Protoceratops
Protoceratops | |
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Mounted P. andrewsi skeleton, Wyoming Dinosaur Center | |
Scientific classification | |
Domain: | Eukaryota |
Kingdom: | Animalia |
Phylum: | Chordata |
Clade: | Dinosauria |
Clade: | †Ornithischia |
Clade: | †Ceratopsia |
Parvorder: | † Coronosauria
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Family: | †Protoceratopsidae |
Genus: | †Protoceratops Gregory , 1923
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Type species | |
†Protoceratops andrewsi Granger & Gregory, 1923
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Other species | |
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Protoceratops (
Protoceratops were small ceratopsians, up to 2–2.5 m (6.6–8.2 ft) long and around 62–104 kg (137–229 lb) in body mass. While adults were largely
Protoceratops, like many other ceratopsians, were
History of discovery
In 1900
In 1923 the expedition prospected the Flaming Cliffs again, this time discovering even more specimens of Protoceratops and also the first remains of
After spending much of 1924 making plans for the next fieldwork seasons, in 1925 Andrews and team explored the Flaming Cliffs yet again. During this year more eggs and nests were collected, alongside well-preserved and complete specimens of Protoceratops. By this time, Protoceratops had become one of the most abundant dinosaurs of the region with more than 100 specimens known, including skulls and skeletons of multiple individuals at different growth stages. Though more remains of Protoceratops were collected in later years of the expeditions, they were most abundant in the 1922 to 1925 seasons.[3][6] Gregory and Charles C. Mook published another description of Protoceratops in 1925, discussing its anatomy and relationships. Thanks to the large collection of skulls found in the expeditions, they concluded that Protoceratops represented a ceratopsian more primitive than ceratopsids and not an ankylosaur-ceratopsian ancestor.[7] In 1940, Barnum Brown and Erich Maren Schlaikjer described the anatomy of P. andrewsi in extensive detail using newly prepared specimens from the Asiatic expeditions.[6]
In 1963, the Mongolian paleontologist Demberelyin Dashzeveg reported the discovery of a new fossiliferous locality of the Djadokhta Formation: Tugriken Shireh. Like the neighbouring Bayn Dzak, this new locality contained an abundance of Protoceratops fossils.[8] During the 1960s to 1970s, Polish-Mongolian and Russian-Mongolian paleontological expeditions collected new, partial to complete specimens of Protoceratops at this locality, making this dinosaur species a common occurrence in Tugriken Shireh.[9][10][11] Since its discovery, the Tugriken Shireh locality has yielded some of the most significant specimens of Protoceratops, such as the Fighting Dinosaurs,[9] in situ individuals—a preservation condition also known as "standing" individuals or specimens in some cases—,[12] authentic nests,[13] and small herd-like groups.[14] Specimens from this locality are usually found in articulation, suggesting possible mass mortality events.[12]
Species and synonyms
Protoceratopsid remains were recovered in the 1970s from the Khulsan locality of the
In 2001 Oliver Lambert with colleagues named a new and distinct species of Protoceratops, P. hellenikorhinus. The first known remains of P. hellenikorhinus were collected from the Bayan Mandahu locality of the Bayan Mandahu Formation, Inner Mongolia, in 1995 and 1996 during Sino-Belgian paleontological expeditions. The holotype (IMM 95BM1/1) and paratype (IMM 96BM1/4) specimens consist of large skulls lacking body remains. The holotype skull was found facing upwards, a pose that has been reported in Protoceratops specimens from Tugriken Shireh. The specific name, hellenikorhinus, is derived from Greek hellenikos (meaning Greek) and rhis (meaning nose) in reference to its broad and angular snout, which is reminiscent of the straight profiles of Greek sculptures.[20] In 2017 abundant protoceratopsid material was reported from Alxa near Bayan Mandahu,[21] and it may be referable to P. hellenikorhinus.[19]
Eggs and nests
As part of the Third Central Asiatic Expedition of 1923, Andrews and team discovered the holotype specimen of
In 1994 the Russian paleontologist Konstantin E. Mikhailov named the new oogenus
However, also during 1994, Norell and colleagues reported and briefly described a fossilized
Nevertheless, in 2011 an authentic nest of Protoceratops was reported and described by David E. Fastovsky and colleagues. The nest (MPC-D 100/530) containing 15 articulated juveniles was collected from the Tugriken Shireh locality of the Djadokhta Formation during the work of Mongolian-Japanese paleontological expeditions.[13] Gregory M. Erickson and team in 2017 reported an embryo-bearing egg clutch (MPC-D 100/1021) of Protoceratops from the also fossiliferous Ukhaa Tolgod locality, discovered during paleontological expeditions of the American Museum of Natural History and Mongolian Academy of Sciences. This clutch comprises at least 12 eggs and embryos with only 6 embryos preserving nearly complete skeletons.[31] Norell with colleagues in 2020 examined fossilized remains around the eggs of this clutch which indicate a soft-shelled composition.[32]
Fighting Dinosaurs
The Fighting Dinosaurs specimen preserves a Protoceratops (MPC-D 100/512) and Velociraptor (MPC-D 100/25) fossilized in combat and provides an important window regarding direct evidence of predator-prey behavior in non-avian dinosaurs.[9][33] In the 1960s and early 1970s, many Polish-Mongolian paleontological expeditions were conducted to the Gobi Desert with the objective of fossil findings. In 1971, the expedition explored several localities of the Djadokhta and Nemegt formations. On August 3 several fossils of Protoceratops and Velociraptor were found including a block containing two of them at the Tugriken Shire locality (Djadokhta Formation) during fieldworks of the expedition. The individuals of this block were identified as a P. andrewsi and V. mongoliensis. Although it was not fully understood the conditions surrounding their burial, it was clear that they died simultaneously in struggle.[9]
The specimen shortly became notorious and was nicknamed the Fighting Dinosaurs. It has been examined and studied by numerous researchers and paleontologists, debating on how the animals got buried and preserved altogether. Though a drowning scenario has been proposed by Barsbold,[33] such hypothesis is considered unlikely given the arid paleoenvironments or settings of the Djadokhta Formation. It is generally accepted that they were buried alive by either a collapsed dune or sandstorm.[34][35][36]
Skin impressions and footprints
During the Third Central Asiatic Expedition in 1923, a nearly complete Protoceratops skeleton (specimen AMNH 6418) was collected at the Flaming Cliffs. Unlike other specimens, it was discovered in a rolled-up position with its
The potential importance of these remains were not recognized and given attention, and by 2020 the specimen has already been completely prepared losing all traces of this skin-like layer. Some elements were damaged in the process such as the rostrum.[37] In 2022 Phil R. Bell and colleagues briefly described these potential soft tissues based on the photographs provided by Brown and Schlaikjer, as well as other ceratopsian soft tissues.[38] However, although the initial perception was that the entire skin-like layer had been removed, photographs shared by Czepiński during the same year have revealed that the right side of the skull remains intact, retaining much of this layer and pending further analysis.[37]
Also from the context of the Polish-Mongolian paleontological expeditions, in 1965 an articulated subadult Protoceratops skeleton (specimen ZPAL Mg D-II/3) was collected from the Bayn Dzak locality of the Djadokhta Formation. In the 2000s during the preparation of the specimen, a fossilized cast of a four-toed digitigrade footprint was found below the pelvic girdle. This footprint was described in 2012 by Grzegorz Niedźwiedzki and colleagues who considered it to represent one of the first reported finds of a dinosaur footprint in association with an articulated skeleton, and also the first one reported for Protoceratops.[39] The limb elements of the skeleton of ZPAL Mg D-II/3 were described in 2019 by paleontologists Justyna Słowiak, Victor S. Tereshchenko and Łucja Fostowicz-Frelik.[40] Tereshchenko in 2021 fully described the axial skeleton of this specimen.[41]
Description
Protoceratops was a relatively small-sized ceratopsian, with both P. andrewsi and P. hellenikorhinus estimated up to 2–2.5 m (6.6–8.2 ft) in length,[42][43] and around 62–104 kg (137–229 lb) in body mass.[44] Although similar in overall body size, the latter had a relatively greater skull length.[20] Both species can be differentiated by the following characteristics:
- P. andrewsi – Two teeth were present at the premaxilla; the snout was low and long; the nasal horn was a single, pointed structure; the bottom edge of the dentary was slightly curved.[6][20]
- P. hellenikorhinus – Absence of premaxillary teeth; the snout was tall and broad; the nasal horn was divided into two pointed ridges; the bottom edge of the dentary was straight.[20]
Skull
The
The
The lower jaw of Protoceratops was a large element composed of the
Protoceratops had leaf-shaped dentary and maxillary teeth that bore several
Postcranial skeleton
The vertebral column of Protoceratops had nine cervical (neck), 12 dorsal (back), eight sacral (pelvic) and over 40 caudal (tail) vertebrae. The centra (centrum; body of the vertebrae) of the first three cervicals were coossified together (atlas, axis and third cervical respectively) creating a rigid structure. The neck was rather short and had poor flexibility. The atlas was the smallest cervical and consisted mainly of the centrum because the neural arch (upper, and pointy vertebral region) was a thin, narrow bar of bone that extended upwards and backwards to the base of the axis neural spine. The capitular facet (attachment site for chevrons; also known as cervical ribs) was formed by a low projection located near the base of the neural arch. The anterior facet of the atlas centrum was highly concave for the articulation of the occipital condyle of the skull. The neural arch and spine of the axis were notably larger than the atlas itself and any other cervical. The axial neural spine was broad and backwards developed being slightly connected to that of the third cervical. From the fourth to the ninth all cervicals were relatively equal in size and proportions. Their neural spines were smaller than the first three vertebrae and the development of the capitular facet diminished from the fourth cervical onwards.[6][47][48]
The dorsal vertebrae were similar in shape and size. Their neural spines were elongated and sub-rectangular in shape with a tendency to become more elongated in posterior vertebrae. The centra were large and predominantly amphiplatian (flat on both facets) and circular when seen from the front. Sometimes in old individuals the last dorsal vertebra was somewhat coosified to the first sacral. The sacral vertebrae were firmly coosified giving form to the sacrum, which was connected to the inner sides of both ilia. Their neural spines were broad, not coosified, and rather consistent in length. The centra were mainly opisthocoelous (concave on the posterior facet and convex on the anterior one) and their size became smaller towards the end. The caudal vertebrae decreased in size progressively towards the end and had very elongated neural spines in the mid-series, forming a sail-like structure. This elongation started from the first to the fourteenth caudal. The centra were heterocoelous (saddle-shaped at both facets). On the anterior caudals they were broad, however, from the twenty-fifth onwards the centra became elongated alongside the neural spines. On the underside of the caudal vertebrae a series of chevrons were attached, giving form to the lower part of the tail. The first chevron was located at the union of the third and fourth caudals. Chevrons three to nine were the largest and from the tenth onwards they became smaller.[6][47][48][49]
All vertebrae of Protoceratops had ribs attached on the lateral sides, except for the series of caudals. The first five cervical ribs (sometimes called chevrons) were some of the shortest ribs, and among them the first two were longer than the rest. The third to the sixth dorsal (thoracic) ribs were the longest ribs in the skeleton of Protoceratops, the following ribs became smaller in size as they progressed toward the end of the vertebral column. The two last dorsal ribs were the smallest, and the last of them was in contact with the internal surfaes of the ilium. Most of the sacral ribs were fused into the sacrum, and had a rather curved shape.[6]
The
The
Classification
Protoceratops was in 1923 placed within the newly named family Protoceratopsidae as the representative species by Granger and Gregory. This family was characterized by their overall primitive morphology in comparison to the more derived Ceratopsidae, such as lack of well-developed horn cores and relative smaller body size. Protoceratops itself was considered by the authors to be somehow related to ankylosaurians based on skull traits, with a more intensified degree to Triceratops and relatives.[2] Gregory and Charles C. Mook in 1925 upon a more deeper analysis of Protoceratops and its overall morphology, concluded that this taxon represents a ceratopsian more primitive than ceratopsids and not an ankylosaur-ceratopsian ancestor.[7] In 1951 Edwin H. Colbert considered Protoceratops to represent a key ancestor for the ceratopsid lineage, suggesting that it ultimately led to the evolution of large-bodied ceratopsians such as Styracosaurus and Triceratops. Such lineage was suggested to have started from the primitive ceratopsian Psittacosaurus. He also regarded Protoceratops as one of the first "frilled" ceratopsians to appear in the fossil record.[50]
However, in 1975 Maryanska and Osmolska argued that it is very unlikely that protoceratopsids evolved from
Furthermore, with the re-examinations of
In 2019 Czepiński analyzed a vast majority of referred specimens to the ceratopsians Bagaceratops and Breviceratops, and concluded that most were in fact specimens of the former. Although the genera Gobiceratops, Lamaceratops, Magnirostris, and Platyceratops, were long considered valid and distinct taxa, and sometimes placed within Protoceratopsidae, Czepiński found the diagnostic (identifier) features used to distinguish these taxa to be largely present in Bagaceratops and thus becoming synonyms of this genus. Under this reasoning, Protoceratopsidae consists of Bagaceratops, Breviceratops, and Protoceratops. Below are the proposed relationships among Protoceratopsidae by Czepiński:[19]
In 2019 Bitnara Kim and colleagues described a relatively well-preserved Bagaceratops skeleton from the
Coronosauria
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Evolution
Longrich and team in 2010 indicated that highly derived morphology of P. hellenikorhinus—when compared to P. andrewsi—indicates that this species may represent a lineage of Protoceratops that had a longer evolutionary history compared to P. andrewsi, or simply a direct descendant of P. andrewsi. The difference in morphologies between Protoceratops also suggests that the nearby Bayan Mandahu Formation is slightly younger than the Djadokhta Formation.[56]
In 2020, Czepiński analyzed several long-undescribed protoceratopsid specimens from the Udyn Sayr and Zamyn Khondt localities of the Djadokhta Formation. One specimen (MPC-D 100/551B) was shown to present skull traits that are intermediate between Bagaceratops rozhdestvenskyi (which is native to adjacent Bayan Mandahu and
Paleobiology
Feeding
In 1955, paleontologist
In 1991, the paleontologist
In 2009, Kyo Tanque and team suggested that basal ceratopsians, such as protoceratopsids, were most likely low
Ontogeny
Brown and Schlaikjer in 1940 upon their large description and revision of Protoceratops remarked that the orbits, frontals, and lacrimals suffered a shrinkage in relative size as the animal aged; the top border of the nostrils became more vertical; the nasal bones progressively became elongated and narrowed; and the neck frill as a whole also increases in size with age. The neck frill specifically, underwent a dramatic change from a small, flat, and almost rounded structure in juveniles to a large, fan-like one in fully mature Protoceratops individuals.[6] In 2001, Lambert and colleagues considered the development of the two nasal "horns" of P. hellenikorhinus to be a trait that was delayed in relation to the appearance of sexual-discriminant traits. This was based on the fact that one small specimen (IMM 96BM2/1) has a skull size slightly larger than a presumed sexually mature P. andrewsi skull (AMNH 6409), and yet it lacks double nasal horns present in fully mature P. hellenikorhinus.[20]
Makovicky and team in 2007 conducted a
David Hone and colleagues in 2016 upon their analysis of P. andrewsi neck frills, found that the frill of Protoceratops was disproportionally smaller in juveniles, grew at a rapid rate than the rest of the animal during its ontogeny, and reached a considerable size only in large adult individuals. Other changes during ontogeny include the elongation of the premaxillary teeth that are smaller in juveniles and enlarged in adults, and the enlargement of middle neural spines in the tail or caudal vertebrae, which appear to grow much taller when approaching adulthood.[64]
In 2017, Mototaka Saneyoshi with team analyzed several Protoceratops specimens from the
In 2018, paleontologists Łucja Fostowicz-Frelik and Justyna Słowiak studied the bone histology of several specimens of P. andrewsi through cross-sections, in order to analyze the growth changes in this dinosaur. The sampled elements consisted of neck frill, femur, tibia, fibula, ribs, humerus and radius bones, and showed that the histology of Protoceratops remained rather uniform throughout ontogeny. It was characterized by simple fibrolamellar bone—bony tissue with an irregular, fibrous texture and filled with blood vessels—with prominent woven-fibered bone and low bone remodeling. Most bones of Protoceratops preserve a large abundance of bone fibers (including Sharpey's fibres), which likely gave strength to the organ and enhanced its elasticity. The team also find that the growth rate of the femur increased at the subadult stage, suggesting changes in bone proportions, such as the elongation of the hindlimbs. This growth rate is mostly similar to that of other small herbivorous dinosaurs such as primitive Psittacosaurus or Scutellosaurus.[66]
Movement
In 1996, Tereshchenko reconstructed the walking model of Protoceratops where he considered the most likely scenario to be Protoceratops as an obligate
Upon the analysis of the forelimbs of several ceratopsians, Phil Senter in 2007 suggested that the hands of Protoceratops could reach the ground when the hindlimbs were upright, and the overall forelimb morphology and range of motion may reflect that it was at least a facultative (optional) quadruped. The forelimbs of Protoceratops could sprawl laterally but not for quadrupedal locomotion, which was accomplished with the elbows tucked in.[68] In 2010 Alexander Kuznetsov and Tereshchenko analyzed several vertebrae series of Protoceratops in order to estimate overall mobility, and concluded that Protoceratops had greater lateral mobility in the presacral (pre-hip) vertebrae series and reduced vertical mobility in the cervical (neck) region.[48] The fossilized footprint associated with the specimen ZPAL Mg D-II/3 described by Niedźwiedzki in 2012 indicates that Protoceratops was digitigrade, meaning that it walked with its toes supporting the body weight.[39]
In 2019 however, Słowiak and team described the limb elements of ZPAL Mg D-II/3, which represents a sub-adult individual, and noted a mix of characters typical of
Digging behavior
Longrich in 2010 proposed that Protoceratops may have used its hindlimbs to
In 2019, Victoria M. Arbour and David C. Evans cited the robusticity of the ulna of Ferrisaurus as a useful feature for digging, which may have been also true for Protoceratops.[70]
Tail function
Gregory and Mook in 1925 suggested that Protoceratops was partially aquatic because of its large feet—being larger than the hands—and the very long neural spines found in the caudal (tail) vertebrae.[7] Brown and Schlaikjer in 1940 indicated that the expansion of the distal (lower) ischial end may reflect a strong ischiocaudalis muscle, which together with the high tail neural spines were used for swimming.[6] Barsbold in his brief 1974 description of the Fighting Dinosaurs specimen accepted this hypothesis and suggested that Protoceratops was amphibious (water-adapted) and had well-developed swimming capacities based on its side to side flattened tail with very high neural spines.[33]
Jack Bowman Bailey in 1997 disagreed with previous aquatic hypotheses and indicated that the high caudal neural spines were instead more reminiscent of bulbous tails of some
In 2008, based on the occurrence of some Protoceratops specimens in
In 2011, during the description of Koreaceratops, Yuong-Nam Lee and colleagues found the above swimming hypotheses hard to prove based on the abundance of Protoceratops in eolian (wind-deposited) sediments that were deposited in prominent arid environments. They also pointed out that while taxa such as Leptoceratops and Montanoceratops are recovered from fluvial sediments, they are estimated to be some of the poorest swimmers. Lee and colleagues concluded that even though the tail morphology of Koreaceratops—and other basal ceratopsians—does not argues against swimming habits, the cited evidence for it is insufficient.[73]
Tereschhenko in 2013 examined the structure of the caudal vertebrae spines of Protoceratops, concluding that it had adaptations for terrestrial and aquatic habits. Observations made found that the high number of caudal vertebrae may have been useful for swimming and use the tail to counter-balance weight. He also indicated that the anterior caudals were devoid of high neural spines and had increased mobility—a mobility that stars to decrease towards the high neural spines—, which suggest that the tail could be largely raised from its base. It is likely that Protoceratops raised its tail as a signal (display) or females could use this method during egg laying in order to expand and relax the cloaca.[49]
In 2016, Hone and team indicated that the tail of Protoceratops, particularly the mid region with elevated neural spines, could have been used in display to impress potential mates and/or for species recognition. The tail may have been related with structures like the frill for displaying behavior.[64]
Kim with team in 2019 cited the elongated tail spines as well-suited for swimming. They indicated that both Bagaceratops and Protoceratops may have used their tails in a similar fashion during similar situations, such as swimming, given how similar their postcranial skeletons were. The team also suggested that a swimming adaptation could have been useful to avoid aquatic predators, such as
Social behavior
Tomasz Jerzykiewiczz in 1993 reported several
In 2014, David W. E. Hone and colleagues reported and described two blocks containing death assemblages of P. andrewsi from Tugriken Shireh. The first block (MPC-D 100/526) comprises four juvenile individuals in close proximity with their heads pointing upwards, and the second block (MPC-D 100/534) is composed of two sub-adults with a horizontal orientation. Based on previous assemblages and the two blocks, the team determined that Protoceratops was a social dinosaur that formed herds throughout its life and such herds would have varied in composition, with some including adults, sub-adults, siblings from a single nest or local members of a herd joining shortly after hatching. However, as the group could have loss members by predation or other factors, the remnants individuals would aggregate into larger groups to increase their survival. Hone and colleagues in particular suggested that juveniles would aggregate primarily as a defense against predators and an increased protection from the multiple adults within the group. The team also indicated that, while Protoceratops provides direct evidence for the formation of single cohort aggregations throughout its lifespan, it cannot be ruled out the possibility that some Protoceratops were solitary.[14]
Sexual dimorphism and display
Brown and Schlaikjer in 1940 upon their large analysis of Protoceratops noted the potential presence of sexual dimorphism among specimens in P. andrewsi, concluding that this condition could be entirely subjective or represent actual differences between sexes. Individuals with a high nasal horn, massive prefrontals, and frontoparietal depression were tentatively determined as males. Females were mostly characterized by the lack of well-developed nasal horns.[6] In 1972 Kurzanov made comparisons between P. andrewsi skulls from Bayn Dzak and Tugriken Shireh, noting differences on the nasal horn within populations.[74]
Peter Dodson in 1996 used anatomical characters of the skull in P. andrewsi in order to quantify areas subject to ontogenic changes and sexual dimorphism. In total, 40 skull characters were measured and compared, including regions like the frill and nasal horn. Dodson found most of these characters to be highly variable across specimens, especially the frill which he interpreted to have had a bigger role in displaying behavior than simply serving as a site of masticatory muscles. He considered unlikely such interpretation based on the relative fragility of some frill bones and the large individual variation, which may have affected the development of those muscles. The length of the frill was found by Dodson to have a rather irregular growth in specimens, as juvenile AMNH 6419 was observed with a frill length smaller than other juveniles. He agreed with Brown and Schlaikjer in that a high, well-developed nasal horn represents a male trait and the opposite indicates females. In addition, Dodson suggested that traits like the nasal horn and frill in male Protoceratops may have been important visual displays for attracting females and repelling other males, or even predators. Lastly, he noted that both males and females had not significant disparity in body size, and that sexual maturity in Protoceratops could be recognised at the moment when males can be distinguished from females.[75]
In 2001, Lambert and team upon the description of P. hellenikorhinus also noted variation within individuals. For instance, some specimens (e.g., holotype IMM 95BM1/1) preserve high nasal bones with a pair of horns; relatively short antorbital length; and vertically oriented nostrils. Such traits were regarded as representing male P. hellenikorhinus. The other group of skulls is characterized by low nasals that have undeveloped horns; a relatively longer antorbital length; and more oblique nostrils. These individuals were considered as females. The team however, was not able to produce deeper analysis regarding sexual dimorphism in P. hellenikorhinus due to the lack of complete specimens.
In 2012, Naoto Handa and colleagues described four specimens of P. andrewsi from the Udyn Sayr locality of the Djadokhta Formation. They indicated that sexual dimorphism in this population was marked by a prominent nasal horn in males—trait also noted by other authors—relative wider nostrils in females, and a wider neck frill in males. Despite maintaining the skull morphology of most Protoceratops specimens (such as premaxillary teeth), the neck frill in this population was straighter with a near triangular shape. Handa and team in addition found variation across this Udyn Sayr sample and classified them in three groups. First group includes individuals with a well-developed bony ridge on the lateral surface of the squamosal bone, and the posterior border of the squamosal is backwards oriented. Second group had a fairly rounded posterior border of the squamosal, and a long and well-developed bony ridge on the posterior border of the parietal bone. Lastly, the third group was characterized by a curved posterior border of the squamosal and a notorious rugose texture on the top surface of the parietal. Such skull traits were regarded as marked intraspecific variation within Protoceratops, and they differ from other populations across the Djadokhta Formation (like Tugriken Shireh), being unique to the Udyn Sayr region. These neck frill morphologies differ from those of Protoceratops from the Djadokhta Formation in the adjacent dinosaur locality Tugrikin Shire. The morphological differences among the Udyn Sayr specimens may indicate intraspecific variation of Protoceratops.[77] A large and well-developed bony ridge on the parietal has been observed on another P. andrewsi specimen, MPC-D 100/551, also from Udyn Sayr.[57]
However, Leonardo Maiorino with team in 2015 performed a large geometric morphometric analysis using 29 skulls of P. andrewsi in order to evaluate actual sexual dimorphism. Obtained results indicated that other than the nasal horn—which remained as the only skull trait with potential sexual dimorphism—all previously suggested characters to differentiate hyphotetical males from females were more linked to ontogenic changes and intraspecific variation independent of sex, most notably the neck frill. The geometrics showed no consistent morphological differences between specimens that were regarded as males and females by previous authors, but also a slight support for differences in the rostrum across the sample. Maiorino and team nevertheless, cited that the typical regarded Protoceratops male, AMNH 6438, pretty much resembles the rostrum morphology of AMNH 6466, a typical regarded female. However, they suggested that authentic differences between sexes could be still present in the postcranial skeleton. Although previously suggested for P. hellenikorhinus, the team argued that the sample used for this species was not sufficient, and given that sexual dimorphism was not recovered in P. andrewsi, it is unlikely that it occurred in P. hellenikorhinus.[78]
In 2016, Hone and colleagues analyzed 37 skulls of P. andrewsi, finding that the neck frill of Protoceratops (in both length and width) underwent positive allometry during ontongeny, that is, a faster growth/development of this region than the rest of the animal. The jugal bones also showed a trend towards an increase in relative size. These results suggest that they functioned as socio-sexual dominance signals, or, they were mostly used in display. The use of the frill as a displaying structure may be related to other anatomical features of Protoceratops such as the premaxillary teeth (at least for P. andrewsi) which could have been used in display or
Tereschenko in 2018 examined the cervical vertebrae series of six P. andrewsi specimens. Most of them had differences in the same exact vertebra, such as the shape and proportions of the vertebral centra and orientation of neural arches. According these differences, four groups were identified, concluding that individual variation was extended to the vertebral column of Protoceratops.[79]
In 2020 nevertheless, Andrew C. Knapp and team conducted morphometric analyses of a large sample of P. andrewsi specimens, primarily confluding that the neck frill of Protoceratops has no indicators or evidence for being sexually dimorphic. Obtained results showed instead that several regions of the skull of Protoceratops independently varied in their rate of growth, ontogenetic shape and morphology; a high growth of the frill during ontogeny in relation to other body regions; and a large variability of the neck frill independent of size. Knapp and team noted that results of the frill indicate that this structure had a major role in signaling within the species, consistent with selection of potential mates with quality ornamentation and hence reproductive success, or dominance signaling. Such use of the frill may suggest that intraspecific social behavior was highly important for Protoceratops. Results also support the general hypothesis that the neck frill of ceratopsians functioned as a socio-sexual signal structure.[80]
Reproduction
In 1989, Walter P. Coombs concluded that
In 2011, the first authentic nest of Protoceratops (MPC-D 100/530) from the Tugriken Shireh locality was described by David E. Fastovsky and team. As some individuals are closely appressed along the well-defined margin of the nest, it may have had a circular or semi-circular shape—as previously hypothetized—with a diameter of 70 cm (700 mm). Most of the individuals within the nest had nearly the same age, size and growth, suggesting that they belonged to a single nest, rather than an aggregate of individuals. Fastovsky and team also suggested that even though the individuals were young, they were not perinates based on the absence of eggshell fragments and their large size compared to even more smaller juveniles from this locality. The fact that the individuals likely spend some time in the nest after hatching for growth suggests that Protoceratops parents might have cared for their young at nests during at least the early stages of life. As Protoceratops was a relatively basal (primitive) ceratopsian, the finding may imply that other ceratopsians provided care for their young as well.[13]
In 2017, Gregory M. Erickson and colleagues determined the
Paleopathology
In 2018, Tereshchenko examined and described several articulated cervical vertebrae of P. andrewsi and reported the presence of two abnormally fused vertebrae (specimen PIN 3143/9). The fusion of the vertebrae was likely a product of disease or external damage.[79]
Predator–prey interactions
Barsbold in 1974 shortly described the Fighting Dinosaurs specimen and discussed possible scenarios. The Velociraptor has its right leg pinned under the Protoceratops body with its left sickle claw oriented into the throat region. The Protoceratops bit the right hand of the predator, implying that it was unable to escape. Barsbold suggested that both animals drowned as they fell into a swamp-like body of water or, the relatively quicksand-like bottom of a lake could have kept them together during the last moments of their fight.[33]
Osmólska in 1993 proposed another two hypotheses in order to explain their preservation. During the death struggle, a large
In 1995, David M. Unwin and colleagues cast doubt on previous explanations especially a scavenging hypothesis as there were numerous indications of a concurrent death event. For instance, the Protoceratops has a semi-erect stance and its skull is nearly horizontal, which could have not been possible if the animal was already dead. The Velociraptor has its right hand trapped within the jaws of the Protoceratops and the left one grasping the Protoceratops skull. Moreover, it lies on the floor with its feet directed to the prey's belly and throat areas, indicating that this Velociraptor was not scavenging. Unwin and colleagues examined the
In 2010, David Hone with team reported a new interaction between Velociraptor and Protoceratops based on
In 2016, Barsbold re-examined the Fighting Dinosaurs specimen and found several anomalies within the Protoceratops individual: both coracoids have small bone fragments indicatives of a breaking of the pectoral girdle; the right forelimb and scapulocoracoid are torn off to the left and backwards relative to its torso. He concluded that the prominent displacement of pectoral elements and right forelimb was caused by an external force that tried to tear them out. Since this event likely occurred after the death of both animals or during a point where movement was not possible, and the Protoceratops is missing other body elements, Barsbold suggested that scavengers were the most likely authors. Because Protoceratops is considered to have been a herding animal, another hypothesis is that members of a herd tried to pull out the already buried Protoceratops, causing the joint dislocation of limbs. However, Barsbold pointed out that there are no related traces within the overall specimen in order to support this latter interpretation. Lastly, he restored the course of the fight with the Protoceratops power-slamming the Velociraptor, which used its feet claws to damage the throat and belly regions and its hand claws to grasp the herbivore's head. Before their burial, the deathmatch ended up on the ground with the Velociraptor lying on its back right under the Protoceratops. After burial, either Protoceratops herd or scavengers tore off the buried Protoceratops to the left and backwards, making both predator and prey to be slightly separated.[36]
Daily activity
In 2010, Nick Longrich examined the relatively large
However, in 2011, Lars Schmitz and Ryosuke Motani measured the dimensions of the sclerotic ring and eye socket in fossil specimens of dinosaurs and pterosaurs, as well as some living species. They noted that whereas photopic (diurnal) animals have smaller sclerotic rings, scotopic (nocturnal) animals tend to have more enlarged rings. Mesopic (
Paleoenvironment
Bayan Mandahu Formation
Based on general similarities between the vertebrate fauna and sediments of Bayan Mandahu and the Djadokhta Formation, the
The
Djadokhta Formation
Protoceratops is known from most localities of the
The Djadokhta Formation is separated into a lower Bayn Dzak Member and upper Turgrugyin Member. Protoceratops is largely known from both members, having P. andrewsi as a dominant and representative species in the overall formation.
The relatively low dinosaur paleodiversity, small body size of most dinosaurs, and
Taphonomy
In 1993 Jerzykiewiczz suggested that many articulated Protoceratops specimens died in the process of trying to free themselves from massive sand bodies that trapped them during sandstorms events and were not transported by environmental factors. He cited the distinctive posture of some Protoceratops involving the body and head arched upwards with forelimbs tucked in at their sides—a condition known as "standing" in particular cases—the absence of sedimentary structures in sediments preserving the individuals, and the Fighting Dinosaurs
Fastovsky in 1997 examined the geology at Tugriken Shireh providing insights into the taphonomy of Protoceratops. He agreed in that the preservation of Protoceratops specimens indicate that they underwent a catastrophic event such as desert storms, and carcasses were not relocated by scavengers or environmental factors. Several isolated burrows found in sediments at this locality have also been reported penetrating in the bone surface of some buried Protoceratops individuals. Fastovsky pointed out these two factors combined indicate that this site was host to high biotic activity, mainly composed of arthropod scavengers who were also involved in the recycling of Protoceratops carcasses. The flexed position of most buried Protoceratops is indicative of desiccation and shrinking of ligaments/tendons in the legs, necks, and tails after death.[120]
In 1998 during a conference abstract at the
Later in 2010, Kirkland and Kenneth Bader redescribed and discussed the numerous feeding traces from this Protoceratops specimen, which they nicknamed Fox Site Protoceratops. They found at least three types of feeding traces on this individual; nearly circular borings—which they found instead to correlate best with feeding traces made by dermestid beetles—of 0.6–1 cm (6.0–10.0 mm) in diameter; semicircular shaped notches at the edge of bones; and destruction of articular surfaces, mostly at the
In 2010 the paleontologists Yukihide Matsumoto and Mototaka Saneyoshi reported multiple borings and bite traces on joint areas of articulated Bagaceratops and Protoceratops specimens from the Tugriken Shireh locality of the
In 2011 Fastovsky with colleagues concluded that the juveniles within the nest MPC-D 100/530 were rapidly overwhelmed by a strong sand-bearing event and entombed alive. The sediments of the nest suggest a deposition through a dune-shift or strong sandstorms, and the orientation of the individuals indicates that sediments were brought from a prevailing west-southwest wind. Most individuals are preserved with their forelimbs splayed and hindlimbs are extended, an arrangement that suggests that young Protoceratops tried to push against the powerful airstream in the initially loose sand. Prior to or during burial, some may have tried to climb on top of others. Because it is generally accepted that most fossil specimens at Tugriken Shireh were preserved by rapidly migrating dunes and sandstorms, Fastovsky with colleagues suggested that the lee side borders of the nest would have been the area where air was sand-free and consequently, all young Protoceratops may have struggled to reach this area, resulting in their final burial and eventual death.[13]
Hone and colleagues in 2014 indicated that two assemblages of Protoceratops at Tugriken Shireh (MPC-D 100/526 and 100/534) suggest that individuals died simultaneously, rather than accumulating over time. For instance, the block of four juveniles preserves the individuals with near-identical postures, spatial positions, and all of them have their heads facing upwards, which indicates that they were alive at the time of burial. During burial, the animals were most likely not completely restricted in their movements at all, given that the individuals of MPC-D 100/526 are in relatively normal life positions and have not been disturbed. At least two individuals within this block are preserved with their arms at a level above the legs, suggestive of attempts of trying to move upwards with the purpose of free themselves. The team also noted the presence of borings on the skulls and skeletons of both assemblages, and these may have been produced by insect larvae after the animals died.[14]
In 2016 Meguru Takeuchi and team reported numerous fossilized feeding traces preserved on skeletons of Protoceratops from the Bayn Dzak, Tugriken Shireh, and Udyn Sayr localities, and also from other dinosaurs. Preserved traces were reported as pits, notches, borings, and tunnels, which they attributed to scavengers. The diameter of the feeding traces preserved on a Protoceratops skull from Bayn Dzak was bigger than traces reported among other specimens, indicating that the scavengers responsible for these traces were notoriously different from other trace makers preserved on specimens.[125]
Cultural significance
Possible Influence on Griffin Legend
The folklorist and historian of science
Dodson in 1996 pointed out Greek writers began describing the griffin around 675 B.C., at the time the first Greek writings about Scythia nomads appeared, although contact with Scythian nomads would have occurred earlier, in the Bronze Age when Greeks imported tin from Afghanistan, transported on the caravan routes across the Gobi and other deserts. Griffins were described as "guarding" the gold deposits in the arid hills and red sandstone formations of the wilderness below the Tien Shan and Altai mountains. The region of Mongolia and China, where many Protoceratops and other dinosaur fossils are found, is rich in placer gold runoff from the neighboring mountains, lending some credence to the theory that these fossils played a role in griffin descriptions of the seventh century BC to Roman times.[127]
Mayor in 2001 and 2011 refined the hypothesis of Protoceratops as an influence on the griffin legend by analyzing written details and artistic imagery. She also cited some other Greek histories about mythological creatures may have been influenced by fossil discoveries by ancient people, such as cyclopes and giants.[128][129]
In 2016 this hypothesis was criticized by the British paleontologist and paleoartist Mark P. Witton, as it ignores pre-Greek "griffin art and accounts." (No written accounts of griffins are known before ca 675 BC, when the word gryps/griffin is first attested.) Witton goes on to point out that the wings of traditional griffins are positioned above the shoulder blades, not behind the neck as the frills of Protoceratops, that the bodies of griffins much more closely resemble the bodies of modern big cats than they do those of Protoceratops, and that the gold deposits of central Asia occur hundreds of kilometers from the known Protoceratops fossil remains, among many other inconsistencies. It is simpler, he argues, to understand the griffin as a mythical combination of well-known extant animal species than as an ancient misunderstanding of fossilized collections of bones.[130]
-
A traditional depiction of the griffin
-
Adrienne Mayor has speculated that the discovery of Protoceratops fossils may have inspired or influenced stories of griffins
See also
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