Protoceratops (; ) is a genus of small protoceratopsid dinosaurs that lived in Asia during the Late Cretaceous, around 75 to 71 million years ago. The genus Protoceratops includes two species: P. andrewsi and the larger P. hellenikorhinus. The former was described in 1923 with fossils from the Mongolian Djadokhta Formation, and the latter in 2001 with fossils from the Chinese Bayan Mandahu Formation. Protoceratops was initially believed to be an ancestor of ankylosaurians and larger ceratopsians, such as Triceratops and relatives, until the discoveries of other protoceratopsids. Populations of P. andrewsi may have evolved into Bagaceratops rozhdestvenskyi through anagenesis.
Protoceratops were small ceratopsians, up to long and around in body mass. While adults were largely quadrupedal, juveniles had the capacity to walk around bipedally if necessary. They were characterized by a proportionally large skull, short and stiff neck, and neck frill. The frill was likely used for display or intraspecific combat, as well as protection of the neck and anchoring of jaw muscles. A horn-like structure was present over the nose, which varied from a single structure in P. andrewsi to a double, paired structure in P. hellenikorhinus. The "horn" and frill were highly variable in shape and size across individuals of the same species, but there is no evidence of sexual dimorphism. They had a prominent parrot-like beak at the tip of the jaws. P. andrewsi had a pair of cylindrical, blunt teeth near the tip of the upper jaw. The forelimbs had five fingers of which only the first three bore wide and flat unguals. The feet were wide and had four toes with flattened, shovel-like unguals, which would have been useful for digging through the sand. The hindlimbs were longer than the forelimbs. The tail was long and had an enigmatic sail-like structure, which may have been used for display, swimming, or metabolic reasons.
Protoceratops, like many other ceratopsians, were herbivores equipped with prominent jaws and teeth suited for chopping foliage and other plant material. They are thought to have lived in highly sociable groups of mixed ages. They appear to have cared for their young. They laid soft-shelled eggs, a rare occurrence in dinosaurs. During maturation, the skull and neck frill underwent rapid growth. Protoceratops were hunted by Velociraptor, and one particularly famous specimen (the Fighting Dinosaurs) preserves a pair of them locked in combat. Protoceratops used to be characterized as nocturnal because of the large scleral ring around the eye, but they are now thought to have been cathemeral (active at dawn and dusk).
History of discovery
thumb|300px|[[Flaming Cliffs of Mongolia. This highly fossiliferous locality of the Gobi Desert yielded the first known remains of Protoceratops.]]
In 1900 Henry Fairfield Osborn suggested that Central Asia may have been the center of origin of most animal species, including humans, which caught the attention of explorer and zoologist Roy Chapman Andrews. This idea later gave rise to the First (1916 to 1917), Second (1919) and Third (1921 to 1930) Central Asiatic Expeditions to China and Mongolia, organized by the American Museum of Natural History under the direction of Osborn and field leadership of Andrews. The team of the third expedition arrived in Beijing in 1921 for the final preparations and started working in the field in 1922. During late 1922 the expedition explored the famous Flaming Cliffs of the Shabarakh Usu region of the Djadokhta Formation, Gobi Desert, now known as the Bayn Dzak region. On 2 September, the photographer James B. Shackelford discovered a partial juvenile skull—which would become the holotype specimen (AMNH 6251) of Protoceratops—in reddish sandstones. It was subsequently analyzed by the paleontologist Walter W. Granger who identified it as reptilian. On 21 September, the expedition returned to Beijing, and even though it was set up to look for remains of human ancestors, the team collected numerous dinosaur fossils and thus provided insights into the rich fossil record of Asia. Back in Beijing, the skull Shackelford had found was sent to the American Museum of Natural History for further study, after which Osborn reached out to Andrews and team via cable, notifying them about the importance of the specimen.
In 1923 the expedition again prospected the Flaming Cliffs, this time discovering even more specimens of Protoceratops and also the first remains of Oviraptor, Saurornithoides and Velociraptor. Most notably, the team discovered the first fossilized dinosaur eggs near the holotype of Oviraptor and given how abundant Protoceratops was, the nest was attributed to this taxon. In the same year, Granger and William K. Gregory formally described the new genus and species Protoceratops andrewsi based on the holotype skull. The specific name, andrewsi, is in honor of Andrews for his prominent leadership during the expeditions. They identified Protoceratops as an ornithischian dinosaur closely related to ceratopsians representing a possible common ancestor between ankylosaurs and ceratopsians. Since Protoceratops was more primitive than any other known ceratopsian at that time, Granger and Gregory coined the new family Protoceratopsidae, mostly characterized by the lack of horns. The co-authors also agreed with Osborn that Asia, if more thoroughly explored, could solve many major evolutionary gaps in the fossil record. Other researchers immediately noted the importance of the Protoceratops finds, and the genus was hailed as the "long-sought ancestor of Triceratops". Most fossils were in an excellent state of preservation with even scleral rings (delicate ocular bones) preserved in some specimens, quickly making Protoceratops one of the best-known dinosaurs from Asia.
thumb|left|Holotype skull of P. andrewsi, collected during the Third Central Asiatic Expedition
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. 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. 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. Since its discovery, the Tugriken Shireh locality has yielded some of the most significant specimens of Protoceratops, such as the Fighting Dinosaurs, authentic nests,
Species and synonyms
thumb|Holotype skull of P. hellenikorhinus at the [[Inner Mongolia Museum]]
Protoceratopsid remains were recovered in the 1970s from the Khulsan locality of the Barun Goyot Formation, Mongolia, during the work of several Polish-Mongolian paleontological expeditions. In 1975, Polish paleontologists Teresa Maryańska and Halszka Osmólska described a second species of Protoceratops which they named P. kozlowskii. This new species was based on the Khulsan material, mostly consisting of juvenile skull specimens. The specific name, kozlowskii, is in tribute to the Polish paleontologist Roman Kozłowski. They also named the new genus and species of protoceratopsid Bagaceratops rozhdestvenskyi, known from specimens of the nearby Hermiin Tsav locality. In 1990 the Russian paleontologist Sergei Mikhailovich Kurzanov referred additional material from Hermiin Tsav to P. kozlowskii. However, he noted that there were enough differences between P. andrewsi and P. kozlowskii, and erected the new genus and combination Breviceratops kozlowskii. Though Breviceratops has been regarded as a synonym and juvenile stage of Bagaceratops, Łukasz Czepiński in 2019 concluded that the former has enough anatomical differences to be considered as a separate taxon.
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. In 2017 abundant protoceratopsid material was reported from Alxa near Bayan Mandahu, and it may be preferable to P. hellenikorhinus. In 2006 North American paleontologists Peter Makovicky and Mark A. Norell suggested that Bainoceratops may be synonymous with Protoceratops as most of the traits used to separate the former from the latter have been reported from other ceratopsians including Protoceratops itself, and they are more likely to fall within the wide intraspecific variation range of the concurring P. andrewsi. The authors Brenda J. Chinnery and Jhon R. Horner in 2007 during their description of Cerasinops stated that Bainoceratops, along with other dubious genera, was determined to be either a variant or immature specimen of other genera. Based on this reasoning, they excluded Bainoceratops from their phylogenetic analysis.
Eggs and nests
As part of the Third Central Asiatic Expedition of 1923, Andrews and team discovered the holotype specimen of Oviraptor in association with some of the first known fossilized dinosaur eggs (nest AMNH 6508), in the Djadokhta Formation. Each egg was elongated and hard-shelled, and due to the proximity and high abundance of Protoceratops in the formation, these eggs were believed at the time to belong to this dinosaur. This resulted in the interpretation of the contemporary Oviraptor as an egg predatory animal, an interpretation also reflected in its generic name.
In 1994 the Russian paleontologist Konstantin E. Mikhailov named the new oogenus Protoceratopsidovum from the Barun Goyot and Djadokhta formations, with the type species P. sincerum and additional P. fluxuosum and P. minimum. This ootaxon was firmly stated as belonging to protoceratopsid dinosaurs since they were the predominant dinosaurs where the eggs were found and some skeletons of Protoceratops were found in close proximity to Protoceratopsidovum eggs. More specifically, Mikhailov stated that P. sincerum and P. minimum were laid by Protoceratops, and P. fluxuosum by Breviceratops.
thumb|Oviraptorid embryo MPC-D 100/971, a specimen that shed light on the identity of elongatoolithid eggs
However, also during 1994, Norell and colleagues reported and briefly described a fossilized theropod embryo inside an egg (MPC-D 100/971) from the Djadokhta Formation. They identified this embryo as an oviraptorid dinosaur and the eggshell, upon close examination, turned out be that of elongatoolithid eggs and thereby the oofamily Elongatoolithidae was concluded to represent the eggs of oviraptorids. This find proved that the nest AMNH 6508 belonged to Oviraptor and rather than an egg-thief, the holotype was actually a mature individual that perished brooding the eggs. Moreover, phylogenetic analyses published in 2008 by Darla K. Zelenitsky and François Therrien have shown that Protoceratopsidovum represents the eggs of a maniraptoran more derived than oviraptorids and not Protoceratops. The description of the eggshell of Protoceratopsidovum has further confirmed that they in fact belong to a maniraptoran, possibly deinonychosaur taxon.
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. 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. 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. 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. Tereshchenko in 2021 fully described the axial skeleton of this specimen.
Description
thumb|left|Size comparison of two Protoceratops species
Protoceratops was a relatively small-sized ceratopsian, with both P. andrewsi and P. hellenikorhinus estimated up to in length, and around in body mass. Although similar in overall body size, the latter had a relatively greater skull length.
Postcranial skeleton
thumb|Skeletal reconstruction of P. andrewsi
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 (, 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 (upper, and pointy vertebral region) was a thin, narrow bar of bone that extended upwards and backward to the base of the axis neural . 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 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 backward 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.
The 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 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 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 (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.
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 surfaces of the ilium. Most of the sacral ribs were fused into the sacrum, and had a rather curved shape.
However, in 1975 Maryanska and Osmolska argued that it is very unlikely that protoceratopsids evolved from psittacosaurids, and also unlikely that they gave rise to the highly derived (advanced) ceratopsids. The first point was supported by the numerous anatomical differences between protoceratopsids and psittacosaurids, most notably the extreme reduction of some hand digits in the latter group—a trait much less pronounced in protoceratopsids. The second point was explained on the basis of the already derived anatomy in protoceratopsids like Bagaceratops or Protoceratops (such as the jaw morphology). Maryanska and Osmolska also emphasized that some early members of the Ceratopsidae reflect a much older evolutionary history.
Furthermore, with the re-examinations of Turanoceratops in 2009 and Zuniceratops—two critical ceratopsian taxa regarding the evolutionary history of ceratopsids—in 2010 it was concluded that the origin of ceratopsids is unrelated to, and older than the fossil record of Protoceratops and relatives. In most recent/modern phylogenetic analyses Protoceratops and Bagaceratops are commonly recovered as sister taxa, leaving the interpretations proposing direct relationships with more derived ceratopsians unsupported.
thumb|Protoceratops (A, D, E) compared to other ceratopsians
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:
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 Barun Goyot) and P. andrewsi. The specimen hails from the Udyn Sayr locality, where Protoceratops remains are dominant, and given the lack of more conclusive anatomical traits, Czepiński assigned the specimen as Bagaceratops sp. He explained that the presence of this Bagaceratops specimen in such unusual locality could be solved by: (1) the coexistence and sympatric (altogether) evolution of both Bagaceratops and Protoceratops at this one locality; (2) the rise of B. rozhdestvenskyi in a different region and eventual migration to Udyn Sayr; (3) hybridization between the two protoceratopsids given the near placement of both Bayan Mandahu and Djadokhta; (4) anagenetic (progressive evolution) evolutionary transition from P. andrewsi to B. rozhdestvenskyi. Among scenarios, an anagenetic transition was best supported by Czepiński given the fact that no definitive B. rozhdestvenskyi fossils are found in Udyn Sayr, as expected from a hybridization event; MPC-D 100/551B lacks a well-developed accessory antorbital fenestra (hole behind the nostril openings), a trait expected to be present if B. rozhdestvenskyi had migrated to the area; and many specimens of P. andrewsi recovered at Udyn Sayr already feature a decrease in the presence of primitive premaxillary teeth, hence supporting a growing change in the populations.
Paleobiology
Feeding
In 1955, paleontologist Georg Haas examined the overall skull shape of Protoceratops and attempted to reconstruct its jaw musculature. He suggested that the large neck frill was likely an attachment site for masticatory muscles. Such placement of the muscles may have helped to anchor the lower jaws, useful for feeding. Yannicke Dauphin and colleagues in 1988 described the enamel microstructure of Protoceratops, observing a non-prismatic outer layer. They concluded that enamel shape does not relate to the diet or function of the teeth as most animals do not necessarily use teeth to process food. The maxillary teeth of ceratopsians were usually packed into a dental battery that formed vertical shearing blades which probably chopped the leaves. This feeding method was likely more efficient in protoceratopsids as the enamel surface of Protoceratops was coarsely-textured and the tips of the micro-serrations developed on the basis of the teeth, probably helping to crumble vegetation. Based on their respective peg-like shape and reduced microornamentation, Dauphin and colleagues suggested that the premaxillary teeth of Protoceratops had no specific function.
In 1991, the paleontologist Gregory S. Paul stated that contrary to the popular view of ornithischians as obligate herbivores, some groups may have been opportunistic meat-eaters, including the members of Ceratopsidae and Protoceratopsidae. He pointed out that their prominent parrot-like beaks and shearing teeth along with powerful muscles on the jaws suggest an omnivore diet instead, much like pigs, hogs, boars and entelodonts. Such scenario indicates a possible competition with the more predatory theropods over carcasses, however, as the animal tissue ingestion was occasional and not the bulk of their diet, the energy flow in ecosystems was relatively simple. You Hailu and Peter Dodson in 2004 suggested that the premaxillary teeth of Protoceratops may have been useful for selective cropping and feeding.
In 2009, Kyo Tanque and team suggested that basal ceratopsians, such as protoceratopsids, were most likely low browsers due to their relatively small body size. This low-browsing method would have allowed to feed on foliage and fruits within range, and large basal ceratopsians may have consumed tougher seeds or plant material not available to smaller basal ceratopsians.
David J. Button and Lindsay E. Zanno in 2019 performed a large phylogenetic analysis based on skull biomechanical characters—provided by 160 Mesozoic dinosaur species—to analyze the multiple emergences of herbivory among non-avian dinosaurs. Their results found that herbivorous dinosaurs mainly followed two distinct modes of feeding, either processing food in the gut—characterized by relatively gracile skulls and low bite forces—or the mouth, which was characterized by features associated with extensive processing such as high bite forces and robust jaw musculature. Ceratopsians (including protoceratopsids), along with Euoplocephalus, Hungarosaurus, parkosaurid, ornithopod and heterodontosaurine dinosaurs, were found to be in the former category, indicating that Protoceratops and relatives had strong bite forces and relied mostly on its jaws to process food.
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.
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.
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.
Movement
thumb|left|Key differences between Protoceratops adults and juveniles
In 1996, Tereshchenko reconstructed the walking model of Protoceratops where he considered the most likely scenario to be Protoceratops as an obligate quadruped given the proportions of its limbs. The main gait of Protoceratops was probably trot-like mostly using its hindlimbs and it is unlikely to have used an asymmetric gait. If trapped in a specific situation (like danger or foraging), Protoceratops could have employed a rapid, facultative bipedalism. He also noted that the flat and wide pedal unguals of Protoceratops may have allowed efficient walking through loose terrain, such as sand which was common on its surroundings. Tereshchenko using speed equations also estimated the average maximum walking speed of Protoceratops at about 3 km/h (kilometres per hour).
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. In 2010 Alexander Kuznetsov and Tereshchenko analyzed several vertebrae series of Protoceratops 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.
Tail function
thumb|left|Elevated neural spines of the caudal (tail) vertebrae of an assigned Protoceratops specimen
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.
In 2008, based on the occurrence of some Protoceratops specimens in fluvial (river-deposited) sediments from the Djadokhta Formation and (vertebral centra that are saddle-shaped at both ends) caudal vertebrae of protoceratopsids, Tereshchenko concluded that the elevated caudal spines are a swimming adaptation. He proposed that protoceratopsids moved through water using their laterally flattened tails as a paddle to aid in swimming. According to Tereschenko, Bagaceratops was fully aquatic while Protoceratops was only partially aquatic. Longrich in 2010 argued that the high tail and frill of Protoceratops may have helped it to shed excess heat during the day—acting as large-surface structures—when the animal was active in order to survive in the relatively arid environments of the Djadokhta Formation without highly developed cooling mechanisms.
thumb|Koreaceratops restored in a swimming behavior. This hypothesis has not yet reached a consensus
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.
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 to expand and relax the cloaca.
Social behavior
Tomasz Jerzykiewiczz in 1993 reported several monospecific (containing only one dominant species) death assemblages of Protoceratops from the Bayan Mandahu and Djadokhta formations. A group of five medium-sized and adult Protoceratops was observed at the Bayan Mandahu locality. Individuals within this assemblage were lying on their bellies with their heads facing upwards, side by side parallel-aligned, and inclined about 21 degrees from the horizontal plane. Two other groups were found at the Tugriken Shireh locality; one group containing six individuals and another group of about 12 skeletons.
Sexual dimorphism and display
thumb|Diagram featuring specimens of P. andrewsi and P. hellenikorhinus, showcasing a wide range of variability
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.
Peter Dodson in 1996 used anatomical characters of the skull in P. andrewsi 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.
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. 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.
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 intraspecific combat, or the high neural spines of tail. On the other hand, Hone and team argued that if neck frills were instead used for protective purposes, a large frill may have acted as an aposematic (warning) signal to predators. However, such strategies are most effective when the taxon is rare in the overall environment, opposed to Protoceratops which appears to be an extremely abundant and medium-sized dinosaur.
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.
Reproduction
thumb|Skeletal mount of Protoceratops with juveniles
In 1989, Walter P. Coombs concluded that crocodilians, ratite and megapode birds were suitable modern analogs for dinosaur nesting behavior. He largely considered elongatoolithid eggs to belong to Protoceratops because adult skeletons were found in close proximity to nests, interpreting this as an evidence for parental care. Furthermore, Coombs considered the large concentration of Protoceratops eggs at small regions as an indicator of marked philopatric nesting (nesting in the same area). The nest of Protoceratops would have been excavated with the hindlimbs and was built in a mound-like, crater-shaped center structure with the eggs arranged in semicircular fashion. Richard A. Thulborn in 1992 analyzed the different types of eggs and nests—the majority of them, in fact, elongatoolithid—referred to Protoceratops and their structure. He identified types A and B, both of them sharing the elongated shape. Type A eggs differed from type B eggs in having a pinched end. Based on comparisons with other ornithischian dinosaurs such as Maiasaura and Orodromeus—known from more complete nests—Thulborn concluded that most depictions of Protoceratops nests were based on incompletely preserved clutches and mostly on type A eggs, which were more likely to have been laid by an ornithopod. He concluded that nests were built in a shallow mound with the eggs laid radially, contrary to popular restorations of crater-like Protoceratops nests.
thumb|left|Protoceratops nest MPC-D 100/530. Scale bar is
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 . 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.
In 2017, Gregory M. Erickson and colleagues determined the incubation periods of P. andrewsi and Hypacrosaurus by using lines of arrested growth (LAGS; lines of growth) of the teeth in embryonic specimens (Protoceratops egg clutch MPC-D 100/1021). The results suggests a mean embryonic tooth replacement period of 30.68 days and relatively plesiomorphically (ancestral-shared) long incubation times for P. andrewsi, with a minimum incubation time of 83.16 days. Norell and team in 2020 analyzed again this clutch and concluded that Protoceratops laid soft-shelled eggs. Most embryos within this clutch have a flexed position and the outlines of eggs are also present, suggesting that they were buried in ovo (in the egg). The outlines of eggs and embryos indicates ellipsoid-shaped eggs in life with dimensions about long and wide. Several of the embryos were associated with a black to white halo (circumference). Norell and team performed histological examinations to its chemical composition, finding traces of proteinaceous eggshells, and when compared to other sauropsids the team concluded that they were not biomineralized in life and thus soft-shelled. Given that soft-shelled eggs are more vulnerable to deshydratation and crushing, Protoceratops may have buried its eggs in moisturized sand or soil. The growing embryos therefore relied on external heat and parental care.
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.
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.
Osmólska in 1993 proposed another two hypotheses to explain their preservation. During the death struggle, a large dune may have collapsed simultaneously burying both Protoceratops and Velociraptor. Another proposal is that the Velociraptor was scavenging an already dead Protoceratops when it got buried and eventually killed by indeterminate circumstances.
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 sediments surrounding the specimen and suggested that the two were buried alive by a powerful sandstorm. They interpreted the interaction as the Protoceratops being grasped and dispatched with kicks delivered by the low-lying Velociraptor. They also considered possible that populations of Velociraptor were aware of crouching behaviors in Protoceratops during high-energy sandstorms and used it for successful hunts.
thumb|left|Size of the Fighting Dinosaurs
Kenneth Carpenter in 1998 considered the Fighting Dinosaurs specimen to be conclusive evidence for theropods as active predators and not scavengers. He suggested another scenario where the multiple wounds delivered by the Velociraptor on the Protoceratops throat had the latter animal bleeding to death. As a last effort, the Protoceratops bit the right hand of the predator and trapped it beneath its own weight, causing the eventual death and desiccation of the Velociraptor. The missing limbs of the Protoceratops were afterwards taken by scavengers. Lastly, both animals were buried by sand. Given that the Velociraptor is relatively complete, Carpenter suggested that it may have been completely or partially buried by sand.
In 2010, David Hone with team reported a new interaction between Velociraptor and Protoceratops based on tooth marks. Several fossils were collected at the Gate locality of the Bayan Mandahu Formation in 2008, including teeth and body remains of protoceratopsid and velociraptorine dinosaurs. The team referred these elements to Protoceratops and Velociraptor mainly based on their abundance across the unit, although they admitted that reported remains could represent different, yet related taxa (in this case, Linheraptor instead of Velociraptor). At least eight body fossils of Protoceratops present active teeth marks, which were interpreted as feeding traces. Much in contrast to the Fighting Dinosaurs specimen, the tooth marks are inferred to have been produced by the dromaeosaurid during late-stage carcass consumption either during scavenging or following a group kill. The team stated that feeding by Velociraptor upon Protoceratops was probably a relatively common occurrence in these environments, and that this ceratopsian actively formed part of the diet of Velociraptor.
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 backward 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 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 backward, making both predator and prey to be slightly separated.
Daily activity
thumb|Skull of P. andrewsi AMNH 6466, preserving scleral ring
In 2010, Nick Longrich examined the relatively large orbital ratio and scleral ring of Protoceratops, which he suggested as evidence for a nocturnal lifestyle. Based on the size of its scleral ring, Protoceratops had an unusually large eyeball among protoceratopsids. In birds, a medium-sized scleral ring indicates that the animal is a predator, a large scleral ring indicates that it is nocturnal, and the largest ring size indicates it is an active nocturnal predator. Eye size is an important adaptation in predators and nocturnal animals because a larger eye ratio poses a higher sensitivity and resolution. Because of the energy necessary to maintain a larger eyeball and the weakness of the skull that corresponds with a larger orbit, Longrich argues that this structure may have been an adaptation for a nocturnal lifestyle. The jaw morphology of Protoceratops—more suitable for processing plant material—and its extreme abundance indicate it was not a predator, so if it was a diurnal animal, then it would have been expected to have a much smaller scleral ring size. However, a subsequent study in 2021 found that Protoceratops had a greater capability of nocturnal vision than did Velociraptor.
Paleoenvironment
Bayan Mandahu Formation
thumb|left|Restoration of a P. hellenikorhinus pair in the Bayan Mandahu Formation
Based on general similarities between the vertebrate fauna and sediments of Bayan Mandahu and the Djadokhta Formation, the Bayan Mandahu Formation is considered to be Late Cretaceous in age, roughly Campanian. The dominant lithology is reddish-brown, poorly cemented, fine grained sandstone with some conglomerate, and caliche. Other facies include alluvial (stream-deposited) and eolian (wind-deposited) sediments. It is likely that sediments at Bayan Mandahu were deposited by short-lived rivers and lakes on an alluvial plain (flat land consisting of sediments deposited by highland rivers) with a combination of dune field paleoenvironments, under a semi-arid climate. The formation is known for its vertebrate fossils in life-like poses, most of which are preserved in unstructured sandstone, indicating a catastrophic rapid burial.
The paleofauna of Bayan Mandahu is very similar in composition to the nearby Djadokhta Formation, with both formations sharing several of the same genera, but differing in the exact species. In this formation, P. hellenikorhinus is the representative species, and it shared its paleoenvironment with numerous dinosaurs such as dromaeosaurids Linheraptor and Velociraptor osmolskae; oviraptorids Machairasaurus and Wulatelong; and troodontids Linhevenator, Papiliovenator, and Philovenator. Other dinosaur members include the alvarezsaurid Linhenykus; ankylosaurid Pinacosaurus mephistocephalus; and closely related protoceratopsid Bagaceratops. and a variety of squamates and mammals.
Djadokhta Formation
thumb|Restoration of a P. andrewsi group in the Djadokhta Formation
Protoceratops is known from most localities of the Djadokhta Formation in Mongolia, which dates back to the Late Cretaceous about 71 million to 75 million years ago, being deposited during a rapid sequence of polarity changes in the late part of the Campanian stage. Dominant sediments at Djadokhta include dominant reddish-orange and pale orange to light gray, medium to fine-grained sands and sandstones, caliche, and sparse fluvial (river-deposited) processes. Based on these components, the paleoenvironments of the Djadokhta Formation are interpreted as having a hot, semiarid climate with large dune fields/sand dunes and several short-lived water bodies, similar to the modern Gobi Desert. It is estimated that at the end of the Campanian age and into the Maastrichtian the climate would shift to the more mesic (humid/wet) conditions seen in the Nemegt Formation.
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. oviraptorid Oviraptor; Ukhaa Tolgod, a highly fossiliferous locality is also included in the Bayn Dzak member. ankylosaurid Minotaurasaurus; birds Apsaravis and Gobipteryx; dromaeosaurid Tsaagan; oviraptorids Citipati and Khaan; troodontids Almas and Byronosaurus; and a new, unnamed protoceratopsid closely related to Protoceratops. In the Turgrugyin Member (mainly Tugriken Shireh locality), P. andrewsi shared its paleoenvironment with the bird Elsornis; dromaeosaurids Mahakala and Velociraptor mongoliensis; and ornithomimid Aepyornithomimus.
The relatively low dinosaur paleodiversity, small body size of most dinosaurs, and arid settings of the Djadokhta Formation compared to those of the Nemegt Formation, suggest that Protoceratops and contemporaneous biota lived in a stressed paleoenvironment (physical factors that generate adverse impacts on the ecosystem).