Spicomellus afer, Maidment & Strachan & Ouarhache & Scheyer & Brown & Fernandez & Johanson & Raven & Barrett, 2021

Maidment, Susannah C. R., Strachan, Sarah J., Ouarhache, Driss, Scheyer, Torsten M., Brown, Emily E., Fernandez, Vincent, Johanson, Zerina, Raven, Thomas J. & Barrett, Paul M., 2021, Bizarre dermal armour suggests the first African ankylosaur, Nature Ecology & Evolution 5 (12), pp. 1576-1581 : 1576

Spicomellus afer gen. et sp. nov.

LSID: urn:lsid:zoobank.org:act:D 12 DDAB4-E164-411D-8406-B7B 3DEC52F71

Etymology. Spicus meaning spike (Latin); mellus, a collar with spikes (Latin). A reference to the morphology of the specimen. Afer (Latin), an inhabitant of Africa.

Holotype. NHMUK PV R37412 , a partial rib bearing four co-ossified spines ( Fig. 1a–d ) housed at the Natural History Museum, London ( NHMUK). Horizon and locality. El Mers III Formation (Upper Bathonian/ Callovian, Middle Jurassic: 168.3–163.5 million years ago), Boulahfa , south of Boulemane, Fez-Meknes, Morocco (detailed locality information can be found in ref. 4). Maidment et al. 4 reported the horizon as lying in the El Mers II Formation, but subsequent field observations at the site suggest that it may lie slightly higher in the stratigraphy.

Diagnosis. Differs from all other armoured dinosaurs in possessing ‘T’-shaped dorsal ribs with a fused, rod-like osteoderm on the dorsal surface, from which projects a series of co-ossified conical dermal spines.

Osteological description. NHMUK PV R37412 is a slightly curved dorsal rib fragment fused to a flat plate-like osteoderm and bearing four elongate, conical spines that project from its dorsal surface ( Fig. 1a–d ). The specimen was scanned using X-ray Computed Tomography (XCT) to confirm that the spines are co-ossified ( Fig. 1c,d , Extended Data Figs. 1–3 and Supplementary video). In cross-section, the rod is strongly ‘T’-shaped, with its dorsal, horizontally oriented flange being broader anteroposteriorly (58 mm maximum width) than the depth of its ventral flange (33 mm maximum depth). The dorsal surface of the horizontal flange bears clear fibres that extend along the surface parallel to the rod’s long axis, as well as several fainter fibres extending perpendicular to the clear fibres. The dorsal, anterior and posterior surfaces of the rod are rugose. The horizontal and vertical flanges merge via a concave, smooth surface. The change in texture from the dorsal, rugose horizontal bar to the smooth, featureless ventral flange is marked by a groove that extends for the entire length of the rod.

The spines are rounded in cross-section and project dorsally ( Fig. 1a–d ). The medialmost spine is the smallest and is complete (54 mm from base to tip). As preserved, the second spine is the tallest (97 mm, but missing its distal tip), and the third spine is broken. The fourth spine is angled slightly medially, although this is probably taphonomic distortion (55 mm long, missing its distal tip). The surfaces of the spines are generally smooth, but there is a fine anastomosing mesh of vascular imprints on the external surface.

Histological description. The spine ( Fig. 2b and Extended Data Fig. 4 ) consists of a ~2.5 mm thick symmetrical cortex of woven bone and an inner core of highly vascularized trabecular bone. Several long pipes 10 extend from the core, opening on the surface. A thin layer, which is translucent in plane-polarized light and birefringent under crossed polars, covers much of the outer surface; it includes many scattered small osteocyte lacunae, and is probably diagenetic. Radial vascular canals also open to the bone surface. At least nine growth lines, visible as thin, dark, undulating lines parallel to the bone surface, extend from the central region of the cortex, becoming more closely spaced towards the outer surface. The woven bone matrix of the cortex is dominated by primary osteons with occasional radial and reticular vascular canals in circumferential arrangement. Scattered secondary osteons are present from the inner core to the mid-cortex. The core is composed of trabecular bone and large resorption cavities lined with lamellar bone and occasional secondary osteons. Many small, irregularly arranged osteocyte lacunae with small or no visible processes are scattered throughout the primary bone. Osteocyte lacunae in remodelled bone have a slightly more ovate shape and more extensive processes.

The horizontal bar of the rod is composed of two distinct histologies ( Figs. 1e–g and 2a,c ). Its upper and lower sections are divided by a strip of structural fibres (mineralized collagenous fibres not associated with ligamentous or tendinous insertion 11) that extend across the width of the section ( Figs. 1e and 2a,c ). The upper half of the rod is dominated by an ordered pattern of structural fibres, which are arranged in regular, orthogonal plywood-like layers 12 that cross each other at approximately 90° and overlie the primary bone matrix. The fibres, visible as darker and lighter strands or bundles under polarized light ( Fig. 1f and Extended Data Fig. 5 ), are arranged approximately perpendicular and parallel to the bone surface and follow the curvature of the bone at its outer edges ( Fig. 2a ). The fibre bundles are 500–600 µm thick and the majority are not interwoven. Simple vascular canals and some primary osteons with occasional radial and reticular vascular canals can be seen in the small sections of primary bone matrix that are not obscured by the fibre bundles ( Fig. 1f ). Small, irregular osteocyte lacunae with short or no visible processes are present.

By contrast, the lower section of the horizontal bar and the vertical flange are composed of highly vascularized, remodelled woven bone with no structural fibres ( Figs. 1g and 2a ). Growth lines are visible near the outer surface. Small, simple vascular canals are present in a circumferential arrangement parallel to the outer surface, followed by a ring of larger primary osteons and then either a sharp transition or smooth gradation to a highly vascularized region populated by resorption cavities with lamellar bone infill forming trabeculae with a high degree of remodelling ( Figs. 1g and 2a ). At least three generations of secondary osteons are present ( Fig. 1g ). Many small osteocyte lacunae are present with short or no visible processes, whereas the osteocyte lacunae in remodelled bone are more ovate with more extensive processes.

Taxonomic identity. Given its unique anatomy, we considered a non-tetrapod osteichthyan affinity for NHMUK PV R37412, but rejected this hypothesis for several reasons. First, the specimen was found in a terrestrial sedimentary sequence 4, which seems an unlikely source for what would have been an exceptionally large fish, but exclusion is also possible based on histological criteria. Teeth are ankylosed to the jaw in a range of osteichthyan fishes 13, similar to the way the spikes are fused to the rod in NHMUK PV R37412. However, fish teeth are usually composed of orthodentine surrounding a pulp cavity, with characteristic elongate odontoblast tubules extending through the dentine 13. Several chondrichthyans 14 – 16 and a few osteichthyans 13 have trabecular bone-like osteodentine within the pulp cavity, but in the latter this is generally surrounded by a pallial layer of orthodentine. However, there is no histological evidence of orthodentine in the specimen and other aspects of its histology and morphology favour a tetrapod origin.

Osteoderms are thought to form via metaplasia, a specific case of intramembranous ossification 11, 17, 18 but see 19. Metaplastic bone typically has low levels of vascularity and small or no osteocyte lacunae that lack visible processes 17, 18. Bone formed via metaplasia from the dermis often exhibits extensive fibre patterns reflecting the incorporation of collagen fibres from the original extracellular matrix 11, 18, 20. The presence of extensive structural fibre bundles in the upper part of the horizontal bar strongly suggests that it is an osteoderm formed via intramembranous ossification within the stratum compactum, and indicates that the skin would have been reinforced with thick striations of structural fibres, adding strength and tear resistance 21. The lower part of the rod bears the histological characteristics of tetrapod postcranial bone 22, and is morphologically consistent with being a dorsal rib.

Consequently, we conclude that NHMUK PV R37412 is a dorsal rib with an osteoderm fused to its external surface ( Fig. 2d ). The morphological and histological characteristics of NHMUK PV R37412, along with its age, suggest referral to Ankylosauria. Possession of dorsal ribs that are ‘T’-shaped in cross-section in their proximal portions is a synapomorphy of Eurypoda (Stegosa uria + Ankylosauria) 1, 23, allowing confident referral to the clade. Among eurypodans, the interwoven, plywood-like arrangement of structural fibres observed in this specimen has previously been described in numerous ankylosaurs 11, 24, 25 ( Fig. 1h ); in contrast, in stegosaurs, only the osteoderms of Stegosaurus have been histologically investigated, and while these possess mineralized fibres around their bases 10, they do not have a plywood-like arrangement 11. Mineralized fibre bundles have been observed in the early-diverging armoured dinosaur Scelidosaurus (which is either the sister taxon to Eurypoda 4 or to Ankylosauria 26), but these do not have a plywood-like arrangement either 11, 24. It has been suggested that the osteoderms of Scelidosaurus represent the plesiomorphic condition for Ankylosauria 11, and that the unique possession of a plywood-like arrangement of structural fibres in the osteoderms of ankylosaurs indicates an increased contribution from the dense connective tissues of the stratum compactum during osteoderm skeletogenesis relative to that of other thyreophorans 25. It is therefore most parsimonious to consider that the plywood-like arrangement of structural fibre bundles is a synapomorphy of Ankylosauria within Thyreophora based on the evidence currently available, a conclusion also reached by other authors 11, 25. The plywood-like arrangement of structural fibres therefore supports referral of S. afer to Ankylosauria 11, 18, 24, 25.

This structural fibre arrangement is also known in other tetrapods, including turtles 24, 27, aetosaurs 28, phytosaurs 29, 30, and titanosaurian sauropods 31, but NHMUK PV R37412 can be excluded from referral to any of these groups on morphological and stratigraphic grounds. No known phytosaur osteoderms are spine-like 32, but those of some aetosaurs are 33. However, both phytosaurs and aetosaurs went extinct before the end of the Triassic 30, 33, so referral to these groups would invoke an unprecedented 30–40 million-year ghost lineage in either case. A few turtles possess osteoderms 24, including conical spines 34, but their osteoderms are much smaller than those of NHMUK PV R37412 and often have a characteristic pustulate surface texture. Titanosaurid sauropods lack spine-like osteoderms 29, 31 and the clade did not originate until the Cretaceous 35, requiring a 23 million-year ghost lineage. By contrast, the armoured dinosaurs possessed a wide variety of plate- and spine-like osteoderms and originated in the Early Jurassic 2, 4.

Figures

Fig. 1 | Morphology and histology of Spicomellus afer, NHMUK PV R37412. a–d, Photographs (a,b) and 3D model produced from XCT scanning (c,d) showing the specimen in anterior/posterior (a,c) and dorsal (b,d) views. Red lines on a and b indicate where the specimen was sectioned for histological analysis. Red colouration on c and d indicates a cement used to consolidate the specimen. e–g, Thin-section photographs of the rod: full section of the rod (e) (see Fig. 2a for larger version); histological section through the dorsal osteodermal part of the rod (f) showing structural fibre bundles in an orthogonal ‘plywood-like’ arrangement; histological section through the rib part of the rod (g) showing heavily remodelled cortical bone. Yellow box in e indicates the position of f, blue box indicates the position of g. h, Histological section from the sacral shield of NHMUK PV R9293, an indeterminate ankylosaur from the Lower Cretaceous Wealden Group of the UK showing fibre bundles arranged in a pattern similar to that of the osteoderm in Spicomellus (f). i, Histological section from the rib of NHMUK PV R36643, an unnamed ankylosaur from the Callovian Oxford Clay Formation of the UK showing well-vascularized, remodelled cortical bone similar to that of the rib section of Spicomellus (g).

Fig. 2 | Details of the histology of Spicomellus afer, NHMUK PV R37142. a,c, Thin-section photographs of the fused rib and osteoderm. The darker region at the top of the image in a and to the top left of the image in c bears the histological characteristics of an osteoderm, while the lighter region below bears histological characteristics of the rib. A strip of structural fibres extending across this interface can be observed in c. b, Thin-section photograph of the spine of NHMUK PV R37142 S. afer showing a cortex of woven bone and an inner core of highly vascularized trabecular bone. d, A section of NHMUK PV R37142 S. afer with the osteoderm and rib sections segmented separately so the morphology of each can be seen. The osteoderm is in blue, while the rib is shown in white.

Extended Data Fig. 4 | Histological thin-section (plane polarized light) showing detail of the spine. A vascular channel can be observed in the top left of the image. The woven bone matrix of the cortex is dominated by primary osteons. Scattered secondary osteons can be observed in the mid and inner cortex. Large resorption cavities lined with lamellar bone can be observed in the trabecular bone of the core (top right). Red arrows indicate growth (=resting) lines.

Extended Data Fig. 5 | Thin section photomicrograph (plane-polarized light) showing detail of the structural fibres in the upper osteodermal part of the rod. Structural fibre bundles intersect roughly perpendicular to each other. The opaque cast in the top half of the image is probably diagenetic alteration.