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