some observations on the locomotion and feeding of the sand dollar, Dendraster excentricus (Eschscholtz). Journal of Experimental Marine Biology and Ecology, 3, 162–170.

    Article  Google Scholar 

  • Chia, F. S. (1973). Sand dollar: a weight belt for the juvenile. Science, 181, 73–74.

    Article  CAS  PubMed  Google Scholar 

  • Chia, F. S. (1985). Selection, storage and elimination of heavy sand particles by the juvenile sand dollar, Dendraster excentricus (Eschscholtz). In B. F. Keegan & B. D. S. O’Connor (Eds.), Echinodermata. Proceedings of the Fifth International Echinoderm Conference (pp. 215–221). Rotterdam: AA Balkema.

    Google Scholar 

  • Clark, H. L. (1909). Scientific results of the trawling expedition of H.M.C.S. “Thetis” off the coast of New South Wales, in February and March, 1898, Echinodermata. Memoirs of the Australian Museum, 4, 519–564.

    Article  Google Scholar 

  • Coe, W. R. (1912). Echinoderms of Connecticut. State Geological and Natural History Survey Bulletin, 19, 1–152.

    Google Scholar 

  • Cuénot, L. (1891). Études morphologiques sur les échinodermes. Archives de Biologie, 11, 21–678.

    Google Scholar 

  • Dartevelle, E. (1953). Échinides fossiles du Congo et de l'Angola. Annales du Musée Royal du Congo Belge, Série 8, Sciences Géologiques, 13, 1–240.

  • De Ridder, C., & Jangoux, M. (1982). Digestive systems: Echinoidea. In M. Jangoux & J. M. Lawrence (Eds.), Echinoderm Nutrition (pp. 213–234). Rotterdam: AA Balkema.

    Google Scholar 

  • Desmoulins, C. (1835–37). Études sur les Échinides. Lafargue, Bordeaux, 520 pp.

  • Elkin, Y. N., Maksimov, S. O., Safronov, P. P., Zvereva, V. P., & Artyukov, A. A. (2012). Selective accumulation of zircons and ilmenites in diverticula of the sea urchin Scaphechinus mirabilis (Agassiz, 1863). Doklady Biological Sciences, 446, 297–299.

    Article  PubMed  Google Scholar 

  • Fewkes, J. W. (1886). Preliminary observations on the development of Ophiopholis and Echinarachnius. Bulletin of the Museum of Comparative Zoology, 12, 105–152.

    Google Scholar 

  • Fox, R. (2001). Mellita quinquiesperforata—sand dollar. Invertebrate Anatomy OnLine, http://lanwebs.lander.edu/faculty/rsfox/invertebrates/mellita.html. Accessed 4 Aug 2015.

  • Grave, C. (1902). Some points in the structure and development of Mellita testudinata. Johns Hopkins University Circulars, 157, 57–59.

    Google Scholar 

  • Gregory, E. R. (1905). An unnoticed organ of the sand-dollar, Echinarachnius parma. Science, 21, 270.

    Article  Google Scholar 

  • Harold, A. S., & Telford, M. (1990). Systematics, phylogeny and biogeography of the genus Mellita (Echinoidea: Clypeasteroida). Journal of Natural History, 24, 987–1026.

    Article  Google Scholar 

  • Koehler, R. (1914). Echinoderma I: Asteroidea, Ophiuroidea et Echinoidea. In W. Michaelsen (Ed.), Beiträge zur Kenntnis der Meeresfauna Westafrikas (pp. 127–303). Hamburg: Friederichsen & Co.

    Google Scholar 

  • Koehler, R. (1922). Échinides du Musée Indien a Calcutta. II. Clypeastridés et Cassidulidés. Calcutta: Trustees of the Indian Museum, 161 pp.

  • Kroh, A., Mooi, R. (2015). The World Echinoidea Database. http://www.marinespecies.org/Echinoidea/. Accessed 4 Aug 2015.

  • Kroh, A., & Smith, A. B. (2010). The phylogeny and classification of post-Palaeozoic echinoids. Journal of Systematic Palaeontology, 8, 147–212.

    Article  Google Scholar 

  • Kroh, A., Jangoux, M., Mirantsev, G. V., & Ziegler, A. (2013). The Echinoderm Files: a database-facilitated access to a hidden treasure trove. Cahiers de Biologie Marine, 54, 549–557.

    Google Scholar 

  • Lares, M. T. (1999). Evaluation of direct and indirect techniques for measuring absorption efficiencies of sea urchins (Echinodermata: Echinoidea) using prepared feeds. Journal of the World Aquaculture Society, 30, 201–207.

    Article  Google Scholar 

  • Lawrence, J. M. (2001). Function of eponymous structures in echinoderms: a review. Canadian Journal of Zoology, 79, 1251–1264.

    Article  Google Scholar 

  • Linder, R.A. (1986). Mid-Tertiary echinoids and Oligocene shallow marine environments in the Oregon central Western Cascades. M.Sc. thesis, University of Oregon, 196 pp.

  • Linder, R. A., Durham, J. W., & Orr, W. N. (1988). New late Oligocene echinoids from the central Western Cascades of Oregon. Journal of Paleontology, 62, 945–958.

    Google Scholar 

  • MacBride, E. W. (1906). Echinoidea. In S. F. Farmer & A. E. Shipley (Eds.), The Cambridge Natural History (pp. 503–559). London: Macmillan & Co.

    Google Scholar 

  • Mihaljević, M., Klug, C., Aguilera, O., Lüthi, T., & Sanchez-Villagra, M. R. (2010). Palaeodiversity of Caribbean echinoids including new material from the Venezuelan Neogene. Palaeontologica Electronica, 13, 13.3.20A.

    Google Scholar 

  • Mihaljević, M., Jerjen, I., & Smith, A. B. (2011). The test architecture of Clypeaster (Echinoidea, Clypeasteroida) and its phylogenetic significance. Zootaxa, 2983, 21–38.

    Google Scholar 

  • Mitchell, B.P. (1972). Rediscovery of Gregory’s diverticulum in the scutellid sand dollars. M.Ed. thesis, Western Washington State College, 32 pp.

  • Mooi, R. (1987). A cladistic analysis of the sand dollars (Clypeasteroida: Scutellina) and the interpretation of heterochronic phenomena. Ph.D. thesis, University of Toronto, 204 pp.

  • Mooi, R. (1989). Living and fossil genera of the Clypeasteroida (Echinoidea: Echinodermata): an illustrated key and annotated checklist. Smithsonian Contributions to Zoology, 488, 1–51.

    Article  Google Scholar 

  • Mooi, R. (1990). Paedomorphosis, Aristotle’s lantern, and the origin of the sand dollars (Echinodermata: Clypeasteroida). Paleobiology, 16, 25–48.

    Google Scholar 

  • Mooi, R., & Chen, C. P. (1996). Weight belts, diverticula, and the phylogeny of the sand dollars. Bulletin of Marine Science, 58, 186–195.

    Google Scholar 

  • Mooi, R., Kroh, A., & Srivastava, D. K. (2014). Phylogenetic re-evaluation of fossil and extant micro-echinoids with revision of Tridium, Cyamidia, and Lenicyamidia (Echinoidea: Clypeasteroida). Zootaxa, 3857, 501–526.

    Article  PubMed  Google Scholar 

  • Moore, A. M. F., & Ellers, O. (1993). A functional morphospace, based on dimensionless numbers, for a circumferential, calcite, stabilizing structure in sand dollars. Journal of Theoretical Biology, 162, 253–266.

    Article  Google Scholar 

  • Mortensen, T. (1948). A monograph of the Echinoidea. IV. 2 Clypeastroida. Clypeastridae, Arachnoididae, Fibulariidae, Laganidae and Scutellidae. Copenhagen: C.A. Reitzel. 471 pp.

    Google Scholar 

  • Phelan, T. F. (1977). Comments on the water vascular system, food grooves, and ancestry of the clypeasteroid echinoids. Bulletin of Marine Science, 27, 400–422.

    Google Scholar 

  • Reisman, A.W. (1965). The histology and anatomy of the intestinal tract of Dendraster excentricus, a clypeasteroid echinoid. M.A. thesis, University of California Los Angeles, 85 pp.

  • Schultz, H. (2005). Sea urchins—a guide to worldwide shallow water species. Hemdingen: Schultz Partner. 484 pp.

    Google Scholar 

  • Seilacher, A. (1979). Constructional morphology of sand dollars. Paleobiology, 5, 191–221.

    Google Scholar 

  • Stara, P., & Borghi, E. (2014). The echinoid genus Amphiope L. Agassiz, 1840 (Echinoidea Astriclypeidae) in the Oligo-Miocene of Sardinia (Italy). Biodiversity Journal, 5, 245–268.

    Google Scholar 

  • Stara, P., & Sanciu, L. (2014). Analysis of some astriclypeids (Echinoidea Clypeasteroida). Biodiversity Journal, 5, 291–358.

    Google Scholar 

  • Telford, M. (1988). Ontogenetic regulatory mechanisms and evolution of mellitid lunules (Echinoidea, Clypeasteroida). Paleobiology, 14, 52–63.

    Google Scholar 

  • Timko, P. L. (1976). Sand dollars as suspension feeders: a new description of feeding in Dendraster excentricus. Biological Bulletin, 151, 247–259.

    Article  Google Scholar 

  • Wagner, C.D. (1963) Revision of the echinoid family Mellitidae. M.A. thesis, University of California, 192 pp.

  • Zachos, L.G. (2006). Encope michelini, five-notched sand dollar. Digital Morphology, http://digimorph.org/specimens/Encope_michelini/NPL4110/. Accessed 4 Aug 2015.

  • Ziegler, A. (2012). Broad application of non-invasive imaging techniques to echinoids and other echinoderm taxa. Zoosymposia, 7, 53–70.

    Google Scholar 

  • Ziegler, A., & Mueller, S. (2011). Analysis of freshly fixed and museum invertebrate specimens using high-resolution, high-throughput MRI. Methods in Molecular Biology, 771, 633–651.

    Article  CAS  PubMed  Google Scholar 

  • Ziegler, A., Faber, C., Mueller, S., & Bartolomaeus, T. (2008). Systematic comparison and reconstruction of sea urchin (Echinoidea) internal anatomy: a novel approach using magnetic resonance imaging. BMC Biology, 6, 33.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ziegler, A., Mooi, R., Rolet, G., & De Ridder, C. (2010). Origin and evolutionary plasticity of the gastric caecum in sea urchins (Echinodermata: Echinoidea). BMC Evolutionary Biology, 10, 313.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ziegler, A., Mietchen, D., Faber, C., von Hausen, W., Schöbel, C., Sellerer, M., & Ziegler, A. (2011). Effectively incorporating selected multimedia content into medical publications. BMC Medicine, 9, 17.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ziegler, A., Faber, C., Mueller, S., Nagelmann, N., & Schröder, L. (2014a). A dataset comprising 141 magnetic resonance imaging scans of 98 extant sea urchin species. GigaScience, 3, 21.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ziegler, A., Faber, C., Mueller, S., Nagelmann, N., Schröder, L. (2014b). MRI scans of whole sea urchin specimens. GigaDB, doi: 10.5524/100124. Accessed 4 Aug 2015.

  • Ziegler, A., Lenihan, J., Zachos, L.G., Faber, C., Mooi, R. (2015). Comparative morphology and phylogenetic significance of Gregory’s diverticulum in sand dollars (Echinoidea: Clypeasteroida). MorphoBank, Project #2202, doi:10.7934/P2202. Accessed 4 Aug 2015.

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Acknowledgments

We would like to thank the following colleagues for providing access to museum specimens: Nadia Améziane (MNHN), Andrew Cabrinovic (BMNH), Jean DeMouthe (CASG), Mariko Kondo (MMBS), Kwen-Shen Lee (NMNS), Carsten Lüter (ZMB), Kelly Markello (CASIZ), Jørgen Olesen (ZMK), David L. Pawson (USNM), Chrissy Piotrowski (CASIZ), Bernhard Ruthensteiner (ZSM), Andreas Schmidt-Rhaesa (ZMH), and Robert M. Woollacott (MCZ). We are grateful to Felix Beckmann, Johannes Müller (ZMB), Nina Nagelmann, and Malte Ogurreck for their kind help with imaging equipment. Adam Baldinger (MCZ), Tom Schiøtte (ZMK), and Berit M. Ullrich provided valuable assistance with specimen handling and shipment. Constructive comments and suggestions by Andreas Kroh and one anonymous reviewer helped to improve the text. We are furthermore indebted to Gonzalo Giribet (MCZ) and Andreas Ziegler for facilitating access to scanning systems.

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Authors and Affiliations

  1. Institut für Zoologie, Rheinische Friedrich-Wilhelms-Universität Bonn, Meckenheimer Allee 169, 53115, Bonn, Germany

    Alexander Ziegler

  2. Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138, USA

    Jennifer Lenihan

  3. Department of Geology and Geological Engineering, University of Mississippi, 120 Carrier Hall, Oxford, MS, 38677, USA

    Louis G. Zachos

  4. Institut für Klinische Radiologie, Westfälische Wilhelms-Universität Münster, Albert-Schweitzer-Campus 1, 48149, Münster, Germany

    Cornelius Faber

  5. California Academy of Sciences, Golden Gate Park, 55 Music Concourse Drive, San Francisco, CA, 94118, USA

    Rich Mooi

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  1. Alexander Ziegler
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Correspondence to Alexander Ziegler.

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Ziegler, A., Lenihan, J., Zachos, L.G. et al. Comparative morphology and phylogenetic significance of Gregory’s diverticulum in sand dollars (Echinoidea: Clypeasteroida). Org Divers Evol 16, 141–166 (2016). https://doi.org/10.1007/s13127-015-0231-9

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