Brontotheriidae

Skull and dental characteristics

The skull was comparatively large in all brontotheres, reaching 60 centimetres (24 in) to sometimes over 80 centimetres (31 in) in length in the larger representatives. Especially the evolutionarily advanced forms also had widely flaring and sometimes clearly arched zygomatic arches. In many brontothere representatives, the cranium was quite broad, with only early forms having a relatively narrow skull. The skull showed prominent parasagittal ridges on the lateral surfaces of the parietal bones serving as muscle attachment points. Also typical was the sometimes strongly elongated occipital bone, especially in the later horned representatives, whose horns usually ran at an acute angle in lateral view and caused a frequently deep head posture. The horns characteristic of late brontotheres were situated on the rostrum at the transition from the frontal bone to the nasal bone. The anterior part of the nasal bone projected freely over the premaxilla and maxilla, similar to rhinoceroses and horses, but differing from tapirs with their much more posteriorly positioned nasal bones.^[9]

The lower jaw was generally robustly built and had a rather short symphysis. The majority of brontotheres showed a complete dentition with three incisors, one canine, four premolars, and three molars per jaw quadrant. Only the evolutionarily youngest forms had a dentition reduced by one incisor anteriorly and sometimes a missing anterior premolar. The incisors in many representatives had a small, globular shape. The generally low-crowned molars were equipped with crescent-shaped (bunoselodont) enamel cusps on the occlusal surfaces.

Their teeth are adapted to shearing (cutting) relatively nonabrasive vegetation. Their molars have a characteristic W-shaped ectoloph (outer shearing blade), which connected the two main cusps there (paracone and metacone). The two lingual main cusps (protocone and hypocone) stood isolated from it. The wear patterns observed on brontothere teeth suggests a folivorous diet. Early Brontotheres had brachydont teeth with thick enamel, while later forms evolved a more hypsodont style tooth with thinner enamel.^[1] Transverse shearing crests between the buccal and lingual main cusps, such as the protoloph and metaloph in rhinoceroses and tapirs, were absent in brontotheres. The structure of the cheek teeth enabled the animals to grind tougher plant material.^[10]

Horns

Unlike the horns of rhinoceroses, the horn formations of brontotheres did not consist of keratin but were outgrowths of the skull bones and were therefore preserved as fossils. They formed from the posterior part of the nasal bone and were overlain by the anterior portions of the frontal bone.^[11] The majority of horn-bearing brontotheres typically possessed two paired horns, frequently located above the orbit, where the width of the nasal bone increased considerably. Also differing from rhinoceroses, the horns did not end in a point but were rounded. At the base they had a round to oval cross-section and sometimes projected obliquely outward; at the tips the horns could also be slightly forked, as in Megacerops.^[12] In many cases the horn formations consisted only of larger or smaller bony swellings, which was especially typical of phylogenetically older forms.^[13]

Some later brontotheres developed horn-like bony projections of the skull. The North American brontothere Megacerops, for example, evolved large sexually dimorphic paired horns above their noses. The sexually dimorphic horns, along with highly developed neck musculature, suggest that brontotheres were highly gregarious and males may have performed some sort of head-clashing behavior in competition for mates.^[14] Females had smaller appendages, which may have been used to ward off predators and protect young. In Asia, another species of brontothere, Embolotherium, evolved a similarly gigantic body size; however, instead of the slingshot-like horns of the Megacerops, they evolved a single elongated bony process that was composed of both nasal and frontal bones.^[14] Embolotherium may have used its large nasal cavity to make vocalizations in order to communicate with others of its species.^[14] In some Asian brontotheres the horns frequently stood very close together or were fused, forming a bony battering ram, most clearly seen in Embolotherium. Some genera, such as Dolichorhinus, evolved highly elongated skulls.

Similar to giraffes, their horns were covered in skin and did not have grooves for nutrient blood vessels. There is some evidence of secondary bone growth, likely due to impact from head clashing. However, it has since been demonstrated for Embolotherium that the entire battering ram was incorporated into the soft tissue covering of the front of the head, giving it a markedly distinctive face.^[1]

Diet

The characteristic bunoselodont (crescent-shaped) enamel pattern on the occlusal surfaces of the molars and their low crown height are usually indicators that the animals fed on soft plant material (browsing).^[24] This is confirmed by a microscopic analyses of the dental wear surfaces of various brontothere genera such as Eotitanops, Telmatherium, Metarhinus, Duchesneodus, and Megacerops. The numerous narrow scratches and small pits found indicate a dietary specialization more strongly focused on foliage, with only occasional incorporation of fine-grained sediment particles from the ground. Only in the earliest forms might a higher proportion of fruits have played a role, similar to what was the case with the earliest horses. Mixed plant diet consisting of bark and branches or seeds can be largely excluded. Since modern herbivores predominantly show a different chewing pattern, researchers conclude that brontotheres were highly selective in their foraging behavior. It was also determined that especially later brontothere representatives from the Upper Eocene showed considerably more traces of small scratches on their dental wear surfaces, which could be related either to a shift in preferred diet or to general landscape changes.^[25][26] Furthermore, isotope analyses of the tooth enamel of the molars showed that the latest brontotheres such as Megacerops derived nearly 100% of their diet from leaves and also had a fairly high water dependency. The dependency on liquid in particular indicates a digestive system similar to that of modern odd-toed ungulates, in which a large part of food is broken down in the hind gut.^[27]

Sexual dimorphism

Within individual brontothere genera, differences in body structure can be identified that are frequently interpreted as sexual dimorphism. In many, especially hornless representatives, differences in dental morphology are noticeable; in some individuals this usually includes a larger canine tooth that greatly exceeds neighboring teeth, while in other individuals it is less distinctly developed. In association with large canine teeth, more robust skulls often appear to show more massive muscle attachment points for the chewing musculature especially at the zygomatic arches, which then manifests as large bony swellings. The combination of more robust skulls and large canine teeth is usually associated with male animals, where similar features can be observed in modern horses as well. A further likely sexual difference is apparent in horn size in some horn-bearing brontotheres, with animals having larger horns and sometimes also associated more robust nasal bones being regarded as male, while female animals show more gracile formations. This is known from forms such as Megacerops, Duchesneodus, and Embolotherium.^[10][28] Notable in this context is that some of the latest brontotheres no longer show any difference between the sexes in dental structure, so that the canine teeth are similarly large in all fossils found. This can be demonstrated especially in Embolotherium, which had a distinctive bony battering ram on the skull, but also from finds of Duchesneodus, which had two individual horns.^[28] Possibly a secondary reduction of tooth dimorphism occurred here in connection with the development of horn formations. Something similar is found in modern horn- and antler-bearing even-toed ungulates: representatives with head weapons generally lack enlarged canines, while those such as musk deer or water chevrotains that do not develop antlers have these strongly elongated at least in the upper jaw. Comparable developments are also known in rhinoceroses.^[13]

Social behavior

Little is known about the social behavior of brontotheres. A marked sexual dimorphism is typically associated with mating of one male with several female animals in a close social group or among territorial animals. The canine teeth and horns may therefore have served for threat display during the rut. Isolated ribs with healed fractures might also indicate rival fights. Individual horns also show evidence of secondary growth, possibly triggered by impacts during fights. Since bony horns are less tough than those made of keratin, it is more likely that any fights were predominantly carried out in shoving or pushing contests rather than by thrusting and ramming.^[6][13]

Locomotion

The principally rhinoceros-like construction of the body skeleton indicates, based on limb proportions, a rather ponderous gait.^[8] However, individual differences exist that allow further conclusions about brontothere locomotion. Especially the hindlimbs had a nearly symmetrically constructed knee joint, so that both condyles of the femur were similarly sized, comparable to those of modern elephants. Rhinoceroses, by contrast, show strongly asymmetric knee joints that developed due to their extreme increase in body mass over the course of their evolutionary history. They enable very fast running up to a gallop in open terrain, something elephants are not capable of. For the very large brontotheres like Megacerops, based on the similar knee structure and great weight, it is assumed that here too a fast run must have been the maximum speed of locomotion.^[29] Something similar can be assumed for Embolotherium, which had very massive long bones suggesting a rather ponderous gait. On the other hand, the phylogenetically older Rhinotitan had considerably more slender limbs, which may have allowed more agile movement.^[30]

Biological functions

In some forms such as Metarhinus, Sphenocoelus, and Telmatherium, the actual internal nasal passages at the base of the skull are closed and replaced by openings shifted further posteriorly toward the vomer. This directs inhaled air through the nose directly to the olfactory mucosa. In the region of the ethmoid bone, a kind of nasal septum is developed that divides the internal airways into two separate tubes. It therefore appears possible that brontotheres were obligate nasal breathers and did not breathe through the mouth. A similar feature is also seen in modern horses, which are considered the closest living relatives of brontotheres, as well as, but to a lesser extent, in rhinoceroses. Less likely, but possible, would be a function in a potential aquatic lifestyle. In this case, the rearward displacement of the internal airways would theoretically support air intake when the throat is filled with water, though this has not yet been anatomically confirmed.^[31][32]

Paleoenvironment

Based on the dietary habits of brontotheres, with their preferred food and required water, these animals likely lived largely in dense, closed forests interspersed with rivers and swamps under humid climatic conditions. This is suggested among other things by isotope analysis on teeth from the Chadron Formation in the drainage basin of the White River, which belongs to the Upper Eocene.^[27] These findings are supported by a large part of the geological and paleontological find circumstances. Analyses of the paleofloristics of the likewise Upper Eocene Australian Creek Formation in British Columbia, which yielded brontothere dental remains, allow the reconstruction of mixed conifer-deciduous forests under temperate climatic conditions. The mean annual temperature is estimated at about 13 °C with a mean for the coldest month of −4 °C. Mean annual precipitation was 115 cm.^[15] By contrast, brontotheres also showed a certain adaptability to extreme environmental conditions, as suggested by the remains from the Lower-Middle Eocene Margaret Formation on Ellesmere Island in the high north of Canada. The former environment can be assumed to have been comparable to that of the Australian Creek and Chadron formations, but was subject to the effects of the polar day and polar night with alternating months-long light and darkness. This probably led to regular seasonal shortages in food plants. To what extent the animals spent the entire year in the far north remains unclear, but juveniles are documented for some species, suggesting a permanent presence.^[18][19][20]

External systematics

Brontotheriidae are an extinct family from the order Perissodactyla (odd-toed ungulates). Perissodactyla are traditionally divided into two major suborder, the Hippomorpha (the horses) and the Ceratomorpha (the related group of rhinoceroses and tapirs), with the Ancylopoda (the extinct chalicotheres) introduced later as a third. These three groups are predominantly regarded as suborders. In this frequently held view, the superordinate taxon of Tapiromorpha in turn underscores the closer relationship of Ceratomorpha and Ancylopoda to each other. In this scheme, brontotheres are usually placed within Hippomorpha and are therefore, despite their divergent appearance in advanced forms, more closely related to horses than to rhinoceroses. The relationship with early horses is shown by numerous skull characteristics, such as the construction of the broad nasal bone or the short symphysis of the lower jaw, and further by dentition. The closest relative group is, however, the likewise extinct Lambdotheriidae, with which brontotheres together form the superfamily Brontotherioidea.^[9][33]

There are also views that brontotheres together with the lambdotheres, occupy a very basal position within Perissodactyla, as they unite numerous very primitive characteristics of this mammalian order. In this case, brontotheres and their relatives are assigned to their own suborder Titanotheriomorpha. However, the exact relationships between horses and brontotheres and in turn with other odd-toed ungulates have not yet been precisely established.^[34]

Internal systematics

Originally, the individual brontothere genera were assigned to various subfamilies such as Brontotheriinae, Telmatheriinae, or Embolotheriinae. The internal systematics of the family were, however, largely well-studied only for North American representatives,^[10] while those of Eurasian forms were rarely considered.^[35][36] Although these were also organized in individual subfamilies,^[8][21] problems existed in connecting them with American representatives. This circumstance was only resolved during a major revision of the brontotheres by Matthew C. Mihlbachler in 2008.^[1] This was followed in 2010 by a partial revision by Bryn J. Mader of the earliest representatives, which Mihlbachler had given little consideration.^[37] After these two revisions, three subfamilies initially remained within brontotheres, with Brontotheriinae containing all more modern forms. Thereby all further higher taxa were shifted to the level of tribes, subtribes, and infratribes. Here, Brontotheriina represents all brontotheres with horn formations, while Telmatheriina shows only bony swellings and Rhadinorhinina shows none of these features. The infratribe Brontotheriita and Embolotheriita differ in horn structure: the former typically has two separate horns, the latter closely set or fused and sometimes battering-ram-like formations. The individual groups and lineages of brontotheres are not geographically bounded but show complex relationships across the different continents of their former distribution. This implies multiple faunal exchanges in different directions between the individual landmasses during the evolutionary history of brontotheres.^[1][38]

Overview of genera

In total, more than 40 genera from the family Brontotheriidae are known today; the last comprehensive revision of the family was carried out, as mentioned, in 2008 by Mihlbachler. New genera described after 2008 are marked with an asterisk and cited to their original description.

Lambdotherium and Xenicohippus were previously included in Brontotheriidae but are no longer considered members of this family. Lambdotherium, though excluded, may be the closest known relative to brontotheres. Xenicohippus is now thought to be an early member of the horse family, Equidae.

Adaptive radiation

General evolutionary trends among brontotheres include an increase in body size and the development of bony horns at the nasal-frontal junction. The considerable increase in weight that brontotheres underwent during their evolutionary history did not proceed in a linear fashion following Cope's rule, but rather in an undirected manner. The reason is that brontotheres were able to occupy ecological niches that were largely unoccupied in the early development of mammals in the Paleogene, allowing larger species to arise more frequently. The undirected nature is evident from the fact that under certain external conditions, smaller representatives of brontotheres repeatedly emerged. According to a 2023 study, the driving factor was the saturation of an ecological niche. Accordingly, the rate of speciation was very high in densely occupied ecological niches, but forms also went extinct more frequently. In less densely occupied areas, brontotheres were subject to less competitive pressure. Fewer species formed there, but they persisted longer and thereby also reached larger body sizes.^[43]

The skull underwent very marked changes. In the most primitive representatives it was still very flat or slightly domed. The progressive elongation of the occipital bone, with the resulting low head posture, additionally caused a sometimes markedly saddled profile of the forehead. Shortenings in the anterior snout region further led to changes in the position of the orbit relative to tooth position. Thus the early brontotheres still had the eye socket above or slightly behind the third molar, while later forms had it above the first or second molar. This also resulted in the modern representatives having a very expansive posterior skull. In the dentition, the premolars became increasingly molariform, and in some lineages a diastema developed. Due to the dietary shift of early representatives from a more fruit-based to a leaf-rich diet, bunodont molars evolved over the course of evolutionary history into distinctly lophodont (with transverse enamel ridges) to selenodont (with crescent-shaped enamel ridges) shaped posterior cheek teeth. The number of teeth changed little; only some late brontotheres had one fewer incisor in the anterior dentition. Faunal exchange most likely occurred via the high latitudes of the north.^[1][44]

Origin and development

The evolution of this group is well known due to the excellent fossil record from North America and East and Central Asia, though its origin has not yet been fully resolved. Some researchers propose a North American origin for brontotheres. There, the earliest forms appeared in the Lower Eocene around 53 million years ago (locally known as the Wasatchian North American land mammal age). The partially accepted possible ancestral form is Lambdotherium, which is sometimes regarded as one of the most basal forms of brontotheres, but is sometimes placed in its own family. Early finds consist of two partial skeletons from the Fossil Butte Member of the Green River Formation in the Green River Basin in the northwestern United States. These date to the local faunal zone Lostcabinian and are around 52 million years old.^[37][44][45] According to some other researchers, the origin of the group might also lie in Asia. There, Danjiangia from the Lingcha Formation in the Chinese province of Henan is recorded as a possible very early member, showing some similarities to Lambdotherium. However, it dates to the Paleocene–Eocene boundary around 56 million years ago (locally referred to as Bumbanian).^[46]

The unambiguous early North American brontotheres were overall still relatively small forms such as Eotitanops or Palaeosyops, with shoulder heights of one meter or less and no horns; for the former a weight of around 140 kg is estimated.^[47] Although they were a relatively rare faunal element at that time, finds are also documented from the very high north of North America, including from the Margaret Formation on what is now Ellesmere Island^[18][19][20] and the Buchanan Lake Formation on what is now Axel Heiberg Island,^[48] which at the time were still covered by swamp forests.^[19] From Asia, other early forms have been reported with Balochititanops from the Ghazij Formation in the Kingri region of Balochistan, appearing roughly contemporaneously with their North American relatives.^[23]

The heyday of brontotheres was the Middle Eocene, from approximately 50 to 37 million years ago; around two dozen genera are known from that epoch.^[44] Marked above all was the strong increase in body size. For the early Middle Eocene finds of the still relatively primitive Bunobrontops from the Pondaung Formation of Myanmar, a weight of 510 to 990 kg is estimated, though the genus is largely known only from teeth.^[49] By contrast, weight estimates for the roughly contemporaneous but phylogenetically more advanced forms Wickia and Metatelmatherium range from about 1.6 to 2.1 t.^[47] Against this trend of increasing body size, dwarf forms also occasionally developed. The process is not yet fully understood, but dwarfism occurred multiple times during brontothere evolutionary history and is documented for example in Nanotitanops^[50] and Xylotitan.^[47]

The general increase in body size was also associated with an increase in skull size. Skulls developed in forms like Dolichorhinus into very elongated shapes with the eyes positioned far anteriorly. Distinct horn formations are first observed in the late Middle Eocene, though the development proceeded in several stages. In some forms, the frontal bone first began to grow small, triangularly shaped bony projections over the nasal bone. This is known, among others, from Telmatherium, which is preserved by exceptionally abundant fossil material from Twin Buttes in the Bridger Basin of Wyoming. The genus was long assumed to be the sister taxon of all other horn-bearing brontotheres. Later, small bony projections developed, as documented in the Asian Rhinotitan and the North American Protitanotherium. Only then did the classic horns form. Also in the late Middle Eocene, brontotheres reached Europe briefly, where this odd-toed ungulate group is only rarely documented. Near Cluj-Napoca in Romania, a lower jaw fragment of Brachydiastematherium was found.^[1] Somewhat younger and already from the Upper Eocene are dental and lower jaw remains from Kameno and Cherno More, both in Bulgaria, though their precise systematic position is disputed.^[51][52] Overall, brontotheres were the most diverse group of large mammals in both North America and Asia during the Middle Eocene. Notably, no independent adaptive radiation took place on either continent; instead, the phylogenetic development is strongly interlinked. Some researchers assume up to a dozen independent intercontinental dispersal waves in both directions.^[1][47][20]

In the Upper Eocene, 37 to 34 million years ago, the number of different brontothere forms gradually declined. About ten genera are known from this time, but most are to be placed in the early phase of the epoch. All documented brontotheres were horn-bearing and predominantly very large, like the possibly up to 3 t heavy Megacerops. Two distinct lineages emerged: those with two widely spaced horns closely related to Megacerops, and those with two closely set or fused horns more closely related to Embolotherium. Toward the end of the Eocene, climatic changes in the form of temperature decline occurred, intensifying through the Oligocene, during which the first grasses spread in association with open landscapes. Brontotheres may have been unable to adapt their highly specialized diet to these landscape changes in the mid and higher latitudes where they were mainly distributed, and were displaced by more competitive herbivores such as the ascending groups of rhinoceroses and chalicotheres.^[24] Most brontotheres had already disappeared before the end of the Eocene; only Megacerops persisted until about 34 million years ago.^[44]