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Keywords:

  • Polychaeta;
  • Sabellidae;
  • Glomerula;
  • Calcisabella;
  • tube ultrastructure;
  • biomineralization

Abstract

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Tube ultrastructure in fossil and recent sabellids
  5. Origin of calcification in sabellidae
  6. Comparison of Glomerula with the other annelid tubes
  7. Acknowledgments
  8. References

Abstract:  Tube ultrastructure of Jurassic and Cretaceous Glomerula is very similar to that of Recent Calcisabella, supporting the synonymy of these genera and the early Mesozoic origin of calcification in sabellids. Tube structure of serpulids differs from that of Glomerula; calcareous tubes probably evolved convergently within Sabellida. The tube wall in Recent Glomerula piloseta is composed of subparallel lamellae of aragonitic, irregular spherulitic prisms in the inner layer, and spherulites in the outer layer. Calcified lamellae are separated by organic films of different thickness. The structure of the internal tube layer in Glomerula piloseta, and the structure of entire wall in fossil Glomerula, are similar to the tube structure of Dodecaceria (Polychaeta, Cirratulidae). The irregular spherulitic prisms of Glomerula are similar to those found in the external layer of Hydroides dianthus and the internal layer of Spiraserpula caribensis.

Within the Polychaeta, calcareous tubes are formed in all species of the family Serpulidae (Simkiss and Wilbur 1989). In addition, calcareous tubes also occur in a few species of Cirratulidae [Dodecaceria fistulicolaEhlers, 1901, D. fewkesiBerkeley and Berkeley, 1954 (Reish 1952; ten Hove and van den Hurk 1993), D. cf. coraliiLeidy, 1855 (Fischer et al. 2000)] and in one species of Recent Sabellidae, Glomerula piloseta (as Calcisabella: Perkins 1991; Jäger 2004). Tube structures in serpulids have been described by various authors (ten Hove and Zibrowius 1986; Zibrowius and ten Hove 1987; ten Hove and Smith 1990; Nishi 1993; Pillai and ten Hove 1994; Weedon 1994; Sanfilippo 1996, 1998) and tube formation has been investigated several times (e.g. Hedley 1958; Neff 1971; Vovelle et al. 1991), but very little has been known hitherto about calcareous sabellid tubes.

Jäger (2004, p. 127) synonymized CalcisabellaPerkins, 1991, in which the animal inhabiting the calcareous tube is clearly a sabellid, with the fossil genus GlomerulaBrünnich Nielsen, 1931 (after comparing paratypes of Recent C. piloseta with his ample fossil material of Glomerula) on the basis of the following morphological criteria pertaining to their tubes: rough surface, absence of chevron-shaped growth lamellae, irregularities in thickness of wall and diameter of lumen. As a consequence, he moved Glomerula from the Serpulidae to the Sabellidae.

The aim of this paper is to describe the tube ultrastructure of the Jurassic and Cretaceous sabellid Glomerula sp. and Recent Glomerula piloseta with the aim of finding further evidence of the synonymy of these genera proposed by Jäger (2004), and to prove the Mesozoic origin of calcification of sabellid tubes. The paper also addresses similarities and differences in the tube ultrastructure of sabellids and serpulids in order to test the hypothesis of convergent evolution of calcareous tubes in the ancestral serpulid and Glomerula. The formation of the calcareous tube in sabellids is compared with that in serpulids and cirratulids.

Material and methods

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Tube ultrastructure in fossil and recent sabellids
  5. Origin of calcification in sabellidae
  6. Comparison of Glomerula with the other annelid tubes
  7. Acknowledgments
  8. References

Tube fragments of fossil Glomerula and Recent serpulids and cirratulids were ground longitudinally, polished and etched with 1 per cent acetic acid for 1 min and examined under the scanning electron microscope (SEM; Table 1). Some tube fragments were taken from four paratypes of Glomerula piloseta (as Calcisabella ZMA V.Pol. 3744, Queensland, Australia; Lizard Island, lagoon near east entrance, depth 2–20 m, sheltered side of reef near sandy bottom, collected by H. A. ten Hove, Station 18, March 3, 1986). The material was fixed in sea-water and 4 per cent formalin, and transferred to 70 per cent ethanol after a few days. SEM examination was carried out on the external, internal and fracture surfaces of a fragment of an untreated tube of Glomerula piloseta. Thereafter, the same fragment was ground in a longitudinal orientation, polished and etched with 1 per cent acetic acid for 1 min and examined under the SEM. The same fragment was finally re-polished and treated with a 1:1 mixture of 25 per cent glutaraldehyde and 1 per cent acetic acid, to which alcian blue was added before SEM study. SEM-EDX analyses were applied to identify aragonite by the high content of strontium (Sr).

Table 1.   Age and locality information of the samples studied.
SpeciesColl. no.Age, locality
  1. MB.M., Natural History Museum in Berlin; ZMA, Zoological Museum, University of Amsterdam; TUG, Museum of Geology, University of Tartu.

1. Glomerula sp.MB.M. 3697bJurassic, Porta Westfalica, Germany
2. Glomerula sp.MB.W. 1301aUpper Cretaceous, Essen an der Ruhr, Germany
3. Glomerula pilosetaZMA.V.Pol. 3744Recent, Australia, Queensland, Lizard Island; paratypes
4. Dodecaceria coraliiZMA.V.Pol. 3803Recent, Mexico, Yucatan, Chicxulub Puerto
5. Dodecaceria caulleryiTUG 1232-3Recent, Atlantic coast of South Africa
6. Ficopomatus enigmaticusZMA.V.Pol. 3779Recent, Lake of Tunis, Tunisia
7. Hydroides dianthusZMA.V.Pol. 3661Recent, Florida, Anna Maria Island, Bradenton
8. Serpula israeliticaZMA.V.Pol. 5253Recent, Cape Verde Islands, Mid Atlantic, CANCAP Station 7.160
9. Spiraserpula caribensisZMA.V.Pol. 5286Recent, Netherlands Antilles, Curaçao, Station 2061A

Tube ultrastructure in fossil and recent sabellids

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Tube ultrastructure in fossil and recent sabellids
  5. Origin of calcification in sabellidae
  6. Comparison of Glomerula with the other annelid tubes
  7. Acknowledgments
  8. References

The tube wall of Recent Glomerula piloseta is composed of two aragonitic layers (Text-fig. 1D–F). The friable outer layer is porous, c. 25 μm thick, and composed of more or less regularly shaped small spherulites. The inner layer is 50–60 μm thick and separated from the outer layer by thin organic films. At the contact of the two layers numerous centres with spherulitic structure originate (Text-fig. 1F). These centres are c. 80 μm apart from each other. Bundles of needle-shaped crystallites forming primitive irregular prisms grow from the spherulitic centres towards the interior. The individual prisms are not encased by an organic film and their distal ends form irregular elevations into the tube lumen. Abundant sphaeromorph bacteria occur at the tube surface and are integrated into the organic films (Text-fig. 1B).

image

Figure TEXT-FIG. 1.. Glomerula pilosetaPerkins 1991, Recent, Australia. A, exterior of untreated tube fragment. B, detail of exterior of untreated tube fragment. C, interior of untreated tube fragment. D–F, longitudinal section of the tube, treated with 1 per cent acetic acid for 2 min. ba, sphaeromorphic bacteria; cc, crystallization centres; exter exterior; inter, interior; orf, organic film; sph, spherulites; spr, spherulitic prisms; um, μm.

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The layers in the tube wall show several growth lamellae separated by thin organic films. The thickness of the mineral lamellae and organic films varies (Text-fig. 1E–F). Some lamellae are continuous throughout the longitudinal tube section studied, whereas others form short lenses (Text-fig. 1E). The lamellae extend obliquely from the tube interior in an apertural direction. SEM-EDX analyses of aragonite in Glomerula piloseta revealed a high Sr content: 0.88 weight per cent or 0.24 atomic per cent, respectively.

In contrast to Recent G. piloseta, the thin, friable outer layer, if it was ever present, is not preserved in the tube wall of Jurassic and Cretaceous Glomerula. The tube wall consists of a single layer identical in structure to the thick internal layer of Recent G. piloseta. It is composed of simple prisms similar to those of Recent Glomerula (Text-fig. 2C–F). The prisms show growth lamellae that in places are continuous through the entire layer (Text-fig. 2C–D). The thickness of growth lamellae varies, just as in G. piloseta.

image

Figure TEXT-FIG. 2..  A–B, Glomerula piloseta, Recent, Australia; longitudinal sections of tubes, treated with GA solution for 5 min. C, Glomerula sp., Jurassic, Porta Westfalica, Germany; longitudinal section, showing spherulitic prismatic ultrastructure, treated with GA solution for 20 min. D–F. Glomerula sp., Upper Cretaceous, Essen an der Ruhr, Germany. D–E, longitudinal sections, showing spherulitic prismatic ultrastructure, treated with GA solution for 20 min. F, oblique section, showing arrangement of spherulitic prisms. Exter, exterior; inter, interior; lm, lamellae; um, μm.

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Origin of calcification in sabellidae

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Tube ultrastructure in fossil and recent sabellids
  5. Origin of calcification in sabellidae
  6. Comparison of Glomerula with the other annelid tubes
  7. Acknowledgments
  8. References

Synonymy of Calcisabella and Glomerula is justified on the basis of the identical tube ultrastructure in addition to the similar tube morphology. Similarities in the tube ultrastructure of Jurassic, Cretaceous and Recent Glomerula can be explained by the comparable, and thus presumably plesiomorphic, mode of tube formation. Calcification in Sabellidae had apparently originated in the early Mesozoic and tube ultrastructure has remained unchanged since then. The appearance of Glomerula coincides with the great diversification of serpulids in the early Mesozoic (Jäger 2004). This event may even be connected with the replacement of Palaeozoic calcifying non-annelid tubeworms of tentaculitid affinity (as described by, e.g. Weedon 1994; Vinn and Mutvei 2005; Taylor and Vinn 2006; Vinn 2006) by calcifying annelid tubeworms.

Comparison of Glomerula with the other annelid tubes

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Tube ultrastructure in fossil and recent sabellids
  5. Origin of calcification in sabellidae
  6. Comparison of Glomerula with the other annelid tubes
  7. Acknowledgments
  8. References

The tubes of sabellids other than Glomerula are formed of organic material secreted by the worm, or of a mixture of mineral grains collected from the habitat and bound together by an organic mucus.

Sabellids are phylogenetically close to serpulids (Kupriyanova 2003). Two different types of tube formation can be distinguished in the latter. In some taxa, such as Pomatoceros, calcareous granules are formed in intracellular vesicles or within calcium-secreting glands. The granules are suspended in an acid mucopolysaccharide matrix that solidifies on contact with sea-water and forms the tube wall (Simkiss and Wilbur 1989). This type of secretion process does not occur in the other phyla. The second type of secretion process in serpulid tube formation resembles that seen in molluscs and many other invertebrate phyla in which the skeleton is formed by extracellular mineralization, mediated and controlled by an organic matrix that is secreted together with calcium ions by a secretory epithelium. The formation of Glomerula tubes probably takes place according to this second procedure.

Sabellid tube structure is uncomplicated and primitive in that the tube wall is composed of an outer layer of spherulites and an inner layer of prisms formed by spherulitic sectors. This kind of two-layered structure has not hitherto been found in serpulid tubes. However, prisms similar to those in sabellid tubes occur in the external tube layer of Hydroides dianthus (Text-fig. 3F) and the internal tube layer and internal keels of Spiraserpula caribensis (Text-fig. 3D–E). Spherulites may occur as occasional inclusions in the tube wall of Ficopomatus enigmaticus, but they do not form a distinct layer (Text-fig. 4A). In contrast to sabellids, serpulid tubes often have a lamello-fibrillar structure (sensuCarter et al. 1990), also termed ordered chevron structure (sensuWeedon 1994), as in Serpula israelitica (Text-fig. 4B). In this structure, the fibre-like granules have a common orientation within a single growth increment and a different orientation in the adjacent growth increment. The most common serpulid ultrastructure is irregularly orientated prismatic structure (IOP), such as in the internal tube layer of Hydroides dianthus (Text-fig. 3F). In IOP structure the elongate, needle-like crystallites forming it have three-dimensionally variable orientations within a single growth increment.

image

Figure TEXT-FIG. 3..  A, Dodecaceria coralii, Recent, Mexico; longitudinal section, treated with GA solution for 5 min. B–C, Dodecaceria caulleryi, Recent, Atlantic coast of South Africa; longitudinal section, treated with GA solution for 5 min. D–E, Spiraserpula caribensis, Recent, Curaçao, Caribbean; cross section, treated with 1 per cent acetic acid for 2 min. F, Hydroides dianthus, Recent, Florida; longitudinal section, treated with acetic acid for 2 min. IOP, irregularly orientated prismatic layer; exter, exterior; inter, interior; lm, lamellae; spr, spherulitic prisms; spr.l, spherulitic prismatic layer; um, μm.

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image

Figure TEXT-FIG. 4..  A, Ficopomatus enigmaticus, Recent, Lake of Tunis, Tunisia; longitudinal section, treated with 1 per cent acetic acid for 2 min. B, Serpula israelitica, Recent, Cape Verde Islands, Mid Atlantic; longitudinal section, treated with 1 per cent acetic acid for 2 min. Sph, spherulites; um, μm.

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In contrast to Glomerula, serpulids have shorter growth lamellae. These are not subparallel to the tube wall and are often chevron-shaped. This indicates a longer secretion zone in Glomerula than in serpulids. Serpulids such as Pomatoceros (Hedley 1958; Weedon 1994) are also possibly capable of much more rapid growth in their tube length than Glomerula because of their short, anteriorly deposited, growth lamellae.

The structure and ultrastructure of the tube of Glomerula is very similar to that of the cirratulid genus Dodecaceria. Both have an irregular spherulitic, prismatic ultrastructure and long growth lamellae subparallel to the tube wall (Text-fig. 3A–C). In contrast to Glomerula, an entirely spherulitic outer layer has not been observed in Dodecaceria. Since Glomerula and Dodecaceria belong to families that are phylogenetically distant (Rouse and Fauchald 1997), the similarities in their tube construction should be regarded as a convergent evolutionary development.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Tube ultrastructure in fossil and recent sabellids
  5. Origin of calcification in sabellidae
  6. Comparison of Glomerula with the other annelid tubes
  7. Acknowledgments
  8. References

Acknowledgements.  Ten Hove thanks the Trustees of the Australian Museum, Sydney, for funding the field-trip to Lizard Island from which Glomerula piloseta was collected. Dodecaceria caulleryi was donated for our study by R. N. Hughes, University of Wales. Vinn acknowledges the financial support of projects NL-TAF-111, SE-TAF-113 and DE-TAF-122 by SYNTHESYS, a program financed by the European Commission under the Sixth Research and Technological Development Framework Program ‘Structuring the European Research Area’, and Estonian Science Foundation grant 6623.

References

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Tube ultrastructure in fossil and recent sabellids
  5. Origin of calcification in sabellidae
  6. Comparison of Glomerula with the other annelid tubes
  7. Acknowledgments
  8. References
  • BERKELEY, E. and BERKELEY, C. 1954. Notes on the life-history of the polychaete Dodecaceria fewkesi (nom.n.). Journal of the Fisheries Research Board of Canada, 11, 326334.
  • BRÜNNICH NIELSEN, K. 1931. Serpulidae from the Senonian and Danian deposits of Denmark. Meddelelser fra Dansk Geologisk Forening, 8, 71113.
  • CARTER, J. G., BANDEL, K., DE BUFFRÈNIL, V., CARLSON, S. J., CASTANET, J., CRENSHAW, M. A., DALINGWATER, J. E., FRANCILLION-VIEILLOT, H., GÉRADIE, J., MEUNIER, F. J., MUTVEI, H., DE RIQLÈS, A., SIRE, J. Y., SMITH, A. B., WENDT, J., WILLIAMS, A. and ZYLBERBERG, L. 1990. Glossary of skeletal biomineralization. 609671. In CARTER, J. G. (ed.). Skeletal biomineralization: patterns, processes and evolutionary trends. Vol. 1. Van Nostrand Reinhold and Co., New York, NY, 832 pp.
  • EHLERS, E. 1901. Die Polychaeten des magellanischen und chilenischen Strandes. Ein faunistischer Versuch. Festschrift zur 150 Jahrigen Bestehens der Königliche Gesellsschaft für Wissenschaften Göttingen, 1232.
  • FISCHER, R., PERNET, B. and REITNER, J. 2000. Organomineralization of cirratulid annelid tubes – fossil and recent examples. Facies, 42, 3550.
  • HEDLEY, R. H. 1958. Tube formation by Pomatoceros triqueter (Polychaeta). Journal of the Marine Biological Association, UK, 37, 315322.
  • HOVE, H. A. ten and HURK, P. van den 1993. A review of Recent and fossil serpulid ‘reefs’; actuopalaeontology and ‘Upper Malm’ serpulid limestones in NW Germany. Geologie en Mijnbouw, 72, 2367.
  • HOVE, H. A. TEN and SMITH, R. S. 1990. A re-description of Ditrupa gracillima Grube, 1878 (Polychaeta, Serpulidae) from the Indo-Pacific, with a discussion of the genus. Records of the Australian Museum, 42, 101118.
  • HOVE, H. A. TEN and ZIBROWIUS, H. 1986. Laminatubus alvini gen. et sp. n. and Protis hydrothermica sp. n. (Polychaeta, Serpulidae) from the bathyal hydrothermal vent communities in the eastern Pacific. Zoologica Scripta, 15, 2131.
  • JÄGER, M. 2004. Serpulidae und Spirorbidae (Polychaeta sedentaria) aus Campan und Maastricht von Norddeutschland, den Niederlanden, Belgien und angrenzenden Gebieten. Geologisches Jahrbuch, A, 157, 121249.
  • KUPRIYANOVA, E. K. 2003. Life history evolution in serpulimorph polychaetes: a phylogenetic analyses. Hydrobiologia, 496, 105114.
  • LEIDY, J. 1855. Contributions towards a knowledge of the marine invertebrate fauna of the coasts of Rhode Island and New Jersey. Journal of the Academy of Natural Sciences of Philadelphia, 3, 135152.
  • NEFF, J. M. 1971. Ultrastructural studies of the secretion of calcium carbonate by the serpulid polychaete worm, Pomatoceros caeruleus. Zeitschrift für Zellforschung, 120, 160186.
  • NISHI, E. 1993. On the internal structure of calcified tube walls in Serpulidae and Spirorbidae (Annelida, Polychaeta). Marine Fouling, 10, 1720.
  • PERKINS, T. H. 1991. Calcisabella piloseta, a new genus and species of Sabellinae (Polychaeta: Sabellidae). Bulletin of Marine Science, 48, 261267.
  • PILLAI, T. G. and HOVE, H. A. ten 1994. On recent species of Spiraserpula Regenhardt, 1961, a serpulid polychaete genus hitherto known only from Cretaceous and Tertiary fossils. Bulletin of the Natural History Museum, London (Zoology), 60, 39104.
  • REISH, D. J. 1952. Discussion of the colonial tube-building polychaetous annelid Dodecaceria fistulicola Ehlers. Bulletin of the South Californian Academy of Sciences, 51, 103107.
  • ROUSE, G. W. and FAUCHALD, K. 1997. Cladistics and polychaetes. Zoologica Scripta, 26, 139204.
  • SANFILIPPO, R. 1996. Micromorphology, microstructure and functional morphology of the Josephella marenzelleri (Polychaeta Serpulidae) tube. In CHERCHI, A. (ed.) Autoecology of selected organisms: achievements and problems. Bollettino della Società Paleontologica Italiana, Special Volume, 3, 205211.
  • SANFILIPPO, R. 1998. Tube morphology and structure of the bathyal Mediterranean serpulid Hyalopomatus variorugosus Ben-Eliahu & Fiege, 1996 (Annelida, Polychaeta). Rivista Italiana di Paleontologia e Stratigrafia, 104, 131138.
  • SIMKISS, K. and WILBUR, K. M. 1989. Biomineralization: cell biology and mineral deposition. Academic Press, New York, NY, 337 pp.
  • TAYLOR, P. D. and VINN, O. 2006. Convergence in small spiral worm tubes (‘Spirorbis’) and its palaeoenvironmental implications. Journal of the Geological Society, London, 163, 225228.
  • VINN, O. 2006. Tentaculitoid affinities of the tubeworm-like fossil Tymbochoos sinclairi (Okulitch, 1937) from the Ordovician of North America. Geobios, 39, 739742.
  • VINN, O. and MUTVEI, H. 2005. Observations on the morphology, and affinities of cornulitids from the Ordovician of Anticosti Island and the Silurian of Gotland. Journal of Paleontology, 79, 725736.
  • VOVELLE, J., GRASSET, M. and TRUCHET, M. 1991. Sites of biomineralization in the polychaete Pomatoceros triqueter (Serpulidae) with comments on some other species. Ophelia, Supplement, 5, 661667.
  • WEEDON, M. J. 1994. Tube microstructure of Recent and Jurassic serpulid polychaetes and the question of the Palaeozoic ‘spirorbids’. Acta Palaeontologica Polonica, 39, 115.
  • ZIBROWIUS, H. and HOVE, H. A. ten 1987. Neovermilia falcigera (Roule, 1898), a deep- and cold-water serpulid polychaete common in the Mediterranean Plio-Pleistocene. Bulletin of the Biological Society of Washington, 7, 259271.