Osteopathology in Rhinocerotidae from 50 Million Years to the Present.

Individual elements of many extinct and extant North American rhinocerotids display osteopathologies, particularly exostoses, abnormal textures, and joint margin porosity, that are commonly associated with localized bone trauma. When we evaluated six extinct rhinocerotid species spanning 50 million years (Ma), we found the incidence of osteopathology increases from 28% of all elements of Eocene Hyrachyus eximius to 65-80% of all elements in more derived species. The only extant species in this study, Diceros bicornis, displayed less osteopathologies (50%) than the more derived extinct taxa. To get a finer-grained picture, we scored each fossil for seven pathological indicators on a scale of 1-4. We estimated the average mass of each taxon using M1-3 length and compared mass to average pathological score for each category. We found that with increasing mass, osteopathology also significantly increases. We then ran a phylogenetically-controlled regression analysis using a time-calibrated phylogeny of our study taxa. Mass estimates were found to significantly covary with abnormal foramen shape and abnormal bone textures. This pattern in osteopathological expression may reflect a part of the complex system of adaptations in the Rhinocerotidae over millions of years, where increased mass, cursoriality, and/or increased life span are selected for, to the detriment of long-term bone health. This work has important implications for the future health of hoofed animals and humans alike.

Introduction

Rhinos diverged from their closest living relative, the tapir, about 50.3 million years ago (Ma) [1,2,3] and quickly increased in abundance and species richness through the mid-Cenozoic. The rhinocerotid lineage is hypothesized to have diversified into four major clades in North America and Eurasia: the Diceratheriinae in the Oligocene, and the Aceratheriinae, Teleoceratinae, and Rhinocerotinae in the Miocene [4, 5]. Cursoriality, or the habit of running, has been hypothesized to have been maintained through the majority of these lineages [5,6]. These grazing and browsing lineages were some of the most numerous and widespread large mammals in the mid-Cenozoic, with frequent periods of migration between North America, Eurasia, and Africa [7, 8, 9]. About five million years ago the last North American genus, Teleoceras, disappeared from the fossil record [5]. North American rhino populations are estimated to have been smaller in size and weight than their Eurasian relatives [10], but both continents record taxa with increasingly robust and graviportal skeletons over time [5,11].

There are five extant species of rhino, all within the Rhinocerotinae. Two species are in Africa and three in Asia. As with many Animalia, a certain percentage of extinct and extant taxa show evidence of bony and soft-tissue pathologies [12, 13,14], with a recent increase in studies of pathologies in captive modern populations and individuals as wild numbers decline. For Rhinocerotidae, the great majority of studies are reports on captive rhinos with foot disorders [4,12,15,16], discovered during surgery or necropsy. For example, a recent study examined 27 modern captive individuals and a subset were scanned using computed tomography [13]. They found the majority displayed osteoarthritis and/or enthesopathy, particularly in the feet, and hypothesized that increased stress or strain, nutritional imbalance, habitat, and/or ascending infection could contribute the observed pathologies. A similar study [14] noted a wide range of osteopathologies in Ceratotherium simum and Rhinoceros unicornis using computed tomography and hypothesized that care, the weight of the animal, nutrition, or age could all contribute to pathological expression [14]. Extinct taxa have also displayed arthritis-like features, the most prominent being an increase in the frequency of spondylarthropathy (inflammatory arthritis, indicated by abnormal joint erosion or bone fusion) from around 10% in Oligocene Equidae and Rhinocerotidae to around 30% in the Holocene [17]. The common thread from these studies is the type of pathology recorded. These pathologies could all be grouped not as sudden traumatic events but, like runner’s knee or tennis elbow, growth or destruction of bone in response to increased physical stress over the lifetime of an individual.

Bone growth in mammals is promoted by a combination of mechanical (low level stress) and hormone stimulation [18]. After primary growth and development of a mammal is complete, bone repair and remodeling responds primarily to local stimulation [16,18,19] caused by mechanical load. Local osteocytes (bone cells) respond to bone damage and wear with cell hyperplasia (increased cell growth or proliferation). Extensive cellular damage, localized biomechanics (e.g. joint loading, genetic predisposition, and the environment are all potential causal factors of bone degeneration, inflammation and infection in the bone or surrounding tissue [12, 16, 20]. Thus, continuous remodeling of bone can result in bone morphologies and pathologies that reflect what happened to the bone when it was part of a living organism.

Increased mechanical load increases the likelihood of arthropathies such as proliferative joint diseases, erosive joint diseases, synovitis, and traumatic injury [16]. We will briefly examine the major arthropathies, but emphasize that the goal of this paper is not to diagnose the Rhinocerotidae lineage with a specific disease, but record and examine the osteopathologies that are possibly the result of these or related diseases. Four indicators of osteoarthritis (i.e. proliferative joint disease) commonly used in anthropologic studies are: eburnation, a wearing away of the bony articular surface, marginal osteophytes (known as lipping), sclerotic lesions or pitting on the articular surfaces, and alteration in the shape of the joint [21,22]. There are many other erosive arthropathies, but the most characteristic is rheumatoid arthritis (RA). RA includes symmetrical erosions of the hands and feet, minimal new bone formation, erosions, and osteoporosis [16]. Synovitis includes cortical erosion and irregular cysting [16]. Cysting, and ankyloses, or the fusion of a joint [16, 22] may also result from increased mechanical load. Other pathologies related to mechanical stress include inflammation of the periosteum, which can form exostoses. Traumatic breaking and healing of the bone may occur, in conjunction with chronic arthropathies.

We initially expected to see a correlation between the severity of pathological expression and an increase in rhino mass and cursorial habits, because of the known correlation between osteopathology and mechanical stress [16, 18, 20, 21, 22], as well as previous observations of pathologies in rhinos [4, 13,14,15]. We reasoned that an increase in mass would put greater stress on bones and joints, increasing the likelihood that arthritis-like pathologies, such as osteophyte formation and articular surface degradation, would occur. If this were the case, the tendency to develop stress-related osteopathologies would be trackable and predictable. We asked two overarching questions in this study: (1) Do these osteopathologic features exhibit a trend over time? And (2) what is the relationship between mass and osteopathology?

Materials and Methods

To determine the relationship between mass and osteopathology through time, we collected data on osteopathologies from a number of extinct and extant taxa in the family Rhinocerotidae, Table 1, and an outgroup, Hyrachyus eximius, a perissodactyl sister group to the Rhinocerotidae [8, 23]. We collected data from localities with a large number of rhino skeletal elements to avoid individual preservation bias as much as possible, forming a series of species-level “snapshots” of the rhino lineage. Fossil species were chosen to span the temporal range of rhinocerotids and for the presence of adequate samples of identified elements, Table 2. Data resolution is not on the order of populations, but species in formations; this lumping of occurrences allows us to achieve a statistically adequate sample. For example, there are 15 different localities that comprise the Hyrachyus eximius sample, but they are all part of the Bridger Formation within Uinta County, Wyoming. No permits were required for the described study, which complied with all relevant regulations.

Table 1

Summary of species in this study.

Name	Age Range (MA)	Mass (kg)	NISP	MNI	Formation
Hyrachyus eximius†	50.5–46.2	36.3	275	116	Bridger
Trigonias osborni†	37.2–33.9	677	115	34	White River
Menoceras arikarense†	24.8–20.4	375	83	61	Harrison
Diceratherium niobrarense†	33.3–30.8	1010	72	26	John Day
Aphelops mutilis†	10.3–4.9	1840	110	53	Ogalla Group
Teleoceras hicksi†	10.3–4.9	1660	65	29	Shutler/ Mascall/ Rattlesnake
Diceros bicornis	0	1080	75	4	——

Summary of species in this study and related age ranges, mass, number of identified specimens (NISP), minimum number of individuals (MNI), and the geological formation the fossils are associated with. Data compiled from Fortelius and Kappelman [24], Cerdeño [8, 10], Prothero [5], Mendoza [25], and Owen-Smith [26]. Mass Estimate M1-3 Length from Radinsky 1967 [23] for H. eximius and Prothero [5] for the rest.

Table 2

Numbers and Localities of all Specimens Used in This Study.

Prefix	Specimen Num.	Genus	Species	element	NISP	Locality Name	Formation	Age
AMNH	1645	Hyrachyus†	eximius†	pelvis	1	Twin Buttes	Bridger	Bridgerian
AMNH	11652	Hyrachyus†	eximius†	pelvis	3	Little Dry Cr'k	Bridger	Bridgerian
AMNH	12364	Hyrachyus†	eximius†	pelvis	2	30 ft. above upper white stratus	Bridger	Bridgerian
AMNH	1621	Hyrachyus†	eximius†	femur	1	Bridger Basin	Bridger	Bridgerian
AMNH	1621	Hyrachyus†	eximius†	tibia	1	Bridger Basin	Bridger	Bridgerian
AMNH	1623	Hyrachyus†	eximius†	radius	1	Bridger Basin	Bridger	Bridgerian
AMNH	1638	Hyrachyus†	eximius†	radius	1	Cottonwood Corral	Bridger	Bridgerian
AMNH	1638	Hyrachyus†	eximius†	ulna	1	Cottonwood Corral	Bridger	Bridgerian
AMNH	1640	Hyrachyus†	eximius†	femur	1	Bridger Basin	Bridger	Bridgerian
AMNH	1640	Hyrachyus†	eximius†	radius	1	Bridger Basin	Bridger	Bridgerian
AMNH	1641	Hyrachyus†	eximius†	femur	1	Bridger Basin	Bridger	Bridgerian
AMNH	1644	Hyrachyus†	eximius†	tibia	1	Bridger Basin	Bridger	Bridgerian
AMNH	1645	Hyrachyus†	eximius†	tibia	1	Twin Buttes	Bridger	Bridgerian
AMNH	1646	Hyrachyus†	eximius†	humerus	1	Twin Buttes	Bridger	Bridgerian
AMNH	1646	Hyrachyus†	eximius†	radius (juvenile)	1	Twin Buttes	Bridger	Bridgerian
AMNH	1646	Hyrachyus†	eximius†	tibia	1	Twin Buttes	Bridger	Bridgerian
AMNH	1646	Hyrachyus†	eximius†	ulna	1	Twin Buttes	Bridger	Bridgerian
AMNH	1903	Hyrachyus†	eximius†	ulna	1	Henry's Fork LT	Bridger	Bridgerian
AMNH	11693	Hyrachyus†	eximius†	femur head	1	Bridger	Bridger	Bridgerian
AMNH	11693	Hyrachyus†	eximius†	radius—broken into two parts	1	Bridger	Bridger	Bridgerian
AMNH	11693	Hyrachyus†	eximius†	tibia	1	Bridger	Bridger	Bridgerian
AMNH	11707	Hyrachyus†	eximius†	femur	1	Henry's Fork LT	Bridger	Bridgerian
AMNH	11712	Hyrachyus†	eximius†	femur	1	Cat-tail Spring	Bridger	Bridgerian
AMNH	11712	Hyrachyus†	eximius†	tibia	1	Church Buttes	Bridger	Bridgerian
AMNH	12179	Hyrachyus†	eximius†	femur	1	Bridger	Bridger	Bridgerian
AMNH	12179	Hyrachyus†	eximius†	tibia- lower	1	Bridger	Bridger	Bridgerian
AMNH	12179	Hyrachyus†	eximius†	tibia- upper	1	Bridger	Bridger	Bridgerian
AMNH	12225	Hyrachyus†	eximius†	humerus	1	Summer's Dry Cr'k	Bridger	Bridgerian
AMNH	12225	Hyrachyus†	eximius†	radius	1	Summer's Dry Cr'k	Bridger	Bridgerian
AMNH	12225	Hyrachyus†	eximius†	ulna	1	Summer's Dry Cr'k	Bridger	Bridgerian
AMNH	12356	Hyrachyus†	eximius†	radius, ulna, distal humerus (articulated)	1	Mouth of Summer's Dry Creek	Bridger	Bridgerian
AMNH	12364	Hyrachyus†	eximius†	distal tibia	1	Henry's Fork	Bridger	Bridgerian
AMNH	12364	Hyrachyus†	eximius†	femur	1	Henry's Fork	Bridger	Bridgerian
AMNH	12364	Hyrachyus†	eximius†	fibula	1	Henry's Fork	Bridger	Bridgerian
AMNH	12364	Hyrachyus†	eximius†	tibia	1	Henry's Fork	Bridger	Bridgerian
AMNH	12665	Hyrachyus†	eximius†	femur	1	Grizzly Buttes	Bridger	Bridgerian
AMNH	12665	Hyrachyus†	eximius†	tibia	1	Grizzly Buttes	Bridger	Bridgerian
AMNH	12673	Hyrachyus†	eximius†	radius	1	Henry's Fork LT	Bridger	Bridgerian
AMNH	12673	Hyrachyus†	eximius†	ulna	1	Henry's Fork LT	Bridger	Bridgerian
AMNH	12675	Hyrachyus†	eximius†	femur	1	Black's Fork above Millersville	Bridger	Bridgerian
AMNH	12675	Hyrachyus†	eximius†	femur	1	Black's Fork above Millersville	Bridger	Bridgerian
AMNH	12675	Hyrachyus†	eximius†	fibula	1	Black's Fork above Millersville	Bridger	Bridgerian
AMNH	12675	Hyrachyus†	eximius†	tibia	1	Black's Fork above Millersville	Bridger	Bridgerian
AMNH	93050	Hyrachyus†	eximius†	femur	1	Henry's Fork LT	Bridger	Bridgerian
AMNH	93050	Hyrachyus†	eximius†	radius	1	Henry's Fork LT	Bridger	Bridgerian
AMNH	93050	Hyrachyus†	eximius†	ulna	1	Henry's Fork LT	Bridger	Bridgerian
AMNH	93052	Hyrachyus†	eximius†	femur	1	Grizzly Buttes	Bridger	Bridgerian
AMNH	93058	Hyrachyus†	eximius†	tibia	1	Grizzly Buttes	Bridger	Bridgerian
AMNH	93059	Hyrachyus†	eximius†	tibia	1	Henry's Fork LT	Bridger	Bridgerian
AMNH	93060	Hyrachyus†	eximius†	femur	1	Bridger Basin	Bridger	Bridgerian
AMNH	93064	Hyrachyus†	eximius†	femur	1	Henry's Fork LT	Bridger	Bridgerian
AMNH	93065	Hyrachyus†	eximius†	tibia	1	Grizzly Buttes	Bridger	Bridgerian
AMNH	93066	Hyrachyus†	eximius†	tibia	1	Bridger	Bridger	Bridgerian
AMNH	1644-A	Hyrachyus†	eximius†	femur	1	Bridger Basin	Bridger	Bridgerian
AMNH	5065-A	Hyrachyus†	eximius†	humerus	1	Bridger Basin	Bridger	Bridgerian
AMNH	5065-A	Hyrachyus†	eximius†	ulna	1	Bridger Basin	Bridger	Bridgerian
AMNH	1602	Hyrachyus†	eximius†	metapodial	8	Bridger Basin	Bridger	Bridgerian
AMNH	1607	Hyrachyus†	eximius†	metapodial	1	Bridger	Bridger	Bridgerian
AMNH	1615	Hyrachyus†	eximius†	metapodial	1	Bridger Basin	Bridger	Bridgerian
AMNH	1621	Hyrachyus†	eximius†	metapodial	1	Bridger Basin	Bridger	Bridgerian
AMNH	1629	Hyrachyus†	eximius†	metapodial	5	Bridger Basin	Bridger	Bridgerian
AMNH	1645	Hyrachyus†	eximius†	metapodial	3	Twin Buttes	Bridger	Bridgerian
AMNH	5181	Hyrachyus†	eximius†	metapodial	3	Bridger Basin	Bridger	Bridgerian
AMNH	11693	Hyrachyus†	eximius†	metapodial	8	Bridger	Bridger	Bridgerian
AMNH	12353	Hyrachyus†	eximius†	metapodial	3	Cat-tail Spring	Bridger	Bridgerian
AMNH	12368	Hyrachyus†	eximius†	metapodial	3	Henry's Fork LT	Bridger	Bridgerian
AMNH	12665	Hyrachyus†	eximius†	metapodial	3	Grizzly Buttes	Bridger	Bridgerian
AMNH	12673	Hyrachyus†	eximius†	metapodial	5	Henry's Fork LT	Bridger	Bridgerian
AMNH	12674	Hyrachyus†	eximius†	metapodial	2	Bridger	Bridger	Bridgerian
AMNH	12675	Hyrachyus†	eximius†	metapodial	5	Kinney Ranch	Bridger	Bridgerian
AMNH	12765	Hyrachyus†	eximius†	metapodial	3	Black's Fork above Millersville	Bridger	Bridgerian
AMNH	93050	Hyrachyus†	eximius†	metapodial	1	Henry's Fork LT	Bridger	Bridgerian
AMNH	93060	Hyrachyus†	eximius†	metapodial	1	Bridger	Bridger	Bridgerian
AMNH	93061	Hyrachyus†	eximius†	metapodial	4	Grizzly Buttes East	Bridger	Bridgerian
AMNH	93064	Hyrachyus†	eximius†	metapodial	1	Henry's Fork LT	Bridger	Bridgerian
AMNH	105435	Hyrachyus†	eximius†	metapodial	1	Tabernacle Butte	Bridger	Bridgerian
AMNH	1644-A	Hyrachyus†	eximius†	metapodial	2	Bridger Basin	Bridger	Bridgerian
AMNH	1602	Hyrachyus†	eximius†	phalanx	3	Bridger Basin	Bridger	Bridgerian
AMNH	1626	Hyrachyus†	eximius†	phalanx	1	Bridger Basin	Bridger	Bridgerian
AMNH	1635	Hyrachyus†	eximius†	phalanx	1	Bridger Basin	Bridger	Bridgerian
AMNH	11693	Hyrachyus†	eximius†	phalanx	11	Bridger	Bridger	Bridgerian
AMNH	12353	Hyrachyus†	eximius†	phalanx	4	Cat-tail Spring	Bridger	Bridgerian
AMNH	12673	Hyrachyus†	eximius†	phalanx	6	Henry's Fork LT	Bridger	Bridgerian
AMNH	12675	Hyrachyus†	eximius†	phalanx	1	Black's Fork above Millersville	Bridger	Bridgerian
AMNH	93064	Hyrachyus†	eximius†	phalanx	4	Henry's Fork LT	Bridger	Bridgerian
AMNH	1644-A	Hyrachyus†	eximius†	phalanx	4	Bridger Basin	Bridger	Bridgerian
AMNH	1602	Hyrachyus†	eximius†	astragalus	1	Bridger Basin	Bridger	Bridgerian
AMNH	1607	Hyrachyus†	eximius†	astragalus	1	Bridger	Bridger	Bridgerian
AMNH	1607	Hyrachyus†	eximius†	podial	1	Bridger	Bridger	Bridgerian
AMNH	1615	Hyrachyus†	eximius†	astragalus	2	Bridger Basin	Bridger	Bridgerian
AMNH	1615	Hyrachyus†	eximius†	calcaneum	1	Bridger Basin	Bridger	Bridgerian
AMNH	1615	Hyrachyus†	eximius†	podial	2	Bridger Basin	Bridger	Bridgerian
AMNH	1621	Hyrachyus†	eximius†	calcaneum	1	Bridger Basin	Bridger	Bridgerian
AMNH	1626	Hyrachyus†	eximius†	podial	2	Bridger Basin	Bridger	Bridgerian
AMNH	1629	Hyrachyus†	eximius†	podial	1	Bridger Basin	Bridger	Bridgerian
AMNH	1635	Hyrachyus†	eximius†	astragalus	2	Bridger Basin	Bridger	Bridgerian
AMNH	1644	Hyrachyus†	eximius†	calcaneum	2	Bridger Basin	Bridger	Bridgerian
AMNH	1644	Hyrachyus†	eximius†	podial	2	Bridger Basin	Bridger	Bridgerian
AMNH	1645	Hyrachyus†	eximius†	astragalus	1	Twin Buttes	Bridger	Bridgerian
AMNH	1645	Hyrachyus†	eximius†	calcaneum	1	Twin Buttes	Bridger	Bridgerian
AMNH	1645	Hyrachyus†	eximius†	podial	2	Twin Buttes	Bridger	Bridgerian
AMNH	5056	Hyrachyus†	eximius†	astragalus	1	Grizzly Buttes	Bridger	Bridgerian
AMNH	5056	Hyrachyus†	eximius†	calcaneum	1	Grizzly Buttes	Bridger	Bridgerian
AMNH	5056	Hyrachyus†	eximius†	navicular	1	Grizzly Buttes	Bridger	Bridgerian
AMNH	5056	Hyrachyus†	eximius†	podial	3	Grizzly Buttes	Bridger	Bridgerian
AMNH	5181	Hyrachyus†	eximius†	magnum	1	Bridger Basin	Bridger	Bridgerian
AMNH	5196	Hyrachyus†	eximius†	astragalus	1	Bridger Basin	Bridger	Bridgerian
AMNH	5196	Hyrachyus†	eximius†	calcaneum	1	Bridger Basin	Bridger	Bridgerian
AMNH	11693	Hyrachyus†	eximius†	podial	9	Bridger	Bridger	Bridgerian
AMNH	11712	Hyrachyus†	eximius†	astragalus	2	Church Buttes	Bridger	Bridgerian
AMNH	11712	Hyrachyus†	eximius†	calcaneum	1	Church Buttes	Bridger	Bridgerian
AMNH	12179	Hyrachyus†	eximius†	astragalus	1	Mid. Cottonwood Cr.	Bridger	Bridgerian
AMNH	12179	Hyrachyus†	eximius†	calcaneum	1	Mid. Cottonwood Cr.	Bridger	Bridgerian
AMNH	12225	Hyrachyus†	eximius†	podial	1	Summer's Dry Cr'k	Bridger	Bridgerian
AMNH	12353	Hyrachyus†	eximius†	calcaneum	1	Cat-tail Spring	Bridger	Bridgerian
AMNH	12353	Hyrachyus†	eximius†	podial	6	Cat-tail Spring	Bridger	Bridgerian
AMNH	12353	Hyrachyus†	eximius†	sesimoid	3	Cat-tail Spring	Bridger	Bridgerian
AMNH	12368	Hyrachyus†	eximius†	podial	11	Henry's Fork LT	Bridger	Bridgerian
AMNH	12665	Hyrachyus†	eximius†	astragalus	2	Grizzly Buttes	Bridger	Bridgerian
AMNH	12665	Hyrachyus†	eximius†	calcaneum	1	Grizzly Buttes	Bridger	Bridgerian
AMNH	12665	Hyrachyus†	eximius†	podial	6	Grizzly Buttes	Bridger	Bridgerian
AMNH	12673	Hyrachyus†	eximius†	calcaneum	1	Henry's Fork LT	Bridger	Bridgerian
AMNH	12673	Hyrachyus†	eximius†	podial	10	Henry's Fork LT	Bridger	Bridgerian
AMNH	12674	Hyrachyus†	eximius†	astragalus	1	Bridger	Bridger	Bridgerian
AMNH	12674	Hyrachyus†	eximius†	calcaneum	1	Bridger	Bridger	Bridgerian
AMNH	12674	Hyrachyus†	eximius†	podial	6	Bridger	Bridger	Bridgerian
AMNH	12675	Hyrachyus†	eximius†	calcaneum	1	Kinney Ranch	Bridger	Bridgerian
AMNH	93050	Hyrachyus†	eximius†	podial	1	Henry's Fork LT	Bridger	Bridgerian
AMNH	93061	Hyrachyus†	eximius†	calcaneum	1	Grizzly Buttes East	Bridger	Bridgerian
AMNH	93061	Hyrachyus†	eximius†	calcaneum partial	1	Grizzly Buttes East	Bridger	Bridgerian
AMNH	93061	Hyrachyus†	eximius†	cuboid	1	Grizzly Buttes East	Bridger	Bridgerian
AMNH	93064	Hyrachyus†	eximius†	astragalus, calcaneum, and podial (articulated)	1	Henry's Fork LT	Bridger	Bridgerian
AMNH	93064	Hyrachyus†	eximius†	podial	1	Henry's Fork LT	Bridger	Bridgerian
AMNH	98726	Hyrachyus†	eximius†	pisiform	1	S. Hyopsodus Hill, Tabernacle Butte	Bridger	Bridgerian
AMNH	105435	Hyrachyus†	eximius†	astragalus	1	Tabernacle Butte	Bridger	Bridgerian
AMNH	12665-A	Hyrachyus†	eximius†	astragalus	1	Grizzly Buttes	Bridger	Bridgerian
AMNH	12665-A	Hyrachyus†	eximius†	calcaneum	1	Grizzly Buttes	Bridger	Bridgerian
AMNH	1536-A	Hyrachyus†	eximius†	astragalus	1	Bridger Basin	Bridger	Bridgerian
AMNH	1592-A	Hyrachyus†	eximius†	astragalus	1	Bridger Basin	Bridger	Bridgerian
AMNH	1596-A	Hyrachyus†	eximius†	astragalus	1	Bridger Basin	Bridger	Bridgerian
AMNH	1644-A	Hyrachyus†	eximius†	calcaneum	1	Bridger Basin	Bridger	Bridgerian
AMNH	1644-A	Hyrachyus†	eximius†	podial	4	Bridger Basin	Bridger	Bridgerian
AMNH	5065-B	Hyrachyus†	eximius†	calcaneum	3	Bridger Basin	Bridger	Bridgerian
AMNH	1602	Hyrachyus†	eximius†	axis	1	Bridger Basin	Bridger	Bridgerian
UCMP	32011	Trigonias†	osborni†	left femur	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	humerus	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	left humerus	2	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	left radius	1	Figgins Quarry	White River	Chadronian
UCMP	32012	Trigonias†	osborni†	left ulna	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	left scapula	2	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	left tibia	2	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	left fibula	1	Figgins Quarry	White River	Chadronian
UCMP	32012	Trigonias†	osborni†	left tibia	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	patella	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	right tibiofibula	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	right ulna	1	Figgins Quarry	White River	Chadronian
UCMP	32012	Trigonias†	osborni†	right radius	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	right ulna	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	left femur	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	patellae	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	left humerus	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	right humerus	2	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	metapodial	23	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	metatarsal	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	left metatarsal	2	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	metatarsal	4	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	metapodial	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	phalanx	33	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	phalanx 3	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	astragalus	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	calcaneum	2	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	cuneiform	8	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	left podial	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	carpal	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	podial	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	pisiform	4	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	podial	2	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	navicular	3	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	left pisiform	1	Figgins Quarry	White River	Chadronian
UCMP	32011	Trigonias†	osborni†	right pisiform	1	Figgins Quarry	White River	Chadronian
AMNH	144571	Menoceras†	arikarense†	scapula	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144572	Menoceras†	arikarense†	scapula	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144573	Menoceras†	arikarense†	scapula	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144574	Menoceras†	arikarense†	scapula	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144575	Menoceras†	arikarense†	scapula	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144576	Menoceras†	arikarense†	scapula	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144577	Menoceras†	arikarense†	scapula	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144578	Menoceras†	arikarense†	scapula	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144579	Menoceras†	arikarense†	scapula	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	14213	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	14213	Menoceras†	arikarense†	radius-ulna	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	14214	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	14214	Menoceras†	arikarense†	proximal tibia	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	22486	Menoceras†	arikarense†	femur	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	22486	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	22486	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	22487	Menoceras†	arikarense†	fibula	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	22487	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	22487	Menoceras†	arikarense†	ulna	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144597	Menoceras†	arikarense†	ulna	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144598	Menoceras†	arikarense†	ulna	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144599	Menoceras†	arikarense†	ulna	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144600	Menoceras†	arikarense†	ulna	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144602	Menoceras†	arikarense†	ulna	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144603	Menoceras†	arikarense†	ulna	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144604	Menoceras†	arikarense†	ulna	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144605	Menoceras†	arikarense†	ulna	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144606	Menoceras†	arikarense†	ulna	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144607	Menoceras†	arikarense†	ulna	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144608	Menoceras†	arikarense†	ulna	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144580	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144581	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144582	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144583	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144585	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144586	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144587	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144588	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144589	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144590	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144591	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144592	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144593	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144594	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144595	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144596	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144609	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144610	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144611	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144612	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144616	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144613	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144614	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144615	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144617	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144618	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144619	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144622	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144621	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144620	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144623	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144625	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144624	Menoceras†	arikarense†	radius	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144633	Menoceras†	arikarense†	femur	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144634	Menoceras†	arikarense†	femur	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144635	Menoceras†	arikarense†	tibia	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144636	Menoceras†	arikarense†	fibula	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144584	Menoceras†	arikarense†	humerus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	86090	Menoceras†	arikarense†	partial metapodials	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144626	Menoceras†	arikarense†	metapodial	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144627	Menoceras†	arikarense†	metapodial	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144628	Menoceras†	arikarense†	metapodial	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	86090	Menoceras†	arikarense†	left phalanx	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	86091	Menoceras†	arikarense†	right phalanx	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	86092	Menoceras†	arikarense†	phalanx	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144629	Menoceras†	arikarense†	phalanx	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144632	Menoceras†	arikarense†	phalanx	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144630	Menoceras†	arikarense†	phalanx	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	144631	Menoceras†	arikarense†	phalanx	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	86090	Menoceras†	arikarense†	astragalus	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	86090	Menoceras†	arikarense†	calcaneum	1	Agate Spring Quarry	Harrison	Arikareean
AMNH	86090	Menoceras†	arikarense†	podial	2	Agate Spring Quarry	Harrison	Arikareean
UW	52334	Diceratherium†	niobrarense†	scapula	1	John Day Formation	John Day Formation	Whitneyan
UW	58203	Diceratherium†	niobrarense†	scapula	1	south canyon	John Day Formation	Whitneyan
UCMP	2289	Diceratherium†	niobrarense†	pelvis frag	1	Logan Butte	John Day Formation	Whitneyan
UW	26414	Diceratherium†	niobrarense†	patella	1	Blue Basin	John Day Formation	Whitneyan
UW	26536	Diceratherium†	niobrarense†	distal femur	1	John Day Formation	John Day Formation	Whitneyan
UW	28151	Diceratherium†	niobrarense†	femoral head	1	John Day Formation	John Day Formation	Whitneyan
UW	52334	Diceratherium†	niobrarense†	distal femur	1	John Day Formation	John Day Formation	Whitneyan
UW	53301	Diceratherium†	niobrarense†	tibia	1	picture gorge 14	John Day Formation	Whitneyan
UW	53302	Diceratherium†	niobrarense†	proximal tibia	1	picture gorge 51	John Day Formation	Whitneyan
UW	53323	Diceratherium†	niobrarense†	tibia (juvenile)	1	picture gorge 54	John Day Formation	Whitneyan
UW	53324	Diceratherium†	niobrarense†	femur (juvenile)	1	picture gorge 54	John Day Formation	Whitneyan
UW	53325	Diceratherium†	niobrarense†	distal femur	1	picture gorge 20	John Day Formation	Whitneyan
UW	53430	Diceratherium†	niobrarense†	distal femur	1	picture gorge 54	John Day Formation	Whitneyan
UW	55086	Diceratherium†	niobrarense†	tibia	1	North Wash Level 5	John Day Formation	Whitneyan
UW	58755	Diceratherium†	niobrarense†	tibia	1	Blue Canyon	John Day Formation	Whitneyan
UW	58755	Diceratherium†	niobrarense†	limb bone	2	Blue Canyon	John Day Formation	Whitneyan
UW	533315	Diceratherium†	niobrarense†	humerus	1	picture gorge 12	John Day Formation	Whitneyan
UCMP	145	Diceratherium†	niobrarense†	distal femur and podial	1	John Day Whitneyan General	John Day Formation	Whitneyan
UCMP	566	Diceratherium†	niobrarense†	proximal radioulna	1	John Day Whitneyan General	John Day Formation	Whitneyan
UCMP	75260	Diceratherium†	niobrarense†	proximal humerus	1	South Canyon 2	John Day Formation	Whitneyain
UCMP	75261	Diceratherium†	niobrarense†	distal humerus	1	South Canyon 2	John Day Formation	Whitneyain
UCMP	75261	Diceratherium†	niobrarense†	proximal humerus	1	South Canyon 2	John Day Formation	Whitneyain
UCMP	75282	Diceratherium†	niobrarense†	femur	1	South Canyon 2	John Day Formation	Whitneyain
UCMP	M1691	Diceratherium†	niobrarense†	distal femur	1	Logan Butte	John Day Formation	Whitneyain
UCMP	M1691	Diceratherium†	niobrarense†	partial fibula	1	Logan Butte	John Day Formation	Whitneyain
UCMP	M1691	Diceratherium†	niobrarense†	tibia	1	Logan Butte	John Day Formation	Whitneyain
UCMP	M2107	Diceratherium†	niobrarense†	distal femur	1	Seigfried's 4	John Day Formation	Whitneyain
UW	26563	Diceratherium†	niobrarense†	distal metapodial	1	John Day Formation	John Day Formation	Whitneyain
UW	26879	Diceratherium†	niobrarense†	distal metapodial	1	John Day Formation	John Day Formation	Whitneyain
UW	43529	Diceratherium†	niobrarense†	metatarsal	1	John Day Formation	John Day Formation	Whitneyain
UW	52334	Diceratherium†	niobrarense†	metapodial	1	picture gorge	John Day Formation	Whitneyain
UW	52334	Diceratherium†	niobrarense†	distal metapodial	1	John Day Formation	John Day Formation	Whitneyain
UW	53322	Diceratherium†	niobrarense†	metapodial	1	picture gorge 16	John Day Formation	Whitneyain
UW	55086	Diceratherium†	niobrarense†	metatarsal	1	North Wash Level 5	John Day Formation	Whitneyain
UCMP	145	Diceratherium†	niobrarense†	right metatarsal 3	1	John Day Whitneyan General	John Day Formation	Whitneyain
UCMP	M1691	Diceratherium†	niobrarense†	left metapodial	1	Logan Butte	John Day Formation	Whitneyain
UCMP	M1691	Diceratherium†	niobrarense†	metapodial	5	Logan Butte	John Day Formation	Whitneyain
UW	52334	Diceratherium†	niobrarense†	phalanx	2	John Day Formation	John Day Formation	Whitneyain
UW	53322	Diceratherium†	niobrarense†	phalanx	1	picture gorge 16	John Day Formation	Whitneyain
UCMP	788	Diceratherium†	niobrarense†	phalanx	1	John Day Whitneyan General	John Day Formation	Whitneyain
UCMP	75403	Diceratherium†	niobrarense†	medial phalanx	1	South Canyon 2	John Day Formation	Whitneyain
UCMP	M1691	Diceratherium†	niobrarense†	phalanx	3	Logan Butte	John Day Formation	Whitneyain
UW	52334	Diceratherium†	niobrarense†	podial	2	John Day Formation	John Day Formation	Whitneyain
UW	53322	Diceratherium†	niobrarense†	podial	2	picture gorge 16	John Day Formation	Whitneyain
UW	54947	Diceratherium†	niobrarense†	astragalus and partial calcanium	1	picture gorge 8 6' up	John Day Formation	Whitneyain
UW	54947	Diceratherium†	niobrarense†	podial	2	picture gorge 8 6' up	John Day Formation	Whitneyain
UW	55086	Diceratherium†	niobrarense†	podial	2	North Wash Level 5	John Day Formation	Whitneyain
UW	75665	Diceratherium†	niobrarense†	distal podial	1	picture gorge 29	John Day Formation	Whitneyain
UCMP	788	Diceratherium†	niobrarense†	tarsal	1	John Day Whitneyan General	John Day Formation	Whitneyain
UCMP	75033	Diceratherium†	niobrarense†	navicular	1	South Canyon 2	John Day Formation	Whitneyain
UCMP	75035	Diceratherium†	niobrarense†	lunar	1	South Canyon 2	John Day Formation	Whitneyain
UCMP	75120	Diceratherium†	niobrarense†	astragalus	1	South Canyon 2	John Day Formation	Whitneyain
UCMP	76104	Diceratherium†	niobrarense†	podial	2	South Canyon 2	John Day Formation	Whitneyain
UCMP	75260	Diceratherium†	niobrarense†	podial	1	South Canyon 2	John Day Formation	Whitneyain
UCMP	75348	Diceratherium†	niobrarense†	middle podial	1	South Canyon 2	John Day Formation	Whitneyain
UCMP	76104	Diceratherium†	niobrarense†	right podial	1	South Canyon 2	John Day Formation	Whitneyain
UCMP	M1691	Diceratherium†	niobrarense†	articulated astragalus and calcaneum	1	Logan Butte	John Day Formation	Whitneyain
UW	58755	Diceratherium†	niobrarense†	centrum	1	Blue Canyon	John Day Formation	Whitneyain
UCMP	22552	Aphelops†	mutilis†	left femur	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30166	Aphelops†	mutilis†	tibia	1	Higgins Quarry A	Ogalla Group	Hemphilian
UCMP	30266	Aphelops†	mutilis†	dist end of ulna	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30266	Aphelops†	mutilis†	distal humerus	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30266	Aphelops†	mutilis†	left femur	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30266	Aphelops†	mutilis†	partial distal tibia	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30266	Aphelops†	mutilis†	patella	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30266	Aphelops†	mutilis†	tibia	2	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30266	Aphelops†	mutilis†	ulna	2	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30267	Aphelops†	mutilis†	partial distal tibia	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30267	Aphelops†	mutilis†	patella	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30268	Aphelops†	mutilis†	patella	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30612	Aphelops†	mutilis†	femur	1	Higgins Quarry A	Ogalla Group	Hemphilian
UCMP	30613	Aphelops†	mutilis†	humerus	1	Higgins Quarry A	Ogalla Group	Hemphilian
UCMP	31117	Aphelops†	mutilis†	ulna	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31118	Aphelops†	mutilis†	tibia	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31119	Aphelops†	mutilis†	humerus	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31120	Aphelops†	mutilis†	humerus	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31121	Aphelops†	mutilis†	humerus	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31122	Aphelops†	mutilis†	humerus	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31127	Aphelops†	mutilis†	patella	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31128	Aphelops†	mutilis†	patella	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31129	Aphelops†	mutilis†	patella	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30266	Aphelops†	mutilis†	partial metacarpal	4	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30266	Aphelops†	mutilis†	metacarpal	5	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31123	Aphelops†	mutilis†	metacarpal	3	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	32066	Aphelops†	mutilis†	metatarsal	11	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	32067	Aphelops†	mutilis†	metatarsal	3	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	32068	Aphelops†	mutilis†	metatarsal	3	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30266	Aphelops†	mutilis†	phalanx 3	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30267	Aphelops†	mutilis†	phalanx	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30268	Aphelops†	mutilis†	phalanx	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30269	Aphelops†	mutilis†	phalanx	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30270	Aphelops†	mutilis†	phalanx	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30271	Aphelops†	mutilis†	phalanx	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30272	Aphelops†	mutilis†	phalanx	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30273	Aphelops†	mutilis†	phalanx	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30274	Aphelops†	mutilis†	phalanx	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30275	Aphelops†	mutilis†	phalanx	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31127	Aphelops†	mutilis†	phalanx	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31128	Aphelops†	mutilis†	phalanx	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31129	Aphelops†	mutilis†	phalanx	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31130	Aphelops†	mutilis†	phalanx	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31131	Aphelops†	mutilis†	phalanx	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31132	Aphelops†	mutilis†	phalanx	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31133	Aphelops†	mutilis†	phalanx	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30266	Aphelops†	mutilis†	carpals	6	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30266	Aphelops†	mutilis†	right calcaneum	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30266	Aphelops†	mutilis†	carpal	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30266	Aphelops†	mutilis†	tarsal	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	30267	Aphelops†	mutilis†	calcaneum	1	Coffee Ranch Quarry 3	Ogalla Group	Hemphilian
UCMP	30267	Aphelops†	mutilis†	tarsal	1	Coffee Ranch Quarry 4	Ogalla Group	Hemphilian
UCMP	30268	Aphelops†	mutilis†	tarsal	1	Coffee Ranch Quarry 5	Ogalla Group	Hemphilian
UCMP	30269	Aphelops†	mutilis†	tarsal	1	Coffee Ranch Quarry 6	Ogalla Group	Hemphilian
UCMP	30270	Aphelops†	mutilis†	tarsal	1	Coffee Ranch Quarry 7	Ogalla Group	Hemphilian
UCMP	31124	Aphelops†	mutilis†	astragalus	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31125	Aphelops†	mutilis†	astragalus	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31125	Aphelops†	mutilis†	calcaneum	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31125	Aphelops†	mutilis†	calcaneum	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31126	Aphelops†	mutilis†	calcaneum	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31127	Aphelops†	mutilis†	calcaneum	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31127	Aphelops†	mutilis†	carpal	9	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	31128	Aphelops†	mutilis†	tarsal	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UCMP	32066	Aphelops†	mutilis†	podial	1	Coffee Ranch Quarry 2	Ogalla Group	Hemphilian
UO	2772	Teleoceras†	hicksi†	distal humerus	1	McKay Reservoir 1	Shutler	Hemphilian
UO	4163	Teleoceras†	hicksi†	proximal radius	1	McKay Reservoir 1	Shutler	Hemphilian
UO	9634	Teleoceras†	hicksi†	ulna	1	McKay Reservoir 1	Shutler	Hemphilian
UO	17071	Teleoceras†	hicksi†	ulna	1	McKay Reservoir 1	Shutler	Hemphilian
UO	17075	Teleoceras†	hicksi†	ulna	1	McKay Reservoir 1	Shutler	Hemphilian
UO	49287	Teleoceras†	hicksi†	distal humerus	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113504	Teleoceras†	hicksi†	humerus	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113507	Teleoceras†	hicksi†	tibiofibula	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113507	Teleoceras†	hicksi†	partial ulna	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113518	Teleoceras†	hicksi†	tibia	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113519	Teleoceras†	hicksi†	distal humerus	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113519	Teleoceras†	hicksi†	partial ulna	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113519	Teleoceras†	hicksi†	proximal humerus	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113526	Teleoceras†	hicksi†	distal humerus	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	303	Teleoceras†	hicksi†	metapodial	1	McKay Reservoir 2	Rattlesnake	Hemphilian
UCMP	306	Teleoceras†	hicksi†	metapodial	1	McKay Reservoir 3	Rattlesnake	Hemphilian
UCMP	474	Teleoceras†	hicksi†	distal metapodial	1	McKay Reservoir 4	Mascall	Barstovian
UCMP	475	Teleoceras†	hicksi†	metapodial	1	McKay Reservoir 5	Mascall	Barstovian
UCMP	477	Teleoceras†	hicksi†	metapodial	1	McKay Reservoir 6	Rattlesnake	Hemphilian
UO	5056	Teleoceras†	hicksi†	metapodial	1	McKay Reservoir 7	Shutler	Hemphilian
UO	8049	Teleoceras†	hicksi†	metapodial	1	McKay Reservoir 8	Shutler	Hemphilian
UO	8053	Teleoceras†	hicksi†	metapodial	1	McKay Reservoir 9	Shutler	Hemphilian
UO	8142	Teleoceras†	hicksi†	metapodial	1	McKay Reservoir 10	Shutler	Hemphilian
UCMP	23181	Teleoceras†	hicksi†	metacarpal 3	1	McKay Reservoir 11	Rattlesnake 11	Hemphilian
UCMP	23182	Teleoceras†	hicksi†	metatarsal 3	1	McKay Reservoir 3	Rattlesnake 11	Hemphilian
UCMP	113514	Teleoceras†	hicksi†	metapodial	1	McKay Reservoir 4	Shutler	Hemphilian
UCMP	113517	Teleoceras†	hicksi†	metapodial	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113520	Teleoceras†	hicksi†	metapodial	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113521	Teleoceras†	hicksi†	metapodial	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113522	Teleoceras†	hicksi†	metapodial	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113523	Teleoceras†	hicksi†	metapodial	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113524	Teleoceras†	hicksi†	metapodial	1	McKay Reservoir 1	Shutler	Hemphilian
UO	10829	Teleoceras†	hicksi†	phalanx	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113505	Teleoceras†	hicksi†	phalanx	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113506	Teleoceras†	hicksi†	phalanx	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113509	Teleoceras†	hicksi†	phalanx	1	McKay Reservoir 1	Shutler	Hemphilian
UO	2094	Teleoceras†	hicksi†	calcaneum	1	McKay Reservoir 1	Shutler	Hemphilian
UO	4136	Teleoceras†	hicksi†	podial	1	McKay Reservoir 1	Shutler	Hemphilian
UO	4167	Teleoceras†	hicksi†	podial	1	McKay Reservoir 1	Shutler	Hemphilian
UO	8054	Teleoceras†	hicksi†	astragalus	1	McKay Reservoir 1	Shutler	Hemphilian
UO	17063	Teleoceras†	hicksi†	podial	1	McKay Reservoir 1	Shutler	Hemphilian
UO	21886	Teleoceras†	hicksi†	astragalus	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	23178	Teleoceras†	hicksi†	lunar	1	McKay Reservoir 2	Rattlesnake 16	Hemphilian
UCMP	23179	Teleoceras†	hicksi†	calcanium	1	McKay Reservoir 3	Rattlesnake	Hemphilian
UCMP	113510	Teleoceras†	hicksi†	pisiform	1	McKay Reservoir 4	Shutler	Hemphilian
UCMP	113511	Teleoceras†	hicksi†	carpal	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113512	Teleoceras†	hicksi†	podial	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113513	Teleoceras†	hicksi†	podial	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113514	Teleoceras†	hicksi†	carpal	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113515	Teleoceras†	hicksi†	pisiform	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113516	Teleoceras†	hicksi†	podial	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113519	Teleoceras†	hicksi†	podial	4	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113523	Teleoceras†	hicksi†	carpal	1	McKay Reservoir 1	Shutler	Hemphilian
UO	10397/ 5703	Teleoceras†	hicksi†	podial	1	McKay Reservoir 1	Shutler	Hemphilian
UCMP	113519	Teleoceras†	hicksi†	podial	3	McKay Reservoir 1	Shutler	Hemphilian
UO	G1675	Teleoceras†	hicksi†	calcaneum	1	McKay Reservoir 1	Shutler	Hemphilian
UO	G1676	Teleoceras†	hicksi†	astragalus	1	McKay Reservoir 1	Shutler	Hemphilian
UO	4184	Teleoceras†	hicksi†	axis	1	McKay Reservoir 1	Shutler	Hemphilian
UO	25504	Teleoceras†	hicksi†	axis	1	McKay Reservoir 1	Shutler	Hemphilian
UO	8055	Teleoceras†	hicksi†	NA	1	McKay Reservoir 1	Shutler	Hemphilian
AMNH	27757	Diceros	bicornis	metapodial	9	Kenya	NA	Recent
AMNH	27757	Diceros	bicornis	patella	2	Kenya	NA	Recent
AMNH	27757	Diceros	bicornis	calcaneum	1	Kenya	NA	Recent
AMNH	27757	Diceros	bicornis	podial	16	Kenya	NA	Recent
AMNH	27757	Diceros	bicornis	pisiform	1	Kenya	NA	Recent
AMNH	27757	Diceros	bicornis	phalanx	24	Kenya	NA	Recent
AMNH	27757	Diceros	bicornis	humerus	1	Kenya	NA	Recent
AMNH	27757	Diceros	bicornis	radius	1	Kenya	NA	Recent
AMNH	27757	Diceros	bicornis	ulna	2	Kenya	NA	Recent
AMNH	27757	Diceros	bicornis	scapula	1	Kenya	NA	Recent
AMNH	27757	Diceros	bicornis	femur	1	Kenya	NA	Recent
AMNH	27757	Diceros	bicornis	tibia	1	Kenya	NA	Recent
AMNH	27757	Diceros	bicornis	fibula	1	Kenya	NA	Recent
AMNH	81805	Diceros	bicornis	ulna	2	South Africa	NA	Recent
AMNH	81805	Diceros	bicornis	radius	1	South Africa	NA	Recent
AMNH	81805	Diceros	bicornis	podial	1	South Africa	NA	Recent
AMNH	81805	Diceros	bicornis	calcaneum	1	South Africa	NA	Recent
AMNH	81805	Diceros	bicornis	metapodial	1	South Africa	NA	Recent
AMNH	34739	Diceros	bicornis	scapula	1	Kenya	NA	Recent
AMNH	34740	Diceros	bicornis	tibia (juvenile)	1	Kenya	NA	Recent
AMNH	34740	Diceros	bicornis	metapodial (juvenile)	1	Kenya	NA	Recent
AMNH	34740	Diceros	bicornis	calcaneum (juvenile)	1	Kenya	NA	Recent
AMNH	14136	Diceros	bicornis	metapodial	1	NA	NA	Recent
AMNH	113779	Diceros	bicornis	femur (fetal)	1	NA	NA	Recent
AMNH	113779	Diceros	bicornis	tibia (fetal)	1	NA	NA	Recent
AMNH	113779	Diceros	bicornis	scapula (fetal)	1	NA	NA	Recent

Abbreviations: AMNH = American Museum of Natural History, UCMP = The University of California Museum of Paleontology, OU = The University of Oregon, UW = The University of Washington. A more detailed form of this table can be found in the supporting information.

Phylogenetic Data, R scripts and digital photographs associated with this study are available at Morphobank (project ID: 1238) [27] with permission from The American Museum of Natural History, The University of Washington Burke Museum, The University of Oregon Museum of Natural and Cultural History, and The University of Texas Jackson School of Geosciences Vertebrate Paleontology Laboratory. Digital photographs of fossils from the UCMP are also available through the Calphotos archive (http://calphotos.berkeley.edu/). S1 File of raw pathology scores available online through PLoS One.

Study Species

Hyrachyus eximius, (50.5–45.4 Ma) (Fig 1) is a sister lineage of both the tapir and rhinos. This species is estimated to have weighed around 36.3 kg (equivalent in mass to a large dog), lacked horns, and was a cursorial browser [11, 23]. The rhinocerotid with the earliest first appearance datum (FAD) included in this study is the basal rhinocerotid Trigonias osborni. T. osborni also lacked horns and was substantially larger than H. eximius at about 677 kg [24,25]. T. osborni is known from the Chadronian (37.2 to 33.9 Ma) and was a cursorial browser.

Fig 1

Time-calibrated phylogeny of rhinocerotid taxa used in this study with outgroup H. eximius.

The thicker bars indicate the actual first and last appearance data (FAD and LAD) of the fossil localities included, not the comprehensive range of the species. D. bicornis has no blue line because only modern bones were examined. Tree was pruned from Cerdeño’s 1998 [10] morphologic phylogeny or Rhinocerotidae and time-calibrated in RStudio using the ‘equal’ setting in the function timePaleoPhy() in the software package ‘Paleotree’ [28]. Tree was set to be fully dichotomous and to extend all the way to the LAD.

Menoceras arikarense emigrated from Europe in the late Oligocene or early Miocene (24.8–20.43 Ma) and had a mass around 375 kg [24,25]. M. arikarense is notable for two firsts: horns and grazing [5]. Diceratherium niobrarense is larger than M. arikarense (about 1010 kg [5]). Although D. niobrarense also displays laterally paired rostral horns, it is thought be descended from Subhyracodon and is not considered a sister group of M. arikarense [5,18]. This rhinocerotid was present in North America in the early and middle Miocene (24.8–20.43 Ma) and was probably a browser [5]. Both M. arikarense and D. niobrarense show morphologies characteristic of increased graviportality: increased bone robusticity, more vertically-oriented pelvis [26], and widening rib cage [5]. Limb length also decreased relative to mass [5].

Aphelops mutilis and Teleoceras hicksi are similar to modern rhinos in graviportal morphology and robust limbs [5]. A. mutilis was a hornless aceratheriine browser known from the mid-Miocene to the beginning of the Pliocene (10.3–4.9 Ma) and is estimated to have weighed around 1840 kg. T. hicksi (10.3–4.9 Ma) is morphologically similar to aquatic hippos [5], but has highly hypsodont teeth [5] with enamel oxygen isotope ratios similar to terrestrial herbivores [29]. T. hicksi is estimated to have weighed around 1660 kg, is thought to have a small nasal horn and is one of the last rhinocerotids in the North American fossil record [30].

From the five modern taxa we examined in planning this study we chose Diceros bicornis (the black rhino) as the modern exemplar. Diceros (5.3332 Ma to present) weighs 800–1,350 kg [24] and is a browser with a prehensile lip specialized to grab foliage [26].

Data Collection Procedure

Diagnosing specific diseases from osteopathologies (often the only pathologies available for study in fossil taxa) is difficult, but not impossible. Certain recognized diseases and disorders can leave distinctive features; e.g., six fingers in a human skeleton are an indicator of polydactyly. The majority of diseases display a common range of pathologies and it is these unique combinations of pathologies that are most informative. For example, irregular holes in a bone can be caused by abnormal nutrient canals, bone infection, soft-tissue swelling, or preservation damage. Arthritis may cause bones to form these irregular holes as well as bone exostoses or thinning, lipping, and fibrous, candlewax, and lumpy bone textures. Arthritis is often labeled spondylarthropathy in non-human paleopathologic studies [17,31] to acknowledge that arthritis itself is not a specific disease, but can be caused by a range of environmental, genetic, and behavioral factors depending on the system under study [16,18,19].

Each specimen was digitally photographed with a Nikon D90 camera. The camera was hand held approximately perpendicular to the photographic plane. Elongate fossils (e.g. femora or metapodials) were photographed in lateral view and fossils with irregular shapes (i.e. podials) were oriented in medial view. Proximal and distal articular surfaces were photographed as well for limb and foot elements. Vertebral elements were photographed in dorsal, ventral, proximal, and distal views. Extra photos were taken if a unique pathology was observed or for striking examples of specific pathologies.

The specimen number and corresponding photo numbers were recorded digitally and associated with a pathology index scoring and any qualitative observations (see supporting information). The presence or absence of pathology was recorded on site, while pathology severity scorings were determined from the digital photographs.

We quantitatively described the visible surface of each bone using a category, or binning, system. We sorted our initial qualitative descriptions of possible symptoms of disease into seven different categories. The seven categories were divided into ranks from 1 (regular bone) to 4 (severe) (Fig 2). These ranks are artificial, but should allow for consistent scoring. All scoring was completed by the first author. The seven categories are exostoses, lipping, bone texture, cavitation, foramen shape, foramen size, and articular surface modification. All categories except for ‘articular surface’ refer to the nonarticular surfaces of the bones. The categories were chosen following the methodology of Aufderheide [16], Rothschild [17, 31], and Bartosiewicz et al. [21]. Analogs of this procedure have been used for decades in anthropologic [21, 22, 32] and modern cattle [21] studies. Our goal was to quantitatively describe all irregularities observed in the osteology of the Rhinocerotidae, even if they could not immediately be categorized as a pathology.

Fig 2

Index of Pathology (IPa) used in this study.

Examples of each pathology category and the 1–4 rating system are given along with a short description.

Category One: Exostoses

Exostoses are formations of new bone on the surface of a bone, caused by inflammation of the periosteum. Extoses appear as bumps or protuberances on an area of the bone that is expected to be smooth or relatively flat. This category includes ossification of the periosteum, ligaments, or muscle. Bones in rank one do not exhibit any exostoses. Bones in rank two show minor irregular bulging of bone. Bones in rank three show clear protrusions of irregular bone. Bones in rank four show a continuous irregular distortion of the non-articular surface of the bone.

Category Two: Lipping

Lipping occurs when osteophytes (commonly referred to as bone spurs) form as new bone on the margin of articular surfaces. They usually form as a series of merging osteophytes around the joint margin, but can occur singly as well. Bones in rank one do not exhibit any lipping. Bones in rank two show slight bulging of the bone adjacent to the articular surface. Bones in rank three show bulging of the bone surrounding the articular surface to the point where a prominent shelf is beginning to form. Bones in rank four show a prominent shelf adjacent to the articular surface. The shelf may be regular or irregular.

Category Three: Textures

Bone constantly remodels and rebuilds itself in response to localized stress. This can result in characteristic external textures. Care must be taken to not conflate exostoses (which has more to do with shape) with texture. Bones in rank one have a smooth texture. Bones in rank two have an elevated linear texture, termed fibrous. Bones in rank three have an elevated linear texture that is slightly bulging or uneven texture, likened to candle wax. Bones in rank four have an elevated, uneven, nonlinear texture.

Category Four: Cavitation

Cavitation is the first category concerned with loss of bone. A cavitation is a hole in the bone, usually caused by infection and/or decreased blood flow. Unlike the categories of foramen shape and size, these are relatively large areas of the bone that cannot be confused with vascularization. Bones in rank one do not exhibit any cavitation. Bones in rank two show a pockmarked appearance where the bone has lost integrity. Bones in rank three show small cavities. Bones in rank four show large cavities that may be linked together.

Category Five: Articular Surface

The articular surface forms the bony portion of a joint. Bones in rank one do not show any irregularities in the joint surface. Bones in rank two show a pockmarked appearance where the cartilage has been worn away. Bones in rank three show bone loss on the articular surface. Bones in rank four show eburnation of the articular surface and/or osteophyte formation.

Category Six: Foramen Shape

We found bone cysts can easily be confounded with vascularization (called ‘lucencies’ in Regnault et al. 2–13 [13]), so we decided to describe the degree of foramen deformation instead of labeling all foramina as cysts. Cysting (pockets or holes where localized infections occurred [16,18]) was divided into two categories (foramen shape and size). Rank one consists of circular foramina on the surface of the bone. Rank two consists of elongate or ovoid foramina. Rank three consists of elongate foramina that are irregularly ovoid, but still linear. Rank four consists of irregular, nonlinear (or bent) foramina.

Category Seven: Foramen Size

Rank one consists of foramina of approximately the same size. Rank two consists of foramina which show little variation in size relative to one another. Rank three consists of foramina which show moderate variation in size relative to one another. Rank four consists of foramina which show a high degrees of variation in size relative to one another.

Each bone was also classified as appendicular and axial. To explore whether there were any overt patters of regionalization in pathological expression, all appendicular elements were then divided into the functional categories: hindlimb or forelimb, and also developmental categories: girdle, stylopod, autopod, zeugopod. The overall percent expression of each category was tabulated and then compared relative to the total number of appendicular element.

Data Analysis

Each fossil was given a score of 1–4 for each pathology, and these scores were then averaged for each taxon and pathological category, yielding 49 results. These averaged scores were then added together for each taxon (i.e. the seven pathology categories were added together for each taxon) to create an index of pathology (IPa). The minimum score possible would therefore be seven (all pathological categories in a taxon having a score of one) and the maximum would be twenty-eight (all pathological categories in a taxon having a score of four). These average scores for each taxon do not behave as ordinal data, because they are subject to the central limit of means. That is, species averages of non-continuous data behave like continuous data, especially with large sample sizes. The smallest number of specimens we analyzed for one species was 65, more than adequate to produce this effect. Consequently, we decided it was appropriate to analyze these values using continuous-data approaches: linear regression and independent contrasts.

We tested whether mass was associated with increased osteopathologic expression in two ways. First, we ran a series of linear regressions in JMP [33] with estimated mass against each individual categorical score as well as the total index. Mass estimates for extinct taxa were calculated using the total molar length (M1-3) [34] from Radinsky 1967 for Hyrachyus eximius [23] and Prothero 2005 [5] for all other extinct taxa, which we found to be the most reliable of available body mass estimators. Other available proxies (femur length and humerus width) produced unreasonable mass estimates [35] for one or more of the included taxa, likely as a result of the changing degree of graviportality through the history of the rhino lineage.

The second test used Felsenstein’s [36] independent contrast (IC) method to examine the influence of shared ancestry on the relationship between mass and pathology. We constructed a fully resolved tree of just the taxa in our study by paring down the results of Cerdeño 1995 [8]. The tree was time-calibrated in RStudio [37] using the packages ‘ape’ [38] and ‘paleotree’ [28] with paleotree’s function TimePaleoPhy. The r code is available in the S2 File. We used the ‘Equal’ method within TimePaleoPhy, which prevents zero-length branches, and the setting ‘add.term = TRUE’, which gave us branch lengths that took LAD into consideration. FAD and LAD for the Equal method were determined by the temporal extent of the formation at the locality where the fossils were excavated. To implement the IC method, we used the package ‘ape’ [38], to calculate the absolute values of the difference for each pair of nodes for both mass and all seven types of pathologies, as well as for the overall IPa, under a Brownian Motion model. The resulting contrasts for pathologic values were regressed against the contrast for the mass values. The r-squared and p-values for the non-phylogenetic linear regression versus the IC regression analysis were then compared.

Results

Overall, geologically older taxa show the smallest relative abundance of pathologic elements, while the greatest pathologic expression was seen in the more derived taxa, which were also the most massive taxa sampled in North America. The one exception is the extant species, D. bicornis, which appears later, yet is less massive and less pathologic overall than A. mutilis and T. hicksi.

When taxa are considered separately, H. eximius displayed low osteopathologic expression (~28%), most of which was expressed as cysting and exostoses in the podials. T. osborni and D. niobrarense also displayed a greater degree of pathologic expression in the distal elements. The M. arikarense fossil assemblage displayed prominent exostoses. In smaller elements (i.e. podials) the non-articular surfaces would be almost entirely composed of exostoses. A. mutilis and T. hicksi commonly contained large visible cysts and rank three, candlewax, bone texture. Only two fossils displayed eburnation, in A. mutilis on the articular surfaces of a proximal tibia (UCMP F-30266) and in T. hicksi on a distal humerus (UO F-2772). A. mutilis also had the highest percent expression of any one pathology (in this case, foramen shape), while D. bicornis had comparatively more foramen variation adjacent to the articular surfaces and fewer exostoses than the other robust taxa. One specimen (VPL M-8259) had flat ‘rice grain’ crystals on the proximal articular surface of right radius and ulna, as well as the distal articular surface of the humerus, a possible indication of gout [16, 18]. Tendon ossification was only seen in A. mutilis and T. hicksi. Of note, most of the articular surfaces of the synovial joints in both extinct and extant taxa appeared smooth and free of damage.

Overall index of pathology (IPa) scores were between 8 and 18, Table 3. The two oldest lineages, H. eximius and T. osborni, had an overall pathologic score of 8.8 and 11.06 respectively. The next oldest lineage, D. niobrarense, had an overall score of 12.81, while M. arikarense had an overall score of 13.31. T. hicksi had an overall score of 14.26, while A. mutilis had an overall score of 17.57. The modern rhino, D. bicornis, had an overall IPa of 12.23.

Table 3

Frequency of Pathology Scores and IPa grouped by Osteopathologies per Taxa.

		Exostoses	Lipping	Abnormal Bone Texture	Cavitation	Foramen Shape	Foramen Size	Articular Surface	Overall
H. eximius†	1	261	345	256	307	277	158	579	2183
	2	127	46	125	81	102	292	16	789
	3	3	0	9	4	13	15	1	45
	4	0	0	0	0	0	0	0	0
	IPa	1.35	1.11	1.36	1.19	1.32	1.40	1.07	8.80
T. osborni†	1	19	78	17	86	56	52	95	403
	2	88	34	81	17	50	42	16	328
	3	7	2	15	11	8	20	3	66
	4	0	0	1	0	0	0	0	1
	IPa	1.90	1.33	2	1.34	1.58	1.72	1.19	11.06
M. arikarense†	1	12	59	9	45	21	10	65	221
	2	58	32	59	21	43	26	21	260
	3	21	1	23	26	26	53	6	156
	4	1	0	1	0	2	3	0	7
	IPa	2.18	1.37	2.16	1.77	2.01	2.51	1.31	13.31
D. niobrarense†	1	14	33	3	36	25	26	52	200
	2	41	36	45	24	33	29	20	245
	3	19	6	23	14	17	20	3	122
	4	1	0	4	1	0	0	0	33
	IPa	2.10	1.61	2.38	1.69	1.85	1.88	1.31	12.81
A. mutilis†	1	0	61	10	35	3	0	73	182
	2	47	49	44	19	25	12	39	235
	3	73	20	53	44	81	74	10	355
	4	11	1	23	33	22	45	1	136
	IPa	2.69	1.75	2.96	2.54	2.86	3.26	1.53	17.57
T. hicksi†	1	12	54	9	27	9	9	70	190
	2	34	26	34	36	33	20	10	193
	3	31	2	37	18	38	46	2	174
	4	5	0	2	1	2	7	0	17
	IPa	2.49	1.37	2.43	1.82	2.4	2.59	1.169	14.26
D. bicornis	1	16	47	9	62	14	7	68	298
	2	56	26	46	13	37	33	7	218
	3	3	2	14	0	24	35	0	78
	4	0	0	6	0	0	0	0	6
	IPa	1.83	1.4	2.23	1.17	2.13	2.37	1.09	12.23

IPa = Index of Pathology, the average of all pathology scores (1 through 4) for all the individuals of a given taxa. Overall IPa is the sum of the seven individual averages. Frequency is unbolded, IPa is bolded.

When we regressed mass for each taxon against each of the seven osteopathology categories Table 4, four of the pathologies (exostoses, abnormal textures, foramen shape, and foramen size variation) had p-values less than or equal to 0.05. A linear correlation of mass against the overall pathologic scores was found to be significant (p = 0.04) and accounted for about 52% of the variation (r2 adj.). The IC analysis comparing mass and the seven osteopathology categories was also significant (p ≤ 0.05) for the both foramen shape and the overall pathologic index, with mass accounting for 42% of the overall variation.

Table 4

Linear Regression and Independent Contrast Regression against Mass.

		Overall Index	Exostoses	Lipping	Abnormal Bone Texture	Cavitation	Foramen Shape	Foramen Size	Articular Surface
Linear Contrasts	R2 Adj	0.5199	0.4772	0.2389	0.659	0.3325	0.6421	0.4797	-0.11
	F	7.498	6.477	2.884	12.6	3.988	11.76	6.532	0.4056
	P	0.04087	0.05158	0.1502	0.0164	0.1023	0.01864	0.05091	0.5522
Independent Contrasts	R2 Adj	0.4235	0.4011	-0.01015	0.5236	0.2023	0.5263	0.3932	-0.1356
	F	5.408	5.018	0.9397	70595	2.522	7.666	4.888	0.2836
	P	0.03759	0.07522	0.3769	0.04003	0.1731	0.03942	0.07802	0.6171

Linear Regression and Independent Contrast Regression Statistics against Mass. R2-adjusted, F Statistic and P values for linear and independent contrast (IC) regressions for each category of pathology are included.

We were also interested in testing whether certain bones or regions of the appendicular skeleton (which comprises the majority of the data) displayed a greater amount of pathology than other bones or regions of the appendicular skeleton. We divided all appendicular elements into the functional categories: hindlimb or forelimb (Fig 3), and also developmental categories: girdle, stylopod, zeugopod, autopod (Fig 4). For example, if the stresses generating the osteopathology were greater in the distal parts of the limb, one might expect greater pathology in the autopod (manus and pes) than the stylopod (humerus and femur). We found no significant difference in pathological expression between different regions of the appendicular skeleton.

Fig 3

Comparison of the forelimb and hindlimb.

A color spectrum is used to indicate the percent of elements displaying any osteopathology in the forelimb and hindlimb, respectively. The closer to the red portion of the color spectrum, the higher percentage. The closer to the violet portion of the color spectrum, the lower the percentage. Rhino figures do not display relative size.

Fig 4

Comparison of limb regions.

A color spectrum is used to indicate the percent of elements displaying any osteopathology in the stylopod, zeugopod, and autopod regions, respectively. The closer to the red portion of the color spectrum, the higher percentage. The closer to the violet portion of the color spectrum, the lower the percentage. Rhino figures do not display relative size.

Discussion

In our study we found that mass can explain roughly 50% of the osteopathological expression. A. mutilis, surprisingly, had the highest pathology scores by a wide margin, while T. hicksi, which was close to A. mutilis in estimated mass, had scores similar to the smaller D. niobrarense and M. arikarense. Both the overall expression of pathology and the subcategory of foramen shape were significant when regressed against mass regardless of whether phylogeny was taken into account or not. However, the r2 value in the vicinity of 0.5 suggests that other factors besides mass, such as bone robusticity, cursoriality or environment, could play a significant role in pathological expression. There might be a tradeoff between a lineage increasing in size or weight and abnormal textures, lipping, and other pathologies that intuitively should be selected against on an evolutionary scale. Lower levels of expression (categories 1 and 2) were more common, but no taxon was entirely pathology-free. The ‘maximum operational level’ of different pathologies may be similar or drastically different in different vertebrate lineages, which in turn could lead to diverse selection pressures.

Longevity could also be a factor in pathological expression. There is a positive correlation in the Mammalia between body mass and lifespan, although there is a great amount of variation [39]. The larger taxa may be living longer, which could increase the likelihood of osteoarthritis, synovitis, traumatic injury, etc. Captive mammals that live longer than their wild counterparts often display these pathologies [4, 13, 14, 15]. Pathology could be a reflection of ontogeny. However, a longer lifespan does not necessarily increase only the geriatric portion of a mammal’s life. In an animal with a longer lifespan bone would presumably stay healthy for the same proportion of a mammal’s life as the shorter-lived counterpart, but this remains to be tested [40]

Our main difficulty in this study was to establish a measurement method for pathology. In anthropology several qualitative and quantitative metrics have been used to study paleopathology [16, 18, 19]; paleontology also has no universal methodology for identifying and analyzing paleopathologies, but several parallel methods [12, 13, 14, 17, 21, 27]. Our method uses a scoring system that is focused on parsing out the severity of symptoms, not direct diagnoses of disease. It is possible to apply these separate pathology categories to studies across the vertebrate kingdom. Comparison of pathological expression between these vastly different taxa could lead to new insights into bone repair, species and lineage-level responses to pathology, and the uniformity of bone-related diseases over time.

Synovitis, not arthritis, may be the proximal cause of the pathologies observed. Notably, we found that most of the pathology in the taxa we studied was located immediately adjacent to the articular surface of joints and not in the articular surface itself. That is, the articular surface itself appeared healthy (that is, not scarred or pitted) in all but five individual specimens even in individuals with advanced exostoses and abnormal bone textures. This could indicate that the joints (and therefore the organism) are functional well after pathologies begin to appear and swelling of the synovium caused the observed cortical erosion [16].

The overall picture painted by our results shows a measureable increase in the percentage of elements that display osteopathologies related to arthritis from the older to newer branches in the North American rhinocerotid lineage, consistent with earlier observations [4, 13, 14, 15, 16, 17]. Our initial hypothesis was that more massive rhino species would display a greater frequency of osteopathologies as increased loading pressure on the limbs caused microfractures that resulted in inflammation and abnormal bone textures. With our current sample, we found a significant correlation of pathology with mass, suggesting that increasing size in the lineage was partially responsible for osteopathologies. This study is not powerful enough to conclude if these pathologies are related primarily to arthritis or is a multifactorial response or a range of diseases. Because size increase is a common adaptation in terrestrial herbivores for both eating low-quality diets [26, 41, 42] and resisting predation pressure in open environments [26, 43], it seems that adaptations for food and predator avoidance may incur a cost in bone stress and osteopathology. The accumulation of pathologies in a lineage may no longer be solely a herald of disaster, but of adaptation as well.

Raw pathology Scores for all Rhinocerotidae specimens used in this study.

Picture numbers correspond to digital photographs uploaded to Morphobank (project ID: 1238) [27]. Information available with permission from The American Museum of Natural History, The University of Washington Burke Museum, The University of Oregon Museum of Natural and Cultural History, and The University of Texas Jackson School of Geosciences Vertebrate Paleontology Laboratory.

(XLSX)

Click here for additional data file.

R Code and Required Files for Analysis.

R Code can be run in RStudio [37] using the packages ‘ape’ [38] and ‘paleotree’ [28] with paleotree’s function TimePaleoPhy. Trees from Cerdeño (1995) [8].

(ZIP)

Click here for additional data file.