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Constructional morphology, origin, and evolution of the gastropod operculum

Published online by Cambridge University Press:  08 February 2016

Antonio G. Checa  and
Antonio P. Jiménez-Jiménez
Antonio G. Checa
Affiliation:
Departamento de Estratigrafía y Paleontología, Facultad de Ciencias, Universidad de Granada, Avenida Fuentenueva S/N, 18071 Granada, Spain. E-mail: acheca@goliat.ugr.es
Antonio P. Jiménez-Jiménez
Affiliation:
Departamento de Estratigrafía y Paleontología, Facultad de Ciencias, Universidad de Granada, Avenida Fuentenueva S/N, 18071 Granada, Spain. E-mail: apablojj@goliat.ugr.es
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Abstract

Gastropod opercula are classified here on a new morphogenetic basis, which distinguishes three main types: (1) flexiclaudent spiral (mostly multispiral) operculum, the shape of which does not coincide with that of the aperture, (2) rigiclaudent spiral (usually paucispiral) operculum, the shape of which fits that of the aperture, and (3) rigiclaudent concentric operculum, also aperture-fitting. The first type fits by flexing into the aperture and is secreted when the soft parts are partly or wholly extended (i.e., when the operculum is not in a closed position). The other two types do not flex upon retraction (except at the very margin) and grow when the operculum closes over the aperture, with or without rotation. A study of opercular types at the family level confirms the systematic and evolutionary significance of opercula. Types 1 and 2 are the only ones present in archaeogastropods, Type 1 being predominant. Opercula (if present) in Neritopsina are always rigiclaudent. Within Caenogastropoda, Type 2 predominates; the only flexiclaudent spiral opercula are found in certain basal cerithioidean families. Concentric opercula are predominant in higher neotaenioglossans and exclusive in neogastropods. Except for one family, opercula in Heterostropha are always rigiclaudent spiral. Morphological, systematic, and histological criteria point to the flexiclaudent spiral operculum as the ancestral form. This leads us to propose the “periostracum shaving” model in prosobranchs to account for the origin of this kind of operculum. According to this model, in the earliest trochospiral gastropods the periostracum ceased to serve a shell-formation function at the band of overlap between whorls (the parietal band). The periostracal band was then extruded from the shell to constitute an incipient operculum, taking on the appearance of a spiral strip coiling opposite to the shell. The parietal segment of the periostracal groove migrated toward the epipodium and became independent from the rest of the mantle. The concomitant development of an opercular disc allowed the successive turns of periostracal strip to seal together. In this way, a spiral operculum emerged, coiling counterclockwise without matching the aperture shape. During the course of prosobranch evolution, rigiclaudent spiral opercula emerged several times from the ancestral flexiclaudent type, although they were always restricted to apertures with a spiral-shaped outer (labral) edge. Such opercula enlarged the range of shell morphologies for which the operculum constituted an efficient protective barrier to include those of neritoidean or naticoidean type. The onset of calcification in opercula took place with the rigiclaudent type. Concentric opercula also evolved independently from rigiclaudent spiral opercula in several gastropod groups, thus further broadening the spectrum of apertures and, hence, of shell morphologies using opercula for protection. From the standpoint of adaptation, the concentric type was probably the only one available to neogastropods having long and wide siphonal canals.

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Paleobiology , Volume 24 , Issue 1 , Winter 1998 , pp. 109 - 132
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Copyright © The Paleontological Society 

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References

Literature Cited

Adanson, M. 1757. Histoire naturelle du Sénégal (Coquillages). Avec la relation abrégée d'un voyage fait en ce pays pendant les années 1749–53. Bauche, Paris.Google Scholar
Angerer, G., and Haszprunar, G. 1996. Anatomy and affinities of lepetid limpets (Patellogastropoda ‘ Docoglossa). Pp. 171–175in Taylor, 1996.Google Scholar
Bandel, K. 1988. Operculum and buccal mass of ammonites. Pp. 653–687in Wiedmann, J. and Kullmann, J., eds. Cephalopods—present and past. Schweizerbart'sche, Stuttgart.Google Scholar
Bandel, K. 1990. Shell structure of the Gastropoda excluding Archaeogastropoda. Pp. 117–134in Carter, J. G., ed. Skeletal biomineralization: patterns, processes and evolutionary trends, Volume I. Van Nostrand Reinhold, New York.Google Scholar
Bandel, K. 1991. Character of a microgastropod fauna from a carbonate sand of Cebu (Philippines). Mittheilungen der Geologisch-Paläontologisches Institut der Universität Hamburg 71:441–485.Google Scholar
Bandel, K., and Riedel, F. 1994. Classification of fossil and Recent Calyptraeoidea (Caenogastropoda) with a discussion on neomesogastropod phylogeny. Berliner Geowissenschaften Abhandlungen (E) 13:329–367.Google Scholar
Bieler, R. 1992. Gastropod phylogeny and systematics. Annual Review of Ecology and Systematics 23:311–338.CrossRefGoogle Scholar
Buck, L. 1991. Observations of Cancellaria cooperi Gabb, 1865, parasitizing two species of invertebrates. Festivus 23:69–70.Google Scholar
Chétail, M., and Krampitz, G. 1982. Calcium and skeletal structures in molluscs: concluding remarks. Malacologia 22:337–339.Google Scholar
Fleischmann, A. 1932. Vergleichende Betrachtungen über das Schalenwachstum der Weichtiere (Mollusca). II. Deckel (Operculum) und Haus (Concha) der Schnecken (Gastropoden). Zeitschrift für Morphologie und Ökologie der Tiere 25:549–622.CrossRefGoogle Scholar
Forney, G. G., Boucot, A. J., and Rohr, D. M. 1981. Silurian and Lower Devonian zoogeography of selected molluscan genera. Pp. 119.164. in Gray, J., Boucot, A. J., and Berry, W. B. N., eds. Communities of the past. Hutchinson Ross, Stroudsburg, Penn.Google Scholar
Fretter, V., and Graham, A. 1962. British prosobranch mollucs, their function, anatomy and ecology. The Ray Society, London.Google Scholar
Gordon, M. Jr., and Yochelson, E. L. 1982a. A Naticopsis operculum found in situ (Gastropoda: Mississippian). Journal of Paleontology 56:260–265.Google Scholar
Gordon, M. Jr., and Yochelson, E. L. 1982b. Aptychus solidum is a Mississippian Naticopsis (Gastropoda) operculum. Journal of Paleontology 56:215–220.Google Scholar
Graham, A. 1985. Evolution within the Gastropoda: Prosobranchia. Pp. 151–186in Trueman, E. R. and Clarke, M. R., eds. The Mollusca, Volume 10. Evolution. Academic Press, London.Google Scholar
Grasset, M., and Vovelle, J. 1982. Données histochimiques et ultrastructurales sur l'opercule de Buccinum undatum (L.) (Mollusca, Gastropoda). Malacologia 22:251–255.Google Scholar
Gubanov, A. P., and Yochelson, E. L. 1994. A Wenlockian (Silurian) gastropod shell and operculum from Siberia. Journal of Paleontology 68:486–491.CrossRefGoogle Scholar
Haszprunar, G. 1988a. A preliminary phylogenetic analysis of the streptoneurous gastropods. Malacological Review, Supplement 4:7–16.Google Scholar
Haszprunar, G. 1988b. Comparative anatomy of cocculiniform gastropods and its bearing on archaeogastropod systematics. Malacological Review, Supplement 4:64–84.Google Scholar
Haszprunar, G. 1988c. On the origin and evolution of major gastropod groups, with especial reference to the streptoneura. Journal of Molluscan Studies 54:367–441.CrossRefGoogle Scholar
Haszprunar, G. 1993. The Archaeogastropoda. A clade, a grade or what else?. American Malacological Bulletin 10:165–177.Google Scholar
Healy, J. M. 1988. Sperm morphology and its systematic importance in the Gastropoda. Malacological Review, Supplement 4:251–266.Google Scholar
Healy, J. M. 1996. Molluscan sperm ultrastructure: correlation with taxonomic units within the Gastropoda, Cephalopoda and Bivalvia. Pp. 99–113in Taylor, 1996.Google Scholar
Hickman, C. S., and McLean, J. H. 1990. Systematic revision and suprageneric classification of trochacean gastropods. Science Series No. 35, Natural History Museum of Los Angeles County.Google Scholar
Houbrick, R.S. 1988. Cerithioidean phylogeny. Malacological Review, Supplement 4:88–128.Google Scholar
Houbrick, R.S. 1990. Aspects of the anatomy of Plesiotrochus (Plesiotrochidae, fam. n.) and its systematic position in Cerithioidea (Prosobranchia, Gastropoda). Pp. 237–250in Wells, F. C., Walker, D. I., Hirckman, N., and Lethbridge, R., eds. The marine fauna and flora of Albany, Western Australia. Western Australian Museum Publications, Perth.Google Scholar
Houssay, F. 1884. Recherches sur l'opercule et les glandes du pied des gastéropodes. Archives de Zoologie expérimentale et générale 2:171–288.Google Scholar
Hubendick, B. 1948. Über den Bau und das Wachstum des konzentrischen Operculartypus bei Gastropoden. Arkiv för Zoologi 40A 10:1–28.Google Scholar
Hunt, S. 1976. The gastropod operculum: a comparative study of the composition of gastropod opercular proteins. Journal of Molluscan Studies 42:251–260.Google Scholar
Kantor, Y. I. 1996. Phylogeny and relationships of Neogastropoda. Pp. 221–230in Taylor, 1996.Google Scholar
Kessel, E. 1942. Über Bau und Bildung des Prosobranchier-Deckels. Zeitschrift für Morphologie und Ökologie der Tiere 38:197–250.CrossRefGoogle Scholar
Knight, J. B., Cox, L. R., Keen, A. M., Batten, R. L., Yochelson, E. L., and Robertson, R. 1960. Gastropoda. Systematic descriptions. Pp. I169–I310in Knight, J. B., Cox, L. R., Keen, A. M., Smith, A. G., Batten, R. L., Yochelson, E. L., Ludbrook, N. H., Robertson, R., Yonge, C. M., and Moore, R. C., eds. Mollusca 1. Part I ofMoore, R. C., ed. Treatise on invertebrate paleontology. Geological Society of America and University of Kansas, New York.Google Scholar
Lindberg, D. R. 1988. The Patellogastropoda. Malacological Review, Supplement 4:35–63.Google Scholar
Linsley, R. M., Mapes, R. H., Hui-Ji, W., and Yochelson, E. L. 1989. Some new Paleozoic gastropod opercula (Pennsylvanian: Texas). Journal of Paleontology 63:206–211.CrossRefGoogle Scholar
Maschino, F., and Vovelle, J. 1972. Comparaison du bourrelet palleal posterieur et du disque operculigère chez Ocinebra erinacea L., gastropode prosobranche. Haliotis 2:187–190.Google Scholar
McLean, L. H. 1989. New archaeogastropod limpets from hydrothermal vents: new family Peltospiridae, new superfamily Peltospiracea. Zoologica Scripta 18:49–66.CrossRefGoogle Scholar
McLean, L. H. 1990a. A new genus and species of neomphalid limpet from the Mariana vents with a review of current understanding of relationships among Neomphalacea and Peltospiracea. The Nautilus 104:77–86.Google Scholar
McLean, L. H. 1990b. Neolepetopsidae, a new decoglossate limpet family from hydrothermal vents and its relevance to patellogastropod evolution. Journal of Zoology 222:485–528.CrossRefGoogle Scholar
Measures, E. A., Rohr, D. M., and Blodgett, R. B. 1991. Depositional environments and some aspects of the fauna of Middle Ordovician rocks of the Teltsina Formation, Northern Kuskokwim Mountains, Alaska. U.S. Geological Survey Bulletin 2041:186–201.Google Scholar
Mikkelsen, P. M. 1996. The evolutionary relationships of Cephalaspidea s.l. (Gastropoda: Opisthobranchia): a phylogenetic analysis. Malacologia 37:375–442.Google Scholar
Nordsieck, H. 1981. Die Evolution des Verschlußapparats der Schließmundsnecken (Gastropoda, Clausiliiidae). Archiv für Molluskenkunde 112:27–43.Google Scholar
Ponder, W. F. 1988. The truncatelloidean (‘ Rissoacean) radiation—a preliminary phylogeny. Malacological Review, Supplement 4:129–164.Google Scholar
Ponder, W. F., and Lindberg, D. R. 1996. Gastropod phylogeny—challenges for the 90s. Pp. 135–154in Taylor, 1996.Google Scholar
Ponder, W. F., and Lindberg, D. R. 1997. Towards a phylogeny of gastropod molluscs: an analysis using morphological characters. Zoological Journal of the Linnean Society 119:83–265.CrossRefGoogle Scholar
Ponder, W. F., and Warén, A. 1988. Classification of the Caenogastropoda and Heterostropha—a list of the family-group names and higher taxa. Malacological Review, Supplement 4:288–326.Google Scholar
Pruvot-Fol, A. 1954. Le bulbe buccal et la symétrie des mollusques. II. Archives de Zoologie expérimentale et générale 91:235–330.Google Scholar
Quinn, J. F. Jr., 1983. A revision of the Seguenziacea Verrill, 1884 (Gastropoda: Prosobranchia). I. Summary and evaluation of the superfamily. Proceedings of the Biological Society of Washington 96:725–757.Google Scholar
Quinn, J. F. Jr., 1991. Systematic position of Basilissopsis and Guttula, and a discussion of the phylogeny of the Seguenzioidea (Gastropoda: Prosobranchia). Bulletin of Marine Science 49:575–598.Google Scholar
Raup, D. M., and Grauss, R. R. 1972. General equations for volume and surface area of a logarithmically coiled shell. Mathematical Geology 4:307–316.CrossRefGoogle Scholar
Riedel, F. 1994. Recognition of the superfamily Ficoidea MEEK 1864 and definition of the Thalassocynidae fam. nov. (Gastropoda). Zoologische Jahrbücher 121:457–474.Google Scholar
Rohr, D. M. 1979. Geographic distribution of the Ordovician gastropod Maclurites. Pp. 45–52in Gray, J. and Boucot, A. J., eds. Historical biogeography, plate tectonics and the changing environment. Oregon State University Press, Corvallis.Google Scholar
Rohr, D. M. 1988. Upper Ordovician gastropods from the Seward Peninsula, Alaska. Journal of Paleontology 62:551–566.Google Scholar
Rohr, D. M. 1994. Ordovician (Whiterockian) gastropods of Nevada: Bellerophontoidea, Macluritoidea, and Euomphaloidea. Journal of Paleontology 68:473–486.CrossRefGoogle Scholar
Rohr, D. M., and Boucot, A. J. 1985. Observations on the operculum of Oriostoma (Silurian Gastropoda). Canadian Journal of Earth Sciences 22:294–296.CrossRefGoogle Scholar
Rohr, D. M., Dutro, J. T. Jr., and Blodgett, R. B. 1992. Gastropods and brachiopods from the Ordovician Telsitna Formation, northern Kuskokwim Mountains, west-central Alaska. Pp. 499–512in Webby, B. D. and Laurie, J. R., eds. Global perspectives in Ordovician geology. Balkema, Rotterdam.Google Scholar
Runnegar, B. 1981. Muscle scars, shell form and torsion in Cambrian and Ordovician univalved molluscs. Lethaia 14:311–322.CrossRefGoogle Scholar
Runnegar, B. 1983. Molluscan phylogeny revisited. Memoirs of the Association of Australasian Paleontologists 1:121–144.Google Scholar
Runnegar, B. 1996. Early evolution of the Molusca: the fossil record. Pp. 77–87in Taylor, 1996.Google Scholar
Runnegar, B., and Pojeta, J. Jr. 1985. Origin and diversification of the Mollusca. Pp. 1–57in Trueman, E. R. and Clarke, M. R., eds. The Mollusca, Volume 10. Evolution. Academic Press, London.Google Scholar
Salvini-Plawen, L. von., and Haszprunar, G. 1987. The Vetigastropoda and the systematics of the streptoneurous Gastropoda (Mollusca). Journal of the Zoological Society of London 211:747–770.CrossRefGoogle Scholar
Salvini-Plawen, L. von., and Steiner, G. 1996. Synapomorphies and plesiomorphies in higher classification of Mollusca. Pp. 29–51in Taylor, 1996.Google Scholar
Savazzi, E. 1990. Biological aspects of theoretical shell morphology. Lethaia 23:195–212.CrossRefGoogle Scholar
Savazzi, E. 1991. Constructional morphology of strombid gastropods. Lethaia 24:311–331.CrossRefGoogle Scholar
Seapy, R. R. 1990. The pelagic family Atlantidae (Gastropoda: Heteropoda) from Hawaiian waters: a faunistic survey. Malacologia 32:107–130.Google Scholar
Seilacher, A. 1973. Fabricational noise in adaptive morphology. Systematic Zoology 22:451–465.CrossRefGoogle Scholar
Seilacher, A. 1993. Ammonite aptychi: how to transform a jaw into an operculum. American Journal of Science 293A:20–32.CrossRefGoogle Scholar
Stanley, S. M. 1982. Gastropod Torsion: predation and the opercular imperative. Neues Jahrbuch für Geologie und Paläontologie Abhandlungen 164:95–107.CrossRefGoogle Scholar
Taki, I. 1950. Morphological observations on the gastropod operculum. Venus 16:32–48.Google Scholar
Taylor, J. D. 1996. Origin and evolutionary radiation of the Mollusca. Oxford University Press, Oxford.Google Scholar
Taylor, J. D., and Morris, N. J. 1988. Relationships of neogastropods. Malacological Review, Supplement 4:167–179.Google Scholar
Taylor, J. D., Morris, N. J., and Taylor, C. N. 1980. Food especialization and the evolution of predatory prosobranch gastropods. Palaeontology 23:375–409.Google Scholar
Taylor, J. D., Kantor, Y. I., and Sisoev, A. V. 1993. Foregut anatomy, feeding mechanisms, relationships and classification of the Conoidea (‘ Toxoglossa) (Gastropoda). Bulletin of the Natural History Museum, London (Zoology) 59:125–170.Google Scholar
Tillier, S., Masselot, M., and Tillier, A. 1996. Phylogenetic relationships of the pulmonate gastropods from rRNA sequences, and tempo and age of the stylommatophoran radiation. Pp. 267–284in Taylor, 1996.Google Scholar
Tracey, S., Todd, J. A., and Erwin, D. H. 1993. Mollusca: Gastropods. Pp. 131–167in Benton, M. J., ed. The Fossil Record 2. Chapman and Hall, London.Google Scholar
Tyler, J. H. 1965. Gastropods from the Middle Devonian Four Mile Limestone (Hamilton) of Michigan. Journal of Paleontology 39:341–349.Google Scholar
Vaught, K. C. 1989. A classification of the living Mollusca. American Malacologists Inc., Melbourne, Fla.Google Scholar
Vermeij, G. J. 1987. Evolution and scalation. An ecological history of life. Princeton University Press, Princeton, N.J..CrossRefGoogle Scholar
Vovelle, J. 1967. Sur l'opercule de Gibbula magus (L.). Gastéropode Prosobranche: édification, nature protéique et durcissement par tannage quinonique. Comptes Rendues de l'Académie des Sciences de Paris 264:141–144.Google Scholar
Vovelle, J. 1969a. Complexity of the opercular material in Astralium rugosum (L.). (Gastropoda, Prosobranchia). Proceedings of the Malacological Society of London 38:557.Google Scholar
Vovelle, J. 1969b. Elaboration de la matière operculaire chez Tricolia pullus (L.), Gastropoda, Prosobranchia. Malacologia 9:293–294.Google Scholar
Vovelle, J. 1971. Étude embryologique, histologique et histochimique comparée de l'opercule chez Neptunea antiqua, Buccinum undatum et Nucella lapillus. Haliotis 1:5–6.Google Scholar
Vovelle, J. 1972. Sclérotisation et minéralisation des structures squelettiques chez les Mollusques. Haliotis 2:133–165.Google Scholar
Vovelle, J. 1973. Transfert du calcium à travers l'épithelium de repli operculaire chez Astraea rugosa L. (Turbinidae). Malacologia 14:47–51.Google Scholar
Vovelle, J., and Grasset, M. 1979. Approche histophysiologyque et cytologyque du rôle des cellules à sphérules calciques du repli operculaire chez Pomatias elegans (Müller), gastéropode prosobranche. Malacologia 18:557–560.Google Scholar
Vovelle, J., and Grasset, M. 1982. Étude cytologique et histochimique comparée de la formation de l'opercule corne chez les prosobranches. Malacologia 22:257–263.Google Scholar
Vovelle, J., Grasset, M., and Meunier, F. 1977. Elaboration de l'opercule calcifié chez Nerita plicata Linnaeus et Pomatias elegans (Müller), gastéropodes prosobranches. Malacologia 16:279–283.Google Scholar
Wagner, P. J.In press. Phylogenetics of the earliest gastropods. Smithsonian Contributions to Paleobiology. Washington, D.C.Google Scholar
Warén, A. and Bouchet, P. 1990. Laubierinidae and Pisaniurinae (Ranellidae), two new deep-sea taxa of the Tonnoidea (Gastropoda: Prosobranchia). The Veliger 33: 56:102.Google Scholar
Warén, A., Gofas, S., and Schander, C. 1993. Systematic position of three European heterobranch gastropods. The Veliger 36:1–15.Google Scholar
Wye, K. R. 1991. The illustrated encyclopaedia of shells. Headline, London.Google Scholar
Yochelson, E. L. 1966. An operculum associated with the Ordovician gastropod Helicotoma. Journal of Paleontology 40:748–749.Google Scholar
Yochelson, E. L. 1975. Early Ordovician gastropod opercula and epicontinental seas. Journal of Research of the U.S. Geological Survey 3:447–450.Google Scholar
Yochelson, E. L. 1979. Gastropod opercula as objects for paleobiogeographic study. Pp. 37–43in Gray, J. and Boucot, A. J., eds. Historical biogeography, plate tectonics and the changing environment. Oregon State University Press, Corvallis.Google Scholar
Yochelson, E. L. 1986. Operculum of the early Middle Ordovician gastropod Palliseria robusta Wilson. Journal of Paleontology 60:656–660.CrossRefGoogle Scholar
Yochelson, E. L. 1990. Billing's second operculum: a late Early Ordovician Maclurites (Gastropoda) from Western Newfoundland and the Canadian Arctic. Canadian Journal of Earth Sciences 27:669–676.CrossRefGoogle Scholar
Yochelson, E. L. 1992. The late Early Ordovician gastropod Teiichispira at Port au Port, Newfoundland. Canadian Journal of Earth Sciences 29:1334–1341.CrossRefGoogle Scholar
Yochelson, E. L., and Barnett, S. G. 1972. The Early Ordovician gastropod Ceratopea in the Plattsburg, New York, area. Journal of Paleontology 46:685–687.Google Scholar
Yochelson, E. L., and Copeland, M. J. 1974. Taphonomy and taxonomy of the Early Ordovician gastropod Ceratopea canadensis (Billings), 1865. Canadian Journal of Earth Sciences 11:189–207.CrossRefGoogle Scholar
Yochelson, E. L., and Linsley, R. M. 1972. Opercula of two gastropods from the Lylidale Limestone (Early Devonian) of Victoria, Australia. Memoirs of the National Museum of Victoria 33:1–13.CrossRefGoogle Scholar
Yochelson, E. L., and Wise, O. A. 1972. A life association of shell and operculum in the Early Ordovician gastropod Ceratopea unguis. Journal of Paleontology 46:681–684.Google Scholar