Triceratops

Type specimen YPM 1820 of the type species, T. horridus

After Triceratops was described, between 1889 and 1891 Hatcher with great effort collected another thirty-one of its skulls. The first species had been named Triceratops horridus by Marsh. Its specific name was derived from the Latin horridus; "rough, rugose", perhaps suggesting the roughened texture of those bones belonging to the type specimen, later identified as an aged individual. The additional skulls varied to a lesser or greater degree from the original Triceratops specimen. This variation is unsurprising, given that Triceratops skulls are large three-dimensional objects, coming from individuals of different ages and both sexes, and which were subjected to different amounts and directions of pressure during fossilization.[5]

However, not a single one of these skulls was referred to T. horridus by Marsh who instead named eight further species and eventually even a new genus Sterrholophus. In 1889, he named two species. Triceratops flabellatus, the "fan-shaped", was based on skull YPM 1821. Triceratops galeus, "the helmeted one", was exceptionally based on a specimen not found by Hatcher, USNM 2410, a horn and frill excavated by George Homans Eldridge in Colorado in the Laramie Formation. In December 1889, Marsh published the first illustration ever of a Triceratops skull, that of T. flabellatus. In January 1890, two additional species were added. Triceratops serratus, "the serrated one", was based on skull YPM 1823, and Triceratops prorsus, "pointing forward", on specimen YPM 1822, a nose horn. In May 1890, Triceratops sulcatus was added, named "the one with troughs" because of grooves on the horns, based on the fragmentary skull USNM 4276. On this occasion, Marsh reported a natural brain cast, that he considered remarkably small. In February 1891, Marsh published additional images, for the first time concluding that the animal walked on all fours: initially he had assumed it was a bipedal form, brought to the brink of extinction by its overly heavy skull. A full skeletal restoration followed in April, together with one of Brontosaurus in the same publication, the first for Mesozoic dinosaurs ever drawn. The same year he renamed T. flabellatus into the separate genus Sterrholophus, the "stiffly crested". In September, he named Triceratops elatus, "the raised one", based on specimen YPM 1201, an enormous skull with an upwards pointing low nose horn found on October 23, 1890 by Hatcher. Marsh named his last Triceratops species in 1898, when part of his collection was transferred from Yale to the Smithsonian Institution. Triceratops calicornis, "the chalice horned", was based on specimen USNM 4928, a skull with a strange depression on the rear of the horn base. Triceratops obtusus, the "stumpy one", was based on specimen USNM 4720 with an obtuse nose horn.

After Marsh's death, Hatcher attempted to revise the material but fell ill writing the study, never to recover. Richard Swann Lull completed his monograph. Lull and subsequent researchers would disagree as to the number of separate species (listed below), and came up with several phylogenetic schemes for how they were related to each other.

In the first attempt to understand the many species, Lull found two groups, although he did not say how he distinguished them: one composed of T. horridus, T. prorsus, and T. brevicornus; the other of T. elatus and T. calicornis. Two species (T. serratus and T. flabellatus) stood apart from these groups.[7] By 1933, and his revision of the landmark 1907 Hatcher-Marsh-Lull monograph of all known ceratopsians, he retained his two groups and two unaffiliated species, with a third lineage of T. obtusus and T. hatcheri that was characterized by a very small nasal horn.[9] T. horridus-T. prorsus-T. brevicornus was now thought to be the most conservative lineage, with an increase in skull size and a decrease in nasal horn size, and T. elatus-T. calicornis was defined by large brow horns and small nasal horn.[9][10] C. M. Sternberg made one modification, adding T. eurycephalus and suggesting that it linked the second and third lineages closer together than they were to the T. horridus lineage.[11] This pattern was followed until the major studies of the 1980s and 1990s.

1896 skeletal restoration of T. prorsus by O. C. Marsh, based on the holotype skull YPM 1822 and referred elements

With time, the idea that the differing skulls might be representative of individual variation within one (or two) species gained popularity. In 1986, John Ostrom and Peter Wellnhofer published a paper in which they proposed that there was only one species, Triceratops horridus.[12] Part of their rationale was that generally there are only one or two species of any large animal in a region. To their findings, Lehman added the old Lull-Sternberg lineages combined with maturity and sexual dimorphism, suggesting that the T. horridus-T. prorsus-T. brevicornus lineage was composed of females, the T. calicornis-T. elatus lineage was made up of males, and the T. obtusus-T. hatcheri lineage was of pathologic old males.[13] His reasoning was that males had taller, more erect horns and larger skulls, and females had smaller skulls with shorter, forward-facing horns.

These findings were contested a few years later by Catherine Forster, who reanalyzed Triceratops material more comprehensively and concluded that the remains fell into two species, T. horridus and T. prorsus, although the distinctive skull of T. ("Nedoceratops") hatcheri differed enough to warrant a separate genus.[14] She found that T. horridus and several other species belonged together, and T. prorsus and T. brevicornus stood alone, and since there were many more specimens in the first group, she suggested that this meant the two groups were two species. It is still possible to interpret the differences as representing a single species with sexual dimorphism.[5][15]

In 2009, John Scannella and Denver Fowler supported the separation of T. prorsus and T. horridus, and noted that the two species are also separated stratigraphically within the Hell Creek Formation, indicating that they did not live together at the same time.[16]

T. prorsus, Carnegie Museum of Natural History

The skull (AMNH 5116) of this T. horridus composite specimen was formerly assigned to T. elatus

• T. horridus (Marsh, 1889) Marsh, 1889 (originally Ceratops) (type species)
• T. prorsus Marsh, 1890

Some of the following species are synonyms, as indicated in parentheses ("=T. horridus" or "=T. prorsus"). All the others are considered nomina dubia ("dubious names") because they are based on remains too poor or incomplete to be distinguished from pre-existing Triceratops species.

• T. albertensis C. M. Sternberg, 1949
• T. alticornis (Marsh 1887) Hatcher, Marsh, and Lull, 1907 [originally Bison alticornis, Marsh 1887, and Ceratops alticornis, Marsh 1888]
• T. brevicornus Hatcher, 1905 (=T. prorsus)
• T. calicornis Marsh, 1898 (=T. horridus)
• T. elatus Marsh, 1891 (=T. horridus)
• T. eurycephalus Schlaikjer, 1935
• T. flabellatus Marsh, 1889 (= Sterrholophus Marsh, 1891) (=T. horridus)
• T. galeus Marsh, 1889
• T. hatcheri (Hatcher & Lull 1905) Lull, 1933 (contentious; see Nedoceratops below)
• T. ingens Marsh vide Lull, 1915
• T. maximus Brown, 1933
• T. mortuarius (Cope, 1874) Kuhn, 1936 (nomen dubium; originally Polyonax mortuarius)
• T. obtusus Marsh, 1898 (=T. horridus)
• T. serratus Marsh, 1890 (=T. horridus)
• T. sulcatus Marsh, 1890
• T. sylvestris (Cope, 1872) Olshevsky, 2000 (nomen dubium; originally Agathaumas sylvestris)

Size comparison with T. horridus in blue and T. prorsus in red

Individual Triceratops are estimated to have reached about 7.9 to 9 meters (26 to 30 ft) in length, 2.9 to 3.0 meters (9.5 to 9.8 ft) in height,[17][18] and 6.1 to 12.0 metric tons (6.7 to 13.2 short tons) in weight.[19] The most distinctive feature is their large skull, among the largest of all land animals. The largest-known skull (specimen MWC 7584, formerly BYU 12183) is estimated to have been 2.5 meters (8.2 ft) in length when complete,[20] and could reach almost a third of the length of the entire animal.[21] A specimen of T. horridus named Kelsey measured 7.3 meters (24 ft) long with a 2-meter (6.5 ft) skull, stood about 2.3 meters (7.5 ft) tall, and was estimated by the Black Hills institute to weight nearly 6 metric tons (6.6 short tons).[22] A Triceratops 8 meters (26 ft) long has been estimated by Gregory S. Paul to have massed 9 metric tons (9.9 short tons).[23]

Skull of Triceratops horridus from the Houston Museum of Natural Science

Like all chasmosaurines, Triceratops had a large skull relative to its body size. The front of the head was equipped with a large beak in front of the teeth. The core of the top beak was formed by a special rostral bone.[24] Behind it, the premaxillae bones were located, embayed from behind by very large circular nostrils. In chasmosaurines, the premaxillae met on their midline in a complex bone plate, the rear edge of which was reinforced by the "narial strut". From the base of this strut, a triangular process jutted out into the nostril. Triceratops differs from most relatives in that this process was hollowed out on the outer side.[24] Behind the toothless premaxilla, the maxilla bore thirty-six to forty tooth positions, in which three to five teeth per position were vertically stacked. The teeth were closely appressed, forming a "dental battery" curving to the inside. The skull bore a single horn on the snout, above the nostrils. In Triceratops, the nose horn is sometimes recognisable as a separate ossification, the epinasal.[24]

The skull also featured a pair of "brow" or supraorbital horns approximately 1 meter (3.3 ft) long, with one above each eye.[25][26] The jugal bones pointed to below at the rear sides of the skull and were capped by separate epijugals. With Triceratops these were not particularly large and sometimes touched the quadratojugals. The bones of the skull roof were fused. By a folding of the frontal bones, a "double" skull roof was created.[24] In Triceratops, some specimens show a fontanelle, an opening in the upper roof layer.[24] The cavity between the layers invaded the bone cores of the brow horns.[24]

At the rear of the skull, the outer squamosal bones and the inner parietal bones grew into a relatively short, bony frill, adorned with epoccipitals in young specimens. These were low triangular processes on the frill edge, representing separate skin ossifications or osteoderms. Typically, with Triceratops specimens there are two epoccipitals present on each parietal bone, with an additional central process on their border. Each squamosal bone had five processes. Most other ceratopsids had large parietal fenestrae, openings, in their frills, but those of Triceratops were noticeably solid,[27] unless the genus Torosaurus represents mature Triceratops individuals. Under the frill, at the rear of the skull, a huge occipital condyle, up to 106 millimeters (4.2 in) in diameter, connected the head to the neck.[24]

The lower jaws were elongated and met at their tips in a shared epidentary bone, the core of the toothless lower beak. In the dentary bone, the tooth battery curved to the outside to meet the battery of the upper jaw. At the rear of the lower jaw, the articular bone was exceptionally wide, matching the general width of the jaw joint.[24] T. horridus can be distinguished from T. prorsus by having a shallower snout.[23]

Life reconstruction of a subadult Triceratops horridus

Chasmosaurines showed little variation in their postcranial skeleton.[24] The skeleton of Triceratops is markedly robust. Both Triceratops species possessed a sturdy build, with strong limbs, short hands with three hooves each, and short feet with four hooves each.[28] The vertebral column consisted of ten neck, twelve back, ten sacral and about forty-five tail vertebrae. The front neck vertebrae were fused into a syncervical. Traditionally, this was assumed to have incorporated the first three vertebrae which would imply that the frontmost atlas was very large and sported a neural spine. Later interpretations revived an old hypothesis by John Bell Hatcher that at the very front a vestige of the real atlas can be observed, the syncervical then consisting of four vertebrae. The vertebral count mentioned, is adjusted to this view. In Triceratops the neural spines of the neck are constant in height, instead of gradually sloping upwards. Another peculiarity is that the neck ribs only begin to lengthen with the ninth cervical vertebra.[24]

The rather short and high vertebrae of the back were in its middle region reinforced by ossified tendons running along the tops of the neural arches. The straight sacrum was long and adult individuals show a fusion of all sacral vertebrae. In Triceratops the first four and last two sacrals had transverse processes, connecting the vertebral column to the pelvis, that were fused at their distal ends. Sacrals seven and eight had longer processes, causing the sacrum to have an oval profile in top view. On top of the sacrum a neural plate was present formed by a fusion of the neural spines of the second through fifth vertebrae. Triceratops had a large pelvis with a long ilium. The ischium was curved downwards. The foot was short with four functional toes. The phalangeal formula of the foot is 2-3-4-5-0.[24]

Closeup of pelvis of Triceratops specimen at the Oxford University Museum of Natural History

Although certainly quadrupedal, the posture of horned dinosaurs has long been the subject of some debate. Originally, it was believed that the front legs of the animal had to be sprawling at a considerable angle from the thorax in order to better bear the weight of the head.[5] This stance can be seen in paintings by Charles Knight and Rudolph Zallinger. Ichnological evidence in the form of trackways from horned dinosaurs and recent reconstructions of skeletons (both physical and digital) seem to show that Triceratops and other ceratopsids maintained an upright stance during normal locomotion, with the elbows flexed to behind and slightly bowed out, in an intermediate state between fully upright and fully sprawling, comparable to the modern rhinoceros.[28][29][30][31]

The hands and forearms of Triceratops retained a fairly primitive structure compared to other quadrupedal dinosaurs such as thyreophorans and many sauropods. In those two groups, the forelimbs of quadrupedal species were usually rotated so that the hands faced forward with palms backward ("pronated") as the animals walked. Triceratops, like other ceratopsians and the related quadrupedal ornithopods, together forming the Cerapoda, walked with most of their fingers pointing out and away from the body, the original condition for dinosaurs, also retained by bipedal forms like the theropods. In Triceratops, the weight of the body was carried by only the first three fingers of the hand, while digits 4 and 5 were vestigial and lacked claws or hooves.[28] The phalangeal formula of the hand is 2-3-4-3-1, meaning that the first or innermost finger of the forelimb has two bones, the next has three, etc.[32]

Close up of the jaws and teeth

Triceratops were herbivorous, and because of their low slung head, their primary food was probably low growing vegetation, although they may have been able to knock down taller plants with their horns, beak, and bulk.[24][49] The jaws were tipped with a deep, narrow beak, believed to have been better at grasping and plucking than biting.[35]

Triceratops teeth were arranged in groups called batteries, of 36 to 40 tooth columns in each side of each jaw, with 3 to 5 stacked teeth per column, depending on the size of the animal.[24] This gives a range of 432 to 800 teeth, of which only a fraction were in use at any given time (tooth replacement was continuous throughout the life of the animal).[24] They functioned by shearing in a vertical to near-vertical orientation.[24] The great size and numerous teeth of Triceratops suggests that they ate large volumes of fibrous plant material, with some researchers suggesting palms and cycads,[50][51] and others suggesting ferns, which then grew in prairies.[52]

Front view of skull with a prominent epoccipital fringe, Houston Museum of Natural Science

There has been much speculation over the functions of Triceratops' head adornments. The two main theories have revolved around use in combat and in courtship display, with the latter now thought to be the most likely primary function.[24]

Early on, Lull postulated that the frills may have served as anchor points for the jaw muscles to aid chewing by allowing increased size and thus power for the muscles.[53] This has been put forward by other authors over the years, but later studies do not find evidence of large muscle attachments on the frill bones.[54]

Triceratops were long thought to have used their horns and frills in combat with predators such as Tyrannosaurus, the idea being discussed first by Charles H. Sternberg in 1917 and 70 years later by Robert Bakker.[46][55] There is evidence that Tyrannosaurus did have aggressive head-on encounters with Triceratops, based on partially healed tyrannosaur tooth marks on a Triceratops brow horn and squamosal; the bitten horn is also broken, with new bone growth after the break. Which animal was the aggressor is not known.[56] Since the Triceratops wounds healed, it is most likely that the Triceratops survived the encounter. Tyrannosaurus is also known to have fed on Triceratops, as shown by a heavily tooth-scored Triceratops ilium and sacrum.[57]

Examples of periosteal reactive bone in selected specimens of Triceratops

In addition to combat with predators using horns, Triceratops are popularly shown engaging each other in combat with horns locked. While studies show that such activity would be feasible, if unlike that of present-day horned animals,[58] there is disagreement about whether they did so. Although pitting, holes, lesions, and other damage on Triceratops skulls (and the skulls of other ceratopsids) are often attributed to horn damage in combat, a 2006 study finds no evidence for horn thrust injuries causing these forms of damage (for example, there is no evidence of infection or healing). Instead, non-pathological bone resorption, or unknown bone diseases, are suggested as causes.[59] A newer study compared incidence rates of skull lesions and periosteal reaction in Triceratops and Centrosaurus and showed that these were consistent with Triceratops using its horns in combat and the frill being adapted as a protective structure, while lower pathology rates in Centrosaurus may indicate visual rather than physical use of cranial ornamentation, or a form of combat focused on the body rather than the head.[60] The frequency of injury was found to be 14% in Triceratops.[61] The researchers also concluded that the damage found on the specimens in the study was often too localized to be caused by bone disease.[62] Histological examination reveals that the frill of Triceratops is composed of fibrolamellar bone[63] which contains fibroblasts that play a critical role in wound healing, and are capable of rapidly depositing bone during remodeling.[64][65]

Juvenile and adult skulls—the juvenile skull is about the size of an adult human head

One skull was found with a hole in the jugal bone, apparently a puncture wound sustained while the animal was alive, as indicated by signs of healing. The hole has a diameter close to that of the distal end of a Triceratops horn. This, and other apparent healed wounds in the skulls of ceratopsians, has been cited as evidence of non-fatal intraspecific competition in these dinosaurs.[66][67]

The large frill also may have helped to increase body area to regulate body temperature.[68] A similar theory has been proposed regarding the plates of Stegosaurus,[69] although this use alone would not account for the bizarre and extravagant variation seen in different members of the Ceratopsidae, which would rather support the sexual display theory.[24]

The theory that frills functioned as a sexual display was first proposed by Davitashvili in 1961 and has gained increasing acceptance since.[13][54][70] Evidence that visual display was important, either in courtship or other social behavior, can be seen in the horned dinosaurs differing markedly in their adornments, making each species highly distinctive. Also, modern living creatures with such displays of horns and adornments use them similarly.[71] A 2006 study of the smallest Triceratops skull, ascertained to be a juvenile, shows the frill and horns developed at a very early age, predating sexual development and thus probably important for visual communication and species recognition in general.[72] The use of the exaggerated structures to enable dinosaurs to recognize their own species has been questioned, as no such function exists for such structures in modern species.[73]

Skull growth series

In 2006, the first extensive ontogenetic study of Triceratops was published in the journal Proceedings of the Royal Society. The study, by John R. Horner and Mark Goodwin, found that individuals of Triceratops could be divided into four general ontogenetic groups, babies, juveniles, subadults, and adults. With a total number of 28 skulls studied, the youngest was only 38 centimeters (15 in) long. Ten of the 28 skulls could be placed in order in a growth series with one representing each age. Each of the four growth stages were found to have identifying features. Multiple ontogenetic trends were discovered, including the size reduction of the epoccipitals, development and reorientation of postorbital horns, and hollowing out of the horns.[74]

Torosaurus is a ceratopsid genus first identified from a pair of skulls in 1891, two years after the identification of Triceratops. The genus Torosaurus resembles Triceratops in geological age, distribution, anatomy and size and it has been recognised as a close relative.[75] Its distinguishing features are an elongated skull and the presence of two fenestrae, or holes, in the frill. Paleontologists investigating dinosaur ontogeny (growth and development of individuals over the life span) in the Hell Creek Formation, Montana, US, have recently presented evidence that the two represent a single genus.

A, Triceratops prorsus holotype YPM 1822 and B, Torosaurus latus ANSP 15192

John Scannella, in a paper presented in Bristol, UK at the conference of the Society of Vertebrate Paleontology (September 25, 2009) reclassified Torosaurus as especially mature Triceratops individuals, perhaps representing a single sex. Jack Horner, Scannella's mentor at Bozeman Campus, Montana State University, noted that ceratopsian skulls consist of metaplastic bone. A characteristic of metaplastic bone is that it lengthens and shortens over time, extending and resorbing to form new shapes. Significant variety is seen even in those skulls already identified as Triceratops, Horner said, "where the horn orientation is backwards in juveniles and forward in adults". Approximately 50% of all subadult Triceratops skulls have two thin areas in the frill that correspond with the placement of "holes" in Torosaurus skulls, suggesting that holes developed to offset the weight that would otherwise have been added as maturing Triceratops individuals grew longer frills.[76] A paper describing these findings in detail was published in July 2010 by Scannella and Horner. It formally argues that Torosaurus and the similar contemporary Nedoceratops are synonymous with Triceratops.[20]

The assertion ignited debate. Andrew Farke had in 2006 stressed that, apart from the frill, no systematic differences could be found between Torosaurus and Triceratops.[75] He nevertheless disputed Scannella's conclusion by arguing in 2011 that the proposed morphological changes required to "age" a Triceratops into a Torosaurus would be without precedent among ceratopsids. Such changes would include the growth of additional epoccipitals, reversion of bone texture from an adult to immature type and back to adult again, and growth of frill holes at a later stage than usual.[77] A study by Nicholas Longrich and Daniel Field analyzed 35 specimens of both Triceratops and Torosaurus. The authors concluded that Triceratops individuals too old to be considered immature forms are represented in the fossil record, as are Torosaurus individuals too young to be considered fully mature adults. The synonymy of Triceratops and Torosaurus cannot be supported, they said, without more convincing intermediate forms than Scannella and Horner initially produced. Scannella's Triceratops specimen with a hole on its frill, they argued, could represent a diseased or malformed individual rather than a transitional stage between an immature Triceratops and mature Torosaurus form.[78][79]

Comparisons between the skulls of Triceratops and Nedoceratops

Opinion has varied on the validity of a separate genus for Nedoceratops. John Scannella and Jack Horner regarded it as an intermediate growth stage between Triceratops and Torosaurus.[20][80] Andrew Farke, in his 2011 redescription of the only known skull, concluded that it was an aged individual of its own valid taxon, Nedoceratops hatcheri.[77] Nicholas Longrich and Daniel Fields also did not consider it a transition between Torosaurus and Triceratops, suggesting that the frill holes were pathological.[79]

As described above, John Scannella had argued in 2010 that Nedoceratops should be considered a synonym of Triceratops.[20] Andrew Farke (2011) maintained that it represents a valid distinct genus.[77] Nick Longrich agreed with Scannella about Nedoceratops and made a further suggestion: that the recently described Ojoceratops was likewise a synonym. The fossils, he argued, are indistinguishable from the T. horridus specimens that were previously attributed to the defunct species T. serratus.

Longrich observed that another newly described genus, Tatankaceratops, displayed a strange mix of characteristics already found in adult and juvenile Triceratops. Rather than representing a distinct genus, Tatankaceratops could as easily represent a dwarf Triceratops or a Triceratops individual with a developmental disorder that caused it to stop growing prematurely.[81]