Hostname: page-component-5c6d5d7d68-7tdvq Total loading time: 0 Render date: 2024-08-08T12:12:47.843Z Has data issue: false hasContentIssue false
  • English
  • Français

A biomechanical model for the morphogenesis of regular echinoid tests

Published online by Cambridge University Press:  08 April 2016

Jacob Dafni
Jacob Dafni*
Affiliation:
Interuniversity Institute of Eilat, H. Steinitz Marine Biology Laboratory, P.O. Box 469, Eilat, 88103 Israel
Get access Rights & Permissions [Opens in a new window]

Abstract

Experiments were conducted to test the hypothesis that biomechanical constraints determine the morphology of regular echinoids. Hard-bottom-dwelling Tripneustes gratilla elatensis were transferred to an artifical sandy habitat to evaluate whether the change in substrate affects their height to diameter ratio (H/D). Within 1–2 months their H/D ratio increased significantly. This change was shown to be reversible to some extent. Surgical damage to the ambulacral system of one ray caused inactivation of tubefeet and atrophy of injured ambulacra. Test shape was also affected: the damaged ray was lower, and the nondamaged ambulacra deflected toward the treated one, producing bilateral symmetry as in recorded cases of teratology. Study of T. g. elatensis tetramers showed that while “perfect” tetramery was apparently associated with genetic aberration, “imperfect” tetramery results from mechanical injury at an early ontogenetic stage. Micromorphological study shows that in the longitudinal sutures, normally under tension, long and slender trabeculae develop, associated with long and well-aligned collagenous sutural fibers, while the latitudinal trabeculae and fibers are short and less organized. A mechanical effect is suggested by the oval cross-section of the fiber-anchoring trabeculae. Further, echinoid plates interact like soap bubbles, whereas the entire test behaves like a balloon, fastened to the substrate by the ambulacral tubefeet. All these observations support earlier hypotheses on the biomechanical control of echinoid test growth. A model is proposed in which the expansion of the inner mass, counteracted by the mechanical activity of the ambulacral tubefeet, mesenterial threads, and lantern muscles, affects sutural growth, thus controlling echinoid morphogenesis.

A morphometric survey among regular echinoids reveals an inverse relationship between ambulacral width and relative ambital height. Although both increase of ambulacral width and lowering of ambitus-line are evolutionary trends, it is suggested that they are a response to a mechanical effect. H/D ratio was not related to ambulacral width on the phylogenetic level. It is therefore suggested that the latter correlation is ontogenetically controlled. Aspects of irregular echonoid evolution, such as bilateral symmetry, flattening, and formation of the ambulacral petaloid, also are explained by this model.

Type
Articles
Information
Paleobiology , Volume 12 , Issue 2 , Spring 1986 , pp. 143 - 160
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Benson, R. H. 1975. Morphological stability in Ostracods. Bull. Am. Paleontol. 65:13–46.Google Scholar
Bonner, J. T., ed. 1961. On growth and form, by D. W. Thompson. Cambridge Univ. Press; Cambridge.Google Scholar
Buchanan, J. B. 1969. Feeding and control of volume within the test of regular sea urchins. J. Zool. Lond. 159:51–64.Google Scholar
Chapman, G. 1958. The hydrostatic skeleton in the invertebrates. Biol. Rev. Cambridge Phil. Soc. 33:338–364.Google Scholar
Culling, C. F. A. 1974. Handbook of histopathological and histochemical techniques. 3d ed.Butterworths; London.Google Scholar
Cuénot, L. 1948. Echinodermata. Pp. 1–363. In: Grassé, P. P., ed. Traité de Zoologie XI. Masson; Paris.Google Scholar
Currey, J. D. 1975. A comparison of the strength of echinoderm spines and mollusc shells. J. Mar. Biol. Ass. UK. 55:419–424.CrossRefGoogle Scholar
Dafni, J. 1980. Abnormal growth patterns in the sea urchin Tripneustes cf. gratilla (L.) under pollution (Echinodermata: Echinoidea). J. Exp. Mar. Biol. Ecol. 47:259–279.Google Scholar
Dafni, J. 1983a. A new sub-species of Tripneustes gratilla (L.) from the northern Red Sea (Echinodermata: Echinoidea: Toxopneustidae). Isr. J. Zool. 32:1–12.Google Scholar
Dafni, J. 1983b. Aboral depressions in the tests of the sea urchin Tripneustes cf. gratilla (L.) in the Gulf of Eilat, Red Sea. J. Exp. Mar. Biol. Ecol. 67:1–15.Google Scholar
Dafni, J. 1985. Effect of mechanical stress on the calcification pattern in regular echinoid skeletal plates. Pp. 233–236. In: Keegan, B. F. and O'Connor, B. D. S., ed. Echinodermata: Proc. 5th Int. Echinoderm Conf. Galway, September 1984.Google Scholar
Dafni, J. and Erez, J. 1982. Differential growth in Tripneustes gratilla (Echinoidea). Pp. 71–75. In: Lawrence, J. M., ed. Echinoderms: Proc. Int. Conf. Tampa Bay, September 1981.Google Scholar
Dafni, J. and Erez, J. In prep. Skeletal calcification patterns in the sea urchin Tripneustes gratilla elatensis.Google Scholar
Deutler, F. 1926. Über das Wachstum des Seeigelskeletts. Zool. Jb. (Anat.). 48:119–200.Google Scholar
Ebert, T. A. 1982. Longevity, life history, and relative body wall size in sea urchins. Ecol. Monogr. 52:353–394.Google Scholar
Emlet, R. B. 1982. Echinoderm calcite: a mechanical analysis from larval spicules. Biol. Bull. 163:264–275.CrossRefGoogle Scholar
Ernst, G. 1973. Aktuopaläontologie und Merkmalsvariabilität bei mediterranen Echiniden und Rückschlusse auf die Ökologie und Artumgrenzung fossiler Formen. Paläontol. Z. 47:188–216.Google Scholar
Ettershank, G. and Ghent, R. L. 1972. Insecta. Pp. 552–613. In: Marshall, A. J. and Williams, W. D., eds. Textbook of Zoology: Invertebrates. MacMillan; London.Google Scholar
Giese, A. C. 1966. On the biochemical constitution of some echinoderms. Pp. 757–796. In: Boolootian, R.A., ed. Physiology of Echinodermata. Interscience; New York.Google Scholar
Gordon, I. 1926. The development of the calcareous test of Echinocardium cordatum. Phil. Trans. 215B:255–313.Google Scholar
Gutmann, W. F. 1977. Phylogenetic reconstruction, theory, methodology and application to chordate evolution. In: Hecht, M. K., Goody, P. C., and Hecht, B. M., eds. Major patterns in vertebrate evolution. Nato Adv. Stud. Inst. 14A:645–669.Google Scholar
Hyman, L. H. 1955. The Invertebrates. Vol. 4. Echinodermata, the Coelomate Bilateria. 763 pp. McGraw-Hill; New York.Google Scholar
Jackson, R. T. 1927. Studies of Arbacia punctulata and allies and of non-pentamerous echinids. Mem. Boston Soc. Nat. Hist. 8:435–565.Google Scholar
Jensen, M. 1972. The ultrastructure of the echinoid skeleton. Sarsia. 48:39–48.Google Scholar
Kier, P. M. 1982. Rapid evolution in echinoids. Palaeontology. 25:1–10.Google Scholar
Kobayashi, S. and Taki, J. 1969. Calcification in the sea urchins. 1. A tetracyclin investigation of growth of the mature test in Strongylocentrotus intermedius. Calc. Tiss. Res. 4:210–223.Google Scholar
Koehler, R. 1924. Anomalies, irregularités et déformations au test chez les echinids. Ann. Inst. Oceanogr. Monaco, N.S. 1:159–480.Google Scholar
Lissner, A. L. 1983. Relationship of water motion to shallow water distribution and morphology of two species of sea urchins. J. Mar. Res. 41:691–709.Google Scholar
Märkel, K. 1975. Wachstum des Coronar skelettes von Paracentrotus lividus Lmk. Zoomorphologie. 82:259–280.Google Scholar
Märkel, K. 1976. Struktur und Wachstum des Coronarskelettes von Arbacia lixula Linne (Echinodermata: Echinoidea). Zoomorphologie. 84:279–299.Google Scholar
Märkel, K. 1981. Experimental morphology of coronar growth in regular echinoids. Zoomorphology. 97:31–52.Google Scholar
McPherson, B. P. 1965. Contribution to the biology of the sea urchin Tripneustes ventricosus. Bull. Mar. Sci. 15:228–244.Google Scholar
Moore, H. B. 1935. A comparative study of the biology of Echinus esculentus in different habitats. II. J. Mar. Biol. Ass. U.K. 20:109–128.Google Scholar
Moore, H. B. 1974. Irregularities in the test of regular sea urchins. Bull. Mar. Sci. 24:545–560.Google Scholar
Moore, R. C., ed. 1966. Treatise on Invertebrate Paleontology. Pt. U. Echinodermata. 695 pp. Geol. Soc. Am. and Univ. Kansas Press.Google Scholar
Mortensen, T. 1928. A monograph of the Echinoidea. 1. Cidaroidea. 551 pp. C.A. Reitzel; Copenhagen.Google Scholar
Mortensen, T. 1935. A monograph of the Echinoidea. 2. Stirodonta. 647 pp. C.A. Reitzel; Copenhagen.Google Scholar
Mortensen, T. 1940. A monograph of the Echinoidea. 3(1). Aulodonta. 370 pp. C.A. Reitzel; Copenhagen.Google Scholar
Mortensen, T. 1943a. A monograph of the Echinoidea. 3(2). Camarodonta. 533 pp. C.A. Reitzel; Copenhagen.Google Scholar
Mortensen, T. 1943b. A monograph of the Echinoidea. 3(3). Camarodonta. 446 pp. C.A. Reitzel; Copenhagen.Google Scholar
Moss, M. L. and Meehan, M. 1967. Sutural connective tissues in the test of an echinoid. Arbacia punctulata. Acta Anat. 66:279–304.Google Scholar
Moss, M. L. and Meehan, M. 1968. Growth of the echinoid test. Acta Anat. 69:409–444.Google Scholar
Motokawa, T. 1983. Mechanical properties and structure of the spine-joint central ligament of the sea urchin, Diadema setosum (Echinodermata, Echinoidea). J. Zool. Lond. 201:223–235.Google Scholar
Nichols, D. and Currey, J. D. 1968. The secretion structure and strength of echinoderm calcite. Pp. 251–261. In: McGee-Russell, S. M. and Ross, K. F. A., eds. Cell Structure and Its Interpretation: Essays Presented to J. R. Baker. Edward Arnold; London.Google Scholar
Otto, F. and Trostel, R. 1967. Tensile Structures. Vols. 1, 2. MIT Press; Cambridge, Mass.Google Scholar
Paine, V. L. 1926. Adhesion of the tube feet in starfish. J. Exp. Zool. 45:361–366.Google Scholar
Pearse, J. S. and Pearse, V. B. 1975. Growth zones in the echinoid skeleton. Am. Zool. 15:731–753.Google Scholar
Prosser, C. L. and Brown, F. A. 1961. Comparative Animal Physiology. 2d ed.Saunders: Philadelphia.Google Scholar
Raup, D. M. 1968. Theoretical morphology of echinoid growth. J. Paleontol. 42:50–63.CrossRefGoogle Scholar
Seilacher, A. 1979. Constructional morphology of sand dollars. Paleobiology, 5:191–221.Google Scholar
Seilacher, A. 1984. Constructional morphology of bivalves: evolutionary pathways in primary versus secondary soft-bottom dwellers. Palaeontology. 27:207–237.Google Scholar
Sharp, D. T. and Gray, I. E. 1962. Studies on factors affecting the local distribution of two sea urchins, Arbacia punctulata and Lytechinus variegatus. Ecology. 43:309–313.Google Scholar
Smith, A. B. 1978. A functional classification of the coronal pores of regular echinoids. Palaeontology. 21:759–790.Google Scholar
Smith, A. B. 1980. Stereom microstructure of the echinoid test. Spec. pap. Palaeontol. Palaeontol. Assoc. Lond. 25:1–81.Google Scholar
Smith, A. B. 1984. Echinoid Palaeontology. 190 pp. Allen & Unwin; London.Google Scholar
Sokal, R. R. and Rohlf, F. J. 1969. Biometry. 776 pp. W. H. Freeman; San Francisco.Google Scholar
Stevens, P. S. 1976. Patterns in Nature. 240 pp. Penguin; Middlesex.Google Scholar
Strathmann, R. R. 1981. The role of spines in preventing structural damage to echinoid tests. Paleobiology. 7:400–406.Google Scholar
Telford, M. 1985. Domes, arches and urchins: the skeletal architecture of echinoids (Echinodermata). Zoomorphology. 105:114–124.Google Scholar
Thompson, D. W. 1917. On Growth and Form. 1st ed.794 pp. Cambridge Univ. Press; Cambridge.CrossRefGoogle Scholar
Thompson, D. W. 1942. On Growth and Form. 2d ed.1116 pp. Cambridge Univ. Press; Cambridge.Google Scholar
Wainwright, S. A., Biggs, W. D., Currey, J. D., and Gosline, J. M. 1976. Mechanical Design in Organisms. Edward Arnold; London.Google Scholar
Weber, E. 1972. Grundriss der Biologischer Statistik. 706 pp. Fischer Verlag; Stuttgart.Google Scholar
Wilkie, I. C. 1984. Variable tensility in echinoderm collagenous tissues: a review. Mar. Behav. Physiol. 11:1–34.Google Scholar