A Lower Cretaceous chondrichthyan dermal denticle assemblage and its bearing on placoid scale diversity and histology

https://doi.org/10.1016/j.cretres.2020.104444Get rights and content

Highlights

  • First observation of a BCE unit in dermal denticles.

  • The highly organised enameloid supports the self-organising theory.

  • A new histotype for dermal denticles is introduced.

  • 17 different morphotypes extends the fossil record from four to nine orders.

Abstract

Dermal denticles of Mesozoic chondrichthyans are rarely documented, which tremendously limits the knowledge of different morphotypes during this time and for the whole clade. Here we describe an extraordinarily diverse assemblage of dermal denticles from deposits of Austria, comprising 17 different morphotypes. Based on the functional types of the denticles and their morphological similarities with both extinct and extant representatives, we attempt an order-level taxonomic attribution of the morphotypes recovered. The herein recorded occurrences of Hexanchiformes, Squaliformes, Squatiniformes, Heterodontiformes, the family Protospinacidae (Squalomorphii incertae sedis), and probably Rajiformes or Chimaeriformes increase previous tooth-based taxic diversity estimates of Valanginian cartilaginous fishes from Austria from four to at least nine orders. Additionally, we discuss the absence of denticles of cladodontomorph chondrichthyans, whose teeth were previously reported from the same deposits. Etched sections and light microscope analysis were carried out using the most abundant morphotypes with the aim of exploring the histology of chondrichthyan dermal denticles. Our results confirm previous studies in reporting a single crystallite enameloid, but we also report for the first time the presence of bundled enameloid in dermal scales, a condition so far restricted to the tooth enameloid of some chondrichthyans. Additionally, a putative new dentine type is observed, leading to the introduction of the descriptive term ‘nepedentine’ for the internal, dense, and poorly supplied dentine core by vascular channels.

Introduction

Elasmobranchii (sharks, rays, and skates) Bonaparte (1838) (sensu Maisey, 2012) (= Neoselachii Compagno, 1977) represent a monophyletic clade and form together with the holocephalans the group of cartilaginous fishes (chondrichthyans). Most members of this group possess non-growing body scales (= placoid scales sensu Thies, 1995), which are shed continuously during lifetime resulting in a rich fossil record for this group. Although this feature is found in most chondrichthyans, evidence indicate that earliest relatives retained postfunctional teeth to form tooth whorls (Ginter et al., 2010, Maisey et al., 2014). Hence, the oldest record of this group is represented by scales from the Ordovician (Sansom et al., 1996, Sansom et al., 2012), whereas the earliest fossil teeth were discovered in lower Devonian strata (Mader, 1986).

Dermal denticles and teeth of chondrichthyans are said to be, in their composition, equivalent structures (Sire and Huysseune, 2003). Both elements possess a pulp cavity surrounded by dentine, which is covered by a hypermineralised tissue, the so-called enameloid (Hertwig, 1874, Reif, 1973b). Contrary to dermal denticles, numerous investigations documenting a diverse ultrastructure of tooth enameloid (e.g. Reif, 1973b, Gillis and Donoghue, 2007, Guinot and Cappetta, 2011, Enault et al., 2015, Cuny et al., 2017, Feichtinger et al., 2018) and dentine histology (e.g. Ørvig, 1967, Poole, 1967, Peyer, 1968, Moyer et al., 2015, Moyer and Bemis, 2016, Schnetz et al., 2016, Jambura et al., 2018, Jambura et al., 2019) have been carried out. These studies have led to an interesting evolutionary scenario from a primitive state of enameloid in teeth of early chondrichthyans to a high diversity of structures in the enameloid of modern representatives (e.g. Cuny et al., 2017) and three common histotypes (ortho-, osteo-, and pseudoosteodont: e.g. Jambura et al., 2018) of tooth dentine, respectively.

Numerous studies dealing with shark tooth enameloid microstructure, composition, and properties have been carried out (e.g. Reif, 1973b, Preuschoft et al., 1974, Enax et al., 2012, Enax et al., 2014, Lübke et al., 2015, Cuny et al., 2017). Similarly, dermal denticles have been largely studied in the way of biomimetic and bionic aims (Sullivan and Regan, 2011, Wen et al., 2014, Pu et al., 2016, Feld et al., 2019), but works focusing on their internal structure are comparatively scarce (e.g. Karatajūté-Talimaa, 1973, Sansom et al., 1996, Cappetta, 2012, Meyer and Seegers, 2012, Manzanares et al., 2014, Enault et al., 2015, Andreev et al., 2016, Cuny et al., 2017). According to these studies, the enameloid of dermal denticles possesses a rather primitive architecture and the dentine consists exclusively of orthodentine, which surrounds a central pulp cavity. This basic organisation can be subdivided into two different processes of denticle development, the growing type [polyodontode, e.g. Cladoselache Dean, 1894, Ctenacanthus Agassiz, 1837 (in 1843) (Reif, 1978a)] and non-growing type [single-odontode e.g. some symmoriids (Coates and Sequeira, 2001) and crown-group elasmobranchs such as Heterodontus De Blainville, 1816, Chlamydoselachus Garman, 1884, and Heptranchias, Rafinesque, 1810 (Reif, 1974b)]. Besides the variation within each type, single-odontode and polyodontode denticles are supposed to occur in a single specimen as in the hybodontiform Hybodus delabechei Charlesworth (1839), that developed both growing and non-growing denticles (Reif, 1978a). Reif (1978a) distinguished four different growing types based on their morphogenesis: (1) Heterodontus-, (2) Protacrodus-, (3) Ctenacanthus costellatus-, and (4) Hybodus delabechei-types. The first type comprises non-growing denticles, which are shed during skin expansion. Denticles of the second type grow by the addition of odontodes, but the number of scales is constant during all ontogenetic stages. Type 3 also comprises growing denticles, but they are replaced during lifetime, and type 4 includes both growing and non-growing ones. This scheme is a rather simplified view of the complex diversity of chondrichthyan denticles, but provides an applicable classification for an overview.

Beside the classifications of different morphogenetic types, most efforts of previous denticle studies were to clarify the taxonomy of early Palaeozoic chondrichthyans (e.g. Karatajūté-Talimaa, 1973, Sansom et al., 1996, Andreev et al., 2016) and therefore overlooked post-Palaeozoic fossil and living taxa. Detailed investigations comprising Mesozoic denticles are rather limited and concentrate solely on the internal architecture of enameloid (e.g. Manzanares et al., 2014, Enault et al., 2015, Cuny et al., 2017).

Based on the extraordinary high diversity of Valanginian denticles in the herein studied samples, we prepared etched sections of the most common sampled morphotypes for a detailed SEM analysis and use light microscopy as a non-invasive technique for studying the vascularisation pattern. The comprehensive study of denticle morphology combined with investigations of internal structures provides the first synopsis of placoid scales of Early Cretaceous chondrichthyans, which contributes to our knowledge about this group during an important diversification period (Guinot and Cavin, 2016).

Section snippets

Geographic and geological context

The outcrop of Klausrieglerbach 1-A (KB1-A, 800 m above sea level) is located 7 km west of Losenstein in Upper Austria (ÖK map 1:50 000, sheet Groβraming; Austromap Online, 2019, Fig. 1). The exact position of the locality was determined by global positioning system: E 14°21′10″, N 47°54′32″. The Losenstein Syncline is part of the Ternberg Nappe, a Lower Bajuvaric Unit of the Northern Calcareous Alps in Upper Austria. A detailed geological context is provided in Lukeneder (2004) and Lukeneder

Materials and methods

The lower Valanginian denticles described herein were collected by one of us (A.L.) in 2012. About seven kilogrammes of rock were dissolved in 12% acetic acid to extract the denticles from the limestone. The residual sediment was screen washed using 500, 250, 125, and 63 μm mesh sizes. For the morphological identification, the denticles were mounted on stubs and coated with gold for preparing SEM (scanning electron microscopy) pictures with a JEOL JSM 6610-LV in the Central Research

Results

A total of 17 different morphotypes of dermal scales were identified. Here, we describe the morphology of each morphotype as well as the histology of selected samples.

The morphological aspect

Contrary to dermal denticles of Palaeozoic chondrichthyans, those of Mesozoic members are surprisingly underrepresented in the literature (Thies, 1995). Only few substantive studies have been conducted to shed light on the evolution (e.g. Karatajūté-Talimaa, 1973, Sansom et al., 1996, Meyer and Seegers, 2012), development (e.g. Hertwig, 1874, Reif, 1978a, Reif, 1985a, Manzanares et al., 2014), and taxonomical value (e.g. Thies and Leidne, 2011, Dillon et al., 2017) of these remains. Although

Conclusions

Based on the extraordinarily diverse assemblage of chondrichthyan dermal denticles from lower Valanginian deposits of Austria, 17 morphotypes are recognised and tentatively assigned to taxonomic groups at ordinal level. The tentatively identified orders would comprise Hexanchiformes, Squaliformes, Squatiniformes, Heterodontiformes, the family Protospinacidae (Squalomorphii incertae sedis), and probably Rajiformes or Chimaeriformes. Considering the previously described tooth assemblage from the

Acknowledgements

We gratefully thank two anonymous reviewers for their constructive comments that greatly improved the manuscript. Dan Topa (Central Research Laboratories, NHM, Vienna) is acknowledged for generating SEM pictures. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

References (129)

  • M.E. Bloch et al.

    Systema Ichthyologiae iconibus ex illustratum. Post obitum auctoris opus inchoatum absolvit

    (1801)
  • C.L. Bonaparte

    Selachorum tabula analytica

    Nuovi annali delle scienze naturali

    (1838)
  • J.P. Bonnaterre

    Tableau encyclopédique et méthodique des trois règnes de la nature

    (1788)
  • B. Błazejowski

    Shark teeth from the Lower Triassic of Spitsbergen and their histology

    Polish Polar Research

    (2004)
  • H. Cappetta

    Les Sélaciens du Crétacé supérieur du Liban. I. Requins

    Palaeontographica Americana

    (1980)
  • H. Cappetta

    Les Sélaciens du Crétacé supérieur du Liban. II. Batoïdes

    Palaeontographica Americana

    (1980)
  • H. Cappetta

    Chondrichthyes: Mesozoic and Cenozoic Elasmobranchii

  • H. Cappetta

    Hexanchiforme nouveau (Neoselachii) du Crétacé inférieur du Sud de la France

    Palaeovertebrata

    (1990)
  • H. Cappetta

    Chondrichthyes: Mesozoic and Cenozoic Elasmobranchii: Teeth

  • I.J. Castro

    The Sharks of North America

    (2011)
  • E. Charlesworth

    On the fossil remains of a species of Hybodus, from Lyme Regis

    The Magazine of Natural History

    (1839)
  • M.I. Coates et al.

    A new stethacanthid chondrichthyan from the Lower Carboniferous of Bearsden, Scotland

    Journal of Vertebrate Paleontology

    (2001)
  • M.I. Coates et al.

    A symmoriiform chondrichthyan braincase and the origin of chimaeroid fishes

    Nature

    (2017)
  • M.I. Coates et al.

    An early chondrichthyan and the evolutionary assembly of a shark body plan

    Proceedings of the Royal Society B

    (2018)
  • L.J.V. Compagno

    Phyletic relationships of living sharks and rays

    American Zoologist

    (1977)
  • F.L. Condamine et al.

    Climate cooling and clade competition likely drove the decline of lamniform sharks

    Proceedings of the National Academy of Sciences

    (2019)
  • G. Cuny et al.

    Evolution of Dental Tissues and Paleobiology in Selachians

    (2017)
  • G. De Beaumont

    Observations préliminaires sur trois Sélaciens nouveaux du calcaire lithographique d'Eichstätt (Bavière)

    Eclogae Geologicae Helvetiae

    (1960)
  • H.M.D. De Blainville

    Prodrome d'une nouvelle distribution systématique du règne animal

    Bulletin des Sciences, par la Société Philomatique de Paris

    (1816)
  • T.F.V. De Sarah et al.

    Taxonomy and morphology of species of the genus Squalus Linnaeus, 1758 from the Southwestern Atlantic Ocean (Chondrichthyes: Squaliformes: Squalidae)

    Zootaxa

    (2016)
  • B. De Sousa Rangel et al.

    Diversity of dermal denticle structure in sharks: Skin surface roughness and three-dimensional

    Microscopy Research and Technique

    (2019)
  • B. Dean

    Contributions to the morphology of Cladoselache (Cladodus)

    Journal of Morphology

    (1894)
  • E.M. Dillon et al.

    Dermal denticles as a tool to reconstruct shark communities

    Marine Ecology Progress Series

    (2017)
  • A.H.A. Dumeril

    Zoologie analytique, ou méthode naturelle de classification des animaux. Paris

    (1806)
  • P.M.G. Egerton

    Palaeospinax priscus. In: Figures and Descriptions of British organic remains

    Memoirs of the Geological Survey of the United Kingdom

    (1872)
  • S. Enault et al.

    Chondrichthyan tooth enameloid: past, present, and future

    Zoological Journal of the Linnean Society

    (2015)
  • I. Feichtinger et al.

    New chondrichthyans characterised by cladodont-like tooth morphologies from the Early Cretaceous of Austria, with Remarks on the microstructural diversity of enameloid

    Historical Biology

    (2018)
  • K. Feld et al.

    Dermal Denticles of Three Slowly Swimming Shark Species. Microscopy and Flow Visualization

    Biomimetics

    (2019)
  • ChK. Flammensbeck et al.

    Of teeth and trees: A fossil tip-dating approach to infer divergence times of extinct and extant squaliform sharks

    Zoologica Scripta

    (2018)
  • L. Frey et al.

    The early elasmobranch Phoebodus: phylogenetic relationships, ecomorphology and a new time-scale for shark evolution

    Proceedings of the Royal Society B

    (2019)
  • S. Garman

    An extraordinary shark

    Bulletin of the Essex Institute

    (1884)
  • J.J. Gilligan et al.

    Comparison of dorsal and pectoral fin denticles for grey nurse, great white, and six whaler sharks from east Australian waters

    Journal and Proceedings of the Royal Society of New South Wales

    (2011)
  • J.A. Gillis et al.

    The Homology and Phylogeny of Chondrichthyan Tooth Enameloid

    Journal of Morphology

    (2007)
  • M. Ginter et al.

    Chondrichthyes. Palaeozoic Elasmobranchii: Teeth

  • M. Ginter et al.

    Late Viséan pelagic chondrichthyans from northern Europe

    Acta Palaeontologica Polonica

    (2015)
  • C.F. Girard

    Characteristics of some cartilaginous fishes of the Pacific coast of North America

    Proceedings of the Academy of Natural Sciences of Philadelphia

    (1855)
  • R. Gravendeel et al.

    An Identification Key for Dermal Denticles of Rajidae from the North Sea

    International Journal of Osteoarchaeology

    (2002)
  • W. Gross

    Kleinschuppen, Flossenstachel und Zähne von Fischen aus Europäischen und Nordamerikanischen Bonebeds des Devons

    Palaeontographica

    (1973)
  • G. Guinot et al.

    Enameloid Microstructure of Some Cretaceous Hexanchiformes and Synechodontiformes (Chondrichthyes, Neoselachii): New Structures and Systematic Implications

    Microscopy Research and Technique

    (2011)
  • G. Guinot et al.

    ‘Fish’ (Actinopterygii and Elasmobranchii) diversification patterns through deep time

    Biological Reviews

    (2016)
  • Cited by (4)

    View full text