Dietary Implications of Jaw Biomechanics in the Rhinocerotoids
Hyracodon and Subhyracodon from Badlands National Park, South Dakota 1
Alfred J. Mead1 and William P. Wall2
2Department of Biology, Georgia College and State University, Milledgeville, GA 31061
1University of Nebraska State Museum, Division of Vertebrate Paleontology, Lincoln, NE 68588-0514
Determining the diets of extinct species is vital for an understanding of the paleoecology of a fossil fauna. Direct evidence of paleodiet (e.g. Voorhies and Thomasson, 1979) is seldom available to the vertebrate paleontologist, and thus alternative avenues of analysis must be pursued. It is readily apparent that the structure of the jaws and teeth and the muscles that move them are indicative of particular modes of feeding (Smith and Savage, 1959; Janis, 1995). Since the shapes and masses of the jaw adductor muscles can never be known (only approximated), biomechanical studies of fossils require that the feeding mechanisms be reduced to a system of forces and levers (DeMar and Barghusen, 1972). Studies of jaw biomechanics utilizing vector analysis have proven useful in the analysis of fossil species (Gingerich, 1971; Naples, 1987; Joeckel, 1990).
The late Eocene/Oligocene sediments of the White
River Group in Badlands National Park (BADL), South Dakota,
have yielded a wide array of Chadronian, Orellan, and
Whitneyan (North American Land Mammal Ages) mammalian taxa.
If their fossil record is a valid indicator of past
abundance, Hyracodon (Hyracodontidae) and
Subhyracodon (Rhinocerotidae) were the most common large (> 100 kg)
herbivores (horses and oreodonts being medium-sized) of
the Orellan in the central Great Plains region.
Subhyracodon was approximately 120 cm at the shoulder and, although
larger, exhibited similar skeletal proportions to modern tapirs
such as Tapirus terrestris (Scott, 1941). The dental formula is
2/2, 0/0, 4/4-3, 3/3. Hyracodon was smaller than
Subhyracodon and more agile, as suggested by the elongate metapodials.
It was approximately 80 cm at the shoulders with a
proportionately longer neck than that of any known rhinocerotoid
(Scott, 1941). The dental formula is 3/3, 1/1, 4/3, 3/3. Recent
mechanical analysis of the locomotor abilities of Hyracodon suggest subcursorial habits, similar to extant wild pigs and peccaries (Wall and Hickerson, 1995).
Hyracodon and Subhyracodon have been cited as indicator species of separate sedimentary facies in BADL. Matthew (1901) determined Hyracodon to be indicative of his Clay fauna (plains dwellers) and Subhyracodon indicative of the Sandstone fauna (forest dwellers). Clark et al. (1967) concluded that Subhyracodon was indicative of a Near Stream fauna of the Lower Nodular Zone (Orellan) while Hyracodon was representative of the Open Plains fauna. Wilson (1975) reported the occurrence of Subhyracodon exclusively in the Protoceras Channels and Hyracodon only in the overbank mudstones of the Leptauchenia Beds (Whitneyan) in the Palmer Creek area.
The purpose of the present study is to: 1) illustrate cranial morphological differences; 2) attempt to reconstruct the jaw adductor musculature; 3) estimate jaw biomechanical abilities; and 4) suggest possible feeding modes for Hyracodon and Subhyracodon that may explain the observed dichotomous facies distribution.
materials and methods
Adult Hyracodon (4 skull/jaws) and
Subhyracodon (3 skull/jaws, 4 jaws) material examined in the present
study was collected from BADL and is housed in the
Georgia College & State University Vertebrate Paleontology
(GCVP) collection. Comparisons with recent mammals are based
on study of specimens housed in the Georgia College &
State University Mammalogy (GCM) collection. To illustrate
relative morphological differences, Cartesian transformations
were constructed (as described by Thompson, 1961) in both the
lateral (Figure 1) and dorsal (Figure 2) aspects for
Hyrachyus (a primitive rhinocerotoid),
Hyracodon and Subhyracodon. Quadrant analyses (Figure 3) of the mandibular angles of middle of M1 in both genera; deep masseter, on the
zygomatic arch with muscle fibers perpendicular to the central
axis of the arch; temporalis, the distal end of the temporal
fossa, anterior edge of the occipital ridge.
Figure 1Lateral distortion grids constructed for (A) Hyrachyus , (B) Hyracodon, and (C) Subhyracodon. Hyrachyus modified from Osborn and Wortman (1894: Plate 2).
Figure 2Dorsal distortion grids for (A) Hyrachyus, (B) Hyracodon, and (C) Subhyracodon. Hyrachyus modified from Osborn and Wortman (1894: Plate 2). Hyracodon and Subhyracodon modified from Scott (1941).
Muscle mass proportions were estimated using
modeling clay as described by Turnbull (1976). The masseter
group includes the superficial masseter, deep masseter,
and zygomaticomandibularis. The pterygoid estimate includes
the lateral and medial pterygoid. The temporalis estimate
includes the deep and superficial temporalis. The proportions of
the superficial and deep masseter and zygomaticomandibularis
in the total masseter group mass were estimated using
known percentages for modern ungulates exhibiting similarly
oriented zygomatic arches and similarly shaped mandibular
angles (Turnbull, 1970). Ovis aries (30% superficial; 70%
deep) was used for Subhyracodon and
Odocoileus virginianus (38%
Hyracodon and Subhyracodon were performed to quantify the attachment areas for the deep and superficial masseters in relation to the cranio-mandibular joint (CMJ). The mandibular angle was systematically divided into four quadrants and a dot grid was used to determine the percentage of the total occurring within each quadrant.
Jaw adductor muscle reconstructions were attempted for Hyracodon and Subhyracodon with the aid of muscle scars on the fossil material mentioned above. Although unknown, all muscles are assumed to exhibit parallel fibers. Fresh heads of the extant Odocoileus virginianus, Alces alces, Antilocapra americana, and Cervus elaphus were dissected and served as general templates for the reconstructions. The following estimates were used for the origins of the adductor musculature: superficial masseter, anterior to the zygomatic arch, above the superficial; 62% deep was used for Hyracodon.
Figure 3 Labial views of left lower jaws of (A) Hyracodon and (B) Subhyracodon with mandibular angles divided into quadrants as discussed in text. Scale = 4 cm.
Figure 4 Left lateral view of the skulls of (A) Hyracodon and (B) Subhyracodon illustrating the length and orientation of each median muscle fiber (heavy solid line), the moment arm of each fiber (light dashed line), and the trend of the central axis of each zygomatic arch (heavy dashed line). Scale = 4 cm.
Lengths of the median muscle fibers for the superficial masseter, deep masseter, and temporalis were estimated using nylon string cut to lengths connecting the middle of the muscle scars for each origin and its corresponding insertion (Naples, 1987; Joeckel, 1990). The median muscle fibers were superimposed upon line drawings of the skulls (Figure 4) at the mid-point of observed muscle scars. Perpendicular moment arms were inserted between the median fibers and the mandibular condyle (CMJ). Force vectors (Figure 5) were estimated based on the lengths and orientation of the median fibers and the approximate proportions of the total adductor muscle mass of each muscle. A total vector length of 15 cm was arbitrarily chosen for each analysis. The angle of each vector was measured against a reference line in the occlusal plane of the cheek teeth. Estimation of the role of the medial and lateral pterygoid in fossil mammals is difficult due in part to the variability exhibited in modern mammals (Janis, 1983). For this reason the pterygoid group is treated as a single force with a line of action the same as the deep masseter.
Distinct differences are evident when the skulls
of Hyracodon and Subhyracodon are compared to the
primitive rhinocerotoid cranial morphology exhibited by
Hyrachyus (Figures 1A and 2A).
Hyracodon (Figure 1B) exhibits a vertically expanded temporal fossa and sagittal crest, and a
shorter, deeper rostrum. The coronoid process is expanded both
vertically and horizontally, as is the posterior half of the
matic arch. The premaxilla is shortened and the maxilla expanded anteroposteriorly. The mandibular angle is enlarged primarily ventrally, but also slightly posteriorly. The frontals are anteroposteriorly expanded above and anterior to the orbits, and also in the posterior-most region of the parietals (Figure 2B). The posterior parietals are laterally constricted. The anterior and posterior zygomatic arch and premolar region of the rostrum are laterally expanded. The nasals above the premolars are anteroposteriorly and laterally reduced.
Figure 5Vector analysis and adductor muscle reconstruction of (A) Hyracodon and (B) Subhyracodon. a = M. masseter pars superficialis; b = M. masseter pars profunda, M. pterygoideus medialis, and M. pterygoideus lateralis; c = M. temporalis. Scale = 4 cm.
Mandibular angle analysis
quad I 20% 34%
quad II 13 % 6 %
quad III 33 % 11 %
quad IV 33 % 49 %
Adductor muscle mass est.
% temporalis 24 20
% pterygoid 32 32
% masseter group 44 48
Median muscle fiber ratios
superficial/deep masseter 1.38 1.39
temporalis/deep masseter 0.79 0.88
Moment arm ratios
superficial/deep masseter 1.57 1.53
temporalis/deep masseter 0.89 0.66
temporalis/superficial masseter 0.57 0.43
Angle of zygomatic arch 41o 30o
superficial masseter 25o 23o
deep masseter 45o 57o
temporalis 20o 25o
The temporal region of Subhyracodon (Figure 1C) is enlarged but not to the extent seen in Hyracodon. The rostrum is longer immediately anterior to the orbit and above the premaxillae, but shortened in the region of the narial notch. The coronoid process is not noticeably changed. The zygomatic arch is enlarged above the CMJ and M3. The premaxillae and maxillae are expanded both anteroposteriorly and vertically. The ascending ramus of the dentary is vertically expanded, the masseteric fossa is enlarged, and the posterior portion of the mandibular angle is reduced. The anterior dentary is vertically thickened below the diastema, and anteroposteriorly expanded below the premolars. The nasals, frontals, and anterior parietals (above the orbits) are anteroposteriorly expanded (Figure 2C). The nasals are laterally expanded above the premolars, yet slightly constricted in the molar region. The posterior region of the zygomatic arch is marginally exproportionately longer temporalis moment arm. A more inclined (41o as opposed to 30o) central axis of the zygomatic arch is evident in Hyracodon. Vector orientations illustrate a more anteriorly inclined deep masseter in Hyracodon and a more vertically elevated temporalis in Subhyracodon (Figure 5A, B).
Analysis of the cranial morphology of Hyracodon and Subhyracodon reveals many differences which suggest differing functional abilities that ultimately determine the feeding category of each rhinocerotoid. For fossil mammalian herbivores, the assigned feeding modes must coincide with available vegetation. The diversity of White River mammalian fauna indicates that a number of habitats existed during the late-Eocene through early-Oligocene in the area of BADL including well drained open gallery forests, bushland prairies, and vegetated swamps (Clark et al., 1967). Paleosols and fossil gastropods in sediments of the White River Group suggest that the general paleo-environment of central North America progressed from moist forests to dry woodlands to wooded bushlands (Retallack, 1992; Evanoff et al., 1992). Evidence of true grasses is absent, but the flora likely included shrubs and bunch grasses (Retallack, 1983).
The limitations of muscle mass reconstructions and vector analyses must be recognized. The absolute size of a given muscle in a fossil species can never be known. The absolute force generated by an estimated muscle mass is indeterminate and not always directly proportional to the mass. However, in light of these limitations, it is possible to discuss meaningful relative differences.
The muscle mass estimations and superficial/deep
masseter moment arm ratios (Table 1) suggest typical
panded and the anterior region is medially constricted. The maxillae are laterally expanded in the premolar region.
Nearly half (Table 1) of the mandibular angle of Subhyracodon (Figure 3B) lies within quadrant IV and 83% lies anterior to the CMJ (quads I and IV). Sixty percent lies beneath the occlusal plane (quads III and IV). The distribution of bone is more uniform across the quadrants in Hyracodon (Figure 3A). Fifty percent of the mandibular angle lies anterior to the CMJ and 66% lies beneath the occlusal plane. Hyracodon exhibits a dominantly larger quadrant III posterior to the CMJ.
Modeling clay muscle mass estimates suggest a proportionately larger temporalis in Hyracodon and larger masseter group in Subhyracodon (Table 1). When compared to known values for modern mammals (Turnbull, 1970), the temporalis, pterygoid, and masseter group percentages of Hyracodon are most similar to those of Odocoileus virginianus and Sus scrofa, while the percentages of Subhyracodon most closely resembles those of Ovis aries and a zebra (GCM 575, Equus sp.). The superficial/deep masseter median fiber ratios are the same for both species. The temporalis/deep masseter median fiber ratios of 0.88 in Subhyracodon and 0.79 in Hyracodon indicate that the latter has a relatively longer temporalis or shorter deep masseter (Figure 4A, B). The superficial/deep masseter moment arm ratios are also identical. Hyracodon exhibits a style masseter-driven mechanical systems in both genera. The low profile of the Subhyracodon skull gives the impression that the deep masseter vector (Figure 5B.b) is considerably longer than that in Hyracodon (Figure 5A.b) when in fact they are nearly identical in length. The primary difference lies in the direction of the vectors.
Hyracodon exhibits a more anteriorly inclined deep masseter due largely to the posterio-ventral expansion of the mandibular angle (Figure 3A) and a 41o inclination of the central axis of the zygomatic arch (Figure 4A). A more anteriorly inclined masseter translates into a greater anterior movement of the lower jaw during the initial phase of the chew cycle, allowing for increased shear as the teeth move into centric occlusion and is beneficial for the comminution of tough browse. Greaves (1991) concluded that the area of attachment for the masseter and pterygoids reflects the gross size of the muscles. The expanded posterior half of the zygomatic arch (Figures 1B, 2B) increases the area of origin for the deep masseter and zygomaticomandibularis. Lateral expansion of the zygomatic arch allows for an increase in the mass of the superficial and deep masseters and the zygomaticomandibularis (44% of the adductor muscle mass).
The posterio-ventral expansion of the mandibular angle in Hyracodon (Figures 1B, 2B, 3A) also allows for an increased distance between the origin and insertion of the superficial and deep masseters and pterygoids. The distance over which a muscle can effect a movement is proportional to its length (Hildebrand, 1995). Assuming that the occlusion of the cheek teeth does not vary with a change in muscle size, absolute greater muscle mass likely reflects greater overall force generation.
The expanded temporal fossa (Figure 2B) and sagittal crest (Figure 1B), enlarged coronoid (Figure 1B), and proportionately longer moment arm (Figure 4A) suggests that the temporalis is of greater importance in Hyracodon than Subhyracodon. The expanded temporal fossa and sagittal crest provide a larger area of origin for the temporalis and the enlargement of the coronoid increases the area of insertion. The proportionately longer moment arm increases the mechanical advantage of the muscle. Increased temporalis leverage could correspond to an increase in orthal retraction movements necessary to snip tough browse.
The less well developed coronoid process, proportionately smaller temporal fossa (Figures 1C, 2C) and estimated temporalis muscle mass, along with a relatively shorter temporalis moment arm (Figure 4B), reflects a reduced importance of the temporalis in Subhyracodon. This condition suggests a lesser importance of orthal retraction movements during food acquisition in Subhyracodon. Vertical expansion of the mandibular angle in Subhyracodon (Figure 1C) increases the area of insertion for the deep masseter (masseteric fossa) and medial pterygoid (pterygoid fossa) anterior to the CMJ (Figure 3B). A muscle mass producing a more vertically oriented (57o to the occlusal plane) force (Figure 5B) would likely increase the occlusal pressure during centric occlusion and thus increase the grinding ability in Subhyracodon.
The mandibular condyle is more elevated above the
row in Subhyracodon (Figure 1C). A more elevated condyle allows the maintenance of vertically oriented occlusal forces (Greaves, 1974), and would benefit the grinding phase of the chew cycle. The expansion of quadrant IV (49%) in Subhyracodon allows for a more anteriorly positioned deep masseter point of insertion (Figure 3B). Coupled with a decreased angle (30o) of the central axis of the zygomatic arch (Figure 4B), enlarged posterior and reduced anterior zygomatic arch (Figure 1C), the total effect is a posterior shift of the origin and anterior shift of the insertion maintaining an effective moment arm for the deep masseter. The medial constriction of the anterior zygomatic arch decreases the area of origin and suggests a decreased importance of the superficial masseter.
The laterally expanded premaxillae, frontals, zygomatic arches, and parietals along with anteroposteriorly reduced anterior maxillae and anterior parietals illustrate the brachy- to mesocephalic nature of the Hyracodon skull (Figure 2B). The laterally constricted maxillae, anterior parietals, and zygomatic arches in combination with anteroposteriorly expanded premaxillae, maxillae, frontals, and parietals illustrate the more dolichocephalic, wedge shaped nature of the Subhyracodon skull (Figure 2C). The relative orientation of the occipital condyles (Figure 1B, C) suggests that head carriage may have varied as indicated by Scott (1941). The skull of Hyracodon was likely held in a snout-down orientation while the Subhyracodon skull was held in a snout-forward manner. The Zeuner (1945) method of estimating rhinoceros feeding habits based on the average head carriage suggests differing feeding modes for Hyracodon and Subhyracodon.
A herbivore utilizing tough browse as a food source would benefit more from cranial musculature arranged to produce a larger amount of shear at the occlusal surface. One utilizing more succulent browse (material that will not break under shearing forces) would derive the greatest benefit from an increase in grinding abilities. In an open bushland environment, the short wide muzzle of a brachycephalic skull and well developed orthal retraction in the chew cycle would be more advantageous to a non-selective browser of tough vegetation. The modern browsing perissodactlys (e.g. tapirs and browsing rhinos) generally exhibit brachycephalic or mesocephalic skulls. The long narrow muzzle of a dolichocephalic skull would allow a selective browser to be very precise in its acquisition of food materials. Dolichocephalic skulls are more indicative of the grazing modern perissodactyls (e.g. horses, zebras, and wild asses) and selective browsing artiodactyls (e.g. giraffe).
Past sedimentological studies have concluded that Hyracodon is more prevalent in the floodplain facies and Subhyracodon generally restricted to the stream channel facies of BADL suggesting different habitat usage and feeding modes in these temporally sympatric rhinocerotoids. Differing cranial morphologies in Hyracodon and Subhyracodon suggest differences in jaw biomechanical abilities and support the earlier conclusions concerning differing habitat us age. A brachy- to mesocephalic skull, complete anterior dentition, well developed temporalis, and more anteriorly directed masseter/pterygoid muscle group, along with a snout-down carriage, relatively long neck, and subcursorial locomotor abilities, indicates that Hyracodon was likely a non-selective browser of tough, low vegetation distal to the Oligocene streams. The dolichocephalic skull, reduced anterior dentition, lesser developed temporalis, vertically enlarged masseteric fossa, more vertically oriented deep masseter and medial pterygoids, and snout-forward carriage suggests that Subhyracodon was a mixed feeder more suited to utilize the succulent vegetation and high browse of the riparian strips.
The senior author thanks W. Wall, D. Parmley and M. Voorhies for advise, encouragement, and many stimulating conversations. We thank R. Benton of BADL for her assistance in the park, and M. Voorhies and P. Freeman of the UNSM for use of specimens in their care. M. Voorhies, B. Bailey, G. Corner, and D. Terry reviewed earlier versions of this manuscript. We thank three anonymous reviewers for their useful comments. We thank P. Tandon for her assistance with computer graphics. The senior author acknowledges H. Mead for her critical reviews, patience, and encouragement. Finally we thank Mr. Vince Santucci for his enthusiasm and support for paleontological research in the National Parks. This work was partially funded by Georgia College & State University Faculty Research Funds.
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