Protoceratops(/ˌproʊtoʊˈsɛrətɒps/;lit. 'first horned face')[1]is agenusof smallprotoceratopsiddinosaurs that lived in Asia during theLate Cretaceous,around 75 to 71 million years ago. The genusProtoceratopsincludes two species:P. andrewsiand the largerP. hellenikorhinus.The former was described in 1923 with fossils from the MongolianDjadokhta Formation,and the latter in 2001 with fossils from the ChineseBayan Mandahu Formation.Protoceratopswas initially believed to be an ancestor ofankylosauriansand larger ceratopsians, such asTriceratopsand relatives, until the discoveries of other protoceratopsids. Populations ofP. andrewsimay haveevolvedintoBagaceratopsthroughanagenesis.
| Protoceratops Temporal range:Late Cretaceous,(Campanian) ~
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| MountedP. andrewsiskeleton,Wyoming Dinosaur Center | |
Scientific classification
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| Domain: | Eukaryota |
| Kingdom: | Animalia |
| Phylum: | Chordata |
| Clade: | Dinosauria |
| Clade: | †Ornithischia |
| Clade: | †Neornithischia |
| Clade: | †Ceratopsia |
| Clade: | †Coronosauria |
| Family: | †Protoceratopsidae |
| Genus: | †Protoceratops Granger&Gregory,1923 |
| Type species | |
| †Protoceratops andrewsi Granger & Gregory, 1923
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| Other species | |
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Protoceratopswere 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 largelyquadrupedal,juveniles had the capacity to walk aroundbipedally if necessary.They were characterized by a proportionally largeskull,short and stiff neck, andneck frill.The frill was likely used fordisplayorintraspecific combat,as well asprotectionof the neck and anchoring of jaw muscles. A horn-like structure was present over the nose, which varied from a single structure inP. andrewsito a double, paired structure inP. hellenikorhinus.The "horn" and frill were highly variable in shape and size across individuals of the same species, but there is no evidence ofsexual dimorphism.They had a prominent parrot-like beak at the tip of the jaws.P. andrewsihad a pair of cylindrical, bluntteethnear the tip of the upper jaw. The forelimbs had fivefingersof which only the first three bore wide and flatunguals.Thefeetwere wide and had four toes with flattened, shovel-like unguals, which would have been useful fordiggingthrough the sand. The hindlimbs were longer than the forelimbs. The tail was long and had an Enigma ticsail-like structure, which may have been used for display,swimming,ormetabolicreasons.
Protoceratops,like many other ceratopsians, wereherbivoresequipped with prominent jaws and teeth suited for choppingfoliageand other plant material. They are thought to have lived in highlysociablegroups of mixed ages. They appear to havecared for their young.They laid soft-shelledeggs,a rare occurrence in dinosaurs. During maturation, the skull and neck frill underwent rapid growth.Protoceratopswere hunted byVelociraptor,and one particularly famous specimen (theFighting Dinosaurs) preserves a pair of them locked in combat.Protoceratopsused to be characterized asnocturnalbecause of the largesclerotic ringaround the eye, but they are now thought to have beencathemeral(active at dawn and dusk).
History of discovery
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In 1900Henry Fairfield Osbornsuggested that Central Asia may have been the center of origin of most animal species,including humans,which caught the attention of explorer andzoologistRoy 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 andMongolia,organized by theAmerican Museum of Natural Historyunder 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 famousFlaming Cliffsof the Shabarakh Usu region of theDjadokhta Formation,Gobi Desert,now known as the Bayn Dzak region. On 2 September, the photographerJames B. Shackelforddiscovered a partial juvenile skull—which would become theholotypespecimen (AMNH 6251) ofProtoceratops—in reddishsandstones.It was subsequently analyzed by the paleontologistWalter W. Grangerwho identified it asreptilian.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 dinosaurfossilsand 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.[2][3]
In 1923 the expedition again prospected the Flaming Cliffs, this time discovering even more specimens ofProtoceratopsand also the first remains ofOviraptor,SaurornithoidesandVelociraptor.Most notably, the team discovered the first fossilized dinosaureggsnear the holotype ofOviraptorand given how abundantProtoceratopswas, the nest was attributed to thistaxon.[3]This would later result in the interpretation ofOviraptoras anegg-thief.[4]In the same year, Granger and William K. Gregory formally described the new genus and speciesProtoceratops andrewsibased on the holotype skull. Thespecific name,andrewsi,is in honor of Andrews for his prominent leadership during the expeditions. They identifiedProtoceratopsas anornithischiandinosaur closely related to ceratopsians representing a possible common ancestor betweenankylosaursandceratopsians.SinceProtoceratopswas more primitive than any other known ceratopsian at that time, Granger and Gregory coined the new familyProtoceratopsidae,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.[2]Although not stated in the original description, thegeneric name,Protoceratops,is intended to mean "first horned face" as it was believed thatProtoceratopsrepresented an early ancestor ofceratopsids.[5]Other researchers immediately noted the importance of theProtoceratopsfinds, and the genus was hailed as the "long-sought ancestor ofTriceratops".Most fossils were in an excellent state of preservation with evensclerotic rings(delicate ocular bones) preserved in some specimens, quickly makingProtoceratopsone of the best-known dinosaurs from Asia.[3][6]
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 ofProtoceratops.By this time,Protoceratopshad 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 ofProtoceratopswere collected in later years of the expeditions, they were most abundant in the 1922 to 1925 seasons.[3][6]Gregory andCharles C. Mookpublished another description ofProtoceratopsin 1925, discussing its anatomy and relationships. Thanks to the large collection of skulls found in the expeditions, they concluded thatProtoceratopsrepresented a ceratopsian more primitive than ceratopsids and not an ankylosaur-ceratopsian ancestor.[7]In 1940,Barnum BrownandErich Maren Schlaikjerdescribed the anatomy ofP. andrewsiin extensive detail using newly prepared specimens from the Asiatic expeditions.[6]
In 1963, the Mongolian paleontologistDemberelyin Dashzevegreported the discovery of a new fossiliferous locality of the Djadokhta Formation: Tugriken Shireh. Like the neighbouring Bayn Dzak, this new locality contained an abundance ofProtoceratopsfossils.[8]During the 1960s to 1970s, Polish-Mongolian and Russian-Mongolian paleontological expeditions collected new, partial to complete specimens ofProtoceratopsat 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 ofProtoceratops,such as theFighting Dinosaurs,[9]in situindividuals—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]
Stephan N. F. Spiekmanand colleagues reported a partialP. andrewsiskull (RGM 818207) in the collections of theNaturalis Biodiversity Center,Netherlandsin 2015. SinceProtoceratopsfossils are only found in the Gobi Desert of Mongolia and this specimen was likely discovered during the Central Asiatic Expeditions, the team concluded that this skull was probably acquired byDelft Universitybetween 1940 and 1972 as part of a collection transfer.[15]
Species and synonyms
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Protoceratopsid remains were recovered in the 1970s from the Khulsan locality of theBarun Goyot Formation,Mongolia, during the work of several Polish-Mongolian paleontological expeditions. In 1975, Polish paleontologistsTeresa MaryańskaandHalszka Osmólskadescribed a second species ofProtoceratopswhich they namedP. 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 paleontologistRoman Kozłowski.They also named the new genus and species of protoceratopsidBagaceratops rozhdestvenskyi,known from specimens of the nearby Hermiin Tsav locality.[10]In 1990 the Russian paleontologistSergei Mikhailovich Kurzanovreferred additional material from Hermiin Tsav toP. kozlowskii.However, he noted that there were enough differences betweenP. andrewsiandP. kozlowskii,and erected the new genus and combinationBreviceratops kozlowskii.[16]ThoughBreviceratopshas been regarded as asynonymand juvenile stage ofBagaceratops,[17][18]Łukasz Czepińskiin 2019 concluded that the former has enough anatomical differences to be considered as a separatetaxon.[19]
In 2001Oliver Lambertwith colleagues named a new and distinct species ofProtoceratops,P. hellenikorhinus.The first known remains ofP. hellenikorhinuswere collected from the Bayan Mandahu locality of theBayan Mandahu Formation,Inner Mongolia, in 1995 and 1996 duringSino-Belgian paleontological expeditions. The holotype (IMM 95BM1/1) andparatype(IMM 96BM1/4) specimens consist of large skulls lacking body remains. The holotype skull was found facing upwards, a pose that has been reported inProtoceratopsspecimens from Tugriken Shireh. The specific name,hellenikorhinus,is derived fromGreekhellenikos (meaning Greek) and rhis (meaning nose) in reference to its broad and angular snout, which is reminiscent of the straight profiles ofGreek sculptures.[20]In 2017 abundant protoceratopsid material was reported fromAlxanear Bayan Mandahu,[21]and it may be preferable toP. hellenikorhinus.[19]
Viktor TereshchenkoandVladimir R. Alifanovin 2003 named a new protoceratopsid dinosaur from the Bayn Dzak locality,Bainoceratops efremovi.This genus was based on a few dorsal (back) vertebrae that were stated to differ from those ofProtoceratops.[22]In 2006 North American paleontologistsPeter MakovickyandMark A. Norellsuggested thatBainoceratopsmay be synonymous withProtoceratopsas most of the traits used to separate the former from the latter have been reported from other ceratopsians includingProtoceratopsitself, and they are more likely to fall within the wide intraspecific variation range of the concurringP. andrewsi.[23]The authorsBrenda J. ChinneryandJhon R. Hornerin 2007 during their description ofCerasinopsstated thatBainoceratops,along with other dubious genera, was determined to be either a variant or immature specimen of other genera. Based on this reasoning, they excludedBainoceratopsfrom their phylogenetic analysis.[24]
Eggs and nests
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As part of the Third Central Asiatic Expedition of 1923, Andrews and team discovered the holotype specimen ofOviraptorin 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 ofProtoceratopsin theformation,these eggs were believed at the time to belong to this dinosaur. This resulted in the interpretation of the contemporaryOviraptoras an egg predatory animal, an interpretation also reflected in its generic name.[25][4]In1975,the Chinese paleontologistZhao Zikuinamed the newoogeneraElongatoolithusandMacroolithus,including them in a newoofamily:theElongatoolithidae.As the name implies, they represent elongated dinosaur eggs, including some of referred ones toProtoceratops.[26]
In 1994 the Russian paleontologist Konstantin E. Mikhailov named the new oogenusProtoceratopsidovumfrom theBarun Goyotand Djadokhta formations, with the type speciesP. sincerumand additionalP. fluxuosumandP. minimum.Thisootaxonwas firmly stated as belonging to protoceratopsid dinosaurs since they were the predominant dinosaurs where the eggs were found and some skeletons ofProtoceratopswere found in close proximity toProtoceratopsidovumeggs. More specifically, Mikhailov stated thatP. sincerumandP. minimumwere laid byProtoceratops,andP. fluxuosumbyBreviceratops.[27]
However, also during 1994, Norell and colleagues reported and briefly described a fossilizedtheropodembryoinside an egg (MPC-D 100/971) from the Djadokhta Formation. They identified this embryo as anoviraptoriddinosaur 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 toOviraptorand rather than an egg-thief, the holotype was actually a mature individual that perished brooding the eggs.[28]Moreover,phylogenetic analysespublished in 2008 by Darla K. Zelenitsky and François Therrien have shown thatProtoceratopsidovumrepresents the eggs of amaniraptoranmore derived than oviraptorids and notProtoceratops.[29]The description of the eggshell ofProtoceratopsidovumhas further confirmed that they in fact belong to a maniraptoran, possiblydeinonychosaurtaxon.[30]
Nevertheless, in 2011 an authentic nest ofProtoceratopswas 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) ofProtoceratopsfrom the also fossiliferous Ukhaa Tolgod locality, discovered during paleontological expeditions of the American Museum of Natural History andMongolian 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
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TheFighting Dinosaursspecimen preserves aProtoceratops(MPC-D 100/512) andVelociraptor(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 andNemegtformations. During fieldwork on 3 August several fossils ofProtoceratopsandVelociraptorwere found at the Tugriken Shire locality (Djadokhta Formation) including a block containing one of each. The individuals in this block were identified as aP. andrewsiandV. mongoliensis.Although the conditions surrounding their burial were not fully understood, it was clear that they died simultaneously in a struggle.[9]
The specimen, nicknamed the "Fighting Dinosaurs", has been examined and studied by numerous researchers and paleontologists, and there are various opinions on how the animals were buried and preserved altogether. Though a drowning scenario has been proposed by Barsbold,[33]such a hypothesis is considered unlikely given the arid paleoenvironments of the Djadokhta Formation. It is generally thought that they were buried alive by a sandstorm or a collapseddune.[34][35][36]
Skin impressions and footprints
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During the Third Central Asiatic Expedition in 1923, a nearly completeProtoceratopsskeleton (specimen AMNH 6418) was collected at the Flaming Cliffs. Unlike other specimens, it was discovered in a rolled-up position with itsskullpreserving a thin, hard, and wrinkled layer ofmatrix(surroundingsediments). This specimen was later described in 1940 by Brown and Schlaikjer, who discussed the nature of the matrix portion. They stated that this layer had a very skin-like texture and covered mostly the left side of the skull from thesnoutto theneck frill.Brown and Schlaikjer discarded the idea of possible skin impressions as this skin-like layer was likely a product of thedecayand burial of the individual, making the sediments become highly attached to the skull.[6]
The potential importance of these remains were unrecognized or 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 therostrum.[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 subadultProtoceratopsskeleton (specimen ZPAL Mg D-II/3) was collected from the Bayn Dzak locality of the Djadokhta Formation. In the 2000s during thepreparationof the specimen, a fossilized cast of a four-toeddigitigradefootprint 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 forProtoceratops.[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
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Protoceratopswas a relatively small-sizedceratopsian,with bothP. andrewsiandP. hellenikorhinusestimated 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
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TheskullofProtoceratopswas relatively large compared to its body and robustly built. The skull of the type species,P. andrewsi,had an average total length of nearly 50 cm (500 mm). On the other handP. hellenikorhinushad a total skull length of about 70 cm (700 mm). The rear of the skull gave form to a pronouncedneck frill(also known as "parietal frill" ) mostly composed of theparietalandsquamosalbones. The exact size and shape of the frill varied by individual; some had short, compact frills, while others had frills nearly half the length of the skull. The squamosal touched thejugal(cheekbone) and was very enlarged and high having a curved end that built the borders of the frill. The parietals were the posteriormost bones of the skull and major elements of the frill. In a top view they had a triangular shape and were joined by thefrontals(bones of theskull roof). Both parietals werecoossified(fused), creating a long ridge on the center of the frill. The jugal was deep and sharply developed and along with thequadratojugalthey formed a horn-like extension that pointed to below at the lateral sides of the skull. Theepijugal(tip region of the jugal) was separated from the jugal by a prominentsuture;this suture was more noticeable in adults. The surfaces around the epijugal were coarse, indicating that it was covered by ahornysheath. Unlike the much derivedceratopsids,the frontal andpostorbitalbones ofProtoceratopswere flat and lacked horn cores or supraorbital horns. Thepalpebral(small spur-like bone) joined the prefrontal over the front of theorbit(eye socket). InP. hellenikorhinusthe palpebral protruded upwards from theprefrontal,just above the orbit and slightly meeting the frontal, creating a small horn-like structure. Thelacrimalwas a near-rectangular bone located in front of the orbit, contributing to the shape of the latter. Thesclerotic ring(structure that supports theeyeball), found inside the orbit, was circular in shape and formed by consecutive bony plates.[6][20]
Thesnoutwas formed by thenasal,maxillar,premaxillar androstralbones. The nasal was generally rounded but some individuals had a sharp nasal Boss (a feature that has been called "nasal horn" ). InP. hellenikorhinusthis Boss was divided in two sharp and long ridges. The maxilla was very deep and had up to 15alveoli(toothsockets) on its underside or teeth bearing surface. The premaxilla had two alveoli on its lower edge—a character that was present at least onP. andrewsi.The rostral bone was devoid of teeth, high and triangular in shape. It had a sharp end and rough texture, which reflects that arhamphotheca(hornybeak) was present. As a whole, the skull had four pairs offenestrae(skull openings). The foremost hole, thenares(nostril opening), was oval-shaped and considerably smaller than the nostrils seen in ceratopsids.Protoceratopshad large orbits, which measured around 5 cm (50 mm) in diameter and had irregular shapes depending on the individual. The forward facing and closely located orbits combined with a narrow snout, gaveProtoceratopsa well-developedbinocular vision.Behind the eye was a slightly smaller fenestra known as theinfratemporal fenestra,formed by the curves of the jugal and squamosal. The last openings of the skull were two parietal fenestrae (holes in the frill).[6][20]
The lower jaw ofProtoceratopswas a large element composed of thepredentary,dentary,coronoid,angularandsurangular.The predentary (frontmost bone) was very pointed and elongated, having a V-shapedsymphyseal(bone union) region at the front. The dentary (teeth-bearing bone) was robust, deep, slightly recurved, and fused to the angular and surangular. A large and thick ridge ran along the lateral surface of the dentary that connected the coronoidprocess—a bony projection that extends upwards from the upper surface of the lower jaw behind the tooth row—and surangular. It bore up to 12–14 alveoli on its top margin. Both predentary and dentary had a series of foramina (small pits), the latter mostly on its anterior end. The coronoid (highest point of the lower jaw) was blunt-shaped and touched by the coronoid process of the dentary, being obscured by the jugal. The surangular was near triangular in shape and in old individuals it was coossified together with the coronoid process. The angular was located below the two latter bones and behind the dentary. It was a large and somewhat rounded bone that complemented the curvature of the dentary. On its inner surface it was attached to thearticular.The articular was a smaller bone and had a concavity on its inner surface for the articulation with the quadrate.[6][20]
Protoceratopshad leaf-shaped dentary and maxillary teeth that bore severaldenticles(serrations) on their respective edges. Thecrowns(upper exposed part) had two faces or lobes that were divided by a central ridge-like structure (also called "primary ridge" ). The teeth were packed into a single row that created a shearing surface. Both dentary and maxillary teeth presented markedhomodonty—a dental condition where the teeth share a similar shape and size.P. andrewsibore two small, peg to spike-like teeth that were located on the underside of each premaxilla. The second premaxillary tooth was larger than the first one. Unlike dentary and maxillary teeth, the premaxillary dentition was devoid of denticles, having a relatively smooth surface. All teeth had a single root (lower part inserted in the alveoli).[6][45][46]
Postcranial skeleton
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Thevertebral columnofProtoceratopshad nine cervical (neck), 12 dorsal (back), eight sacral (pelvic) and over 40 caudal (tail) vertebrae. Thecentra(centrum; body of the vertebrae) of the first three cervicals were coossified together (atlas,axisand 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 theneural arch(upper, and pointy vertebral region) was a thin, narrow bar of bone that extended upwards and backward to the base of the axis neuralspine.The capitular facet (attachment site forchevrons;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 theoccipital condyleof 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.[6][47][48]
Thedorsal vertebraewere 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. Thesacral vertebraewere 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. Thecaudal vertebraedecreased in size progressively towards the end and had very elongated neural spines in the mid-series, forming asail-like structure. This elongation started from the first to the fourteenth caudal. The centra wereheterocoelous(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 ofProtoceratopshad 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 ofProtoceratops,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.[6]
Thepectoral girdleofProtoceratopswas formed by thescapulocoracoid(fusion of the coracoid and scapula) and clavicle. Thescapulae(shoulder blades) were relatively large and rounded on their inner sides. At their upper region, the scapulae were wide. At their lower region, the scapulae meet the coracoids. Thecoracoidswere relatively elliptical, and sometimes coosified (fused) to the scapulae. The clavicle ofProtoceratopswas an U to slightly V-shaped element that joined to the upper border of the scapulocoracoid. In its general form, the forelimbs ofProtoceratopswere shorted than the hindlimbs, and composed by the humerus, radius, and ulna. Thehumerus(upper arm bone) was large and slender, and at the lower part it met with both radius and ulna. Theradiushad a slightly recurved shape and was longer than the ulna. A concavity was present on its upper part, serving as the connection with the humerus and forming the elbow. Theulnawas a rather short bone with a straight shape. Themanus(hand) ofProtoceratopshad fivedigits(fingers). The first three fingers hadunguals(claw bones) and were the largest digits. The last two were devoid of unguals and had a small size, mostlyvestigial(retained, but without important function). Both hand and feet unguals were flat, blunt and hoof-like.[6][40]
Thepelvic girdlewas formed by theilium,pubis,andischium.The ilium was a large element, having a narrow preacetabular process (anterior end) and a wide postacetabular process (posterior end). The pubis was the smallest element of the pelvic girdle and it had an irregular shape, although its lower end was developed into a pointed bony projection downward. The ischium was the longest bone of the pelvic girdle. It had an elongated shaft with a somewhat wide lower end. The hindlimbs ofProtoceratopswere rather long, with a slighter longer tibia (lower leg bone) than femur (thigh bone). Thefemur(thighbone) was robust and had a rather rounded and pronouncedgreater trochanter,which was slightly recurved into the inner sides. Thetibia(shinbone) was long and slender with a wide lower end. On its upper region a concavity was developed for the joint with the smallerfibula.Thepes(foot) were composed of fourmetatarsaland four toes which bore shovel-like pedal unguals. The first metatarsal and toe were the smallest, while the other elements were of similar shape and length.[6][40]
Classification
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Protoceratopswas in 1923 placed within the newly namedfamilyProtoceratopsidaeas the representative species by Granger and Gregory. This family was characterized by their overall primitive morphology in comparison to the more derivedCeratopsidae,such as lack of well-developed horn cores and relative smaller body size.Protoceratopsitself was considered by the authors to be somehow related toankylosauriansbased on skull traits, with a more intensified degree toTriceratopsand relatives.[2]Gregory and Charles C. Mook in 1925 upon a more deeper analysis ofProtoceratopsand its overall morphology, concluded that thistaxonrepresents a ceratopsian more primitive than ceratopsids and not an ankylosaur-ceratopsian ancestor.[7]In 1951 Edwin H. Colbert consideredProtoceratopsto represent a key ancestor for the ceratopsid lineage, suggesting that it ultimately led to the evolution of large-bodied ceratopsians such asStyracosaurusandTriceratops.Such lineage was suggested to have started from the primitive ceratopsianPsittacosaurus.He also regardedProtoceratopsas 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 frompsittacosaurids,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 likeBagaceratopsorProtoceratops(such as the jaw morphology). Maryanska and Osmolska also emphasized that some early members of the Ceratopsidae reflect a much older evolutionary history.[10]In 1998, paleontologistPaul Serenoformally defined Protoceratopsidae as thebranch-basedcladeincluding allcoronosaurscloser toProtoceratopsthan toTriceratops.[51]
Furthermore, with the re-examinations ofTuranoceratopsin 2009 andZuniceratops—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 ofProtoceratopsand relatives.[52][53]In most recent/modern phylogenetic analysesProtoceratopsandBagaceratopsare commonly recovered assister taxa,leaving the interpretations proposing direct relationships with more derived ceratopsians unsupported.[54]
In 2019 Czepiński analyzed a vast majority of referred specimens to the ceratopsiansBagaceratopsandBreviceratops,and concluded that most were in fact specimens of the former. Although the generaGobiceratops,Lamaceratops,Magnirostris,andPlatyceratops,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 inBagaceratopsand thus becoming synonyms of this genus. Under this reasoning, Protoceratopsidae consists ofBagaceratops,Breviceratops,andProtoceratops.Below are the proposed relationships among Protoceratopsidae by Czepiński:[19]
In 2019 Bitnara Kim and colleagues described a relatively well-preservedBagaceratopsskeleton from theBarun Goyot Formation,noting numerous similarities withProtoceratops.Even though their respective skull anatomy had substantial differences, their postcranial skeleton was virtually the same. Thephylogenetic analysisperformed by the team recovered both protoceratopsids as sister taxa, indicating thatBagaceratopsandProtoceratopswere anatomically andsystematicallyrelated. Below is the obtainedcladogram,showing the position ofProtoceratopsandBagaceratops:[55]
Evolution
edit
Longrich and team in 2010 indicated that highly derived morphology ofP. hellenikorhinus—when compared toP. andrewsi—indicates that this species may represent a lineage ofProtoceratopsthat had a longer evolutionary history compared toP. andrewsi,or simply a direct descendant ofP. andrewsi.The difference in morphologies betweenProtoceratopsalso suggests that the nearbyBayan Mandahu Formationis 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 betweenBagaceratops rozhdestvenskyi(which is native to adjacent Bayan Mandahu andBarun Goyot) andP. andrewsi.The specimen hails from the Udyn Sayr locality, whereProtoceratopsremains are dominant, and given the lack of more conclusive anatomical traits, Czepiński assigned the specimen asBagaceratopssp. He explained that the presence of thisBagaceratopsspecimen in such unusual locality could be solved by: (1) the coexistence andsympatric(altogether) evolution of bothBagaceratopsandProtoceratopsat this one locality; (2) the rise ofB. rozhdestvenskyiin a different region and eventual migration to Udyn Sayr; (3)hybridizationbetween the two protoceratopsids given the near placement of both Bayan Mandahu and Djadokhta; (4)anagenetic(progressive evolution) evolutionary transition fromP. andrewsitoB. rozhdestvenskyi.Among scenarios, an anagenetic transition was best supported by Czepiński given the fact that no definitiveB. rozhdestvenskyifossils 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 ifB. rozhdestvenskyihad migrated to the area; and many specimens ofP. andrewsirecovered at Udyn Sayr already feature a decrease in the presence of primitive premaxillary teeth, hence supporting a growing change in the populations.[57]
Paleobiology
editFeeding
editIn 1955, paleontologistGeorg Haasexamined the overall skull shape ofProtoceratopsand attempted to reconstruct itsjaw musculature.He suggested that the largeneck frillwas likely an attachment site for masticatory muscles. Such placement of the muscles may have helped to anchor the lower jaws, useful for feeding.[58]Yannicke Dauphin and colleagues in 1988 described theenamelmicrostructure ofProtoceratops,observing a non-prismatic outer layer. They concluded that enamel shape does not relate to thedietor function of theteethas most animals do not necessarily use teeth to process food. The maxillary teeth of ceratopsians were usually packed into adental batterythat formed vertical shearing blades which probably chopped theleaves.This feeding method was likely more efficient in protoceratopsids as the enamel surface ofProtoceratopswas 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 ofProtoceratopshad no specific function.[45]
In 1991, the paleontologistGregory S. Paulstated that contrary to the popular view of ornithischians as obligateherbivores,some groups may have been opportunisticmeat-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,boarsandentelodonts.Such scenario indicates a possible competition with the more predatorytheropodsovercarcasses,however, as the animal tissue ingestion was occasional and not the bulk of their diet, theenergy flowinecosystemswas relatively simple.[59]You Hailu and Peter Dodson in 2004 suggested that the premaxillary teeth ofProtoceratopsmay have been useful for selective cropping and feeding.[60]
In 2009, Kyo Tanque and team suggested that basal ceratopsians, such as protoceratopsids, were most likely lowbrowsersdue to their relatively small body size. This low-browsing method would have allowed to feed onfoliageand fruits within range, and large basal ceratopsians may have consumed tougherseedsor plant material not available to smaller basal ceratopsians.[61]
David J. ButtonandLindsay E. Zannoin 2019 performed a large phylogenetic analysis based on skullbiomechanicalcharacters—provided by 160Mesozoicdinosaur 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 lowbite 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 withEuoplocephalus,Hungarosaurus,parkosaurid,ornithopodandheterodontosaurinedinosaurs, were found to be in the former category, indicating thatProtoceratopsand relatives had strong bite forces and relied mostly on its jaws to process food.[62]
Ontogeny
edit
Brown and Schlaikjer in 1940 upon their large description and revision ofProtoceratopsremarked 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 theneck frillas 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 matureProtoceratopsindividuals.[6]In 2001, Lambert and colleagues considered the development of the two nasal "horns" ofP. hellenikorhinusto 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 matureP. andrewsiskull (AMNH 6409), and yet it lacks double nasal horns present in fully matureP. hellenikorhinus.[20]
Makovicky and team in 2007 conducted ahistologicalanalysis on several specimens ofProtoceratopsfrom theAmerican Museum of Natural Historycollections to provide insights into the life history ofProtoceratops.The examined fossil bones indicated thatProtoceratopsslowed itsontogeny(growth) around 9–10 years of life, and it ceased around 11–13 years. They also observed that the maximum or latest stage of development of the neck frill and nasal horn occurred in the oldestProtoceratopsindividuals, indicating that such traits were ontogenically variable (meaning that they varied with age). Makovicky and team also stated that as the maximum/radical changes on the neck frill and nasal horn were present in most adult individuals, trying to differentiatesexual dimorphism(anatomical differences between sexes) in adultProtoceratopsmay not be a good practice.[63]
David Hone and colleagues in 2016 upon their analysis ofP. andrewsineck frills, found that the frill ofProtoceratopswas 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 approachingadulthood.[64]
In 2017, Mototaka Saneyoshi with team analyzed severalProtoceratopsspecimens from theDjadokhta Formation,noting that fromperinate/juvenile to subadult individuals, the parietal and squamosal bones increased their sides to posterior sides of the skull. From subadult to adult individuals, the squamosal bone increased in size more than the parietal bone, and the frill expanded to a top direction. The team concluded that the frill ofProtoceratopscan be characterized by these ontogenetic changes.[65]
In 2018, paleontologists Łucja Fostowicz-Frelik and Justyna Słowiak studied the bone histology of several specimens ofP. andrewsithrough 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 ofProtoceratopsremained rather uniform throughout ontogeny. It was characterized by simple fibrolamellar bone—bony tissue with an irregular,fibroustexture and filled withblood vessels—with prominentwoven-fibered bone and lowbone remodeling.Most bones ofProtoceratopspreserve a large abundance of bone fibers (includingSharpey's fibres), which likely gave strength to theorganand 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 primitivePsittacosaurusorScutellosaurus.[66]
Movement
edit
In 1996, Tereshchenko reconstructed the walking model ofProtoceratopswhere he considered the most likely scenario to beProtoceratopsas an obligatequadrupedgiven the proportions of its limbs. The main gait ofProtoceratopswas probablytrot-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),Protoceratopscould have employed a rapid,facultative bipedalism.He also noted that the flat and wide pedal unguals ofProtoceratopsmay have allowed efficient walking through loose terrain, such assandwhich was common on its surroundings. Tereshchenko usingspeedequationsalso estimated the average maximum walking speed ofProtoceratopsat about 3 km/h (kilometres per hour).[67]
Upon the analysis of the forelimbs of several ceratopsians, Phil Senter in 2007 suggested that the hands ofProtoceratopscould 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 ofProtoceratopscould 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 ofProtoceratopsto estimate overall mobility, and concluded thatProtoceratopshad 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 thatProtoceratopswasdigitigrade,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 ofbipedalceratopsians such as a narrow glenoid with scapular blade and an arched femur. The absence of these traits in mature individuals indicates that youngProtoceratopswere capable of facultative bipedal locomotion and adults had an obligate quadrupedal stance. Even though adultProtoceratopswere stocky and quadruped, their tibia-femur length ratio—the tibia being longer than femur, a trait present in bipedal ceratopsians—suggests the ability to occasionally stand on their hindlimbs. Słowiak and team also suggested that the flat and wide hand unguals (claw bone) ofProtoceratopsmay have been useful for moving on loose terrain (such as sand) without sinking.[40]
Digging behavior
edit
Longrich in 2010 proposed thatProtoceratopsmay have used its hindlimbs todig burrowsor take shelter underbushesand/or scrapes to escape the hottest temperatures of theday.A digging action with the hindlimbs was likely facilitated by the strongcaudofemoralismuscle and its large feet equipped with flat, shovel-like unguals. As this behavior would have been common inProtoceratops,it predisposed individuals to become entombed alive during the sudden collapse of theirburrowsand high energy sand-bearing events—such assandstorms—and thus explaining the standingin-situposture of some specimens. Additionally, Longrich suggested that a backward burrowing could explain the preservation of some specimens pointing forward with curved tails.[69]
In 2019, Victoria M. Arbour and David C. Evans cited the robusticity of the ulna ofFerrisaurusas a useful feature for digging, which may have been also true forProtoceratops.[70]
Tail function
edit
Gregory and Mook in 1925 suggested thatProtoceratopswas partiallyaquaticbecause 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 forswimming.[6]Barsbold in his brief 1974 description of theFighting Dinosaursspecimen accepted this hypothesis and suggested thatProtoceratopswas 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 somedesertlizard species (such asHelodermaorUromastyx), which are related to store fat withmetabolic waterin the tail. He considered a swimming adaptation unlikely given thearidsettings of the Djadokhta Formation.[71]
In 2008, based on the occurrence of someProtoceratopsspecimens influvial(river-deposited)sedimentsfrom the Djadokhta Formation andheterocoelous(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 apaddleto aid in swimming. According to Tereschenko,Bagaceratopswas fully aquatic whileProtoceratopswas only partially aquatic.[72]Longrich in 2010 argued that the high tail and frill ofProtoceratopsmay 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 developedcooling mechanisms.[69]
In 2011, during the description ofKoreaceratops,Yuong-Nam Lee and colleagues found the above swimming hypotheses hard to prove based on the abundance ofProtoceratopsineolian(wind-deposited) sediments that were deposited in prominent arid environments. They also pointed out that while taxa such asLeptoceratopsandMontanoceratopsare recovered from fluvial sediments, they are estimated to be some of the poorest swimmers. Lee and colleagues concluded that even though the tail morphology ofKoreaceratops—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 ofProtoceratops,concluding that it had adaptations forterrestrialand 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 thatProtoceratopsraised its tail as a signal (display) or females could use this method duringegg layingto expand and relax thecloaca.[49]
In 2016, Hone and team indicated that the tail ofProtoceratops,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 bothBagaceratopsandProtoceratopsmay 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 ascrocodylomorphs.[55]
Social behavior
edit
Tomasz Jerzykiewiczz in 1993 reported severalmonospecific(containing only one dominant species) death assemblages ofProtoceratopsfrom the Bayan Mandahu and Djadokhta formations. A group of five medium-sized and adultProtoceratopswas 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 21degreesfrom 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.[12]
In 2014, David W. E. Hone and colleagues reported and described two blocks containing death assemblages ofP. andrewsifrom 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 thatProtoceratopswas asocial dinosaurthat formedherdsthroughout 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 bypredationor other factors, the remnants individuals wouldaggregateinto larger groups to increase their survival. Hone and colleagues in particular suggested that juveniles would aggregate primarily as adefense against predatorsand an increased protection from the multiple adults within the group. The team also indicated that, whileProtoceratopsprovides direct evidence for the formation of single cohort aggregations throughout its lifespan, it cannot be ruled out the possibility that someProtoceratopswere solitary.[14]
Sexual dimorphism and display
edit
Brown and Schlaikjer in 1940 upon their large analysis ofProtoceratopsnoted the potential presence ofsexual dimorphismamong specimens inP. 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 betweenP. andrewsiskulls from Bayn Dzak and Tugriken Shireh, noting differences on the nasal horn within populations.[74]
Peter Dodsonin 1996 used anatomical characters of the skull inP. andrewsito 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 indisplaying behaviorthan 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 maleProtoceratopsmay 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 thatsexual maturityinProtoceratopscould be recognised at the moment when males can be distinguished from females.[75]
In 2001, Lambert and team upon the description ofP. hellenikorhinusalso 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 maleP. 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 inP. hellenikorhinusdue to the lack of complete specimens.[20]Also in 2001, Tereschhenko analized several specimens ofP. andrewsito evaluate sexual dimorphism. He found 19 anatomical differences in thevertebral columnandpelvic regionof regarded male and femaleProtoceratopsindividuals, which he considered to represent actual sexual characters.[76]
In 2012, Naoto Handa and colleagues described four specimens ofP. andrewsifrom 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 mostProtoceratopsspecimens (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 markedintraspecific variationwithinProtoceratops,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 ofProtoceratopsfrom the Djadokhta Formation in the adjacent dinosaur locality Tugrikin Shire. The morphological differences among the Udyn Sayr specimens may indicate intraspecific variation ofProtoceratops.[77]A large and well-developed bony ridge on the parietal has been observed on anotherP. andrewsispecimen, MPC-D 100/551, also from Udyn Sayr.[57]
However, Leonardo Maiorino with team in 2015 performed a largegeometric morphometricanalysis using 29 skulls ofP. andrewsito 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 regardedProtoceratopsmale, 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 forP. hellenikorhinus,the team argued that the sample used for this species was not sufficient, and given that sexual dimorphism was not recovered inP. andrewsi,it is unlikely that it occurred inP. hellenikorhinus.[78]
In 2016, Hone and colleagues analyzed 37 skulls ofP. andrewsi,finding that the neck frill ofProtoceratops(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 ofProtoceratopssuch as the premaxillary teeth (at least forP. andrewsi) which could have been used in display orintraspecific combat,or the high neural spines of tail. On the other hand, Hone and team argued that if neck frills were instead used forprotectivepurposes, a large frill may have acted as anaposematic(warning) signal to predators. However, such strategies are most effective when the taxon is rare in the overall environment, opposed toProtoceratopswhich appears to be an extremelyabundantand medium-sized dinosaur.[64]
Tereschenko in 2018 examined the cervical vertebrae series of sixP. andrewsispecimens. 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 ofProtoceratops.[79]
In 2020 nevertheless, Andrew C. Knapp and team conducted morphometric analyses of a large sample ofP. andrewsispecimens, primarily confluding that the neck frill ofProtoceratopshas no indicators or evidence for being sexually dimorphic. Obtained results showed instead that several regions of the skull ofProtoceratopsindependently 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 insignalingwithin the species, consistent withselection of potential mateswith qualityornamentationand hencereproductive success,ordominance signaling.Such use of the frill may suggest that intraspecificsocial behaviorwas highly important forProtoceratops.Results also support the general hypothesis that the neck frill of ceratopsians functioned as a socio-sexual signal structure.[80]
Reproduction
edit
In 1989, Walter P. Coombs concluded thatcrocodilians,ratiteandmegapodebirds were suitable modern analogs for dinosaurnesting behavior.He largely consideredelongatoolithideggs to belong toProtoceratopsbecause adult skeletons were found in close proximity tonests,interpreting this as an evidence forparental care.Furthermore, Coombs considered the large concentration ofProtoceratopseggs at small regions as an indicator of markedphilopatric nesting(nesting in the same area). The nest ofProtoceratopswould have been excavated with the hindlimbs and was built in a mound-like,crater-shaped center structure with the eggs arranged in semicircular fashion.[81]Richard A. Thulborn in 1992 analyzed the different types of eggs and nests—the majority of them, in fact, elongatoolithid—referred toProtoceratopsand 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 asMaiasauraandOrodromeus—known from more complete nests—Thulborn concluded that most depictions ofProtoceratopsnests 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-likeProtoceratopsnests.[82]
In 2011, the first authentic nest ofProtoceratops(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 notperinatesbased on the absence ofeggshellfragments 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 thatProtoceratopsparents might have cared for their young at nests during at least the early stages of life. AsProtoceratopswas a relativelybasal(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 theincubationperiods ofP. andrewsiandHypacrosaurusby usinglines of arrested growth(LAGS; lines of growth) of the teeth inembryonicspecimens (Protoceratopsegg clutch MPC-D 100/1021). The results suggests a mean embryonic tooth replacement period of 30.68 days and relativelyplesiomorphically(ancestral-shared) long incubation times forP. andrewsi,with a minimum incubation time of 83.16 days.[31]Norell and team in 2020 analyzed again this clutch and concluded thatProtoceratopslaid soft-shelled eggs. Most embryos within this clutch have a flexed position and the outlines of eggs are also present, suggesting that they were buriedin ovo(in the egg). The outlines of eggs and embryos indicates ellipsoid-shaped eggs in life with dimensions about 12 cm (120 mm) long and 6 cm (60 mm) wide. Several of the embryos were associated with a black to white halo (circumference). Norell and team performed histological examinations to itschemical composition,finding traces ofproteinaceouseggshells, and when compared to othersauropsidsthe team concluded that they were notbiomineralizedin life and thus soft-shelled. Given that soft-shelled eggs are more vulnerable todeshydratationand crushing,Protoceratopsmay have buried its eggs inmoisturizedsand orsoil.The growing embryos therefore relied on external heat and parental care.[32]
Paleopathology
editIn 2018, Tereshchenko examined and described several articulated cervical vertebrae ofP. andrewsiand reported the presence of two abnormally fused vertebrae (specimen PIN 3143/9). The fusion of the vertebrae was likely a product of disease orexternal damage.[79]
Predator–prey interactions
edit
Barsbold in 1974 shortly described theFighting Dinosaursspecimen and discussed possible scenarios. TheVelociraptorhas its right leg pinned under theProtoceratopsbody with its left sickle claw oriented into the throat region. TheProtoceratopsbit the right hand of the predator, implying that it was unable to escape. Barsbold suggested that both animals drowned as they fell into aswamp-likebody of wateror, the relativelyquicksand-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 to explain their preservation. During the death struggle, a largedunemay have collapsed simultaneously burying bothProtoceratopsandVelociraptor.Another proposal is that theVelociraptorwasscavengingan already deadProtoceratopswhen it got buried and eventually killed by indeterminate circumstances.[34]
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, theProtoceratopshas a semi-erect stance and its skull is nearly horizontal, which could have not been possible if the animal was already dead. TheVelociraptorhas its right hand trapped within the jaws of theProtoceratopsand the left one grasping theProtoceratopsskull. Moreover, it lies on the floor with its feet directed to the prey's belly and throat areas, indicating that thisVelociraptorwas not scavenging. Unwin and colleagues examined thesedimentssurrounding the specimen and suggested that the two were buried alive by a powerfulsandstorm.They interpreted the interaction as theProtoceratopsbeing grasped and dispatched with kicks delivered by the low-lyingVelociraptor.They also considered possible that populations ofVelociraptorwere aware of crouching behaviors inProtoceratopsduring high-energy sandstorms and used it for successful hunts.[35]
Kenneth Carpenterin 1998 considered the Fighting Dinosaurs specimen to be conclusive evidence for theropods as activepredatorsand not scavengers. He suggested another scenario where the multiplewoundsdelivered by theVelociraptoron theProtoceratopsthroat had the latter animal bleeding to death. As a last effort, theProtoceratopsbit the right hand of the predator and trapped it beneath its own weight, causing the eventual death anddesiccationof theVelociraptor.The missing limbs of theProtoceratopswere afterwards taken by scavengers. Lastly, both animals were buried by sand. Given that theVelociraptoris relatively complete, Carpenter suggested that it may have been completely or partially buried by sand.[83]
In 2010, David Hone with team reported a new interaction betweenVelociraptorandProtoceratopsbased ontooth marks.Several fossils were collected at the Gate locality of theBayan Mandahu Formationin 2008, including teeth and body remains of protoceratopsid andvelociraptorinedinosaurs. The team referred these elements toProtoceratopsandVelociraptormainly based on their abundance across the unit, although they admitted that reported remains could represent different, yet related taxa (in this case,Linheraptorinstead ofVelociraptor). At least eight body fossils ofProtoceratopspresent 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-stagecarcassconsumption either during scavenging or following agroup kill.The team stated that feeding byVelociraptoruponProtoceratopswas probably a relatively common occurrence in these environments, and that this ceratopsian actively formed part of the diet ofVelociraptor.[84]
In 2016, Barsbold re-examined the Fighting Dinosaurs specimen and found several anomalies within theProtoceratopsindividual: both coracoids have small bone fragments indicatives of abreakingof the pectoral girdle; the right forelimb and scapulocoracoid are torn off to the left and backward relative to itstorso.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 theProtoceratopsis missing other body elements, Barsbold suggested that scavengers were the most likely authors. BecauseProtoceratopsis considered to have been aherdinganimal, another hypothesis is that members of a herd tried to pull out the already buriedProtoceratops,causing thejoint dislocationof 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 theProtoceratopspower-slamming theVelociraptor,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 theVelociraptorlying on its back right under theProtoceratops.After burial, eitherProtoceratopsherd or scavengers tore off the buriedProtoceratopsto the left and backward, making both predator and prey to be slightly separated.[36]
Daily activity
edit
In 2010, Nick Longrich examined the relatively largeorbitalratio andsclerotic ringofProtoceratops,which he suggested as evidence for anocturnallifestyle. Based on the size of its sclerotic ring,Protoceratopshad an unusually largeeyeballamong protoceratopsids. In birds, a medium-sized sclerotic ring indicates that the animal is a predator, a large sclerotic 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 ofProtoceratops—more suitable for processing plant material—and its extremeabundanceindicate it was not a predator, so if it was adiurnalanimal, then it would have been expected to have a much smaller sclerotic ring size.[69]
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 (cathemeral) animals—which are irregularly active throughout the day and night—are between these two ranges. Schmitz and Motani separated ecological andphylogeneticfactors and by examining 164 living species and noticed that eye measurements are quite accurate when inferring diurnality, cathemerality, or nocturnality in extincttetrapods.The results indicated thatProtoceratopswas a cathemeral herbivore andVelociraptorprimarily nocturnal, suggesting that the Fighting Dinosaurs deathmatch may have occurred at twilight or under low-light conditions. Lastly, Schmitz and Motani concluded thatecological nichewas a potential main driver in the development of daily activity.[85]However, a subsequent study in 2021 found thatProtoceratopshad a greater capability of nocturnal vision than didVelociraptor.[86]
Paleoenvironment
editBayan Mandahu Formation
edit
Based on general similarities between the vertebrate fauna and sediments of Bayan Mandahu and the Djadokhta Formation, theBayan Mandahu Formationis considered to beLate Cretaceousin age, roughlyCampanian.The dominantlithologyis reddish-brown, poorly cemented, fine grainedsandstonewith someconglomerate,andcaliche.Other facies includealluvial(stream-deposited) andeolian(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 ofdunefield paleoenvironments, under asemi-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.[12][87]
Thepaleofaunaof 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. hellenikorhinusis the representative species, and it shared its paleoenvironment with numerous dinosaurs such asdromaeosauridsLinheraptorandVelociraptorosmolskae;[88][89]oviraptoridsMachairasaurusandWulatelong;[56][90]andtroodontidsLinhevenator,Papiliovenator,andPhilovenator.[91]Other dinosaur members include thealvarezsauridLinhenykus;[92]ankylosauridPinacosaurusmephistocephalus;[93][94]and closely relatedprotoceratopsidBagaceratops.[19]Additional fauna from this unit comprisesnanhsiungchelyidsturtles,[95]and a variety ofsquamatesandmammals.[96][97]
Djadokhta Formation
edit
Protoceratopsis known from most localities of theDjadokhta Formationin 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.[98]Dominant sediments at Djadokhta include dominant reddish-orange and pale orange to light gray, medium to fine-grainedsandsand sandstones, caliche, and sparsefluvial(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-livedwater bodies,similar to the modernGobi Desert.It is estimated that at the end of the Campanian age and into theMaastrichtianthe climate would shift to the moremesic(humid/wet) conditions seen in theNemegt Formation.[99][100][101]
The Djadokhta Formation is separated into a lower Bayn Dzak Member and upper Turgrugyin Member.Protoceratopsis largely known from both members, havingP. andrewsias a dominant and representative species in the overall formation.[98][100]The Bayn Dzak member (mostly the Bayn Dzak locality) has yielded the dromaeosauridsHalszkaraptorandVelociraptor mongoliensis;[102][103]oviraptoridOviraptor;[4]ankylosauridPinacosaurus grangeri;[94]and troodontidSaurornithoides.[104]Ukhaa Tolgod, a highly fossiliferous locality is also included in the Bayn Dzak member.[100]and its dinosaur paleofauna is composed of alvarezsauridsKolandShuvuuia;[105][106]ankylosauridMinotaurasaurus;[107]birdsApsaravisandGobipteryx;[108][109]dromaeosauridTsaagan;[110]oviraptoridsCitipatiandKhaan;[111]troodontidsAlmasandByronosaurus;[112][113]and a new, unnamed protoceratopsid closely related toProtoceratops.[114]In the Turgrugyin Member (mainly Tugriken Shireh locality),P. andrewsishared its paleoenvironment with the birdElsornis;[115]dromaeosauridsMahakalaandVelociraptor mongoliensis;[102][116]andornithomimidAepyornithomimus.[101]P. andrewsiis also abundant at Udyn Sayr,[77][57]whereAvimimusandUdanoceratopshave been recovered.[117][118]
The relatively low dinosaur paleodiversity, small body size of most dinosaurs, andaridsettings of the Djadokhta Formation compared to those of the Nemegt Formation, suggest thatProtoceratopsand contemporaneous biota lived in astressedpaleoenvironment (physical factors that generate adverse impacts on the ecosystem).[69]In addition, the high occurrence of protoceratopsid fossils in arid-deposited formations indicates that these ceratopsians preferred warm environments.[56][69]AlthoughP. andrewsiwas the predominant protoceratopsid on this formation, tentative remains ofP. hellenikorhinushave been reported from the Udyn Sayr and Bor Tolgoi localities, suggesting that both species co-existed. WhereasP. andrewsiis found in aeolian sediments (Bayn Dzak or Tugriken Shireh),P. hellenikorhinusis found in the aeolian-fluvial sediments. As the latter type of sediments is also found in the Bayan Mandahu Formation, it is likely thatP. hellenikorhinuspreferred environments combininghumidand arid conditions.[119]
Taphonomy
edit
In 1993 Jerzykiewiczz suggested that many articulatedProtoceratopsspecimens 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 someProtoceratopsinvolving 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 Dinosaurstaphonomichistory itself as evidence for this catastrophic preservation. Given that this posture is exhibited by populations from both Bayan Mandahu and Djadokhta formations, Jerzykiewiczz indicated that this behavior was not unique to any locality. He also considered it unlikely that theseProtoceratopsindividuals died after burying themselves in the sand given that these specimens are only found in structureless sandstones; an arched posture would pose hardbreathingconditions; andburrowersare known to excavate headfirst and sub horizontally.[12]
Fastovsky in 1997 examined the geology at Tugriken Shireh providing insights into the taphonomy ofProtoceratops.He agreed in that the preservation ofProtoceratopsspecimens 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 buriedProtoceratopsindividuals. Fastovsky pointed out these two factors combined indicate that this site was host to high biotic activity, mainly composed ofarthropodscavengers who were also involved in the recycling ofProtoceratopscarcasses.The flexed position of most buriedProtoceratopsis indicative ofdesiccationand shrinking ofligaments/tendonsin the legs, necks, and tails after death.[120]
In 1998 during a conference abstract at theSociety of Vertebrate Paleontology,James I. Kirklandand team reported multiple arthropod pupae casts and borings (tunnels) on a largely articulatedProtoceratopsspecimen from Tugriken Shireh, found in 1997. A notorious amount ofpupaewere found in clusters and singly along the bone surfaces, mostly in the joint areas, where the trace makers would have feed on dried ligaments, tendons andcartilage.The examined pupae from the specimen are more cylindrical structures with rounded ends. The pupae found in thisProtoceratopsindividual were reported as measuring as much a 2.5 cm (25 mm) long and 1 cm (10 mm) wide and compare best with pupae attributed tosolitary wasps.Additionally, the reported borings have a structure that differs from traces made bydermestidbeetles.The team indicated that both pupae and boring traces reflect a marked ecological relationship between dinosaur carcasses and a relatively largenecrophagousinsect taxon.[121]
Later in 2010, Kirkland and Kenneth Bader redescribed and discussed the numerous feeding traces from thisProtoceratopsspecimen, which they nicknamed Fox SiteProtoceratops.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 thejointsof the limbs. The co-workers also noted that the Fox SiteProtoceratopspreserves associated traces in the encasing sediment, indicative of necrophagous activity after the animal was buried. Kirkland and Bader concluded that adults of a largebeetletaxon would detectdecayingcarcasses buried below the sand and dig down to feed and lay their eggs. After emerging from the eggs,larvaewould have fed on the carcass prior to pupating. The last larvae to emerge would have feed on the dried tendons and cartilage in the joint areas—thereby explaining the notorious poor preservation of these areas in the specimen—and subsequently chewing on the bone itself, prior to pupating. After reaching full maturity, adult beetles would have then dig back to the surface, most likely leaving borings through bones, and finally beginning to search for new carcasses and thus continuing the recycling ofProtoceratopscarcasses.[122]
In 2010 the paleontologists Yukihide Matsumoto and Mototaka Saneyoshi reported multiple borings and bite traces on joint areas of articulatedBagaceratopsandProtoceratopsspecimens from the Tugriken Shireh locality of theDjadokhta Formationand Hermiin Tsav locality of theBarun Goyot Formation,respectively. They interpreted the damaged areas in theProtoceratopsspecimen as product of active feeding by burrowing arthropods, most likely insects.[123]These specimens were formally described and discussed in 2011 by Saneyoshi and team, including fossils fromVelociraptorand anankylosaurid.Reported traces were identified as pits, notches, borings, and channels across the skeletons, most notably at limb joint areas. The team indicated that it is very likely that these were made by scavenging insects, however, relatively large borings (about 3 cm (30 mm) wide) in the ribs and scapulae of oneProtoceratopsspecimen (MPC-D100/534) indicates that insects were not the only scavengers involved in the bone damage, but alsomammals.Given the dry/harsh paleoenvironmental conditions of units like the Djadokhta Formation, medium to large-sized dinosaur carcasses may have been an important source of nutrition for small animals. Saneyoshi and team emphasized that the high frequency of feeding traces at the limb joints of numerous specimens and reports of previous studies, indicates that small animals may have targeted thecollagenfound in the joint cartilage of dried dinosaur carcasses as a source ofnitrogen,which was low in the desert-dry conditions of these dinosaur fossils.[124]
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 youngProtoceratopstried 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 youngProtoceratopsmay have struggled to reach this area, resulting in their final burial and eventual death.[13]
Hone and colleagues in 2014 indicated that two assemblages ofProtoceratopsat 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 ofProtoceratopsfrom 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 aProtoceratopsskull 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
editPossible Influence on Griffin Legend
editThe folklorist and historian of scienceAdrienne MayorofStanford Universityhas suggested that the exquisitely preserved fossil skeletons ofProtoceratops,Psittacosaurusand other beaked dinosaurs, found by ancientScythiannomads who mined gold in theTian ShanandAltai Mountainsof Central Asia, may have played a role in the image of the mythical creature known as thegriffin.Griffins were described as wolf- or lion-sized quadrupeds with large claws and a raptor-bird-like beak; they laid their eggs in nests on the ground.[126]
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 ofMongoliaand China, where manyProtoceratopsand 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 ofProtoceratopsas 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 ascyclopesandgiants.[128][129]
In 2016 this hypothesis was criticized by the British paleontologist andpaleoartistMark 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 ofProtoceratops,that the bodies of griffins much more closely resemble the bodies of modern big cats than they do those ofProtoceratops,and that the gold deposits of central Asia occur hundreds of kilometers from the knownProtoceratopsfossil 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]Witton later co-published with Richard Hing a 2024 paper expanding on his points regarding the tenuous link between griffins andProtoceratops.[131]
-
A traditional depiction of thegriffin -
Adrienne Mayorhas speculated that the discovery ofProtoceratopsfossils may have inspired or influenced stories of griffins
See also
edit
References
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