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. 2022 Apr 20;241(3):616–627. doi: 10.1111/joa.13676

Complex enameloid microstructure of †Ischyrhiza mira rostral denticles

Todd D Cook 1,✉, Jack Prothero 1, Michael Brudy 1, Jerome A Magraw 1
PMCID: PMC9358731  PMID: 35445396

Abstract

Serving in a foraging or self‐defense capacity, pristiophorids, pristids, and the extinct sclerorhynchoids independently evolved an elongated rostrum lined with modified dermal denticles called rostral denticles. Isolated rostral denticles of the sclerorhynchoid Ischyrhiza mira are commonly recovered from Late Cretaceous North American marine deposits. Although the external morphology has been thoroughly presented in the literature, very little is known about the histological composition and organization of these curious structures. Using acid‐etching techniques and scanning electron microscopy, we show that the microstructure of I. mira rostral denticles are considerably more complex than that of previously described dermal denticles situated elsewhere on the body. The apical cap consists of outer single crystallite enameloid (SCE) and inner bundled crystallite enameloid (BCE) overlying a region of orthodentine. The BCE has distinct parallel bundled enameloid (PBE), tangled bundled enameloid (TBE), and radial bundled enameloid (RBE) components. Additionally, the cutting edge of the rostral denticle is produced by a superficial layer of SCE and a deeper ridges/cutting edge layer (RCEL) of the BCE. The highly organized enameloid observed in the rostral denticles of this batomorph resembles that of the multifaceted tissue architecture observed in the oral teeth of selachimorphs and demonstrates that dermal scales have the capacity to evolve histologically similar complex tooth‐like structures both inside and outside the oropharyngeal cavity.

Keywords: cretaceous, dentine, enameloid, histology, Ischyrhiza, rostral denticles, sclerorhynchoid

The highly organized enameloid observed in the rostral denticles of the sclerorhynchoid Ischyrhiza mira resembles that of the multifaceted tissue architecture observed in the oral teeth of selachimorphs and demonstrates that dermal scales have the capacity to evolve histologically similar complex tooth‐like structures both inside and outside the oropharyngeal cavity.

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1. INTRODUCTION

An elongated rostrum lined with enlarged rostral denticles (= rostral saw‐teeth, rostral spines) possessed by certain selachimorph (sharks) and batomorph (skates and rays) neoselachians likely served as a foraging, predation, and/or self‐defense adaptation (Kriwet & Kussius, 2001; Nevatte et al., 2017; Sternes & Shimada, 2018; Welten et al., 2015; Wüeringer et al., 2009). The pristiophorids (extant sawsharks), pristids (extant sawfishes), and sclerorhynchoids (extinct sawfishes) independently evolved this curious morphology (Cappetta, 2012; Villalobos‐Segura et al., 2021). Ischyrhiza mira Leidy, 1856 is a chronostratigraphically long‐ranging (Turonian–Maastrichtian) North American sclerorhynchoid (Cappetta, 2012). Individual rostral denticles and dental remains are frequently recovered from Western Interior Seaway (e.g., Beavan & Russell, 1999; Becker et al., 2004; Case & Cappetta, 1997; McNulty & Slaughter, 1962; Schubert et al., 2017; Welton & Farish, 1993; Wolberg, 1985) and Atlantic and Gulf Coastal plain (e.g., Becker et al., 2006; Cappetta & Case, 1975; Case, 1991; Case et al., 2017, 2019; Case & Schwimmer, 1988) deposits. Although the external morphology of I. mira and other sclerorhynchoid rostral denticles has been thoroughly presented in the literature, few studies have focused on the histological organization of these structures.

Chondrichthyan oral dentition and dermal denticles (= placoid scales) are derived from odontodes and share a similar tissue architecture consisting of a hypermineralized enameloid layer overlying a dentine region that surrounds a pulp cavity (e.g., Fraser et al., 2010; Huysseune & Sire, 1998; Ørvig, 1977; Reif, 1982; Sire & Huysseune, 2003; Witten et al., 2014). The enameloid of selachimorph teeth has a complex organization consisting of superficial single crystallite enameloid (SCE) and deeper bundled crystallite enameloid (BCE) units (Cuny et al., 2017; Enault et al., 2015). The latter encompasses three distinct components: (1) parallel bundled enameloid (PBE), crystallite bundles oriented parallel to the crown surface; (2) tangled bundled enameloid (TBE), randomly oriented crystallite bundles; and (3) radial bundled enameloid (RBE), crystallite bundles oriented perpendicular to the crown surface. Additionally, a ridges/cutting edge layer (RCEL), part of the BCE, and overlying SCE contribute to crown cutting edges (Cuny et al., 2017; Cuny & Risnes, 2005; Enault et al., 2015). Conversely, batomorph enameloid microstructure varies considerably with some taxa possessing only SCE, whereas others also have BCE; although this unit is not as defined as that observed in selachimorph dentition (Cuny et al., 2017; Enault et al., 2015). Only recently has the enameloid of neoselachian dermal denticles been shown to exhibit some degree of crystallite organization. Manzanares et al. (2014: p. 1063) revealed that the denticles of Scyliorhinus canicula (Linnaeus, 1758) include a SCE consisting of superficial compact crystallites and a deeper region of crystallites arranged parallel to the surface. Furthermore, Feichtinger et al. (2020: p. 13) determined that the denticles of some taxa include a deeper BCE, consisting of a “PBE‐like” component and a “seemingly” TBE, underlying the SCE.

Histological studies involving sclerorhynchoid rostral denticles have been largely limited to properties associated with dentine and the pulp cavity. For example, Slaughter and Steiner (1968) assigned two subspecies to I. mira based on differing dentine composition and pulp cavity structure: the stratigraphically older I. mira schneideri (Turonian–Santonian) and the younger I. mira mira (Campanian–Maastrichtian). Nevertheless, the enameloid microstructure of rostral denticles remains fundamentally unknown. Herein, we describe the microstructure of I. mira rostral denticles and reveal that the enameloid has a more complex organization than that of generalized body dermal denticles and approximates that of selachimorph oral dentition.

2. METHODS AND MATERIALS

The I. mira rostral denticles studied herein were recovered from the early Maastrichtian Navesink Formation of New Jersey, USA. Only incomplete specimens were utilized in the histological examination requiring sectioning. Primarily following the methods described by Guinot and Cappetta (2011), the rostral denticles were transversely or longitudinally sectioned by hand using 800, 1000, 1500, and 2000‐grit carborundum paper, sequentially. The specimens were then etched in diluted 10% HCl for 5, 10, or 30 s (depending on the depth of etching required) and placed in distilled water for 24 h. An FEI Quanta 650 FEG Scanning Electron Microscope was used for histological imaging, whereas gross structure imaging of the rostral denticles utilized ammonium chloride coating and digital photography. Image brightness and contrast were adjusted using Adobe Photoshop (23.1.0 Release). The described specimens are cataloged in the collections of the University of Alberta Laboratory of Vertebrate Paleontology (UALVP).

3. RESULTS

3.1. Rostral denticle macrostructure

Rostral denticle UALVP61460 consists of a crown and a slightly shorter root and has an overall ventral curvature (Figure 1a–d). The smooth crown is dorsoventrally compressed. The apical cap, representing the multilayered enameloid region, encompasses approximately one‐sixth of the crown height. This structure is observably distinct from the remainder of the crown. The anterior margin of the crown is more or less straight from the crown base to the proximal region of the apical cap, whereas the posterior margin is slightly convex. The anterior cutting edge extends along the crown margin but does not reach the crown base or distal portion of the apical cap. The posterior cutting edge extends farther than the anterior cutting edge proximally and distally along the crown margin. The basal bulge of the crown is obliquely directed in dorsal and ventral views and slightly expanded over the root. The anterior margin of the root is convex, whereas the posterior margin is concave. The basal region of the root is expanded dorsoventrally to form two short lobes that bear multiple folds and are divided by a distinct groove. Internally, the root of UALVP61461 has a large pulp cavity that narrows to a canal at the crown‐root junction. This canal extends distally toward the crown apex. There is a distinct compact tissue within the pulp canal at the crown‐root junction (Figure 1e).

FIGURE 1.

FIGURE 1

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Ischyrhiza mira rostral denticle macrostructure and mid‐crown surface microstructure with and without acid etching. (a) Dorsal view of I. mira rostral denticle UALVP61460, arrow indicates apical cap consisting of complex enameloid microstructure; (b) anterior view of UALVP61460; (c) ventral view of UALVP61460; (d) posterior view of UALVP61460; (e) internal macrostructure of UALVP61461 showing pulp cavity and pulp canal, arrow indicates compact tissue obstructing the pulp canal at crown‐root junction; (f) mid‐crown surface region of UALVP61460 showing unetched SCE; (g) mid‐crown surface region of UALVP61460 following 5 s of 10% HCl etching showing fragmented SCE and underlying orthodentine; (h) higher magnification of image (g). (a–e) are digital images, whereas (f–h) are scanning electron microscopy images

3.2. Rostral denticle surface microstructure following surface acid etching

The entire crown surface of UALVP61460 is covered by a relatively thin but compact SCE layer that is essentially amorphous in an unetched state (Figure 1f). Following 5 s of surface acid etching, the SCE layer below the apical cap is fragmented, exposing a deeper orthodentine layer (Figure 1g, h). After 10 s of surface acid etching, the SCE enveloping the crown apical cap has been more‐or‐less degraded revealing distinct crystallite bundles that are oriented parallel to the long axis of the rostral denticle that constitute the PBE region of the BCE layer (Figure 2a–c). These parallel bundles rapidly disappear at an observable transitional zone at the base of the apical cap (Figure 2d, e). Below this zone, the remainder of the crown consists of exposed orthodentine and small fragments of degraded SCE (Figure 2f). Much of the root surface consists of orthodentine (Figure 2g); however, the base of the root lacks distinct dentinal tubules and represents osteodentine (Figure 2h).

FIGURE 2.

FIGURE 2

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Ischyrhiza mira rostral denticle surface microstructure following acid etching. (a) Dorsal view of UALVP61460 following 10 s of 10% HCl etching with approximate locations of higher magnification images (b–h); (b) apical cap without the SCE; (c) exposed PBE crystallite bundles of the BCE; (d) transitional zone between apical cap and remainder of crown; (e) higher magnification of image (d) showing scarce PBE crystallite bundles overlying orthodentine; (f) mid‐crown region showing small SCE fragments overlying orthodentine; (g) mid‐root region showing orthodentine; (h) root lobe region showing osteodentine. (a) is a digital image, whereas (b–h) are scanning electron microscopy images

3.3. Cutting edge microstructure following acid etching

Following 30 s of acid etching, the cutting edge along the lower apical cap of UALVP61460 and UALVP61462 exposes the RCEL of the BCE (Figure 3a–c). The RCEL consists of parallel crystallite bundles that become oriented perpendicular to the axis of the crown distally (Figure 3a) and extend across the width of the cutting edge (Figure 3b, c). The bundles spanning the cutting edge appear somewhat thinner than the parallel crystallite bundles flanking the cutting edge. This may suggest that not all the crystallite within each parallel bundle contributes to the cutting edge, or this may simply be an artifact of the acid etching. The cutting edge below the apical cap consists of areas of thick SCE, as portions of it remain intact following the acid‐etching treatment (Figure 3d). In regions along the cutting edge with SCE degradation, RCEL bundles are not observed and orthodentine is exposed. The proximal one‐third of each cutting edge becomes trough‐like in structure and has a fine layer of SCE (Figure 3e, f).

FIGURE 3.

FIGURE 3

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Ischyrhiza mira rostral denticle microstructure of the cutting edge following acid etching. (a) Longitudinal section of UALVP61462 following 30 s of 10% HCl etching showing PBE crystallite bundles oriented perpendicular to the axis of the crown forming the lower RCEL, same image as Figure 4D; (b) surface view of UALVP61460 cutting edge following 10 s of 10% HCl acid etching showing the RCEL of the lower apical cap; (c) higher magnification of image (b) showing the PBE crystallite bundles of the RCEL crossing the width of the cutting edge; (d) surface view of the same cutting edge mid‐crown, arrow indicates preserved thicker regions of SCE along the cutting edge; (e) surface view of the same cutting edge at proximal one‐third of the crown, arrow indicates trough‐like structure of cutting edge; (f) higher magnification of image (e) showing the cutting edge trough‐like structure and thinner SCE layer. (a–f) are scanning electron microscopy images

3.4. Rostral denticle internal microstructure following longitudinal sectioning and acid etching

UALVP61462 is longitudinally sectioned lateral to the pulp cavity and most of the pulp canal (Figure 4a). The multilayered enameloid apical cap is observably distinct from the reminder of the crown (Figure 4b). Following 30 s of acid etching, the SCE enveloping the apical cap is completely degraded and the underlying PBE of the BCE is exposed (Figure 4c). The distal portion of the PBE bundles associated with each cutting edge changes orientation to become perpendicular to the long axis of the crown, forming the RCEL (Figure 4d). Deep into the PBE is the meshwork of crystallite bundles that constitutes the TBE of the BCE (Figure 4e). Crystallite bundles of the TBE secure the enameloid to the underlying orthodentine at the enameloid‐denticle junction (Figure 4f). The orthodentine consists of a series of dentinal tubules separated by intertubular dentine (Figure 4g, h).

FIGURE 4.

FIGURE 4

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Ischyrhiza mira rostral denticle internal microstructure of the apical cap following longitudinal sectioning and acid etching. (a) Longitudinal section of UALVP61462 lateral to the pulp cavity and most of the pulp canal followed by 30 s of 10% HCl etching with the location of higher magnification image (b), arrow indicates apical cap; (b) apical cap with approximate locations of higher magnification images (c–h); (c) PBE crystallite bundles of the BCE; (d) PBE crystallite bundles oriented perpendicular to the axis of the crown forming the lower RCEL, same image as Figure 3a; (e) haphazard orientation of TBE crystallite bundles of the BCE; (f) higher magnification of TBE crystallite bundles securing the enameloid to the underlying orthodentine at the enameloid‐denticle junction, arrows indicate individual crystallites of the TBE bundles; (g) orthodentine showing dentinal tubules separated by intertubular dentine; (h) higher magnification of image (g). (a) Is a digital image, whereas (b–h) are scanning electron microscopy images

UALVP61463 is longitudinally sectioned through the pulp cavity and most of the pulp canal (Figure 5a). Following 30 s of acid etching, the SCE surrounding the entire crown is absent. The enameloid at the base of the apical cap consists of scarce PBE bundles directly overlying orthodentine (Figure 5b). Below this zone, the crown consists exclusively of exposed orthodentine (Figure 5c). This layer, in turn, surrounds a rather narrow pulp canal (Figure 5d–f). At the crown‐root junction, the pulp canal is filled by a small unit of compact non‐vasculature tissue, possibly that of nepedentine (Figure 5g). The enlarged pulp cavity, which is confined to the root, consists of an apical region surrounded by orthodentine composed of diverging dentinal tubules (Figure 5h, i). The basal region surrounding the pulp cavity lacks dentinal tubules and thus is composed of osteodentine (Figure 5j, k).

FIGURE 5.

FIGURE 5

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Ischyrhiza mira rostral denticle internal microstructure below the apical cap following longitudinal sectioning and acid etching. (a) Longitudinal section UALVP61463 through the pulp cavity and most of the pulp canal followed by 30 s of 10% HCl etching with approximate locations of higher magnification images (b–k); (b) lower region of transitional zone between apical cap and remainder of crown showing a few PBE crystallite bundles of the PBE overlying orthodentine; (c) exposed orthodentine; (d) pulp canal surrounded by orthodentine; (e) higher magnification of image (d); (f) dentinal tubules separated by intertubular dentine; (g) compact and non‐vascularized tissue obstructing the pulp canal at crown‐root junction, possibly nepedentine; (h) apex of pulp cavity and pulp canal showing diverging dentinal tubules; (i) apex of pulp cavity lined with orthodentine; (j) basal region of pulp cavity lined with osteodentine; (k) higher magnification of image (j). (a) and (h) are digital images, whereas (b–g) and (i–k) are scanning electron microscopy images

3.5. Rostral denticle internal microstructure following transverse sectioning and acid etching

Transverse sectioning at the apical cap of UALVP61464 clearly exhibits the complex organization of the enameloid (Figures 6a, b and 7a, b). Following 30 s of acid etching, the SCE is completely degraded, but a thick region of PBE containing crystallite bundles that are more or less oriented parallel to the long axis of the rostral denticle is evident (Figures 6c and 7c). Within this area are distinct radial crystallite bundles that are oriented perpendicular to the long axis of the rostral denticle that constitute the RBE. Adjacent radial crystallite bundles are more‐or‐less equidistant and appear to extend from the surface of the rostral denticle to the deeper regions of the PBE (Figures 6d, e and 7d). Underlying the PBE are crystallite bundles of a somewhat haphazard orientation that constitute the TBE of the BCE (Figures 6f and 7e, f). Many of the larger bundles appear to form a circumferential meshwork encircling the deepest area of the enameloid (Figure 7g). Although the PBE and TBE regions are approximately the same width throughout most of the rostral denticle, the TBE bundles extend considerably closer and have a more perpendicular orientation to that of the surface at the anterior and posterior margins. The enameloid‐dentine junction is sharp and distinct (Figures 6g and 7g). The orthodentine layer surrounds the narrow but patent pulp canal (Figures 6h and 7h).

FIGURE 6.

FIGURE 6

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Ischyrhiza mira rostral denticle internal microstructure of the apical cap following transverse sectioning and acid etching. (a) Transverse section of UALVP61464 at the apical cap followed by 30 s of 10% HCl etching; (b) transverse section at the apical cap showing the multilayered enameloid surrounding orthodentine and pulp canal with approximate locations of higher magnification images (c–h); (c) SCE degraded exposing crystallite bundles of the PBE and RBE; (d) radially oriented crystallite bundles of the RBE extending from the surface to the lower region of the PBE; (e) higher magnification image of (d) showing that adjacent RBE crystallite bundles are equidistantly spaced within the PBE; (f) transition between PBE and underlying TBE; (g) TBE crystallite bundles securing the enameloid to the underlying orthodentine at the enameloid‐denticle junction; (h) pulp canal surrounded by orthodentine, material within pulp canal is likely orthodentine ‘debris’ from sectioning preparation. (a) is a digital image, whereas (b–h) are scanning electron microscopy images

FIGURE 7.

FIGURE 7

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Ischyrhiza mira rostral denticle internal microstructure at the anterior margin of the apical cap following transverse sectioning and acid etching. (a) Transverse section of UALVP61464 at the apical cap followed by 30 s of 10% HCl etching; (b) transverse section at the anterior margin of the apical cap showing the multilayered enameloid surrounding orthodentine and pulp canal with approximate locations of higher magnification images (c–h); (c) SCE degraded exposing crystallite bundles of the PBE and RBE; (d) crystallite bundles of the outer TBE region have a more perpendicular orientation and extend closer to the surface at the anterior margin; (e) crystallite bundles of the middle TBE region have a haphazard orientation; (f) higher magnification image of (e); (g) crystallite bundles of the inner TBE region have a circumferential orientation around the orthodentine layer and are thicker; (h) TBE crystallite bundles securing the enameloid to the underlying orthodentine at the enameloid‐dentine junction. (a) is a digital image, whereas (b–h) are scanning electron microscopy images

Transverse sectioning of UALVP61465 near the crown base reveals a simpler organization than that of the apical cap (Figure 8a, b). Following 30 s of etching, the SCE is completely degraded, and the crown consists entirely of dentine (Figure 8c–e). Like that of UALVP61461 and UALVP61463, the pulp canal near the crown‐root junction is filled with a small segment of dense tissue, possibly nepedentine, which in turn is surrounded by orthodentine (Figure 8f).

FIGURE 8.

FIGURE 8

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Ischyrhiza mira rostral denticle internal microstructure near the crown base following transverse sectioning and acid etching. (a) Transverse section of UALVP61465 near the crown base followed by 30 s of 10% HCl etching; (b) transverse section at the posterior margin showing orthodentine extending from the pulp cavity to the surface with approximate locations of higher magnification images (c–e); (c) SCE degraded and orthodentine is exposed at the surface; (d) higher magnification of image (c) at the surface; (e) higher magnification of image (c) at the middle region of the orthodentine layer; (f) orthodentine surrounding the pulp canal that is obstructed by compact and non‐vascularized tissue, possibly nepedentine. (a) is a digital image, whereas (b–f) are scanning electron microscopy images

4. DISCUSSION

The ability to designate subspecies in the fossil record is, at best, questionable and “most often proposed and used by paleontologists unsure that formal designation of new taxa is warranted” (Gingerich, 1985: p. 30). Notwithstanding, the internal morphology of the early Maastrichtian rostral denticles described herein challenges the validation of I. mira subspecies. Slaughter and Steiner (1968) proposed that the rostral denticle root of the stratigraphically older I. mira schneideri (Turonian–Santonian) has a reduced pulp cavity that is situated further from the rostrum attachment site and possesses a basal region composed of osteodentine. Conversely, the pulp cavity of the younger I. mira mira (Campanian–Maastrichtian) is much larger, surrounded by orthodentine, and may possess an osteodentine “plug” situated adjacent to the attachment surface of the rostrum (Slaughter & Steiner, 1968: text‐Figure 4a, b). The overall morphology and tissue composition of the pulp cavity observed in UALVP61461and UALVP61463 are more akin to that of the older I. mira schneideri, despite being recovered from the early Maastrichtian Navesink Formation of New Jersey, USA (Figures 1e and 5a, h–k). Thus, characters associated with pulp cavity structure and histology do not support the erection of I. mira subspecies.

Based on external morphology and location along the rostrum, it is a long‐held notion that rostral denticles are derived from dermal denticles (e.g., Cappetta, 2012; Slaughter & Springer, 1968; Wüeringer et al., 2009). Nevertheless, I. mira rostral denticle microstructure, specifically the apical cap, is considerably more complex than that of previously described denticles. The BCE of the rostral denticle consists of distinct PBE and TBE components that are clearly more structured than that of “PBE‐like” and “seemingly” TBE of generalized dermal denticles (Feichtinger et al., 2020: p. 13). Additionally, the rostral denticles possess distinct RBE and RCEL. The RCEL component deep into the SCE is produced by a directional change in the PBE bundles of the BCE and not produced by the overlying SCE, which supports Enault et al.’s (2015) description of cutting edge microstructure in oral dentition. The histological organization of the enameloid layer in I. mira rostral denticles is evidently more similar to that of selachimorph teeth than that of previously described batomorph oral dentition or dermal denticles situated elsewhere on the body.

Rostral denticle development in pristiophorids and sclerorhynchoids, at least in those species where the developmental process has been preserved, begins with the formation of the crown apex (e.g., Slaughter & Springer, 1968; Smith et al., 2015; Underwood et al., 2016; Welten et al., 2015). It is assumed herein that the rostral denticles of I. mira develop in a similar ontogenetic order beginning with the apical cap. At the base of the apical cap, there is a distinct zone where the multilayered enameloid transitions to a thin layer of SCE overlying orthodentine (Figure 2d, e). Since the bulk of the rostral denticle is composed of the latter tissues, growth of this structure must occur at or below this transitional zone. Additionally, Underwood et al. (2016: p. 134) noted that the rostral denticles of the sclerorhynchoid Onchopristis Stromer, 1917 exhibited a “gradual infilling of the pulp cavity during development”. The presence of pulp canal “infill” at the crown‐root junction of UALVP61461, UALVP61463, and UALVP61465 may be a normal part of the mineralization process of development (Figures 1e, 5g and 8f). The tissue is very compact and does not appear to be osteodentine but does compare favorably to that of dense poorly vascularized nepedentine observed in certain dermal denticles (Feichtinger et al., 2020).

The origin of oral dentition has been an intriguing debate (e.g., Debiais‐Thibaud et al., 2011; Donoghue & Rücklin, 2016; Fraser et al., 2010; Fraser & Smith, 2011; Huysseune et al., 2022; Rücklin & Donoghue, 2019; Witten et al., 2014). The ‘outside‐in’ hypothesis claims teeth evolved from dermal denticles that expanded into the oropharynx and became specialized in feeding (Blais et al., 2011). Welten et al. (2015: p. 18) revealed that the “spatio‐temporal patterning and ordered replacement” of rostral denticles are more akin to dermal denticles than that of dentition. Whereas multiple replacement teeth develop within a tooth file, and functional teeth are replaced in a regulated timely manner, a single replacement rostral denticle will only develop after space becomes available following the loss of the functional rostral denticle in pristiophorids (Slaughter & Springer, 1968; Underwood et al., 2016; Welten et al., 2015; Wüeringer et al., 2009). A somewhat similar replacement pattern is observed in the sclerorhynchoid Sclerorhynchus atavus Woodward, 1889, where a single developed recumbent‐positioned replacement rostral denticle becomes erect only if the functional rostral denticle is displaced and space becomes available (Slaughter & Springer, 1968; Underwood et al., 2016; Welten et al., 2015). Recently, Sternes and Shimada (2018) revealed that I. mira has a rostral denticle replacement process similar to that of S. atavus. Recognizing that the developmental properties between rostral denticles and oral dentition is disparate, it is evident that the specimens described herein have convergently evolved oral tooth‐like characters including a BCE with well‐differentiated PBE, TBE, and RBE components, and cutting edges formed by SCE and RCEL. The occurrence of multifarious selachimorph‐like enameloid outside the oral tooth morphogenetic field (Welten et al., 2015) in the rostral denticles of a batomorph lends support to the ‘outside‐in’ hypothesis by demonstrating that dermal scales have the capacity to evolve similar complex tooth‐like architecture both inside and outside the oropharyngeal cavity.

The increased microstructural complexity observed in selachimorph dentition is likely an adapted response to resist mechanical stress associated with feeding. The PBE increases tensile strength, whereas the TBE resists compressional forces and, along with the RBE, increases fracture resistance (Duffin & Cuny, 2008; Gillis & Donoghue, 2007; Preuschoft et al., 1974; Wilmers et al., 2021). Though not subjected to strong tensile or compressional force, Manzanares et al. (2014) suggested that the enameloid layering observed in the body dermal denticles in some taxa may be the result of a “self‐organization process” of growing crystallites and proteins, which has been demonstrated to produce structural pattern in amniote enamel (e.g., Margolis et al., 2006; Sander, 2000). Rostral denticles are subjected to greater forces than that of generalized dermal denticles, particularly at the crown apex, thus an augmented enameloid arrangement at the apical cap likely evolved to mitigate the mechanical stresses related to feeding and/or self‐defense. The occurrence of a multifaceted enameloid, through the self‐organization process observed in dermal denticles, likely served as an exaptation to resist mechanical stress in both teeth and rostral denticles, at least in I. mira.

ACKNOWLEDGMENTS

This paper is dedicated to the memory of Gerard R. Case, for his valuable contribution to the field of palaeoichthyology. ‘Jerry’ also kindly provided the specimens used in this study. We would also like to thank Mary Brown (Penn State Behrend) for her assistance in specimen preparation. Comments by Jürgen Kriwet (University of Vienna) and an anonymous reviewer greatly improved the manuscript. This project was supported by a Penn State Behrend Undergraduate Student Research Grant.

Cook, T.D. , Prothero, J. , Brudy, M. & Magraw, J.A. (2022) Complex enameloid microstructure of †Ischyrhiza mira rostral denticles. Journal of Anatomy, 241, 616–627. Available from: 10.1111/joa.13676

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Associated Data

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Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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