Changes in Enamel Ultrastructure at the Early Stages ...

Paleontological Journal, Vol. 34, Suppl. 2, 2000, pp. S242–S249. Original Russian Text Copyright © 2000 by Vislobokova, Dmitrieva. English Translation Copyright © 2000 by MAIK “Nauka /Interperiodica” (Russia).

Changes in Enamel Ultrastructure at the Early Stages of Ruminant Evolution I. A. Vislobokova and E. L. Dmitrieva Paleontological Institute, Russian Academy of Sciences, ul. Profsoyuznaya 123, Moscow, 117868 Russia Received June 3, 1999

Abstract—The ultrastructure of molar enamel in early ruminants was studied based on collections housed at the Paleontological Institute of the Russian Academy of Sciences, American Museum of Natural History, and Natural History Museum (London). The main trends in the perfection of the enamel structure were observed. A primitive type of enamel ultrastructure characteristic of archaeomerycids is described. The main features of enamel ultrastructure in various groups of the Tragulina and early higher ruminants are analyzed.

INTRODUCTION

RESULTS

The perfection of the enamel structure of teeth is a particular trend in ungulate evolution associated with adaptation to herbivory. Even at the early evolutionary stages, ruminants varied widely in the enamel ultrastructure of the teeth as a result of an increased diversity of diets and changes of the masticatory mechanism. The enamel structure in early ruminants was substantially influenced by increased pressure on the occlusal surface that promoted a structural reorganization.

The Initial Type of Enamel Ultrastructure in the Molars of Early Ruminants

The purpose of this study was (1) to investigate the main trends in the complication in the enamel ultrastructure of molars of early ruminants and (2) to estimate the significance of the data on enamel ultrastructure in relation to phylogeny and taxonomy. The study revealed the main types of enamel ultrastructure in the molars of early ruminants and the main characteristics of enamel transformations in the course of evolution, including both common features revealed in all groups and specialized features characteristic of particular groups only. The study considers the results of the examination of enamel ultrastructure with the aid of a scanning electron microscope (SEM) in the first lower molars of the Paleogene Tragulina, Cervoidea, and the Bovidae from Eurasia, North America, and Africa housed in the Paleontological Institute of the Russian Academy of Sciences (PIN), American Museum of Natural History (AMNH), and The Natural History Museum, London (BMNH). The first lower molars are of particular interest for our study, since they undergo the highest loading. Table 1 shows the list of specimens examined in this study. To remove the external nonprismatic layer, we placed the specimens in 5% HCl for 10 s, according to the technique proposed by Carlson and Krause (1985).

The initial type of enamel ultrastructure in the molars of early ruminants, retained in tragulines of the family Archaeomerycidae (found in the Middle Eocene to the Early Oligocene of Asia), was archaic. The Archaeomerycidae of the genera Archaeomeryx and Miomeryx had the most primitive enamel ultrastructure of all tragulines. They are characterized by a simple radial enamel covering relatively low tooth crowns. In Archaeomeryx and Miomeryx, the surface of molar wear almost completely corresponds to the transverse section of prisms. In this plane, the dental enamel is composed of large arcade-shaped prisms (P) distributed uniformly and not forming chains (Fig. 1). In Archaeomeryx, the density of the prisms is approximately 32 thousand per mm2, i.e., is comparable to those in some insectivores of the family Ptilodontidae (Carlson and Krause, 1985). In longitudinal section, the prisms are relatively short, oriented radially, almost parallel to each other, and surrounded by well developed interprismatic crystallites (IPC). They lie almost perpendicular to the surface of wear and the plane of the enamel-dentin junction (EDJ). The enamel structure of archaeomerycids is probably inherited from primitive eutherian mammals, as a number of morphological characters (Vislobokova and Trofimov, 2000). Enamel of archaeomerycids is similar to that of multituberculate mammals and Late Cretaceous eutherians (including Protungulatum donnae, an early arctocyonid) in shape and simple arrangement of prisms located almost in parallel to each other (Carlson and Krause, 1985; Koenigswald et al., 1987).

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Table 1. Material Family Archaeomerycidae Archaeomerycidae Lophiomerycidae Lophiomerycidae Lophiomerycidae Gelocidae Gelocidae Leptomerycidae Hypertragulidae Hypertragulidae Hypisodontidae Simimerycidae Tragulidae Cervidae Cervidae Cervidae Bovidae Bovidae Bovidae

Species

Institution

Archaeomeryx optatus Miomeryx altaicus Lophiomeryx cf. angarae Lophiomeryx cf. mouchelini Lophiomeryx chalaniati Gobiomeryx dubius Pseudomeryx gobiensis Leptomeryx sp. Hypertragulus calaratus Nanotragulus sp. Hypisodus sp. Praetragulus electus Dorcatherium sp. Eumeryx sp. Amphitragulus cf. quercyi Dremotherium cf. guthi Palaeohypsodontus asiaticus Gabiocerus mongolicus Gazella sp.

PIN PIN PIN PIN PIN PIN PIN AMNH AMNH AMNH AMNH PIN BMNH PIN PIN PIN PIN PIN PIN

The Main Trends in the Molar Enamel Evolution in Early Ruminants

Locality

Age

Ula-Usu, China Tatal-Gol, Mongolia Tatal-Gol, Mongolia Tatal-Gol, Mongolia Quersi, France Tatal-Gol, Mongolia Tatal-Gol, Mongolia White River, South Dakota Cedar Creek, Colorado Muddy Creek, Wyoming Morris Ranch, Nebraska Khoer-Dzan, Mongolia Rusinga, Kenya Tatal-Gol, Mongolia Yagan-Tologoi, Mongolia Yagan-Tologoi, Mongolia Menkhen-Teg, Mongolia Shine-Us, Mongolia Mongolia

Middle Eocene Early Oligocene Early Oligocene Early Oligocene Late Oligocene Early Oligocene Early Oligocene Early Oligocene Early Oligocene Late Oligocene Early Oligocene Early Oligocene Early Miocene Late Oligocene Late Oligocene Late Oligocene Early Oligocene Early Miocene Recent

In contrast to most large mammals, a number of Eocene ruminants are characterized by a primitive enamel structure and lack the Hunter-Schreger bands (HSB); according to the data obtained by Koenigswald et al. (1987), the latter were typical of many large mam-

Enamel complication followed the same pattern in various mammalian groups, distinguished by the degree of complication. (b)

(a)

(c)

Archaeomeryx

00:10

3 μm

(d)

Gobiomeryx

00:03

3 μm

Eumeryx

00:29

3 μm

3 μm

Fig. 1. Shape of enamel prisms in molars of early ruminants: (a, b) arcade-shaped, (c) composite (arcade-shaped and circular), and (d) circular; (a) Archaeomeryx optatus, PIN, no. 2198/166; (b) Gobiomeryx dubius, PIN, no. 3935/587; (c) Eumeryx imbellis, PIN, no. 3935/583; and (d) Gobiocerus mongolicus, specimen PIN, no. 532/8. PALEONTOLOGICAL JOURNAL

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mals, beginning from the Early Paleocene. Among all living eutherians, the Hunter-Schreger bands are absent in insectivores and chiropterans. Previously, it was proposed that all ungulates were characterized by a relatively progressive enamel structure and the earliest members should possess the Hunter-Schreger bands. In perissodactyls, crossing Hunter-Schreger bands are well-pronounced even in the Early Eocene Hyracotherium. They are also observed in the Phenacodontidae, the probable ancestors of horses (Koenigswald et al., 1992). Koenigswald et al. (1987) believe that the presence of the HunterSchreger bands was associated with the transition to new types of feeding, i.e., the origin of herbivores and carnivores from insectivores. They indicated that the appearance of Hunter-Schreger bands was associated with an increase in body sizes (in particular, in primates). They proposed that Hunter-Schreger bands had arisen when the molars had become more than 4 mm wide. In actual fact, a correlation between the extent of structural complication and an increase in body size is not linear, but appears as a component of the general advantages in feeding adaptations, involving primarily the digestive system, masticatory muscles, and dental apparatus. Progressive changes were not necessarily accompanied by an increase in body size (for example, in a number of gelocids and hypertraguloids). In early ruminants, the enamel structure changed in passing from feeding on a relatively soft mixed food (such as insects and fruit) to a rough food and herbivory. These changes are distinguishable in different phylogenetic lineages of early ruminants and reach the maximal development in highly specialized forms. In many early ruminants, lateral chewing movements prevailed over vertical movements that predominated in the Archaeomerycidae. This is evidenced by the pattern of inclination of the occlusal surface and by the orientation of scratches on this surface. Cheek teeth of early ruminants gained increased resistance to wear by both an increase in crown height and changes of dental tissue. At the early stages, the advantage in dental enamel was achieved by a more effective arrangement and orientation of crystallites in the prisms and interprismatic spaces. In early ruminants, the main trends in the development of enamel ultrastructure associated with an increase in grinding pressure consist of the following: (1) Complication of prism orientation. Structural changes from a simple radial pattern to a more complex structure consisting of simple parallel chains, bands, or intersecting Hunter-Schreger bands. In progressive species, simple straight chains, characteristic of early stages of transformation of radial enamel, become curved. Weak waves are replaced by a sinusoid curvature; subsequently, the decussate pattern developed. (2) An increase in prism inclination in relation to the surface of enamel-dentin junction and to the wear sur-

face. At the primitive stage, the prisms are oriented almost perpendicular to the wear surfaces, whereas at the most advanced stage, they are at an angle of approximately 45° to these surfaces. (3) Organization of interprismatic crystallites in the plates lying in parallel to each other and isolating the chains of the prisms. (4) An increase in enamel durability by an increase in prism density. The density increases by a decrease in prism diameter and thinning of the interprismatic plates. (5) An increase in enamel thickness by prism lengthening and complication of the repetitive pattern (Schmelmuster). In addition, in some forms, arcade-shaped prisms are transformed into circular prisms by prism closing, i.e., complete development of organic cover isolating the prisms from the interprismatic crystallites. These trends are developed to different degree in different phylogenetic lineages of early ruminants. Enamel Ultrastructure in Molars of the Tragulina The Tragulina is a relatively homogeneous group with reference to prism shape (Table 2). The prisms vary in size, orientation, extent of lengthening, density of distribution, and in certain interprismatic characteristics. Almost all tragulines possess arcade-shaped prisms. Prism closing occurs in the family Lophiomerycidae only. In Lophiomeryx angarae, the prisms are almost closed but distributed uniformly. In L. chalaniati, the prisms are closed and form chains. The density of prisms increases from 57 thousand per 1 mm2 in L. angarae to 89 thousand per 1 mm2 in L. chalaniati. The latter value is equal to that in Leptomeryx sp. and only slightly lower than in Gazella. Among the Tragulina, the density of prisms is relatively high in gelocids of the genus Pseudomeryx and hypertraguloids of the genera Hypisodus and Praetragulus (Vislobokova, 1998). In addition to the basal (initial) enamel type, i.e., simple radial ultrastructure preserved in the Archaeomerycidae, three advanced types of enamel ultrastructure are recorded in early ruminants. These types present different ways of increasing dental durability and of the resistance of dental tissue to wear (Fig. 2, Pl. 6). The first two are advanced derivatives of the radial structure. (1) Radial chain ultrastructure. The prisms form chains oriented almost perpendicular to the surfaces of the enamel-dentin junction. They are weakly inclined in relation to the wear surface. The genera of the Gelocidae, Lophiomerycidae, and Hypertraguloidea differ from each other by the degree of prism inclination and the thickness and compactness of enamel. The primitive weak inclination of prisms relative to the wear surface and preservation of the primitive perpendicular position relative to the enamel-dentin junction

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Table 2. Features of enamel ultrastructure in the lower molars of early ruminants Species

Prism shape

HSB

2r

d

f

a a a a o a a a a a a a a

– – – – – + – – – – – – –

5.25 4.5 4.1 3.9 2.9 4.1 3.0 3.6 4.5 4.2 2.8 2.6 3.8

6.0 5.36 4.5 4.3 3.6 4.5 3.75 3.6 4.87 4.8 3.8 3.9 4.5

32100 40200 57000 62450 89100 57000 80100 89100 48700 50100 80000 75900 57000

a+o o o

+ + +

3.9 3.6 3.8

4.7 4.3 4.7

52300 62450 52300

a+o o o

+ + +

4.0 2.4 2.7

4.6 3.9 3.4

54600 75900 99900

TRAGULINA Archaeomeryx optatus Miomeryx altaicus Lophiomerux cf. angarae Lophiomeryx cf. mouchelini Lophiomeryx chalaniati Gobiomeryx dubius Pseudomeryx gobiensis Leptomeryx sp. Hypertagulus calcaratus Nanotragulus sp. Hypisodus sp. Praetragulus electus Dorcatherium sp. PECORA Cervidae Eumeryx imbellis Amphitragulus cf. quercyi Dremotherium cf. guthi Bovidae Palaeohypsodontus asiaticus Gobiocerus mongolicus Gazella sp.

Note: (a) arcade-shaped prisms; (o) circular prisms; (a + o) combination of arched and circular prisms; (HSB) Hunter-Schreger bands: (–) undeveloped and (+) developed; (2r) mean transverse diameter of prism; (d) mean distance between the centers of neighboring prisms; (f) frequency of prisms, estimated as the ratio between the area of the hexahedron of a prism and 1 mm 2 using the formula, N = 2 × 106/ d where d is the distance between the centers of the neighboring prisms (or diameter of the inner circle of the hexahedron).

are characteristic of gelocids of the genus Pseudomeryx and hypisodontids of the genus Hypisodus. In hypertragulids, of the genus Hypertragulus, the prisms are inclined to a greater extent relative to the occlusal surface. The slope increases in Nanotragulus, another member of the Hypertragulidae, a descendant of Hypertragulus. In addition, Nanotragulus is characterized by thicker and more dense enamel. It is undoubtedly more progressive than Hypertragulus in all the mentioned features of the enamel ultrastructure. (2) Radial banded ultrastructure. The prisms compose simple bands enclosed between parallel plates of interprismatic crystallites. The prisms are still almost perpendicular to the wear surface, as in the initial type observed in the Archaeomerycidae. A similar type of enamel ultrastructure of molars is characteristic of leptomerycids and some tragulids. Progressive changes of this type are associated with prism lengthening and enamel thickening. With reference to the enamel thickness, the Early Miocene Dorcatherium from Africa is at PALEONTOLOGICAL JOURNAL

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a lower evolutionary stage than the Early Oligocene Leptomeryx from North America that is characterized by a thicker dental enamel. Thus, the features of enamel structure together with other morphological data on early members of the genus Dorcatherium give additional evidence that the tragulid lineage originated earlier than the Leptomerycidae. (3) The prisms and interprismatic crystallites are arranged in relatively primitive and short HunterSchreger bands located some distance away from the enamel-dentin junction and crossing each other at a small angle. At the enamel-dentin junction, the prisms form lines confined to vertical plates of interprismatic crystallites. The lines curve only slightly. The same enamel structure is observed in some gelocids, in particular, in the genus Gobiomeryx (Pl. 6, fig. 2). This resembles the enamel structure of some Paleocene arctocyonids (Koenigswald et al., 1987) and higher ruminants (Pecora). 2000

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VISLOBOKOVA, DMITRIEVA (‡)

(b)

10 μm

10 μm

(c)

(d)

10 μm

10 μm

Fig. 2. Various types of enamel ultrastructure in early ruminants, occlusal surfaces: (a) radial chains (at the lower right, enamel-dentin junction is seen); (b) radial bands; and (c, d) decussate intersection of Hunter-Schreger bands; (a) Pseudomeryx gobiensis, PIN, no. 3935/585; (b) Leptomeryx sp., from AMNH collection; (c) Gobiomeryx dubius, PIN, no. 3935/587; and (d) Palaeohypsodontus asiaticus, PIN, no. 4567/1.

Enamel Ultrastructure in the Molars of Early Higher Ruminants The higher ruminants are distinguished from tragulines by thicker enamel and advanced ultrastructure, in particular, by well developed Hunter-Schreger bands crossing each other at almost right angles within a considerable area (Fig. 3). The intersections of these bands form a relatively complex decussate structure consisting of a wavy repetitive pattern (Schmelmuster). A combination of the apical inclination and curvature of

the lines gives a high degree of durability to the thickened enamel. This combination was indicated by Koenigswald et al. (1987) as a progressive character. In a subsequent study, these researchers showed that the Bovidae were characterized by a multilayered enamel consisting of the main layer of multiserial HSB underlain by a layer of nonserial HSB and covered by a layer of radial enamel, as in rodents of the genus Marmota (Koenigswald et al., 1992). This is true for relatively highly specialized bovids, in particular, for Gazella.

Explanation of Plate 6 Fig. 1. Hypertragulus calcaratus, AMNH, no. 6833; on the left, enamel-dentin junction. Fig. 2. Gobiomeryx dubius, PIN, no. 3935/587; on the right, arched enamel-dentin junction. Fig. 3. Palaeohypsodontus asiaticus, PIN, no. 4567/1; on the right, enamel-dentin junction. Fig. 4. Amphitragulus cf. quercyi, PIN, no. 3985/3; at the upper left, enamel-dentin junction. Fig. 5. Dremotherium cf. guthi, PIN, no. 3985/8. Fig. 6. Gobiocerus mongolicus, PIN, no. 532/8; enamel-dentin junction extends from the upper left to the lower right. Fig. 7. Hypertragulus calcaratus, AMNH, no. 6833. Fig. 8. Pseudomeryx gobiensis, PIN, no. 3935/585. Fig. 9. Dorcatherium sp., BMNH. Fig. 10. Pseudomeryx gobiensis, PIN, no. 3935/585. Fig. 11. Lophiomeryx chalaniati, PIN. Fig. 12. Lophiomeryx cf. angarae, PIN, no. 3935/589. Fig. 13. Eumeryx imbellis, PIN, no. 3935/583. Fig. 14. Dremotherium cf. guthi, PIN, no. 3985/6. Fig. 15. Gobiocerus mongolicus, PIN, no. 532/8. PALEONTOLOGICAL JOURNAL

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S247 Plate 6

30 μm

30 μm

(1)

30 μm

(2)

30 μm

(3)

30 μm

(4)

30 μm

(5)

3 μm

(6)

3 μm

(7)

3 μm

(8)

3 μm

10 μm

(10)

10 μm

(11)

3 μm

10 μm

(13) PALEONTOLOGICAL JOURNAL

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(15)

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VISLOBOKOVA, DMITRIEVA Middle Eocene

Late Eocene

Early Oligocene

Archaeomeryx

a

Pseudomeryx b

a

Leptomeryx

a

b

Gobiomeryx

a

Hupertragulus

a

b

b

b

Eumeryx

a

b

Palaeohypsodontus

b

‡

1

2

3

4

5

6

Fig. 3. The scheme of the main types of enamel ultrastructure in early ruminants and the age of their origin: (1) simple radial (arcadeshaped prisms); (2) simple radial (arcade-shaped and circular prisms); (3) radial chain; (4) radial band; (5) parallel arrangement of prisms; and (6) decussate arrangement of prisms; (a) prism shape on the enamel surface and (b) longitudinal section of enamel.

The enamel of primitive forms of higher ruminants remained relatively primitive, although it reached a substantial thickness even in Oligocene forms. Almost all higher ruminants are characterized by closed prisms of round or oval cross sections. Incomplete closing and preservation of an arcade shape by a small part of the prisms is recorded in the earliest members (Early Oligocene) of the families Cervidae (genus Eumeryx) and Bovidae (genus Palaeohypsodontus). Both genera demonstrate a gradual transformation of the arcade prism shape to a closed (circular) shape. In these genera, the prism density is higher than in the Archaeomerycidae and some Hypertraguloidea, but lower than those of many specialized tragulines. Regarding the sizes of enamel prisms, they are substantially advanced in comparison with archaeomerycids and surpass all tragulines in the extent to which the enamel is complicated. These features of enamel ultrastructure in early higher ruminants are not contrary to the hypothesis of the radiation of higher ruminants from the Archaeomerycidae proposed previously. Judging from the material examined in this study, the enamel structure of early cervids is more primitive than those of bovids. The early Cervidae vary in prism shape and in the extent to which interprismatic material is

structured. In the genus Eumeryx, the prisms are mainly circular or pear-shaped and do not form distinct chains (Fig. 1d; Pl. 6, fig. 13). In this genus and Amphitragulus, the intersection of Hunter-Schreger bands is at an extremely low stage of development, and bands cross each other at a small angle. The genus Dremotherium is characterized by oval prisms arranged in sinusoidal rows; within relatively large sites of enamel, the interprismatic material forms plates, and the intersection of the Hunter-Schreger bands is developed to a substantially greater extent than in the first two species (Pl. 6, fig. 5). In the genus Palaeohypsodontus, the prisms are arcade-shaped, either close to encircling or are almost completely closed. The prisms do not form chains, they cross each other and form an original decussate pattern (Fig. 2d; Pl. 6, fig. 3), as in all bovids. In the genus Gobiocerus, the prisms are irregularly oval, the interprismatic crystallites are arranged in plates. In the genera Palaeohypsodontus and Gobiocerus, the decussate structure prevails in the enamel, in contrast to that of tragulines of the genus Gobiomeryx. The radial structure remains within small sites at the base of enamel at the enamel-dentin junction (Pl. 6, fig. 6) and on the surface of enamel.

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CONCLUSION (1) The changes of enamel structure reflect a trend in the adaptatiogenesis. The enamel structure depends on the characteristics of consumed food and correlates with the level of evolutionary advantage of groups. The data on enamel ultrastructure together with other characteristics enable one to reveal the trends in the evolutionary processes and specify the phylogeny and taxonomy of individual groups. (2) A primitive enamel structure, in particular, the absence of Hunter-Schreger bands in early tragulines is probably associated with an extremely low specialization to herbivory. This structure should be regarded as a plesiomorphic character inherited from a remote ancestor. (3) The type of enamel observed in the Archaeomerycidae, is probably similar to the initial state giving rise to complicated types of enamel characteristics of other ruminant groups. The enamel structure corroborates the position of the Archaeomerycidae at the base of the radiation of a number of progressive traguline groups (in particular, leptomerycids and gelocids) and higher ruminants. Regarding the enamel structure (and many other characteristics), archaeomerycids are the least specialized tragulines. The trends in the evolutionary transformation of the enamel ultrastructure in tragulines and early ruminants are the same as the main trends in the evolution of these groups and correspond to the relationships revealed on the basis of morphological features of the skull and postcranial skeleton. (4) The enamel structure of higher ruminants is substantially complicated in comparison with those of the Tragulina. It corresponds to a higher level of adaptation to herbivory and probably belongs to the complex of features reflecting an essentially new and progressive level of organization of these animals. This level of

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organization is associated with a great advance in adaptatiogenesis resulting in the emergence of true ruminants. ACKNOWLEDGMENTS We are grateful to R.H. Tedford and J.J. Hooker for providing us with the specimens from the collections in their care, to workers of the Laboratory of Electron Microscopy of PIN, and to V.R. Alifanov for help in the preparation of the figures. This study was supported by the Russian Foundation for Basic Research, projects nos. 98-04-49089 and 99-04-48636. REFERENCES Carlson, S. and Krause, D., Enamel Ultrastructure of Multituberculate Mammals: An Investigation of Variability, Contrib. Mus. Paleontol. Univ. Michigan, 1985, vol. 27, no. 1, pp. 1–50. Koenigswald, W. von, Rensberger, J.M., and Pretzschner, H.U., Changes in the Tooth Enamel of Early Paleocene Mammals Allowing Increased Diet Diversity, Nature, 1987, vol. 328, no. 6126, pp. 150–152. Koenigswald, W. von, Martin, Th., and Pretzschner, H.U., Phylogenetic Interpretation of Enamel Structure in Mammalian Teeth: Possibilities and Problems, in Mammal Phylogeny: Placentals, New York: Springer Verlag, 1992, pp. 303– 314. Vislobokova, I., A New Representative of the Hypertraguloidea (Tragulina, Ruminantia) from the Khoer-Dzan Locality in Mongolia, with Remarks on the Relationships of the Hypertragulidae, Am. Mus. Novit., 1998, no. 3225, pp. 1–24. Vislobokova, I.A. and Trofimov, B.A., The Family Archaeomerycidae (Tragulina): Classification and Role in the Evolution of Ruminants, Paleontol. Zh., 2000, no. 4, pp. 455–461.

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