The Exquisitely Preserved Dinosaur Skin of Psittacosaurus and the Scaly Skin of Ceratopsian Dinosaurs

doi:10.21203/rs.3.rs-1374507/v1

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The Exquisitely Preserved Dinosaur Skin of Psittacosaurus and the Scaly Skin of Ceratopsian Dinosaurs

https://doi.org/10.21203/rs.3.rs-1374507/v1

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published 12 Aug, 2022

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The Frankfurt specimen of the early-branching ceratopsian dinosaur Psittacosaurus is remarkable for the exquisite preservation of squamous (scaly) skin and other soft tissues that cover almost its entire body. Newly detected details revealed under Laser-Stimulated Fluorescence (LSF) reveals the complexity of the squamous skin of Psittacosaurus, including several unique features and details of newly detected and previously-described integumentary structures. Variations in the scaly skin are found to be strongly regionalised in Psittacosaurus. For example, feature scales consist of truncated cone-shaped scales on the shoulder, but form a longitudinal row of quadrangular scales on the tail. Re-examined through LSF, the cloaca of Psittacosaurus has a longitudinal opening, or vent; a condition that it shares only with crocodylians. This implies that the cloaca had crocodylian-like internal anatomy, including a single, ventrally-positioned copulatory organ. Combined with these new integumentary data, a comprehensive review of integument in ceratopsian dinosaurs reveals that scalation was generally conservative in ceratopsians and typically consisted of large subcircular-to-polygonal feature scales surrounded by a network of smaller non-overlapping polygonal basement scales. This study highlights the importance of combining exceptional specimens with modern imaging techniques, which are helping to redefine the perceived complexity of squamation in ceratopsians and other dinosaurs.

integument

scales

skin

cloaca

reproduction

Ceratopsia

Dinosauria.

the first REPORT of scaly skin in a non-avian dinosaur (hereafter, dinosaur) was that of a sauropod by Mantell in 1852, but which was incorrectly identified as a giant crocodylian at the time (Mantell 1852, Czerkas 1997, Upchurch et al. 2015, Pittman et al. in press). The discovery of ‘typical’ reptilian scales among dinosaurs for the remainder of the 19th and much of the 20th Century has been regarded with some degree of ambivalence (Czerkas 1994, Hendrickx et al. 2022), although the discovery of feathered specimens from Liaoning Province of China in the 1990s (e.g., Chiappe and Witmer 2002, Chiappe 2007) has since spurred an intense interest in the integument of dinosaurs. However, outside Hadrosauridae, which includes several ‘mummified’ specimens covered with skin (see review by Bell 2014), the scaly integument of dinosaurs is still surprisingly poorly known. This is particularly the case of marginocephalians, in which the skin has been reported in only six ceratopsian taxa, namely, Centrosaurus (Brown 1917, Lull 1933), Chasmosaurus (Sternberg 1925), Nasutoceratops (Lund et al. 2016), Protoceratops (Brown and Schlaikjer 1940), Psittacosaurus (Mayr et al. 2002, Lingham-Soliar 2008, Lingham-Soliar and Plodowski 2010, Vinther et al. 2016), and Triceratops (Larson et al. 2007). Aside from Psittacosaurus, preserved skin in other ceratopsians is restricted to Coronosauria (i.e., Protoceratopsidae + Ceratopsoidea) and limited in body coverage. Scalation in Ceratopsia frequently consists of large rounded feature scales surrounded by smaller polygonal basement scales (e.g., Brown 1917, Sternberg 1925, Lund 2010, Lingham-Soliar and Plodowski 2010), but despite such generalisations, ceratopsians also show diverse skin morphologies with recognisable interspecific differences in the architecture of both feature and basement scales (Lund et al. 2016).

The famous Frankfurt specimen of Psittacosaurus sp. (SMF R 4970) is endowed with one of the most complete coverings of squamous skin in any dinosaur and is one of the few non-hadrosaurid ornithischians with integument covering a large portion of the body (Fig. 1). It is also the sole marginocephalian to include skin from the region of the head, limbs and tail and the only dinosaur in which the keratinous cranial horn is preserved (Mayr et al. 2016; see ‘skin morphology in ceratopsian dinosaurs’ below). More importantly, the integument of Psittacosaurus SMF R 4970 preserves evidence of colour patterns and countershading and is the only dinosaur to preserve the cloaca (Vinther et al. 2016, 2021). The latter was recently revealed to be unique among tetrapods in having a V-shaped convergence of the two darkly-pigmented lateral lips, in addition to a bulbous dorsal lobe (Vinther et al. 2021).

Psittacosaurus integument was first reported in a subadult individual of P. mongoliensis (AMNH FARB 6260) by Sereno (1987, p. 248) on the plantar surface of the right pes (metatarsals I-IV). The reticulate scales were described as minute (< 1 mm), rounded tubercules that did not form any pattern (Sereno 1987). Ji (1999) was, however, the first to formally describe scales in Psittacosaurus, which consisted of small (< 3–4 mm in diameter) polygonal and triangular scales, near the left humerus. Three years later, Mayr et al. (2002) provided a brief account of the skin morphology in Psittacosaurus based on the exquisitely preserved specimen SMF R 4970, focusing their attention on the bristle-like integumentary structures of the tail. The latter received a more thorough treatment by Mayr et al. (2016) who argued that the ‘bristles’ were homologous to the monofilaments of theropods such as Beipiaosaurus. Lingham-Soliar and Plodowski (2010) also described the scale pattern and distribution in Psittacosaurus in more detail, listing three types of scales in SMF R 4970, i.e., large, rounded plate-like scales, smaller polygonal scales or tubercles, and round pebble-like scales. Nevertheless, Lingham-Soliar and Plodowski (2010) only superficially described each scale morphotype and did not provide information on the scale pattern and morphology in the manus, pes and cloaca region. Those authors, however, revealed light and dark cryptic patterns created by the association of the tubercles and plate-like scales which were described as the first evidence of countershading in a dinosaur (see also Vinther et al. 2016).

In recent years, Laser-Stimulated Fluorescence (LSF) has become a powerful tool in palaeontology for highlighting and/or revealing additional soft tissue details in fossils that are otherwise unseen under white light conditions (Kaye et al. 2015, Wang et al. 2017). The application of this technology to Psittacosaurus SMF R 4970 has quite literally illuminated new aspects of the tail bristles (Mayr et al. 2016) and colour patterns (Vinther et al. 2016) in spectacular detail. In addition, Vinther et al. (2016, supp. inf.) provided some preliminary observations of the scale architecture of SMF R 4970 using this technique. The purpose of this study is to augment these earlier descriptions with strict attention to the scale architecture with the aim of providing an even clearer picture of the appearance and palaeobiology of one of the most well-preserved dinosaurs in existence. We use this to inform a detailed review of skin morphology and distribution across ceratopsians with an aim of better understanding squamation patterns across Dinosauria.

Institutional abbreviations: AMNH FARB, American Museum of Natural History, fossil amphibian, reptile, and bird collections, New York, USA; CMN, Canadian Museum of Nature, Ottawa, Quebec, Canada; IVPP, Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, China; HMNS, Houston Museum of Natural Science, Houston, Texas, USA; LPM, Liaoning Paleontological Museum, Shenyang, Liaoning Province, China; MN, Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil; MV, Palaeontological Museum (Nanjing Institute of Geology and Palaeontology), Nanjing, Jiangsu Province, China; NGMC, National Geological Museum of China, Beijing, China; PKUVP, Peking University Vertebrate Paleontology, Beijing, China; SMF, Senckenberg Natural History Museum, Frankfurt, Hesse, Germany; STM, Shandong Tianyu Museum of Nature, Pingyi, Shandong Province, China; SUP, Shenandoah University Collection, Winchester, Virginia, USA; UALVP, University of Alberta vertebrate palaeontology collection, Edmonton, Alberta, Canada; YFM, Yizou Fossil Museum, Yixian County, Liaoning Province, China.

The specimen SMF R 4970, referred to Psittacosaurus sp. (Mayr et al. 2002, Vinther et al. 2016; Fig. 1), comes from the Early Cretaceous Jehol deposits of the Liaoning Province, China, and most likely from the Jianshangou Bed, Yixian Formation (126–130 Ma; Barremian/Aptian; Chang et al. 2009, 2017) of the Sihetun locality, Beipiao County (Mayr et al. 2002). SMF R 4970 was photographed using Laser-Stimulated Fluorescence (LSF) performed using an updated version of the methodology proposed by Kaye et al. (2015) and refined in Wang et al. (2017). A 405 nm blue near-UV laser diode was used to fluoresce the specimen following standard laser safety protocol. Long exposure images were taken in a darkened room with a Nikon D810 DSLR camera fitted with a 425 nm blocking filter and controlled from a laptop using digiCamControl. Image post-processing (equalization, saturation and colour balance) was performed uniformly across the entire field of view in Photoshop CS6. Because soft tissue outlines in SMF R 4970 are best visible using LSF, the observations made using this technique and the resulting digital images formed the basis for the following descriptions. All measurements of the integument were taken using digital images uploaded and calibrated in ImageJ v1.52q. Average scale dimensions for each body region (Table 1) were calculated from measurements of at least five randomly-selected scales per body region (see DataS1).

Table 1

Scale morphology in the ceratopsian dinosaur *Psittacosaurus* sp. (SMF R 4970).
Body region	Basement scales		Feature scales
Body region	Morphology	Diameter (mm)	Morphology	Diameter (mm)
Head	Oval to subcircular	0.5-3	Absent	-
Neck	Lenticular, elliptical to rounded polygonal	0.7-2	Absent	-
Shoulder	Polygonal or rounded-polygonal	1-1.4	Cylindrical or truncated-cone shaped, stripped	6.7–9.8 mm
Forelimbs	Polygonal or rounded-polygonal; hexagram arrangement	1-1.5	Absent	-
Manus	Reticulate	0.5	Absent	-
Flank	Diamond-shaped	1.1–2.8	Circular to irregular	3–4 mm
Abdomen	Rectangular	1.1–2.2	Absent	-
Hindlimbs	Diamond-shaped; hexagram pattern	0.5–3.1	Absent	-
Tarsus	Reticulate	0.9–1.8	Absent	-
Cloaca and ischial callosity	lenticular, sub-triangular, rounded-rectangular or hexagonal	3-6.8	Absent	-
Tail	rounded-quadrangular	1.3–6.8	Quadrangular	> 8 mm

The scaly skin of SMF R 4970 was compared to that of other dinosaurs, with a particular attention to ceratopsians (Table 1), as well as snakes, lizards, birds, and crocodylians (see Appendix 1). A representative sample of each of these extant groups were observed in the collections of the University of New England’s Natural History Museum (Armidale, Australia) and photographed using an Olympus S7X7 stereomicroscope fitted with an Olympus SC50 digital camera (see DataS1). Multifocal image stacks were manually captured using cellSens Standard (www.olympus-lifescience.com) imaging software and stacked in Adobe Photoshop CC 2019. Data on cloacal morphologies as well as horn dimensions were also gathered in various amniotes based on the literature or personal observations for comparison (see Appendix 1).

Age of the Individual

The right femur of SMF R 4970 is ~ 140mm long. This is similar to the femoral lengths of P. lujiatunensis IVPP V12617 (138mm) and V18344 (145mm), LPM R00128 (135mm) and R00138 (144mm) and PKUVP V1053 (149mm) and V1056 (135mm) which belong to ~ 6–7 year old subadults [see Table 1 and Fig. 5 of Erickson et al. (2009) and Supplementary table S2 of Zhao et al. (2013)]. This age is just shy of sexual maturity and at the beginning of the exponential growth phase [see Table 1 and Fig. 5 of Erickson et al. (2009) and Supplementary table S2 of Zhao et al. (2013)]. The femoral length of SMF R 4970 is the closest match to a nearly sexually mature subadult [see Table 1 and Fig. 5 of Erickson et al. (2009) and Supplementary table S2 of Zhao et al. (2013)].

Terminology, taxonomy and horn measurements

Scale terminology largely follows that outlined by Bell (2012) and Hendrickx et al. (2022). The term ‘inclusion’ (or scale inclusion) follows its use in crocodylian literature to refer to small, variably-shaped scales that fill irregular gaps between adjacent larger, more uniformly sized/shaped scales that form the main basement. In reference to the shape of the feature scales, ‘basal’ is defined as the towards the dermis (i.e., anatomically deep), whereas ‘apex/apical’ is away from the dermis (anatomically superficial). Psittacosaurus taxonomy follows that of Sereno (2010) and Hedrick and Dodson (2013), although we acknowledge the differing opinions of other authors (e.g., Napoli et al. 2019). The lengths of the bony core and keratinous ‘sheath’ of the jugal horn were measured following Brown’s (2017) method for the “spine length (SL)”, i.e., from the anterior margin of the bony core and keratinous ‘sheath’ to its apex.

Head and neck

Integument on the head and neck is the least well preserved in SMF R 4970 (Fig. 2). Discontinuous patches of darkly pigmented skin are present on various parts of the underside of the skull with individual basement scales best discerned on the medial surface of the left mandible, the lateral surface of the right mandible, the posterior extremity of the palate and the right jugal (Fig. 2D–F). That which covers the left mandible and the palate likely corresponds to the skin formerly covering the throat region between the lower jaws. Scale shapes are often difficult to distinguish but the patches on the palate (Fig. 2E) and the medial side of the left mandible show oval to subcircular basement scales (Fig. 2D, F). The smallest scales are found on the palate where they range between 0.5–1 mm in diameter whereas those from the two patches on the medial side of the mandible, next to the dentition and on the distal portion of the ramus, are 1–3 mm in diameter.

The most conspicuous feature of the cranial integument is a darkly-pigmented triangle of soft tissue on the left side of the skull interpreted as the keratinous ‘sheath’ of the jugal horn (Vinther et al. 2016; Fig. 2A–C, I). Although clearly associated with the osseous jugal horn, the ‘sheath’ is offset anterior to and projects at least 23 mm laterally beyond the tip of the jugal horn (Fig. 2C). A break in the rock truncates the anterolateral edge of the ‘sheath’, which lies at a deeper level in the rock matrix than the bone itself indicating the ‘sheath’ was anatomically dorsal to the bony core. The surface of the ‘sheath’ is uniform to somewhat granular or mottled in appearance and devoid of scales. The ventral surface of the right osseous jugal horn, however, preserves darkly-coloured globular and branching structures that appear to represent the pigmented interstitial tissue between non-pigmented epidermal scales (Fig. 2I). The scales themselves are polygonal (hexagonal?), 3–4 mm in diameter. On the ventral surface of the jugal horn on the left side, however, individual scales are not discernible, only indistinct dark mottling.

Skin and scales are well preserved on either side of the cervical vertebrae delimiting a thick neck, which tapers from the back of the skull to a minimum width equal to approximately three times the width of the cervical vertebrae (as preserved in ventrolateral view) in line with the third post-axial vertebra (Fig. 2A). Scales on the neck form a basement of typically anteroposteriorly elongated (\(\stackrel{-}{x}\) length = 1.6 mm; Table 1), lenticular-to-weakly polygonal scales, and transitioning posteriorly to more elliptical or rounded-polygonal (i.e. less elongated) scales in the vicinity of the third and fourth post-axial vertebrae (Fig. 2D,E).

Shoulder and forelimbs

The soft tissue outline describes a forelimb that was robust, stocky and almost columnar, the greatest measurable width occurring at the mid-length of the humerus (4.5 times wider than the minimum width of the humerus), tapering distally with a modest constriction associated with the inner elbow (Fig. 3A). The pectoral girdle and forelimb are covered in a basement of typically small (\(\stackrel{-}{x}\) diameter = 1.9 mm), non-overlapping polygonal or rounded-polygonal (3–6 sided) scales. Interstitial tissue is relatively wide in the region of the coracoid (~ 1 mm wide) but elsewhere the scales closely abut one another. The arrangement of the scales differs somewhat along the forelimb: immediately anterior to the humerus, scales are more proximodistally elongate (~ 2 \(\times\) 1 mm) and form columns parallel to the long axis of the humerus. On the distal humerus and the area posterior to the mid-shaft, the scales form patterns consisting of a central polygonal scale (\(\stackrel{-}{x}\) diameter = 1.2 mm) surrounded by five or six small triangular elements (\(\stackrel{-}{x}\) length = 0.4 mm). This arrangement recalls the hexagram, or 6-pointed star (Fig. 3C). Each ‘star’ closely abuts its neighbour so that the pattern is continuous across this region. This unusual pattern is also present on the hindlimb (see below) and has been described from the proximal humerus of Nasutoceratops, where the ‘stars’ are comparatively large (central scale diameter up to 11 mm; Lund 2010). Elsewhere on the forelimb of SMF R 4970, the basement scales are less regularly arranged but each scale is always surrounded by six of its neighbours. Set within this basement are relatively large feature scales disposed along the presumed anterior–anteromedial surface of the girdle and forelimb between the coracoid to a point in line with the mid-length of the humerus. The feature scales themselves are almost cylindrical or truncated-cone shaped, with a circular basal cross-section (\(\stackrel{-}{x}\) diameter = 8.8 mm) and a height of up to 6.8 mm (Fig. 3D). The surfaces appear smooth but are pigmented by five or six broad dark stripes that extend from the scale base, converging apically but terminating to form an unpigmented star-shaped pattern at the scale apex (Fig. 3D). Feature scales are spaced ~ 6–9 mm apart along two or three roughly-formed vertical rows (parallel to the long axis of the humerus) ~ 5–6 mm apart. The basement scales immediately surrounding the feature scales do not differ in size or arrangement from the remaining basement scales (i.e. they do not form a rosette pattern sensu Pittman et al. in press). Whether feature scales continued onto the lateral surface of the forelimb is unknown. The pattern of small (~ 2 mm) polygonal basement scales continues distally on the forelimb with the exception of the inner elbow where they are even smaller (\(\stackrel{-}{x}\) diameter = 1.1 mm). At the junction between the distal antebrachium and the manus, the scale covering abruptly transitions to tiny reticulate scales (\(\stackrel{-}{x}\) diameter = 0.5 mm) on the palmar surface of the manus. Although incomplete, the contour of the soft tissues surrounding the manus indicate the presence of a fleshy ‘heel’ (Fig. 3E).

Trunk and abdomen

The integument covering the trunk can be divided into (and differs between) two broad regions: the soft abdomen between the rib cage and extending posteriorly to the pelvic girdle, and the lateral flanks associated with the ribs. Despite extensive integument on the right flank (i.e. lateral to the rib cage), individual scales are not easily identified due to the heavy pattern of pigmentation. Individual scales from the flanks are better seen on the left side where they are preserved medial and lateral to the thoracic ribs. Basement scales in this region are anteroposteriorly-elongated and roughly diamond-shaped (\(\stackrel{-}{x}\) = 2.3 \(\times\) 1.7 mm). A small number of larger circular-to-irregular feature scales (3–4 mm diameter) are interspersed throughout these diamond-shaped basement scales although not enough are discernible to identify any clear pattern in the arrangement of the feature scales. The latter are smaller, do not appear to be significantly elevated, and are uniformly dark compared to the striped, cylindrical feature scales in the shoulder region. The second region, corresponding to the soft underparts of the animal, between the rib cage and extending posteriorly between the ischia, are covered by quadrangular scales arranged into distinct transverse ‘bands’ as is typical of modern crocodylians and some squamates (e.g., Uromastix; pers. obs.; Fig. 4A–C; see DataS1). Scales are small (\(\stackrel{-}{x}\)length = 1.4 mm), becoming slightly larger (\(\stackrel{-}{x}\)length = 1.8 mm) and less distinctly banded in the anterior part of the abdomen (i.e. anterior of the presumed gastric mill). Extending anteriorly from the ischial callosity (see ‘tail and cloaca’ below), the transverse bands are broken along the ventral mid-line of the animal by a distinct longitudinal row of paired quadrangular scales (\(\stackrel{-}{x}\) length = 2.5 mm) (Fig. 4A–D). This mid-line row extends from just in front of the ischiadic symphysis anteriorly for approximately 13 cm.

Hindlimbs

The soft tissues surrounding the hind limb show a remarkably broad (anteroposteriorly) crus (i.e., part of the leg between the knee and the foot). As preserved, the soft tissues are broadest around the left knee (~ 3 times the anteroposterior length of the proximal tibia) tapering distally to the ankle joint at which point the flesh more closely shrouds the foot skeleton (Fig. 5A). The bulk of this tissue is posterior to the tibia, presumably corresponding to a large area of powerful leg retractor muscles. The tibia itself is close to and nearly parallel to the anterior edge of the integumentary outline. Although the pose of the animal obscures both femora, the volume of flesh shrouding the crus makes it unlikely that the upper leg was well separated from the body; there is no indication of a crease in the flesh at the back of the knee. Instead, the web of tissue extending proximally from the ankle joint probably bound the upper leg closely to the body as in many extant quadrupedal mammals (e.g., Equus, Bos).

Scales on the lower leg are hard to discern due to the heavy pigmentation and patterning of the skin. In the region posterior to the tibia, close to where the leg meets the torso, scales occasionally form a hexagram pattern consisting of a central subcircular scale (\(\stackrel{-}{x}\) diameter = 1.3 mm) surrounded by a number of smaller triangular scales (\(\stackrel{-}{x}\) length – 0.5 mm) similar to those on the forelimb (Figs. 5A, D, E). The precise number of triangular scales cannot be determined on the hindlimb, but number at least five on the best-preserved scales, suggesting at least six scales completed each ‘star’. In some cases, the central scale is darkly pigmented, whereas the triangular scales are lighter coloured. It is unclear whether this hexagram pattern continues more distally on the crus as the dense pigmentation, or lack thereof, makes individual scales less conspicuous; dark spots visible on other parts of the hindlimb probably pertain to pigmented sub-circular scales although the margins of the scales themselves are not always visible. Similarly, individual scales are not visible over the tibia itself, although darkly pigmented, anteroposteriorly-oriented stripes are densely distributed on the surface of the bone, matching the stripped pattern seen on the fleshy parts of the lower leg (Vinther et al. 2016; Fig. 5A).

On the posterior and anterior surfaces of the ankle, including the dorsal surface of the tarsus, the scales are larger than most other parts of the body (\(\stackrel{-}{x}\) diameter = 3.1 mm) and are distinctively diamond shaped. The relatively large size of these scales and the somewhat ‘swollen’ appearance of the integument (particularly posterior to the ankle joint) invokes the presence of a distinct callosity around the ankle (Fig. 5B). The dorsal surface of the pes and lateral surfaces of the leg are not clearly exposed on either hindlimb. The plantar surfaces of the tarsus and pes are covered in ovoid reticulate scales (\(\stackrel{-}{x}\) diameter = 1.2 mm). This pattern is superimposed on the plantar surface of the metatarsals themselves as well as the soft tissue adjacent to the bones (Fig. 5B). An arthral digital pad arrangement—in which the interpad creases do not correspond to the interphalangeal joints—appears to be present on the fourth pedal digit, which is the only digit where the toe pads are observable (Fig. 5C). Soft tissues are not preserved on the distalmost phalanges, nor can the keratinous ungual sheaths be seen, either because of damage/preparation or due to the position of the animal.

Tail and cloaca

The caudal vertebrae are centrally positioned along the long axis of the fleshy part of the tail. The soft tissues maintain a dorsoventral height equal to ~ 5.5 times the height of the corresponding centrum, increasing to ~ 6.3 times around caudal vertebra 19, posterior to which the soft tissues and vertebrae are incompletely preserved/truncated. The distal ends of the ischia are covered by comparatively large, polygonal scales that range from sub-triangular, rounded-rectangular to hexagonal and forming an ischiadic callosity ~ 4 cm in diameter (Vinther et al. 2016). Scales are largest (up to 6.8 mm diameter) at the centre of the callosity, decreasing in size (\(\stackrel{-}{x}\) diameter = 3.2 mm) centrifugally (Fig. 6A, B). A small number of scale inclusions are present on the callosity. Immediately posterior to the ischiadic callosity is the fleshy aperture (or vent) of the cloaca (Fig. 6A, B). Vinther et al. (2021) described the cloaca as consisting of slightly protruding left and right lateral lips that converge anteriorly, forming an inverted ‘V’. Importantly, LSF resolves the anterior convergence of these lips as continuing anteriorly in a straight line for a length of ~ 2 cm, which we interpret as forming a longitudinally-oriented vent. Thus, the cloaca is shaped more like an inverted ‘Y’. The lateral lips are darkly pigmented and wrinkled, the creases of which are roughly parallel and extend in a posterolateral direction (~ 3 cm long) towards the ventral tip of the second haemal arch (Fig. 6A, B). Rock breakage above this point (i.e. between the haemal arches themselves) has obscured further details of the integument in this region. Posterior to the lateral lips is another protruding region identified as the dorsal lobe (Vinther et al. 2021). The dorsal lobe is pale in colour (less pigmented) but also wrinkled; wrinkles are parallel, posteriorly oriented and 1–3 cm in length. Scales covering the lateral lips and dorsal lobe are almost lenticular (\(\stackrel{-}{x}\) length = 3.4 mm), the long axes of which are oriented parallel to the surrounding wrinkles, thereby forming a radial pattern around the vent (Fig. 6A, B). Posterior to the cloaca, and for the remaining length of the tail, the integument ventral to the caudal vertebrae consists of vertical bands (mediolaterally oriented in life) of typically rounded-quadrangular scales (Fig. 7). The shapes and sizes of these scales are, however, variable along the length of the tail. Between caudal vertebrae 10–12, the scales increase in size towards the ventral margin of the tail (from \(\stackrel{-}{x}\) = 1.7 to 3.3 mm in height; Fig. 7D). Further distally (between caudal vertebrae 14–15), scales are more uniformly large and rounded-quadrangular (\(\stackrel{-}{x}\) height = 2.8 mm). On the preserved distal part of the tail (i.e. immediately ventral to the haemal arches between caudal vertebrae 16 and 21), the vertical banding of scales (\(\stackrel{-}{x}\) = 2.4 mm in height) is broken dorsally by a longitudinal row of much larger quadrangular feature scales (Fig. 7C). None of these feature scales are complete although they have an average anteroposterior length of 5.4 mm and a maximum height exceeding 8 mm, making them among the largest scales on the entire body of SMF R 4970. These form a longitudinal row at a level roughly in line with the ventral edges of the haemal arches, but whether or not they continued more dorsally or constituted any more than a single row is unknown as the scales are not well preserved over the surface of the bones. Dorsal to the caudal vertebrae, individual scales are difficult to discern, obscured by dark patches of pigmentation (Vinther et al. 2016). Although pigment spots approximate the size and, to a lesser extent, shape of epidermal scales on other parts of the tail, there is not necessarily a direct relationship between pigmentation and scale morphology (Vinther et al. 2016, supplementary information). Indeed, on the dorsal part of the proximal tail (between caudal vertebrae 1–5) where pigmentation is dense (80% coverage; Vinther et al. 2016) and scales are better preserved, pigmented regions span 10 or more adjacent scales, separated by unpigmented strips one or two scales wide. Scales in both the pigmented and unpigmented regions appear subcircular/ovoid (\(\stackrel{-}{x}\) = 2.8 mm in diameter). Smaller inclusions are also present but there is no evidence of the vertical banding or larger feature scales seen on the ventral and distal parts of the tail.

The bristles lining the dorsal margin of the tail between caudal vertebrae 5–19 were described in detail by Mayr et al. (2016; Fig. 7A, B). It is not necessary to repeat those descriptions here.

SMF R 4970 is remarkable for the extent of soft tissue preservation, which has revealed unprecedented integumentary structures including the dorsal plume of bristles on the tail, the cloaca, as well as evidence of countershading (Mayr et al. 2002, 2016, Vinther et al. 2016, 2021). Additional integumentary features either not previously recognised or expounded upon include: (1) the keratinous jugal ‘horn’ (Mayr et al. 2016); (2) enlarged scales of the ischial callosity (Vinther et al. 2016, 2021); (3) the row(s) of feature scales on the mid-distal tail, and; (4) the arthral arrangement of the digital pads. We elaborate on each of these structures and discuss additional findings on the cloaca and the general skin morphology in ceratopsians below.

Keratinous jugal horn

The prominent jugal horn is one of the most characteristic features of Psittacosaurus spp., and ceratopsians more generally (You et al. 2008, Sereno 2010). Anastomosing vascular channels on the surface of the jugal horn in P. xinjianensis were cited as probable evidence for a keratinous sheath in life (Sereno and Shichin 1988). The taxonomy of Psittacosaurus is complex but consensus is starting to emerge (Sereno 2010, Hedrick and Dodson 2013) revealing variation in the presence/absence of such neurovascular channels on the jugal horn (Sereno 2010). Neurovascular channels are present on both dorsal and ventral surfaces of the jugal horn in P. xinjiangensis (Sereno and Shichin 1988) and P. gobiensis (Sereno et al. 2010), present only on the dorsal surface in P. lujiatunensis (You et al. 2008), present posteriorly in P. sibiricus (Averianov et al. 2006), and entirely absent in P. meileyingensis (Sereno et al. 1988). Intraspecific variation in this feature reported in P. sibericus may also be influenced by sex and/or ontogeny (Averianov et al. 2006). Therefore, taxonomic interpretations based on horn size, form, and orientation in Psittacosaurus should be regarded with caution (see Sereno 2010). Nevertheless, based on variation in osteological correlates on the jugal (Hieronymus et al. 2009), the epidermal covering too would be expected to differ between species—and possibly life stages—, and consequently not all species of Psittacosaurus would have had keratinous sheaths that covered the entirety of the jugal horn. Psittacosaurus SMF R 4970 appears to show direct evidence of this: rather than a keratinous ‘sheath’, the right jugal horn preserves evidence of polygonal scales directly on the ventral surface of the bone. On the left side, individual scales are not discernible; however, the dark-coloured triangle of soft tissue preserved at a deeper level below the jugal (i.e. anatomically dorsal) almost certainly represents the keratinous ‘sheath’ (Mayr et al. 2016). Unlike in some previous reconstructions (e.g., Vinther et al. 2016), we interpret the ventral surface of the jugal horn in Psittacosaurus SMF R 4970 as covered in epidermal scales, whereas the dorsal surface had a keratinous covering, perhaps more analogous to a fingernail than a sheath. This interpretation is also consistent with the osteological correlates of such structures (Hieronymus et al. 2009): in SMF R 4970, the relatively smooth, porous bone texture of the ventral jugal horn is not congruent with a thick keratinous covering (Hieronymus et al. 2009). Although the dorsal surface is not visible in SMF R 4970, You et al. (2008) described the jugal horn of P. lujiatunensis (= P. major)—a potential candidate for the identity of SMF R 4970 (Vinther et al. 2016, supplementary information)—as smooth ventrally and bearing vascular grooves dorsally. Thus, based on osteological correlates alone (Hieronymus et al. 2009), there is a precedent for the condition in which only the dorsal surface of the jugal horn would have had a keratinous covering. This interpretation also explains the preservation of the keratinous jugal ‘horn’ in SMF R 4970 in which it appears to have shifted anteriorly (and perhaps laterally) from the jugal horn (Mayr et al. 2016). Such a shift would be difficult to reconcile had the jugal horn been entirely sheathed in keratin. As also acknowledged by those authors, it is possible that the dark triangle was not associated with the jugal at all, but from a more dorsal position on the skull (Mayr et al. 2016), which we agree with. We nevertheless interpret the presence of a unique keratinous plate or nail-like covering in SMF R 4970 and likely P. lujiatunensis (You et al. 2008), and which probably differed in other species of Psittacosaurus—and potentially at different life stages—based on differing bone textures on the jugal horn.

Although the jugal horn and the keratinous ‘sheath’ are misaligned (Mayr et al. 2016), preservation of the latter in Psittacosaurus permits some tentative estimations on horn dimensions in other ceratopsians. By following the preserved curvature of the margin of the bony core and its horn ‘sheath’, we estimate that the latter is around 140% larger than the bony core in SMF R 4970. This value is greater than in the largest osteoderms in ankylosaurian Borealopelta (125% for the parascapular spine; Brown 2017), but within the range of some modern bovids such as the bison and bull (Brown 2017). Applying the same value (140%) to other ceratopsian horn cores, the estimated length of the nasal horns of Styracosaurus (horn core length = 53.4 cm in CMN 344; Brown and Henderson 2015) and Centrosaurus (45.8 cm in AMNH FARB 5351; Brown and Henderson 2015) would be of 75 cm and 64 cm, respectively, including the keratinous sheath (see DataS1). Likewise, the postorbital horns of Triceratops (estimated horn core length = 115 cm in MOR 3027 using Scannella et al. (2014), figure S1); Titanoceratops (91 cm in OMNH 10165; Lehman 1998) and Torosaurus (85.3 cm in MOR 981; Farke 2006) would be estimated to reach 160, 127, 119 cm in length, respectively, whereas the largest parietal spike of Styracosaurus (estimated horn core length = 56 cm in CMN 344; Ryan et al. 2007) may have reached 78 cm in length (see DataS1). These estimations are, however, tentative given that the ‘sheath’ in SMF R 4970 has evidently shifted and that the relative proportions of the jugal horn of Psittacosaurus and that of nasal and postorbital horns of ceratopsids might be significantly different. Nevertheless, these ranges illustrate the importance of soft tissues in enhancing the external appearance of even comparatively modest horns, such as the jugal horn in Psittacosaurus.

Ischial callosity

The enlarged scales forming the ischial callosity have been remarked upon previously (Vinther et al. 2016, 2021). Other ornithischian examples of an ischial callosity are unknown but are occasionally preserved in the theropod ichnological record. In rare ichnites of ‘sitting’ theropods (Kayentapus, Grallator and Eubrontes), the ischial callosity may impress as a circular, crescentic or subtriangular depression (Lockley et al. 2003, Kundrát 2004, Milner et al. 2009). In one specimen of Grallator that preserves skin impressions from the Lower Jurassic Turners Falls Formation, Kundrát (2004; p. 359 reported the ischial callosity bore “small trapezoid scales…similar in size to those preserved on the pedal surface of Anomoepus intermedius”. From this description, the ischial callosity in Grallator differs from the ‘reinforced’ condition in Psittacosaurus. Enlarged scales in this region of Psittacosaurus (Figs. 6, 9A) would have reduced the surface area of interstitial skin (i.e., hinge areas) exposed and therefore helped protect these soft parts from abrasion. Melanisation of the scales covering the ischial callosity might also have played a role in structural strengthening of this region (Vinther et al. 2016) but could also have played a visual role. As in bipedal theropods, it can be reasonably concluded that the ischial callosity in Psittacosaurus would have been used to support part of the animal’s weight when sitting or crouching (Vinther et al. 2016, supplementary information).

Caudal feature scales

At least one longitudinal row of feature scales is present on the lateral part of the tail between caudal vertebrae 16 and 21 (Fig. 7A–C). These do not have the same raised morphology of the feature scales in the pectoral region but are plate-like and more similar to (albeit much larger than) the ventral scales on the tail. We do not consider these scutate ventral scales (e.g., as seen in the tail of the theropods Concavenator and Juravenator or lining the ventrum of living snakes; Cuesta 2017, Bell and Hendrickx 2020, 2021) as they do not occur along the ventral midline, which can be traced posteriorly based on the position of the cloaca and ischial callus, and which indicate a lateral, or ventrolateral, position on the tail for the feature scales (Vinther et al. 2016, supplementary information). Similar rows of enlarged scales have also been described in the embryonic Auca Mahuevo titanosaurs (Chiappe et al. 1998, Coria and Chiappe 2007) and along the tail of the early-branching ornithischian Kulindadromeus (Godefroit et al. 2014, 2020). Colouration in SMF R 4970 may also belie the function(s) of these scales, although their ultimate role remains equivocal. Relatively large scales reduce the exposure of softer interstitial skin and afford greater protection compared to small scales (Soulé and Kerfoot 1972, Bell and Hendrickx 2021). However, the uniformly dark colouration of the feature scales—in comparison to the pale ventral and more mottled dorsal parts of the tail (Vinther et al. 2016)—might also imply a visual function. Dark feature scales occur in close association with the elaborate plume of ‘bristles’ on the dorsal tail, which has been interpreted as a display device for sociosexual signalling (Mayr et al. 2002, 2016). Dark feature scales would have added additional visual contrast to the tail and, combined with striped feature scales on the chest and forelimb and an overall countershaded body colouration (Vinther et al. 2016), invoke an unusual and visually striking animal.

Digital pads

Psittacosaurus presents an arthral arrangement of the pads on the pedal digits (those of the manus are not preserved; Fig. 5C). Several authors have proposed that the arthral condition—in which the interpad crease does not align with the interphalangeal joint—is the primitive condition among dinosaurs (Rainforth 2003), which is supported by its presence in a number of non-avian theropods and basal birds (Milàn 2006, Pu et al. 2013). More derived birds evolved a mesarthral condition, in which the interpad crease corresponds to the interphalangeal joint; however, both conditions are present in extant birds and can vary among individuals (Smith and Farlow 2003). In non-avian theropods, an arthral arrangement is present in allosauroids (Concavenator; Cuesta et al. 2015), tyrannosauroids (Santanaraptor; Hendrickx et al. 2022), and maniraptorans (Sinornithosaurus [NGMC 91, STM 5-172]; Anchiornis [STM-0-7]; Wang et al. 2017, Hendrickx et al. 2022). To our knowledge, Psittacosaurus is the first ornithischian to preserve direct evidence of the arthral pad configuration. This configuration is not directly observable from footprints and the few body fossils with skin in this region (e.g., Corythosaurus, Kulindadromeus) do not reveal the shapes of the pads (Brown 1916, Godefroit et al. 2020). Arthrally-arranged pads do, however, appear to be present on the manus of the early-branching ornithischian Kulindadromeus (Godefroit et al. 2020, Fig. 4a,c). The identification of arthral pads in Psittacosaurus, therefore, upholds Rainforth’s (2003) hypothesis that all dinosaurs retained the arthral condition in the pes, at least plesiomorphically.

Cloaca

One of the most surprising features of SMF R 4970 is the preservation of the cloaca, which was recently described by Vinther et al. (2021). Those authors identified the unique V-shaped convergence of the lateral lips and the presence of a bulbous dorsal lobe but were unable to decipher the precise shape of the opening (or vent) under white light. LSF resolves this issue and clearly shows the vent as a longitudinal slit, approximately 2 cm long, anterior to the dorsal lobe, between the left and right lateral lips (Figs. 6, 9C). This is notable, as the shape of the vent in living sauropsids has taxonomic relevance and is accompanied by various configurations of the internal anatomy of the cloaca (see DataS1). The cloaca of living sauropsids is divisible into three types (Gadow 1887): transversely opening (snakes and lizards), longitudinally opening (crocodylians; Fig. 8B, D), or round/square (birds; see DataS1). Our observations reveal that the integumentary covering across these three types differs accordingly. In snakes, the transverse vent is covered by one or two cloacal scales that are modifications of the broad ventral scales present elsewhere on the underbelly (see DataS1). The condition in lizards is highly variable but the vent is always transverse and accompanied by a variable number of cloacal scales that may or may not differ from the surrounding scales. Among birds, the area immediately surrounding the cloaca is naked, bearing neither scales nor feathers. In crocodylians, the longitudinal vent is surrounded by elliptical-to-polygonal scales that radiate and increase in size from the vent itself (Fig. 8D). This rosette arrangement of cloacal scales was not observed in any squamate and is distinct from the transverse rows of comparatively large quadrangular scales in crocodylians that extend along the ventral surfaces of the abdomen and tail (Fig. 8B). Despite the difference in the configuration of the lateral lips and dorsal lobe (Vinther et al. 2021), the gross morphology of the vent and surrounding scales in Psittacosaurus—which combines a longitudinally opening vent with a rosette pattern of cloacal scales and transverse rows of quadrangular ventral scales on the ventral tail and abdomen (Figs. 6, 8A, C)—most closely matches that of crocodylians (Fig. 8C–D).

The internal anatomy of the cloaca also differs between crocodylians, squamates, and birds, which correspond to the three cloacal morphotypes (longitudinal, transverse, round/square, respectively; Gadow 1887, Gabe and Saint Girons 1965, King 1981, Oliveira et al. 2004; see DataS1). Therefore, the longitudinal vent of Psittacosaurus potentially implies a crocodylian-like internal anatomy of the cloaca. In archosaurian and lepidosaurian reptiles, the cloaca forms the common opening of the digestive and urogenital tract and consists of a series of chambers—the coprodeum, urodeum, and proctodeum—separated by muscular sphincters and which terminates in the vent (Gabe and Saint Girons 1965, Oliveira et al. 2004). The coprodeum, the most proximal of the chambers, receives waste from the intestines, the urodeum receives products from both the genital and urinary ducts, and the proctodeum houses the male copulatory organ. Squamates follow this general pattern although the copulatory organ—the paired hemipenes—is unique and dorsally situated within the proctodeum (Gadow 1887, Gabe and Saint Girons 1965). In contrast, crocodylians, and some birds possess a single, ventrally-positioned copulatory organ, but the majority of birds lack a phallus entirely (King 1981, Oliveira et al. 2004). Also in contrast to squamates and late-diverging birds (Neognathae), the ureter in crocodylians opens into the coprodeum, rather than the urodeum (Oliveira et al. 2004); a condition also found in some palaeognaths (e.g., Rhea, tinamous; Oliveira et al. 2004). Based solely on the external anatomy of the vent in Psittacosaurus and its similarity to crocodylians, we hypothesise the presence in the former of a muscular, unpaired, and ventrally-positioned copulatory organ (e.g., Sanger et al. 2015) and a ureter that empties into the coprodeum (Oliveira et al. 2004), which is consistent with prior studies based on the extant phylogenetic bracket (Witmer 1995, Isles 2009). Like crocodylians, birds also use internal fertilisation (regardless of the presence of a phallus), which is the presumed method in Psittacosaurus (Isles 2009), although the sex of SMF R 4970 cannot be determined at present (Vinther et al. 2021). The presumably paired oviducts in Psittacosaurus (Sato et al. 2005) would have opened into the urodeum as well.

Skin morphology in ceratopsian dinosaurs.

Ceratopsia is an extremely taxonomically diverse group (> 60 genus-level taxa) of herbivorous ornithischians from the Middle Jurassic to the Late Cretaceous characterized by a toothless and keratin-covered beak and, in most members, a frill extending over the rear of the skull and horns at the level of the cheek, nose and/or eyes (Dodson et al. 2004, Hailu and Dodson 2004, Makovicky 2012, Yu et al. 2020). Despite this diversity, the preserved integument is currently known from a handful of specimens (< 15) and restricted to six ceratopsian genera (Table 2; Fig. 9; see DataS1). Psittacosaurus is the only non-coronosaurian ceratopsian with preserved integument, which has been described or reported in six specimens (including three exquisitely preserved and nearly complete specimens) making it the ceratopsian with the most extensively preserved integument (Table 2; Ji 1999, Mayr et al. 2002, Lingham-Soliar 2008, Lingham-Soliar and Plodowski 2010, Vinther et al. 2016; see DataS1). Within Coronosauria, squamous skin is preserved in the protoceratopsid Protoceratops andrewsi (Brown and Schlaikjer 1940), the centrosaurines Centrosaurus apertus (AMNH FARB 5351, AMNH FARB 5427; Brown 1917; Lull 1933) and Nasutoceratops titusi (UMNH VP 16800; Lund 2010, Lund et al. 2016), and in the chasmosaurines Chasmosaurus belli (CMN 2245, UALVP 52613; Lambe 1914, Sternberg 1925, Lull 1933, Currie et al. 2016) and Triceratops horridus (HMNS PV.1506; Larson et al. 2007; Table 2; see DataS1). Chasmosaurus is the only ceratopsid with skin from both juvenile and adult individuals (Sternberg 1925, Currie et al. 2016).

Table 2

Skin distribution in ceratopsian dinosaurs.
Genus	Specimen	Locality	Formation and age	Body region	Type of integument	Author(s)
Psittacosaurus mongoliensis	AMNH FARB 6260	Red Mesa, Artsa Bogdo, Mongolian Peoples Republic, Asia, Oshih Basin, Mongolia	Öösh Formation; ?Hauterivian	Pes	Reticulate scales	(Sereno 1987)
Psittacosaurus sp.	YFM-R001	Sihetun Village in Beipiao City, western Liaoning Province, China	Jianshangou Bed, Yixian Formation; Upper Barremian - Lower Aptian	Shoulder, forelimb	Hexagonal basement scales	(Ji and Bo 1998, Ji 1999, Glut 2002)
Psittacosaurus sp.	MV 53	Nanjing, Liaoning Province, China	Jehol Biota, Yixian Formation; Upper Barremian - Lower Aptian	Flank	Collagen fibers	(Feduccia et al. 2005, Lingham-Soliar 2008)
Psittacosaurus lujiatunensis	PKUV V105	China	NA; Lower Cretaceous	Hips	Skin	(Li et al. 2014)
Psittacosaurus lujiatunensis	PKUV V1051	China	NA; Lower Cretaceous	Tail + ?	Skin	(Li et al. 2014)
Psittacosaurus sp.	SMF R 497	Jehol deposits of the Liaoning Province; most likely from the Sihetun locality, Beipiao County, Liaoning Province, China	Most likely Jianshangou Bed, Yixian Formation; Barremian - Aptian	Head, neck, shoulder, forelimbs, manus, flank, abdomen, hips, hindlimbs, tail	Quadrangular, rectangular, polygonal, irregular basement scales; reticulate scales; rounded feature scales	(Mayr et al. 2002, 2016, Lingham-Soliar and Plodowski 2010, Vinther et al. 2016, 2021)
Protoceratops andrewsi	AMNH FARB 6418	Shabarakh Usu, Omnogov Province, Mongolia	Bayn Dzak Member; Djadochta Formation; Upper Campanian	Head	Pebbly basement scales	(Brown and Schlaikjer 1940)
Centrosaurus apertus	AMNH FARB 5351	RTMP Quarry 105, Sand Creek; 100 feet below top of beds, north fork of Sand Creek, 12 miles below Steveville, Red Deer River, Alberta, Canada	Dinosaur Park Formation; Upper Campanian	Flank, abdomen?	Polygonal basement scales; dermal plates	(Brown 1917)
Centrosaurus apertus	AMNH FARB 5427	north fork, Sand Creek, Alberta, right bank 50 feet above river Red Deer River, Canada	Oldman Formation; Campanian	Flank	Polygonal basement scales; rounded feature scales	(Brown 1917, Lull 1933)
Chasmosaurus belli	CMN 2245	Chasmosaurus type, Berry Creek, Red Deer River, Alberta, Canada	Dinosaur Park Formation; Upper Campanian	Hips	Polygonal basement scales; rounded feature scales	(Lambe 1914, Sternberg 1925, Lull 1933)
Chasmosaurus belli	UALVP 52613	Quarry Q255 in northeastern part of Dinosaur Provincial Park, Alberta, Canada	Dinosaur Park Formation; Upper Campanian	Flank, hindlimbs	Polygonal basement scales	(Currie et al. 2016)
Nasutoceratops titusi	UMNH VP 16800	Grand Staircase–Escalante National Monument, southern Utah, USA	Kaiparowits Formation; Upper Campanian	Shoulder, forelimb	Triangular basement scales; oval to subcircular and hexagonal feature scales	(Lund 2010, Lund et al. 2016)
Triceratops horridus	HMNS PV.1506	Zerbst Ranch, Converse County, Niobrara (county), Wyoming, USA	Lance Formation; Maastrichtian	Neck, forelimb, flank, abdomen	Polygonal basement scales; Polygonal feature scales with nipple like structures	(Larson et al. 2007)
Triceratops prosus	CMNFV 56508	north side, Frenchman River, Eastend, Saskatchewan, Canada	Frenchman Formation; Maastrichtian	Head	Polygonal basement scales	(McDonald 2018)
Triceratops sp.	?	Jordan, Garfield County, Montana, USA	Hell Creek Formation; Maastrichtian	?	NA	(Happ and Morrow 1997)
Triceratops sp.	?	Montana, USA	Late Cretaceous	Head	?	(Lessem 1989)

The skin of ceratopsians is best represented on the flank, hindlimb and pelvic regions, being preserved in these parts of the body in Centrosaurus (AMNH FARB 5351 [holotype of Monoclonius nasicornis]; AMNH FARB 5427 [holotype of Monoclonius cutleri]), Chasmosaurus (CMN 2245; UALVP 52613), and Triceratops (HMNS PV.1506). Nasutoceratops (UMNH VP 16800) preserves skin on the brachium and shoulder regions, whereas virtually the entire integument is known for Psittacosaurus, including multiple specimens that preserve skin on the flank (MV 53; SMF R 4970), shoulder (SMF R 497; YFM-R001), pedes (AMNH FARB 6260; SMF R 4970) and tail (PKUV V1051; SMF R 4970). Besides Psittacosaurus (SMF R 4970), skin covering the head has only been found in Protoceratops (Czerkas 1997) and Triceratops (CMN FV 56508; J. Mallon, pers. comm. 2021), although these have yet to be formally described. Additional specimens preserving squamous skin in Psittacosaurus (Sereno 1987), Centrosaurus (AMNH FARB 5351), a juvenile Triceratops (Happ and Morrow 1997) and a particularly complete specimen of Triceratops horridus (Larson et al. 2007) have also never been illustrated nor described in detail. Three large sections of skin belonging to the Triceratops specimen (HMNS PV.1506) reported by Larson et al. (2007) are, however, on display at the Houston Museum of Natural Science; our observations on Triceratops integument rely on these specimens, pending a thorough description of the material by Peter Larson and colleagues.

Like many dinosaurs (Coria and Chiappe 2007, Tschopp and Christiansen 2009, Bell 2014, Hendrickx et al. 2022), ceratopsian skin typically consists of subcircular-to-polygonal feature scales surrounded by a network of low and smaller non-overlapping polygonal basement scales separated by narrow interstitial tissue; however, the basement scales are usually relatively larger than in ornithopods and theropods (Fig. 10; see DataS1). Important variations in scale size, shape and pattern also occur between ceratopsian taxa and over different body parts. Psittacosaurus (SMF R 4970) is to our knowledge the only non-ceratopsid ceratopsian with a preserved keratinous horn ‘sheath’, which is ~ 140% larger than the bony core of the jugal horn (see above). Several authors have, however, reported the presence of a horn ‘sheath’ in other ceratopsids. American palaeontologist John Bell Hatcher was the first to report such a discovery in the Triceratops specimen YPM 1821, writing that “a portion of the investing horny material was still in place about the left horn core, though in such a decomposed condition that it was impossible to preserve it.” (Hatcher et al. (1907), p. 32). Likewise, Czerkas (1997) briefly mentioned the probable remains of the outer sheath—consisting of a carbonaceous powdery layer up to two centimetres thick—in a young Triceratops skull. More recently, Happ (2010) reported the discovery of a claystone layer grading from 7 to 33 mm thick and distinct in composition from the bony core in the left postorbital of an adult specimen of Triceratops (SUP9713.0). This mineralized layer, which covers a 1.2–5.3 mm thick outer bone layer composed of compact Haversian bone, is interpreted by Happ (2010) as a replacement of the horn sheath.

Other than Psittacosaurus, skin from the head has not been formally described for any ceratopsian although there are several reports. In Protoceratops (AMNH FARB 6418), a thin, wrinkled layer of matrix covering a large portion of the cranium and mandible was interpreted as skin by Brown and Schlaikjer (1940). Presumably based on the photos published by Brown and Schlaikjer (1940, plate 13), Czerkas (1997) also considered the presence of desiccated and sunken eyelids; however, the presumed integument has since been entirely prepared off the specimen and is now lost. Brown and Schlaikjer’s (1940) plate 13 nevertheless illustrates what appears to be a mummified skull of Protoceratops (Fig. 9B), strongly suggesting a scaly integument of small pebbly scales covered the entire head. The latter can be noticed in some zones of the beak and the nostrils, anterior and ventral to the orbit, and in some parts of the jugal (Fig. 9C–E). Davis (2014, Supplementary Online Material) also reported skin covering the head of a possible Triceratops comprising large circular feature scales surrounded by smaller polygonal basement scales based on a photograph in Lessem (1989, p. 41). However, the photograph is actually from the flank of Chasmosaurus (CMN 2245; Sylvia Czerkas, pers. comm. May 2021). A small piece of skin associated with the frill of the Triceratops specimen CMNFV 56508 (J. Mallon, pers. comm. 2021) reveals that the frill of this taxon, and probably all ceratopsians, were covered with polygonal basement scales. Using osteological and histological correlates in extant amniotes, Hieronymus et al. (2009) showed that several rows of epidermal scales were present on the surface of the cranium in centrosaurine ceratopsids, namely, a median row of shallow scales on the parietal bar (Centrosaurus, Achelousaurus, Pachyrhinosaurus), a series of scales lining the dorsal rim of the orbit and onto the squamosal (Centrosaurus, Einiosaurus), a second row of scales anteroventral to the former on the squamosal (Centrosaurus), and a midline row of epidermal scales between the horny beak and the nasal boss (Pachyrhinosaurus).

Scaly integument from the neck is only know from Psittacosaurus (SMF R 4970). In the Psittacosaurus specimen YFM-R001, the pectoral girdle and forelimb is covered with small (3–5 mm), polygonal (4–6 sided) basement scales and minute (1–2 mm) triangular scales (Ji 1999), although there is no indication of the raised feature scales seen in this area of SMF R 497. Whether this difference is due to intra- or interspecific variation or some other factor is unknown. The hexagonal and triangular scales in YFM-R001 together form a hexagram pattern anterior to the mid-shaft of the humerus (Ji 1999, Fig. 2), identical to that on the posterior part of the brachium and hindlimb of SMF R 497. This pattern is also seen on the brachium of Nasutoceratops, where medium (8–12 mm) hexagonal basement scales are framed by six small (3–4 mm) triangular scales (Lund 2010, Lund et al. 2016; Fig. 9F). As scales with a hexagram arrangement occur in Psittacosaurus (SMF R 497, brachium, inner thigh; YFM-R001, brachium) and Nasutoceratops (brachium), such a pattern might have been common on the limbs of ceratopsians. It is worth noting that the hexagram pattern differs from the multi-pointed feature scales seen in some hadrosaurids (Bell 2012) and that this appears to be an integumentary design unique to ceratopsians. Other types of scales from the shoulder region include proximodistally elongate polygonal or rounded-polygonal (3–6 sided) scales in SMF R 497, and, in Nasutoceratops, medium to large (10‒20 mm) subcircular, elliptical or rhomboid basement scales arranged in irregular rows and surrounded by smaller (5‒10 mm) subcircular to triangular scales (Lund 2010, Lund et al. 2016). Nasutoceratops also shows an array of variably-sized (2–8 mm), tightly-packed, oval-to-subcircular scales arranged in irregular rows anterior to the humeral head (Lund 2010, Lund et al. 2016; Fig. 9G). The integument on the rest of the forelimb and manus of ceratopsians is only known in Psittacosaurus (SMF R 4970). Reticulate scales on the palmar surface of the manus are only found in SMF R 4970; they are not known from other ceratopsian body fossils or tracks.

Scales over the flank strongly vary among ceratopsians, but all involve feature scales set within a basement of smaller scales. The feature scales are small (3–4 mm), low, and circular-to-irregular in Psittacosaurus (SMF R 4970); larger (50–80 mm), flat or weakly convex, and subcircular-to-elliptical in both Centrosaurus (AMNH FARB 5427; Brown 1917) and Chasmosaurus (CMN 2245, UALVP 52613; Sternberg 1925; Fig. 9J), and; large (> 100 mm), hexagonal-to-heptagonal, and characterized by a centrally-positioned or weakly off-centre nipple-like structure in Triceratops (HMNS PV.1506; Larson et al. 2007, Bell and Hendrickx 2021; Fig. 9K). Unlike the truncated-cone or conical feature scales of Psittacosaurus and other dinosaurs, such as the abelisaurid Carnotaurus (Hendrickx and Bell 2021), the nipple-like structure of Triceratops, which corresponds to an elevated volcano-like prominence (~ 1‒3 cm in height), occupies only half of the feature scale surface, the rest of the feature scale being flat (Fig. 9K). In all of these taxa (Psittacosaurus, Carnotaurus, Triceratops), it is unlikely that the feature scale bore a spine or a ‘bristle’-like structure—similar to those seen on the tail of Psittacosaurus—, although bristle-like projections are present on some scales in the early-branching neornithischian Kulindadromeus (Godefroit et al. 2014, 2020). No discernible pattern in the arrangement of the feature scales can be observed in Psittacosaurus (SMF R 4970) or Centrosaurus (AMNH FARB 5427) given the preservation of only a single feature scale in the latter. The feature scales from the adult Chasmosaurus (CMN 2245) are, however, arranged in irregular, longitudinal rows and are spaced 5–10 cm apart (Sternberg 1925; Fig. 9J). They are delimited by wide and deep interstitial tissue (the “circumscribing groove” of Sternberg [1925]), which is also seen on the single feature scale of Centrosaurus (Brown 1917). In Chasmosaurus (CMN 2245), the general arrangement of feature scales remains consistent over the large patch of preserved skin, but scale diameter decreases ventrally (Sternberg 1925). The polygonal feature scales of Triceratops also do not seem to form any particular pattern but, unlike Chasmosaurus, they are more regularly spaced (~ 15‒20 cm) and less variable in size. The basement scales on the flank of ceratopsians form a mosaic of polygonal scales varying in size, shape and elongation. They are, however, typically pentagonal or hexagonal and delimited by deep interstitial tissues (Fig. 9H–K). The basement scales are flat or weakly convex in Protoceratops, Centrosaurus (Fig. 9H) and Chasmosaurus (Fig. 9I‒J) whereas those of Triceratops are nearly flat-to-strongly convex and only slightly smaller than the feature scales (Fig. 9K). The basement scales of centrosaurines are significantly smaller (up to 10 mm and 25 mm in Centrosaurus and Chasmosaurus, respectively; Fig. 9H, J) than those of Triceratops which, with a diameter of up to 90 mm (Fig. 9K), has the largest basement scales among dinosaurs (Fig. 10). The number of basement scales delimiting the largest feature scales also varies from more than ten scales in Chasmosaurus (Fig. 9J) to typically seven or eight in Triceratops (Fig. 9K).

Psittacosaurus is to our knowledge the only ceratopsian that preserves skin from the hindlimb and tail, as well as details of the cloaca and ischial callosity (Vinther et al. 2021; this paper). Skin is also preserve in the tail region of Psittacosaurus lujiatunensis PKUP V1051 (Li et al. 2014) but its integument was neither described nor illustrated in detail and it is unknown whether the tail of SMF R 4970 and PKUP V1051 shared the same scale morphology and arrangement.

The Frankfurt specimen of Psittacosaurus retains the highest percentage body covering and best-preserved squamous skin of any dinosaur and is therefore central to the understanding of dinosaur appearance and biology. Although tail ‘bristles’ in Psittacosaurus were described nearly two decades ago (Mayr et al. 2002), LSF has afforded a far more detailed view of its integument, including new information on the anatomy and homology of the tail ‘bristles’ as well as providing evidence for countershading in this taxon (Mayr et al. 2016, Vinther et al. 2016). A thorough analysis of the specimen under LSF here reveals the full complexity and variation in the squamous integument of Psittacosaurus. Such complexity is in line with the emerging picture from other squamous-skinned ornithischians and saurischians, and which deviates from the over-simplified ‘scaly reptile’ image of many dinosaurs (Bell 2012, Bell and Hendrickx 2020, 2021, Gallagher et al. 2021, Hendrickx and Bell 2021, Hendrickx et al. 2022, Pittman et al. in press). Ironically, complexity in both architecture and function of epidermal scales is a commonality shared between dinosaurs and extant sauropsids (e.g., Rutland et al. 2019, Höfling and Abourachid 2021), although the potential functionality of various scale types is only now being explored in the former (Bell and Hendrickx 2020, 2021).

LSF provides remarkable resolution of the scales of SMF R 4970. In particular, new details are revealed regarding the keratinous jugal covering, the ischial callosity, feature scales on the mid-distal tail, and the arthral arrangement of the digital pads. The cloaca (Vinther et al. 2021) is revealed here to have had a longitudinal vent, a similarity it shares only with modern crocodylians and which implies similar cloacal anatomy in Psittacosaurus that combines a ventrally-positioned copulatory organ (Isles 2009), and a decoupled ureter that empties into the coprodeum. Other crocodile-like integumentary features include quadrangular and transversely-banded abdominal and caudal scales on the ventral part of the animal. The jugal horn was apparently covered dorsally by a sheet-like keratinous covering, which differs from earlier reconstructions (e.g., Vinther et al. 2016) but which was potentially variable between species and life stages.

Compared to other ornithischians (e.g., hadrosaurids), few ceratopsians are known to preserve skin and even fewer have been formally described. Nevertheless, some patterns are emerging. A hexagram arrangement of scales present on the limbs of Psittacosaurus and Nasutoceratops is, at this stage, a unique ceratopsian feature. In all ceratopsians where skin is preserved, the flank bears feature scales set into a matrix of smaller basement scales. However, Triceratops is unique in having polygonal feature scales that are only slightly larger than the basement scales, and which have a central, nipple-like protrusion. Interspecific differences in the architecture of both feature scales and basement scales support early comments on the taxonomic utility of scale patterns in Ceratopsia (Sternberg 1925) and dinosaurs more broadly (e.g., Lull and Wright 1942, Czerkas 1997, Bell 2012, 2014, Hendrickx et al. 2022).

Acknowledgements.We thank Rainer Brocke and Olaf Vogel (SMF) for specimen access; K. Vernes (UNE) for access to comparative collections;Jordan Mallon (CMN) forinformation onTriceratopsintegument,and;Carl Mehling (AMNH), David C. Evans (ROM),Eric K. Lund (NCM),Marshal A. Fazio, Victoria Arbour (RBCM) and Albert Prieto-Marquez (Catalan Institute of Paleontology Miquel Crusafont) for sharing photos of the skin of Centrosaurus, Chasmosaurus, Nasutoceratops,Triceratops, Liaoningosaurus and Edmontosaurus, respectively.We especially thank Philip J. Currie (University of Alberta) for sharing numerous photos of the skin of Triceratops and the juvenile and adult individuals of Chasmosaurus. Waylon Rowley is warmly thanked for sharing Lessem (1989)’s article from Discover. The authors additionally thank Eydie Rojas (HMNS) for providing the specimen number of the Triceratops skinat the HMNS. C.H. is supported by the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and Agencia Nacional de Promoción Científica y Tecnológica, Argentina (Beca Pos-doctoral CONICET Legajo 181417). M.P. and T.G.K. are supported by a RAE Improvement Fund of the Faculty of Science, The University of Hong Kong (HKU) and HKU MOOC course Dinosaur Ecosystems.

Averianov, A. O., A. V. Voronkevich, S. V. Leshchinskiy, and A. V. Fayngertz. 2006. A ceratopsian dinosaur Psittacosaurus sibiricus from the Early Cretaceous of West Siberia, Russia and its phylogenetic relationships. Journal of Systematic Palaeontology 4:359–395.
Bell, P. R. 2012. Standardized terminology and potential taxonomic utility for hadrosaurid skin impressions: a case study for Saurolophus from Canada and Mongolia. PLoS ONE 7:e31295.
Bell, P. R. 2014. A review of hadrosaurid skin impressions. Pages 572–590 in D. A. Eberth and D. C. Evans, editors. Hadrosaurs. Indiana University Press, Bloomington, Indiana.
Bell, P. R., and C. Hendrickx. 2020. Crocodile-like sensory scales in a Late Jurassic theropod dinosaur. Current Biology 30:R1068–R1070.
Bell, P. R., and C. Hendrickx. 2021. Epidermal complexity in the theropod dinosaur Juravenator from the Late Jurassic of Germany. Palaeontology 64:203–223.
Brown, B. 1916. Corythosaurus casuarius: skeleton, musculature and epidermis. Bulletin of the American Museum of Natural History 35:709–716.
Brown, B. 1917. A complete skeleton of the horned dinosaur Monoclonius, and description of a second skeleton showing skin impressions. Bulletin of the American Museum of Natural History 37:298–306.
Brown, B., and E. M. Schlaikjer. 1940. The structure and relationships of Protoceratops. Annals of the New York Academy of Sciences 40:133–266.
Brown, C. M. 2017. An exceptionally preserved armored dinosaur reveals the morphology and allometry of osteoderms and their horny epidermal coverings. PeerJ 5:e4066.
Brown, C. M., and D. M. Henderson. 2015. A new horned dinosaur reveals convergent evolution in cranial ornamentation in Ceratopsidae. Current Biology 25:1641–1648.
Chang, S., H. Zhang, P. R. Renne, and Y. Fang. 2009. High-precision 40Ar/39Ar age for the Jehol Biota. Palaeogeography, Palaeoclimatology, Palaeoecology 280:94–104.
Chang, S.-C., K.-Q. Gao, C.-F. Zhou, and F. Jourdan. 2017. New chronostratigraphic constraints on the Yixian Formation with implications for the Jehol Biota. Palaeogeography, Palaeoclimatology, Palaeoecology 487:399–406.
Chiappe, L. M. 2007. Glorified Dinosaurs: The Origin and Early Evolution of Birds. 1 edition. Wiley-Liss, Hoboken, NJ.
Chiappe, L. M., R. A. Coria, L. Dingus, F. Jackson, A. Chinsamy, and M. Fox. 1998. Sauropod dinosaur embryos from the Late Cretaceous of Patagonia. Nature 396:258–261.
Chiappe, L. M., and L. M. Witmer. 2002. Mesozoic Birds: Above the Heads of Dinosaurs. University of California Press.
Coria, R. A., and L. M. Chiappe. 2007. Embryonic skin from Late Cretaceous sauropods (Dinosauria) of Auca Mahuevo, Patagonia, Argentina. Journal of Paleontology 81:1528–1532.
Cuesta, E. 2017. Concavenator corcovatus (Theropoda, Dinosauria) from Las Hoyas fossil site (Early Cretaceous, Cuenca, Spain): taphonomic, phylogenetic and morphofunctional analyses. PhD Thesis, Universidad Autónoma de Madrid.
Cuesta, E., I. Díaz-Martínez, F. Ortega, and J. L. Sanz. 2015. Did all theropods have chicken-like feet? First evidence of a non-avian dinosaur podotheca. Cretaceous Research 56:53–59.
Currie, P. J., R. B. Holmes, M. J. Ryan, and C. Coy. 2016. A juvenile chasmosaurine ceratopsid (Dinosauria, Ornithischia) from the Dinosaur Park Formation, Alberta, Canada. Journal of Vertebrate Paleontology 36:e1048348.
Czerkas, S. A. 1997. Skin. Pages 669–675 in P. J. Currie and K. Padian, editors. Encyclopedia of Dinosaurs. Academic Press, San Diego, California.
Davis, M. 2014. Census of dinosaur skin reveals lithology may not be the most important factor in increased preservation of hadrosaurid skin. Acta Palaeontologica Polonica 59:601–605.
Dodson, P., C. A. Forster, and S. D. Sampson. 2004. Ceratopsidae. Pages 494–513 in D. B. Weishampel, P. Dodson, and H. Osmólska, editors. The Dinosauria. Second Edition. University of California Press, Berkeley, California.
Erickson, G. M., P. J. Makovicky, B. D. Inouye, C.-F. Zhou, and K.-Q. Gao. 2009. A life table for Psittacosaurus lujiatunensis: Initial insights into ornithischian dinosaur population biology. The Anatomical Record 292:1514–1521.
Farke, A. A. 2006. Cranial osteology and phylogenetic relationships of the chasmosaurine ceratopsid Torosaurus latus. Pages 235–257 in K. Carpenter, editor. Horns and Beaks: Ceratopsian and Ornithopod Dinosaurs. Indiana University Press, Bloomington.
Feduccia, A., T. Lingham-Soliar, and J. R. Hinchliffe. 2005. Do feathered dinosaurs exist? Testing the hypothesis on neontological and paleontological evidence. Journal of Morphology 266:125–166.
Gabe, M., and H. Saint Girons. 1965. Contribution a la morphologie comparée du cloaque et des glandes épidermoïdes de la region cloacale chez les lépidosauriens. Mémoires du Muséum national d’Histoire naturelle, Sér. A – Zoologie 33:149–292.
Gadow, H. 1887. Remarks on the cloaca and on the copulatory organs of the Amniota. Philosophical Transactions of the Royal Society of London. B 178:5–37.
Gallagher, T., J. Poole, and J. P. Schein. 2021. Evidence of integumentary scale diversity in the late Jurassic sauropod Diplodocus sp. from the Mother’s Day Quarry, Montana. PeerJ 9:e11202.
Glut, D. F. 2002. Dinosaurs: The Encyclopedia, Supplement 2. Jefferson, N.C.
Godefroit, P., S. M. Sinitsa, A. Cincotta, M. E. McNamara, S. A. Reshetova, and D. Dhouailly. 2020. Integumentary structures in Kulindadromeus zabaikalicus, a basal neornithischian dinosaur from the Jurassic of Siberia. Pages 47–65 in C. Foth and O. W. M. Rauhut, editors. The Evolution of Feathers: From Their Origin to the Present. Springer International Publishing, Cham.
Godefroit, P., S. M. Sinitsa, D. Dhouailly, Y. L. Bolotsky, A. V. Sizov, M. E. McNamara, M. J. Benton, and P. Spagna. 2014. A Jurassic ornithischian dinosaur from Siberia with both feathers and scales. Science 345:451–455.
Hailu, H., and P. Dodson. 2004. Basal Ceratopsia. Pages 478–493 in D. Weishampel, P. Dodson, and H. Osmólska, editors. The Dinosauria. Second Edition. University of California Press, Berkeley, California.
Happ, J. W. 2010. New evidence regarding the structure and function of the horns in Triceratops (Dinosauris: Caratopsidae). Pages 271–281 in M. J. Ryan, B. J. Chinnery-Algeier, and D. A. Eberth, editors. New Perspectives on Horned Dinosaurs: The Royal Tyrrell Museum Ceratopsian Symposium. Indiana University Press Bloomington.
Happ, J. W., and C. M. Morrow. 1997. Bone modification of subadult Triceratops (Dinosauria: Ceratopsidae) by crocodilian and theropod dining. Page 51A Abstract of Papers. Fifty-Seventh Annual Meeting, Society of Vertebrate Paleontology. Journal of Vertebrate Paleontology, Chicago, Illinois.
Hatcher, J. B., O. C. Marsh, and R. S. Lull. 1907. The Ceratopsia (Monographs of the United States Geological Survey XLIX). United States Geological Survey.
Hedrick, B. P., and P. Dodson. 2013. Lujiatun psittacosaurids: understanding individual and taphonomic variation using 3D geometric morphometrics. PLOS ONE 8:e69265.
Hendrickx, C., and P. R. Bell. 2021. The scaly skin of the abelisaurid Carnotaurus sastrei (Theropoda: Ceratosauria) from the Upper Cretaceous of Patagonia. Cretaceous Research 128:104994.
Hendrickx, C., P. R. Bell, M. Pittman, A. R. C. Milner, E. Cuesta, J. O’Connor, M. A. Loewen, P. J. Currie, O. Mateus, T. G. Kaye, and R. Delcourt. 2022. Morphology and distribution of scales, dermal ossifications, and other non-feather integumentary structures in non-avialan theropod dinosaurs. Biological Reviews. https://doi.org/10.1111/brv.12829
Hieronymus, T. L., L. M. Witmer, D. H. Tanke, and P. J. Currie. 2009. The facial integument of centrosaurine ceratopsids: morphological and histological correlates of novel skin structures. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 292:1370–1396.
Höfling, E., and A. Abourachid. 2021. The skin of birds’ feet: Morphological adaptations of the plantar surface. Journal of Morphology 282:88–97.
Isles, T. E. 2009. The socio-sexual behaviour of extant archosaurs: implications for understanding dinosaur behaviour. Historical Biology 21:139–214.
Ji, S. 1999. Initial report of fossil psittacosaurid skin impression from the uppermost Jurassic of Sihetun, northeastern China. Earth Science (Chikyu Kagaku) 53:314–316.
Ji, S. A., and H. C. Bo. 1998. Discovery of the psittacosaurid skin impressions and its significance. Geological Review 44:603–606.
Kaye, T. G., A. R. Falk, M. Pittman, P. C. Sereno, L. D. Martin, D. A. Burnham, E. Gong, X. Xu, and Y. Wang. 2015. Laser-Stimulated Fluorescence in Paleontology. PLOS ONE 10:e0125923.
King, A. S. 1981. Phallus. Pages 107–147 in A. S. King and J. McLelland, editors. Form and Function in Birds. London: Academic Press, London, UK.
Kundrát, M. 2004. When did theropods become feathered?—evidence for pre-archaeopteryx feathery appendages. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 302B:355–364.
Lambe, L. M. 1914. On the fore-limb of a carnivorous dinosaur from the Belly River Formation of Alberta, and a new genus of Ceratopsia from the same horizon, with remarks on the integument of some Cretaceous herbivorous dinosaurs. The Ottawa Naturalist 27:129–135.
Larson, P., M. Larson, C. Ott, and B. Robert. 2007. Skinning a Triceratops. Page 104A Journal of Vertebrate Paleontology.
Lehman, T. M. 1998. A gigantic skull and skeleton of the horned dinosaur Pentaceratops sternbergi from New Mexico. Journal of Paleontology 72:894–906.
Lessem, D. 1989. Skinning the Dinosaur. Discover 10:38–44.
Li, Q., J. A. Clarke, K.-Q. Gao, C.-F. Zhou, Q. Meng, D. Li, L. D’Alba, and M. D. Shawkey. 2014. Melanosome evolution indicates a key physiological shift within feathered dinosaurs. Nature 507:350–353.
Lingham-Soliar, T. 2008. A unique cross section through the skin of the dinosaur Psittacosaurus from China showing a complex fibre architecture. Proceedings of the Royal Society B: Biological Sciences 275:775–780.
Lingham-Soliar, T., and G. Plodowski. 2010. The integument of Psittacosaurus from Liaoning Province, China: taphonomy, epidermal patterns and color of a ceratopsian dinosaur. Naturwissenschaften 97:479–486.
Lockley, M., M. Matsukawa, and L. Jianjun. 2003. Crouching theropods in taxonomic jungles: ichnological and ichnotaxonomic investigations of footprints with metatarsal and ischial impressions. Ichnos 10:169–177.
Lull, R. S. 1933. A revision of the Ceratopsia or horned dinosaurs. Peabody Museum of Natural History Bulletin 3:1–175.
Lull, R. S., and N. E. Wright. 1942. Hadrosaurian dinosaurs of North America. The Geological Society of America 40:1–270.
Lund, E. K. 2010. Nasutuceratops titusi, a new basal centrosaurine dinosaur (Ornithischia: Ceratopsidae) from the Upper Cretaceous Kaiparowits Formation, southern Utah. MSc. Dissertation, The University of Utah, Salt Lake City, Utah, USA.
Lund, E. K., S. D. Sampson, and M. A. Loewen. 2016. Nasutoceratops titusi (Ornithischia, Ceratopsidae), a basal centrosaurine ceratopsid from the Kaiparowits Formation, southern Utah. Journal of Vertebrate Paleontology 36:e1054936.
Makovicky, P. J. 2012. Marginocephalia. Pages 527–549 in M. K. Brett-Surman, T. R. J. Holtz, and J. O. Farlow, editors. The Complete Dinosaur, Second Edition. Indiana University Press, Bloomington, Indiana.
Mantell, G. A. 1852. On the structure of the Iguanodon, and on the fauna and flora of the Wealden Formation. Notice Proceedings, Royal Institute of Great Britain 1:141–146.
Mayr, G., S. D. Peters, G. Plodowski, and O. Vogel. 2002. Bristle-like integumentary structures at the tail of the horned dinosaur Psittacosaurus. Naturwissenschaften 89:361–365.
Mayr, G., M. Pittman, E. Saitta, T. G. Kaye, and J. Vinther. 2016. Structure and homology of Psittacosaurus tail bristles. Palaeontology 59:793–802.
McDonald, A. 2018, December 12. Triceratops skull delivers a Wow! of a Christmas gift.
Milàn, J. 2006. Variations in the morphology of emu (Dromaius novaehollandiae) tracks reflecting differences in walking pattern and substrate consistency: ichnotaxonomic implications. Palaeontology 49:405–420.
Milner, A. R. C., J. D. Harris, M. G. Lockley, J. I. Kirkland, and N. A. Matthews. 2009. Bird-like anatomy, posture, and behavior revealed by an Early Jurassic theropod dinosaur resting trace. PLOS ONE 4:e4591.
Napoli, J. G., T. Hunt, G. M. Erickson, and M. A. Norell. 2019. Psittacosaurus amitabha, a new species of ceratopsian dinosaur from the Ondai Sayr locality, Central Mongolia. American Museum Novitates 2019:1–36.
Oliveira, C. A., R. M. Silva, M. M. Santos, and G. A. B. Mahecha. 2004. Location of the ureteral openings in the cloacas of tinamous, some ratite birds, and crocodilians: A primitive character. Journal of Morphology 260:234–246.
Pittman, M. D., N. J. Enriquez, P. R. Bell, T. G. Kaye, and P. Upchurch. in press. Newly detected skin data from historic sauropod Haestasaurus and review of sauropod skin morphology suggests Early Jurassic origin of skin papillae. Communications Biology.
Pu, H., H. Chang, J. Lü, Y. Wu, L. Xu, J. Zhang, and S. Jia. 2013. A new juvenile specimen of Sapeornis (Pygostylia: Aves) from the Lower Cretaceous of Northeast China and allometric scaling of this basal bird. Paleontological Research 17:27–38.
Rainforth, E. C. 2003. Revision and re-evaluation of the Early Jurassic dinosaurian ichnogenus Otozoum. Palaeontology 46:803–838.
Rutland, C. S., P. Cigler, and V. D. Kubale. 2019. Reptilian skin and its special histological structures. Pages 135–156 in C. S. Rutland and V. D. Kubale, editors. Veterinary Anatomy and Physiology. IntechOpen. InTech, London, UK.
Ryan, M. J., R. Holmes, and A. P. Russell. 2007. A revision of the late Campanian centrosaurine ceratopsid genus Styracosaurus from the Western Interior of North America. Journal of Vertebrate Paleontology 27:944–962.
Sanger, T. J., M. L. Gredler, and M. J. Cohn. 2015. Resurrecting embryos of the tuatara, Sphenodon punctatus, to resolve vertebrate phallus evolution. Biology Letters 11:20150694.
Sato, T., Y. Cheng, X. Wu, D. K. Zelenitsky, and Y. Hsiao. 2005. A pair of shelled eggs inside a female dinosaur. Science 308:375–375.
Scannella, J. B., D. W. Fowler, M. B. Goodwin, and J. R. Horner. 2014. Evolutionary trends in Triceratops from the Hell Creek Formation, Montana. Proceedings of the National Academy of Sciences 111:10245–10250.
Sereno, P. C. 1987. The ornithischian dinosaur Psittacosaurus from the Lower Cretaceous of Asia and the relationships of the Ceratopsia. Ph.D. Dissertation, Columbia University, New York, New York.
Sereno, P. C. 2010. Taxonomy, cranial morphology, and relationships of parrot-beaked dinosaurs (Ceratopsia: Psittacosaurus). Pages 21–58 New perspectives on horned dinosaurs: The Royal Tyrrell Museum ceratopsian symposium. Indiana University Press Bloomington.
Sereno, P. C., and C. Shichin. 1988. Psittacosaurus xinjiangensis (Ornithischia: Ceratopsia), a new psittacosaur from the Lower Cretaceous of northwestern China. Journal of Vertebrate Paleontology 8:353–365.
Sereno, P. C., C. Shichin, C. Zhengwu, and R. Chenggang. 1988. Psittacosaurus meileyingensis (Ornithischia: Ceratopsia), a new psittacosaur from the Lower Cretaceous of northeastern China. Journal of Vertebrate Paleontology 8:366–377.
Sereno, P. C., Z. Xijin, and T. Lin. 2010. A new psittacosaur from Inner Mongolia and the parrot-like structure and function of the psittacosaur skull. Proceedings of the Royal Society B: Biological Sciences 277:199–209.
Smith, J. B., and J. O. Farlow. 2003. Osteometric approaches to trackmaker assignment for the Newark Supergroup. Pages 273–292 in P. M. LeTourneau and P. E. Olsen, editors. The Great Rift Valleys of Pangea in Eastern North America: Sedimentology, Stratigraphy, and Paleontology. Columbia University Press.
Soulé, M., and W. C. Kerfoot. 1972. On the climatic determination of scale size in a lizard. Systematic Biology 21:97–105.
Sternberg, C. M. 1925. Integument of Chasmosaurus belli. Canadian Field Naturalist 39:108–110.
Tschopp, E., and N. A. Christiansen. 2009. Stegosaur skin impressions from the Howe Quarry: morphology and preservation. Page 5 Abstracts of the Scientific Meeting at the Sauriermuseum Aathal. Sauriermuseum Aathal, Aathal, Switzerland.
Upchurch, P., P. D. Mannion, and M. P. Taylor. 2015. The anatomy and phylogenetic relationships of “Pelorosaurus"becklesii (Neosauropoda, Macronaria) from the Early Cretaceous of England. PLOS ONE 10:e0125819.
Vinther, J., R. Nicholls, and D. A. Kelly. 2021. A cloacal opening in a non-avian dinosaur. Current Biology 31:R182–R183.
Vinther, J., R. Nicholls, S. Lautenschlager, M. Pittman, T. G. Kaye, E. Rayfield, G. Mayr, and I. C. Cuthill. 2016. 3D camouflage in an ornithischian dinosaur. Current Biology 26:2456–2462.
Wang, X., M. Pittman, X. Zheng, T. G. Kaye, A. R. Falk, S. A. Hartman, and X. Xu. 2017. Basal paravian functional anatomy illuminated by high-detail body outline. Nature Communications 8:14576.
Witmer, L. M. 1995. The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. Functional morphology in vertebrate paleontology 1:19–33.
Xu, X., X.-L. Wang, and H.-L. You. 2001. A juvenile ankylosaur from China. Naturwissenschaften 88:297–300.
You, H.-L., K. Tanoue, and P. Dodson. 2008. New data on cranial anatomy of the ceratopsian dinosaur Psittacosaurus major. Acta Palaeontologica Polonica 53:183–196.
Yu, C., A. Prieto-Marquez, T. Chinzorig, Z. Badamkhatan, and M. Norell. 2020. A neoceratopsian dinosaur from the early Cretaceous of Mongolia and the early evolution of Ceratopsia. Communications Biology 3:1–8.
Zhao, Q., M. J. Benton, C. Sullivan, M. P. Sander, and X. Xu. 2013. Histology and postural change during the growth of the ceratopsian dinosaur Psittacosaurus lujiatunensis. Nature Communications 4:2079.

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The Exquisitely Preserved Dinosaur Skin of Psittacosaurus and the Scaly Skin of Ceratopsian Dinosaurs

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Abstract

Figures

Introduction

Material And Methods

Age of the Individual

Terminology, taxonomy and horn measurements

Results

Head and neck

Shoulder and forelimbs

Trunk and abdomen

Hindlimbs

Tail and cloaca

Discussion

Keratinous jugal horn

Ischial callosity

Caudal feature scales

Digital pads

Cloaca

Conclusions

Declarations

References

Additional Declarations

Supplementary Files

Status:

Journal Publication

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