Aspects of enameloid ontogeny in fossil and recent selachians with comments on enameloids and their occurrence during early lower vertebrate phylogeny

Svend Erik Bendix-Almgreen and Bente Soltau Bang, Section of Vertebrate Palaeontology, Geological Museum, Øster Voldgade 5-7, DK-1350 Copenhagen K.

Comparative studies of the inorganochemical composition of fossil and recent selachian teeth were carried out on the basis of electron microprobe (EPM) and X-ray diffraction (XRD) analyses. The obtained data were processed for precise determination of inorganic constituents of the respective biogenic apatites. The results were then evaluated in conjunction with information from histological and ultrastructural investigations of the dental hard tissues including the hypermineralized hard tissue coronoin (elasmobranch tooth enameloid; Bendix-Almgreen 1983) occurring superficially on the tooth crowns.

Among the obtained observations we report briefly on those bearing on certain aspects of the i.d.e. (inner dental epithelium) cells during selachian phylogeny. The documentation for this (tables with data, diagrams, photos etc) will be available for readers when our work (Bendix-Almgreen & Bang manuscr.) occurs in print. For reasons considered in the following we have found it appropriate to include, as a prelude, a brief review of information available in the literature on histogenesis and mature properties of recent coronoin. We have decided to present also some considerations regarding aspects related to the enameloids occurring in early lower vertebates.

Recent coronoin: histogenetic and mature properties

Studies by Shellis (1978) of ontogenetic stages of teeth from extant selachians and batoids indicate that coronoin formation (like that of the actinopterygian acrodin; Ørvig 1978) takes place by a complex sequence of histogenetic interactions between the i.d.e. cells, located immediately above the basement membrane, and a mesodermal organic matrix (the pre-coronoin) situated just beneath that membrane in the tooth germ. The exclusively mesenchymatically derived, collagen-rich pre-coronoin is deposited by scleroblasts (at the initial stage unspecialized) during their “movement” inwards in the dental papilla. Synchronously with the phase of pre-coronoin formation, the i.d.e. cells show notable change in shape: each becomes elongate in the superficial direction and its nucleus is relocated towards the top of the cell. Subsequently, when coronoin forms out of the pre-coronoin, the i.d.e. cells secrete proteins (including enamelin) of which some participate in the degradation of the collagens, making them ready for removal prior to mineralization and the following final hypermineralization. Thei.d.e. cells are apparently also active in the supply of the mineral constituents and even seem to participate in the removal of degraded organic constituents including collagens. During initial mineralization biogenic apatite crystallite rudiments are laid down in alignment with the pre-coronoin collagen fibres already under degradation. Subsequently, this same orientation is retained by all crystallites growing and developing during further mineralization and final hypermineralization when virtually all degraded collagens have gone (see Ørvig 1978, 1980; Bendix-Almgreen 1983).

Thus, in the mature state recent coronoin have such specific properties as: (1) the virtual absence of any organic material including remains of collagen (a feature shared with acrodin and enamel s.s.); (2) the mineral constituent occurs in the form of carbonate-fluorapatite (carFap) crystallites; and (3) the crystallites reflect perfectly the orientation of the original collagen fibre-bundles of the pre-coronoin.

Fossil coronoin

The fibre-bundle images just referred to are distinguishing ultrastructural features which are displayed also by well preserved fossil coronoin varieties (like those of acrodin) and thus indicate that even these once formed by histogenetic processes essentially corresponding to those of the recent material.

Enameloids versus dentines

By virtue of their histogeny and mature properties such hypermineralized hard tissues as coronoin and acrodin (recent as well as fossil) are clearly distinguished from, and cannot possibly qualify as, any sort of dentines. They obviously constitute a group of their own – the enameloids. Accordingly, to refer to them by a term like “vitrodentine” used by Zangerl et al. (1993) is obviously inappropriate. The usage of this term reflects (like other comments made by Zangerl et al. 1993) an apparent fatal failure by these writers to grasp the significance of evidence readily available from recent material, presented by Shellis (1978; see also Shellis & Miles 1974, 1976) and reviewed by Ørvig (e.g. 1978, 1980) and Bendix-Almgreen (1983) when they consider fossil material.

Observations and interpretations

Investigations by SEM of the coronoin from our late Palaeozoic selachian (probably a species of Polyacrodus) show it to be of the radial parallel-textured kind: all fibre-bundle images maintain an orthogonal direction relative to the tooth surface, towards which they exhibit a slight twining around their axes. The coronoin of extant Carcharhinus falciformis used for comparison is, on the other hand, of the cross-textured kind: parallel or subparallel fibre-bundle images arranged orthogonally to each other, some being directed longitudinally to the tooth surface, towards which others radiate perpendicularly (for texture terminology see e.g. Bendix-Almgreen 1983).

Data from our EPM and XRD survey show the inorganochemical composition of the fossil coronoin to be that of the carFap francolite, but its content of F is slightly lower than that found in its equivalent from extant C. falciformis. Considering what is normally the case with vertebrate hard tissues during fossilization, one may perhaps expect that our fossil coronoin had been subject to an enrichment in F. That this is not necessarily so is suggested by a variety of features, in particular the large size of the crystallites (revealed by SEM) and contents of the trace elements Mg and Si.

Large crystallites are known to be distinctive for carFap where it constitutes the mineral in recent vertebrate hard tissues (see e.g. Francillon-Vieillot et al. 1990) and no secondary enlargement of crystallite size has been observed in such fossil material that, like ours, exhibits well preserved ultrastructural and histological features.

Our EPM survey shows, moreover, that the fossil coronoin contains Mg and Si in quantities which differ remarkably little from those in similarly analyzed coronoin of extant C. falciformis. In contrast to this, contents of the same trace elements in our fossil dentines differ considerably from those found in their recent equivalents.

The features just touched upon, in our opinion, suggest that the analyzed fossil coronoin has probably been preserved virtually as intact with respect to its inorganochemical composition as it has with regard to its ultrastructure and histology. If it has suffered some enrichment in F, this has in all probability been on a considerably smaller scale than that found for our analyzed fossil dentines, judging from comparison of these with data from their equivalents in extant C. falciformis. Thus, as far as the evidence goes, it suggests that hypermineralized hard tissues like our fossil coronoin can remain inorganochemically fairly stable during fossilization, and that our fossil coronoin apatite even in the living state occurred in the form of a carFap.

Nevertheless, the fact remains that our fossil coronoin apatite has a slightly lower F content than that of coronoin of certain extant selachians generally regarded as phyletically advanced forms, e.g. Carcharodon carcharias and Somniosus pacificus (Suga et al. 1991).

Based on survey of extant selachian and teleostean material Suga et al. (1991) presented a hypothesis to the effect that certain “enameloid forming cells” (i.e. those now recognized as the i.d.e. cells) in the course of phylogeny widened their ability to concentrate and secrete F. Due to this, the biogenic apatite of coronoin gradually acquired a higher percentage of F and ultimately became an almost pure carFap.

The results from our survey of coronoin apatite from the late Palaeozoic selachian provide in fact the first evidence from palaeozoology which significantly strengthens the credibility of such a hypothesis.

Enameloids in early lower vertebrates: comments and conclusions

The earliest known undisputable vertebrates from which well preserved dermal skeletal units are available, include Eriptychius, Astraspis andPycnaspis from Ordovician times. Evidence to show that inductive interactions between the corium mesenchyme and the adjoining epidermis leading to enameloid formation were accomplished in these early agnathans, occurs in the form of several enameloid varieties distinguished, among others, by their respective ultrastructural features (see e.g. Reif 1979; Dzik 1986; Ørvig 1989). Dzik (1986) even claimed that the “… dermal tubercles of Astraspis have an enamel microstructure …”. Unconvincing are also the reasons given by Smith & Hall (1990) for interpreting as enamel that hypermineralized hard tissue which covers odontodes (“dermal teeth”; Ørvig 1967, 1977) in their material of Eripthychiidae. In fact, far from showing optical and ultrastructural or other similarities with conditions distinguishing enamel proper, the hypermineralized hard tissues of the material dealt with by Hall & Smith at the occasion referred to, have properties justifying their classification among Reif´s (1979) so-called ´single-crystallite´ enameloid (see also Bendix-Almgreen 1983).

Turning to the gnathostomes, the earliest known occurrence of enameloid recorded from them appears to be that in scales of certain Silurian and early Devonian acanthodians (Brotzen 1934; Gross 1971a). However, no sort of enameloid has so far been reported present on the cusps of tooth-whorls or dentigerous jaw bones in known representatives of these fishes (see e.g. Gross 1971a; Ørvig 1973). Thus, though certain acanthodians had acquired the capacity for enameloid formation in some part of their dermal skeleton, a similar capacity apparently never developed to be part of the histogenetic processes active during dental ontogeny in these fishes. One may conclude that while the i.d.e. cells no doubt were functionally significant during the papillary stage of tooth-cusps formation in these fishes, the cells under consideration apparently lacked the capacity to perform those specific activities which are required for enameloid formation.

As regards the elasmobranchs those known from detached scales or teeth (e.g. species of Ohiolepis, Cladolepis, Phoebodus; see Gross 1973), deriving from late Lower and Middle Devonian deposits, are distinguished by among others the lack of any kind of enameloid, including coronoin. (In this respect conditions remain undocumented in Antarctilamna prisca (Young 1982) and this late Gevetian/early Frasnian shark has to be left unconsidered here). A similar lack of enameloid is shown by scales and teeth of the Upper Devonian Cladoselache, scales of the Upper Carboniferous Holmesella, teeth and pharyngeal scales of the Lower Permian Xenacanthus, and the scales and teeth of Adamantina benedictae from the Upper Permian (Dean 1909; Ørvig 1966; Bendix-Almgreen 1993, 1994). However, several other elasmobranchs of the late Devonian (e.g. Phoebodus politus, Protacrodus sp., ‘Cladodus’ sp., ‘Helodus’ sp.) and the Carboniferous (e.g. Dicrenodus sp., Psephodus magnus, Psammodus rugosus) had acquired the capacity for enameloid formation during tooth ontogeny as shown by the presence of several kinds of coronoin (Gross 1973; see also Bendix-Almgreen 1983). When once acquired, this capacity was clearly retained within a variety of elasmobranch lineages (including those of the helicoprionids and the bradyodontid selachians; Bendix-Almgreen, 1966, 1983) during the late Palaeozoic and perhaps by all lineages in post-Palaeozoic times.

Finally, undisputed occurrences of the actinopterygian enameloid acrodin are, according to Ørvig (1978), met with in teeth of representatives of this group from the Carboniferous. Whether it occurs in geologically older material (including the possibly oldest known actinopterygianAndreolepis hedei from the Silurian; see Ørvig 1978) remains to be clarified. It may be added that the teeth of the late Silurian Lophosteus superbus, according to Gross (1971b), “… besteht nur aus Dentine …”, but the classification of this form relative to other teleostomes (including the actinopterygians) remains undecided.

From this brief review it would appear that: Although several varieties of enameloid can be recognized in dermal skeletal units of the earliest agnathans (like in various post-Ordovician ones), this cannot be taken to imply that those specifics of the epithelial-mesenchymal interactions on which enameloid formation depends, evolved just once and for all during early lower vertebrate phylogeny. All evidence from the fossil record suggests, rather conclusively in our opinion, that such enameloids as for example coronoin and acrodin cannot possibly have had a common origin from some ancestral enameloid type (see also Bendix-Almgreen 1983). Leaving aside discussions of any specific examples, the evidence so far available seems to favour a conclusion to the effect that: In the course of dermal skeleton phylogeny, the capacity for enameloid formation evolved separately within each major group of early lower vertebrates.


Bendix-Almgreen, S. E. 1966: New investigations of Helicoprion from the Phosphoria Formation of South-East Idaho, U.S.A. Biol. Skr. 14, 1-54.

Bendix-Almgreen, S. E. 1983: Carcharodon megalodon from the Upper Miocene of Denmark, with comments on elasmobranch tooth enameloid: coronoin. Bull. geol. Soc. Denmark32, 1-32.

Bendix-Almgreen, S. E. 1993: Adamantina benedictae n.g. et sp. – en nyhed fra Østgrønlands marine øvre Perm. In Johnsen, O. (ed):Geologisk Museum 100 år på Øster Vold, 48-58. København: Rhodos. (In Danish).

Bendix-Almgreen, S. E. 1994: Adamantina benedictae n.g. et sp. – a new elasmobranch from the marine Upper Premian of East Greenland.Ichthyolith Issues14, 21-22. (Abstract).

Bendix-Almgreen, S. E. & Bang, B. S. (manuscr.): Biogenic apatites in fossil and extant selachians, with comments on holocephalan pleromin apatite and dentition.

Brotzen, F. 1934: Die Morphologie und Histologie der Proostea-(Acanthodiden) Schuppen. Ark. Zool. 26A (23), 1-27.

Dean, B. 1909: Studies on fossil fishes (sharks, chimaeroids and arthrodires). Mem. Am. Mus. nat. Hist. 9, 211-287.

Dzik, J. 1986: Chordate affinities of the conodonts. In Hoffmann, A. & Nitecki, M. H. (eds): Problematic Fossil Taxa, 240-254. New York: Oxford Univ. Press.

Francillon-Vieillot, H., de Buffrénil, V., Casternet, J., Géraudie, J., Meunier, F. J., Sire, Y. J., Zylberberg, L. & de Ricqlès, A. 1990: Microstructure and mineralization of vertebrate skeletal tissues. In Carter, J. G. (ed): Skeletal Biomineralization: Patterns, Processes and Evolutionary TrendsI, 471-530. New York: Van Nostrand Reinhold.

Gross, W. 1971a: Downtonische und Dittonische Acanthodier-Reste des Ostseegebietes. Palaeontographica136(A), 1-82.

Gross, W. 1971b: Lophosteus superbus Pander: Zähne, Zahnknochen und besondere Schuppenformen. Lethaia4, 131-152.

Gross, W. 1973: Kleinschuppen, Flossenstacheln und Zähne von Fischen aus Europäischen und Nordamerikanischen Bonebeds des Devons.Palaeontographica142(A), 51-155.

Ørvig, T. 1966: Histologic studies of ostracoderms, placoderms and fossil elasmobranchs. 2. On the dermal skeleton of two late Palaeozoic elasmobranchs. Ark. Zool. (2) 19, 1-39.

Ørvig, T. 1967: Phylogeny of tooth tissues: evolution of some calcified tissues in early vertebrates. In Miles, A. E. W. (ed): Structural and Chemical Organization of Teeth1, 45-110. New York & London: Academic Press.

Ørvig, T. 1973: Acanthodian dentition and its bearing on the relationships of the group. Palaeontographica143(A), 119-150.

Ørvig, T. 1977: A survey of odontodes (“dermal teeth”) from developmental, structural, functional and phyletic points of view. In Andrews, S. M., Miles, R. S. & Walker, A. D. (eds): Problems in Vertebrate Evolution, Linn. Soc. Symp. Ser. 4, 53-75. London: Academic Press.

Ørvig, T. 1978: Microstructure and growth of the dermal skeleton in fossil actinopterygian fishes: Nephrotus and Colobodus, with remarks on the dentition in other forms. Zool. Scr. 7, 297-326.

Ørvig, T. 1980: Histologic studies of ostracoderms, placoderms and fossil elasmobranchs. 4. Ptyctodontid tooth plates and their bearing on holocephalan ancestry: the conditions of Ctenurella and Ptyctodus. Zool. Scr. 9, 219-239.

Ørvig, T. 1989: Histologic studies of ostracoderms, placoderms and fossil elasmobranchs.

6. Hard tissues of Ordovician vertebrates. Zool. Scr. 18, 427-446.

Reif, W.-E. 1979: Structural convergence between enameloid of actinopterygian teeth and of shark teeth. Scanning Electron Microsc. 2, 546-554.

Shellis, R. P. 1978: The role of the inner dental epithelium in the formation of the teeth in fish. In Butler, P. M. & Joysey, K. A. (eds):Development, Function and Evolution of Teeth, 31-42. London: Academic Press..

Shellis, R. P. & Miles, A. E. W. 1974: Autoradiographic study of the formation of enameloid and dentine matrices in teleost fishes using tritriated amino acids. Proc. R. Soc. Lond., B. 185, 51-72.

Shellis, R. P. & Miles, A. E. W. 1976: Observations with the electron microscope on enameloid formation in the common eel (Anguilla anguilla; Teleostei). Proc. R. Soc. Lond., B. 194, 253-269.

Smith, M. M. & Hall, B. K. 1990: Development and evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biol. Rev. 65, 277-373.

Suga, S., Taki, Y., Wada, K. & Ogawa, M. 1991: Evolution of fluoride and iron concentrations in the enameloid of fish teeth. In Suga, S. & Nakahara, H. (eds): Mechanisms and Phylogeny of Mineralization in Biological Systems, 439-446. Tokyo: Springer-Verlag.

Young, G. C. 1982: Devonian sharks from South-Eastern Australia and Antarctica. Palaeontology25(4), 817-843.

Zangerl, R., Winter, H. F. & Hansen, M. C. 1993: Comparative microscopic dental anatomy in the Petalodontida (Chondrichthyes, Elasmobranchii). Fieldiana: Geology, n.s., 26, 1-43.

Tilmelding til DGF Nyhedsbrev