The Effect of Wear on the Cheek Teeth and Associated Dental Tissues of the Lizard Urornastix aegyptius (Agamidae) GAYLORD S. THROCKMORTON Department of Cell Biology, The University of Texas, Health Science Center at Dallas, Dallas. Texas 75235
ABSTRACT Serial coronal sections of the teeth and their surrounding tissues in the agamid lizard, Urornastix aegyptius, were examined with the light microscope in order to determine how these structures change as the teeth wear. Because new teeth are added only a t the posterior end of the tooth row and older teeth are not replaced, the series of sections included the youngest as well as the oldest teeth. Two types of changes occur as the teeth become older: bone under the teeth changes from cancellous to compact, and the pulp chamber of the tooth is obliterated. Although the labial surface of the dentary lacks a periosteal covering and some of the bone lacks any covering a t all, it remains functional throughout the life of the animal. Living reptiles exhibit a variety of methods ject to wear throughout the life of the animal. Several additional features characteristic of attaching the teeth to the jaw bones (Edmund, '69). In crocodilians, the teeth are in of acrodont teeth can be illustrated by exsockets formed in distinct alveolar bone and amining the lower jaw of Urornastix aegyptius, supported by a periodontal membrane (theco- a large herbivorous agamid (fig. 1). Posterior dont implantation). In squamates, the dentine to the single large incisiform tooth is a row of of t h e tooth is fused to t h e bone of t h e jaws via cheek teeth of increasing size. In Urornastix a special bone of attachment (Tomes, 1874- the incisor teeth are not replaced (Cooper and 1875). This fusion is termed ankylosis. The Poole, '73). As the animal grows, new teeth are tooth may be in a socket (subthecodont im- added a t the posterior end of the tooth row and plantation); the lingual wall of the socket the more anterior, older teeth are gradually may be reduced leaving the base of the tooth worn away. In Uromastix, the teeth must ocexposed (pleurodont implantation); or the clude in order to shear plant material and, tooth may be attached directly to the occlusal therefore, wear against each other to mainsurface of the jaws, and the tooth lacks a tain a cutting edge (Cooper and Poole, '73; root or base (acrodont implantation) (Ed- Robinson, '76; Throckmorton, '76). Wear facets develop on the labial surface of the mund,'69). Recently there has been increased interest lower teeth and on the lingual surface of the in the biology of acrodont dentitions (Cooper upper teeth. On the lower jaw, these wear et al., '70; Cooper and Poole, '73; Robinson, facets extend down into the dentary 2-3 mm '76). Acrodont implantation occurs in two re- below the bases of the teeth (Cooper and Poole, lated families of lizards, the Agamidae and '73). As the teeth age, the wear facet becomes Chameleontidae, and in Sphenodon puncta- more extensive, eventually covering the enturn (Rhynchocephalia). The dentition of tire occlusal surface of the tooth. The anterior agamid lizards has been most extensively teeth of old individuals may be completely studied (Cooper et al., '70; Cooper and Poole, worn away leaving the jaw bone to perform '73). In agamids the anterior incisiform teeth tooth function (Cooper et al., '70; Cooper and are pleurodont while the cheek teeth are acro- Poole, '73). Acrodont dentitions also are characterized dont. Acrodont teeth are of interest because, unlike the condition in a majority of reptiles, by a lack of soft tissue covering the teeth a t acrodont teeth are not replaced, and are sub- their junction with the jaw bone. This is parJ. MORPH. (1979) 160; 195-208.
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GAYLORD S. THROCKMORTON
ticularly noticeable on t h e labial aspect of t h e lower jaw when the lips a r e retracted (fig. 1 ) . Apparently t h e bone lacks any covering for a considerable space between the teeth and attachment of t h e lips. Whereas this “bare area” characterizes all other species of agamids examined (Amphibolurus barbatus, Calotes spp., and Liolepis belliana) i t is absent in nonagamids examined (Basiliscus uitatus, Crotaphytus collaris, Iguana iguana, Zguanidae; Cnemidophorus lemniscatus, Cnemidophorus sexlineatus, Teiidae; Lacerta muralis, Lacertidae). In the non-agamid species, a thick layer of mucous membrane surrounds each tooth and is attached to t h e jaw bone and the lips. In the agamid species, t h e mucous membrane does not extend between adjacent teeth and because i t is attached only to t h e lips i t is pulled away from t h e teeth when t h e lips are retracted. Another feature of t h e teeth of Uromastix is a bony core in the pulp chamber (fig. 2). This bony core appears in radiographs of t h e upper and lower cheek teeth of all four specimens of Uromastix examined but not in other species of agamids (Amphibolurus barbatus, Calotes spp., Liolepis belliana). In order to remain functional, there are two problems which acrodont teeth must overcome: (1) the teeth must be resistant to wear throughout a relatively long period of use; and (2) if they are to remain in occlusion the teeth must somehow alter their position as they wear and as t h e jaws grow. In most reptiles continuous replacement allows t h e dentition to grow with t h e jaws (Osborn, ’741, and because t h e teeth are regularly replaced they a r e subject to relatively little wear. The purpose of this study was to determine how t h e t e e t h a n d t h e i r surrounding tissues a r e modified as t h e teeth wear in Uromastix aegyptius. MATERIALS AND METHODS
An adult specimen of Uromastix aegyptius (specimen No. R-10) was perfused with normal saline followed by 10% formalin. The lower jaws were removed and immersed in 10%formalin for several weeks. The jaws were decalcified in formic acid and then cut into seven blocks: one contained t h e symphysis, two were cut from each tooth row, and a pair contained t h e mandibular joints. Each block was embedded in 14% celloidin and coronal sections were made at 12-15 p m . From each block every fifth section was stained with
hematoxylin and eosin. Thus, a series of sections was formed from t h e youngest tooth posteriorly to t h e oldest tooth anteriorly. Some of t h e other sections were stained with Mallory’s stain (Pantin and Picro Mallory methods), Gomori silver stain, Van Gieson stain, and PAS to clarify t h e nature of specific structures. The sections were examined with the light microscope. In t h e present study, it was more convenient to number t h e teeth from t h e posterior end of t h e tooth row. Excessive wear of t h e anterior teeth made i t difficult to determine the total number of teeth in t h e jaws. The specimen used in this study apparently had 12 teeth in each quadrant, 1 incisiform and 11 cheek teeth. RESULTS
There were two types of major changes observed in progressively older teeth. First, there was a gradual change from cancellous bone supporting t h e posterior-most tooth to completely compact bone supporting the anterior teeth. Secondly, there was gradual obliteration of t h e pulp chamber of the tooth by growth of secondary dentine.
Growth of bone under the teeth The posterior-most tooth in the tooth row, tooth number 1,is supported a t its base entirely by a layer of cancellous bone (fig. 3). The layer is relatively thin and blood vessels run through t h e interspaces. The interspaces open onto t h e lingual side of t h e jaw bone. In the more anterior teeth, bone gradually has grown into the cancellous spaces. This bone growth proceeds from t h e labial to t h e lingual side so t h a t the labial half of tooth number 3 (fig. 4)is supported by compact bone and t h e lingual half is supported by cancellous bone. By tooth number 6 (fig. 5 ) t h e process is complete, and t h e supporting tissue is entirely compact coarse-cancellous bone (Enlow, ’69). This corresponds to t h e bone of attachment of Tomes (1874-1875) and can be distinguished from the bone of t h e dentary by its complex pattern of resting lines which truncate t h e more laminar resting lines of t h e dentary. All of t h e more anterior teeth are supported by this type of compact bone. This process of bone compaction may be simply t h e result of t h e older bone h a v i n g more t i m e for bone deposition. Whether increasing t h e amount of compact bone serves a functional purpose is uncertain, especially because t h e posterior teeth are
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EFFECT OF WEAR ON ACRODONT TEETH
functional while supported by cancellous bone. Obliteration of the pulp chamber One unusual feature of the cheek teeth in Uromastix is the presence of a bony core within the pulp chamber. Only in tooth number 1 (fig. 3) was the bony core still developing. When completed, the bony core typically appears in coronal section as a roughly triangular process of laminar bone. However, there may be considerable variation in the shape of the core from section to section. For example, in a section near the posterior third of tooth number 2, the bony core appears dome-like, whereas in a section near the middle of the tooth, the core consists of two distinct peaks. Several sections show a channel through the bony core (fig. 6) which allows the entrance of blood vessels into the pulp chamber. The bony core is found in all of the teeth but apparently stops growing shortly after the tooth is ankylosed to the jaw. It does not seem to be smaller in the younger teeth, nor is there a layer of osteoblasts found on the outer surface of the bony core, which would indicate that the core is growing as the teeth wear. The pulp chambers of the more posterior teeth are cone-shaped with the apex of the cone a t the occlusal end of the tooth. As tooth wear occurs, primarily on the labial side of the lower teeth, the dentine becomes thinner. Presumably, this thinning stimulates the odontoblasts to begin formation of secondary dentine. By tooth number 6 (fig. 7), secondary dentine begins to develop a t the apex of the pulp chamber. The secondary dentine progressively fills the pulp chamber in the more anterior teeth. By tooth number 7 (fig. 81, the secondary dentine is in contact with the bony core. This contact increases (fig. 9) until by tooth number 10 (fig. 10) the pulp chamber is completely obliterated. Wear is primarily on the labial side of the tooth. In tooth number 10 (fig. 101, the dentine on the labial side is nearly worn away, while on the lingual side, the dentine is still substantially intact. Also, in tooth number 10, the enamel and dentine have been worn away sufficiently to expose the secondary dentine which is now being worn. Finally, in tooth number 11 (fig. ll),the dentine is entirely gone on the labial side, the cap of secondary dentine has been worn away, and the bony core is now subject to wear. At the extreme anterior end of the tooth row
sections occur in which no tooth tissue is found (fig. 12).This part of the jaw is triangular in coronal section and may play some role in shearing food. This bony structure comes to make up more and more of the functional surface of the jaw bone as the dentition wears. Relationship of soft tissues to the teeth A normal soft tissue covering is seen posterior to the tooth row (fig. 13). Here the bone is covered by a layer of periosteum which in turn is covered by a layer of epithelium. However, along the labial side of the tooth row these soft tissues rapidly retreat inferiorly and are found adjacent only to tooth number 1. In a section near the anterior edge of tooth number 1 (fig. 14) the soft tissue covering already is incomplete a t the base of the tooth. The two layers of soft tissue are found a t the line of a t tachment of the lips to the jaw bone, but above this line, they become progressively thinner until they disappear. First, the periosteal layer thins superiorly until the epithelium is in contact with the bone. The epithelial layer continues superiorly, but it also gradually thins and disappears. Superior to the epithelium is an acellular layer of uncertain composition (fig. 15). This layer covers the rest of the labial surface of the jaw bone except those areas which have wear facets formed by the upper teeth. The acellular layer apparently helps maintain the viability of the bone. Directly beneath this layer, the lacunae contain visible cell nuclei. Where there are wear facets (fig. 161, the bone is devoid of any covering. The lacunae directly beneath this surface are empty, but deeper bone remains viable. Bone which lacks any soft tissue covering also occurs a t the extreme anterior end of the tooth row (fig. 12). DISCUSSION
In organisms in which the teeth are not continuously replaced, mechanisms would be expected which increase the functional life of the individual teeth. In Uromastix there are three such mechanisms. First, the enamel and dentine layers are relatively thickened, thus the tooth is relatively more massive than those of other lizards and in a t least one species, Uromastix hardwickii, the enamel has a prismatic structure (Cooper and Poole, '73). It is not known whether this structural difference increases resistance to wear. Secondly, the growth of secondary dentine in the pulp chamber increases the amount of time in
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which a functional dentine layer is available on the side of the tooth receiving the greatest amount of wear. Eventually, the secondary dentine obliterates the pulp chamber, but in doing so, the functional lifespan of the tooth is extended greatly. Thirdly, the presence of a bony core in the pulp chamber effectively decreases the volume of the pulp, thus facilitating eventual obliteration of the pulp chamber. These modifications may be especially important in Uromastix because of its herbivorous diet. Tooth wear is increased because of the fibrous nature of the plant material and because the teeth wear against each other to maintain a sharp shearing edge (Cooper and Poole, ' 7 3 ) . The presence of a bony core may be unique to Uromastix. Each of four specimens of Uromastix examined radiographically had bony cores in the more posterior teeth. Bony cores were not found in Amphibolurus barbatus, Calotes spp. or Leiolepis belliana. None of the previous histologic studies of acrodont teeth (Carlssen, 1896; Cooper et al., '70; Cooper and Poole, ' 7 3 ; Harrison, '01; Osawa, 1897; Rose, 18931, mentions bone in the pulp chamber. Bone or osteodentine has been reported in the pulp chambers of whales and sloths (Tomes, '14). Bone also can appear in the pulp chamber of mammalian teeth after trauma and reimplantation (Anderson et al., '68; Kaqueler and Massler, '69). But this bone is symptomatic of a pathological condition which leads to the eventual ankylosis of the tooth. The mechanism and functional reasons for bone appearing in the pulp chamber in mammals are not clearly understood. In addition to increasing the functional life of the teeth, the jaw bone is able to perform a shearing function once the teeth are completely worn away. Cooper and Poole ('73) described the development of a process of the premaxilla which replaces the upper incisors in Uromastix. This incisiform process is used to crop plant material (Throckmorton, '76). Similarly, the jaw bone is able to assume the function of the cheek teeth. I have observed feeding in one specimen of Uromastix in which nearly the entire dentition had been worn away. This specimen was able to feed on the same food as specimens with complete dentitions, although i t did require more chewing and twisting to bite through the food. Nonetheless, the jaw bone was able to shear through the food adequately.
The ability of jaw bone to perform tooth function is surprising in relation to some of our present concepts of bone biology. In the dental literature, it often is stated that bone must be protected from direct compressive forces (Orban, '66; Noble, '69; Shpiro, ' 7 5 ) . While a n evaluation of this concept is beyond the scope of the present paper, it is clear that in reptiles with acrodont dentitions, the jaw bones can survive when subjected to direct biting pressures. The ability of portions of the jaw bone to survive without a periosteal covering is unique to reptiles with acrodont dentitions (Donald H. Enlow, personal communication). Apparently t h e bone remains viable when covered by epithelium or the acellular layer. In areas deep to the wear facets, however, the lacunae are empty. The extent of these empty lacunae seems to be limited to particular areas bounded by the resting lines in the bone. The nature of the acellular layer remains uncertain. Although it may be a thin layer of acellular bone such as described by Harrison ('01) and Tomes ('14), in my preparations, it stains differently from adjacent bone. In a Van Gieson stain, this layer is the same yellow color as the epithelium, rather than the red of the bone. Permanently implanted dentitions must have some mechanism which allows repositioning of the teeth as the jaws grow, if precise occlusion is to be maintained. The presence of a peridontal ligament in mammals allows the teeth to move horizontally as the jaws grow to move vertically as they wear (Orban, '66; Noble, '69). This problem is more acute in reptiles than in mammals where the jaws may increase in size by as much as a factor of ten after implantation of the first set of teeth (Edmund, '62) compared to 15%to 20%increase in mammals (Crompton and Parker, '78). Although maintenance of occulusion is not important in most reptiles, it is essential to the "precision shear" mechanism in Uromastix (Robinson, '76). On the basis of growth patterns of the maxilla, she suggests remodeling of the maxilla to maintain the upper teeth in proper alignment. A similar mechanism may occur in the dentary; however, most of the remodeling seen in this study was associated with replacing of cancellous bone by compact bone (figs. 3-51 and the narrowing of channels for blood vessels (figs. 15, 16). Remodeling on the lateral side of the jaws also would seem to be prohibited because the labial
EFFECT OF WEAR ON ACRODONT TEETH
surface of the dentary and tooth-bearing parts of the maxilla are not covered by periosteum. Long term growth studies using bone markers are needed to understand the full extent of the remodeling. In reptiles with acrodont dentitions the continuous replacement of the teeth has been suppressed. Without replacement the teeth are subject to wear throughout the life of the animal and they must adjust their position as the jaws grow. In Uromastix the structure of the enamel has been modified and its thickness increased; as the teeth wear the bone supporting the teeth changes from cancellous to compact bone, the pulp chamber is obliterated, and finally the bone of the jaws is capable of shearing food. These changes ensure a functional shearing mechanism throughout the lifespan of the animal. ACKNOWLEDGMENTS
Special thanks are due Mr. K. V. Katele and Doctor T. C. Lakars for their help with this project. Mr. Katele and his staff sectioned the material and did the H & E staining. Doctor Lakars helped and advised on the other stains. Doctor Harry Hoogstraal, Doctor Jos Schall, and Doctor William Neaves supplied lizard specimens examined in this study. LITERATURE CITED Anderson, A. W., Y. Sharov and M. Massler 1968 Reparative dentine formation and pulp morphology. Oral Surg., 26: 837-847. Carlssen, A. 1896 Ueber den Zahnartz bei Agarna colonorurn. Anat. Anz., 1 1 : 758-766. Cooper, J. S., D. F. G. Poole and R. Lawson 1970 The dentition of agamid lizards with special reference to tooth replacement. J. Zool. Lond., 162; 85-98. Cooper, 3. S., and D. F. G. Poole 1973 The dentition and den-
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tal tissues of t h e agamid lizard Urornastix. J. Zool. Lond., 169: 85-100. Crompton, A. W., and P. Parker 1978 Evolution of the mammalian masticatory a p p a r a t u s . Am. Sci., 66: 192-201. Edmund, A. G. 1962 Sequence and fate of tooth replacement in the croccdilia. Contrib. Roy Ont. Mus., Life Sci. Div., 56: 1-41. 1969 Dentition. In: Biology of the Reptilia. Vol. I. C. Gans, A. Bellairs and T. Parsons, eds. Academic Press, London, New York, pp. 117-200. Enlow, D. H. 1969 The bone of reptiles. In: Biology of the Reptilia. Vol. I. C. Gans, A. Bellairs and T. Parsons, eds. Academic Press, London, New York, pp. 45-80. Harrison, H. S. 1901 The development and succession of teeth in Hatteria punctata. Quart. J. Microsc. Sci., 44: 161-219. Kaqueler, J. C., and M. Massler 1969 Healing following tooth replantation. J. Dent. Child., 36: 303-314. Noble, H. W. 1969 The evolution of the mammalian periodontium. In: Biology of the Periodontium. A. H. Melcher and W. H. Bowen, eds. Academic Press, New York, pp. 1-26. Orban, B. 1966 Oral Histology and Embryology. Sixth ed. H. Sicher, ed. Mosby, St. Louis, 176-196. Osawa, G. 1897 Beitrage zur Lehre von Eingeweiden der Hatteria punctata. Arch. Mikros. Anat., 49: 113-226. Osborn, J. W. 1974 On the control of tooth replacement in reptiles and its relationship to growth. J. Theor. Biol., 46: 509-527. Robinson, P. L. 1976 How Sphenodon and Urornastyx grow their teeth and use them. In: Morphology and Biology of Reptiles. A. d’A. Bellairs and C. B. Cox, eds. Linnean Society Symposium, Series No. 3. Academic Press, London, pp. 43-64. Rose, C. 1893 Ueber die Zahnentwicklung von Chamaeleon. Anat. Anz., 8: 566-577. Shpiro, P. 1975 The shape of implants in masticatory force distribution. J. Prosthet. Dent., 33: 567-570. Throckmorton, G. S. 1976 Oral food processing in two herbivorous lizards Iguana iguana (Iguanidae) and Urornastir aegyptius (Agamidae). J. Morph., 148: 363-390. Tomes, C. S. 1874-1875 Studies upon the attachment of teeth. Trans. Odont. SOC.Great Britain, 7: 41-66. 1914 A Manual of Dental Anatomy, Human and Comparative. Seventh ed. H. W. Marett-Tims and H. Smith, eds. P. Blakiston’s Son & Co., Philadelphia.
N 0 0
X
5.
dentary; a, cancellous bone of attachment; c, compact bone of attachment. Arrow marks resting line between the compact bone of the dentary and the bone of attachment. H & E stain. X 150.
4 Coronal section through tooth number 3 near middle of tooth. D, dentine; b, bony core; d, compact bone of
3 Coronal section through tooth number 1 near middle of tooth. D, dentine; b, bony core; p, pulp chamber; d, compact bone of dentary; a, cancellous bone of attachment. Labial is to the right. Arrow marks the resting line between t h e compact bone of the dentary and the bone of attachment. H & E stain. X 115.
pulp chamber.
2 Radiograph of right lower jaw of Urornastix aegyptius (specimen No. R-13). Arrow points to bony core in
covered by connective tissue, C, which joins the lip to t h e lower jaw. The anterior-most tooth is an incisor; the rest are cheek teeth. Arrow points to wear facet in dentary. X 3.
1 Right lower jaw of Urornastix aegyptius, (specimen No. R-12) labial view. The lip, L, has been reflected away from the jaw. The dentition is adjacent to apparently bare bone, B. More inferiorly the bone is
EXPLANATION OF FIGURES
PLATE 1
EFFECT OF WEAR ON ACRODONT TEETH Gaylord S. Throckmorton
PLATE 1
PLATE 2 EXPLANATION OF FIGURES
5 Coronal section through tooth number 6 near posterior one-third of tooth. D, den-
tine; b, bony core; p, pulp chamber; a, compact course-cancellous bone of attachment. Labial is to the right. H & E stain. X 150. 6 Coronal section through tooth number 2 near posterior one-third of tooth. D, den-
tine; b, bony core; p, pulp chamber; a, bone of attachment. Arrow points to blood vessel. Labial is to t h e right. H & E stain. X 115. 7 Coronal section through tooth number 6 near posterior one-fourth of tooth. D, dentine; b, bony core; p, pulp chamber, arrow marks position of secondary dentine a t apex of pulp chamber. Labial is to t h e right. H & E stain. X 285. 8 Coronal section through tooth number 7 near anterior one-third of tooth. D, dentine; b, bony core; p, pulp chamber: s, secondary dentine. Labial is to the right. H & E stain. X 285.
202
EFFECT OF WEAR ON ACRODONT TEETH Gaylord S. Throckmorton
PLATE 2
203
PLATE 3 EXPLANATION OF FIGURES
9 Coronal section through tooth number 8 near middle of tooth. D, dentine; b, bony core; p, pulp chamber; s , secondary dentine. Labial is to t h e right. H & E stain. X 285. 10 Coronal section through tooth number 10, near middle of tooth. D, dentine; b, bony core; s, secondary dentine. Labial is to the right. H & E stain. X 365.
11 Coronal section through tooth number 11,near middle of tooth. D, dentine; b, bony core; s , secondary dentine; a, bone of attachment. The space between the bony core and the secondary dentine is an artifact. Labial is to the right. H & E stain. X 285. 12 Coronal section through jaw bone between teeth 10 and 11. Labial is to the right. H & E stain. X 285.
204
ESFECT OF WEAR ON ACRODONT TEETH Caylord S. Throckmorton
PLATE 3
205
PLATE 4 EXPLANATION OF FIGURES
13 Coronal section through lower jaw posterior to the tooth row. e, epithelium; d, compact bone of dentary. Arrow points to layer of periosteum. Labial is to the right. H & E stain. X 285. 14 Coronal section through jaw a t level of anterior one-third of tooth number 1. d, compact bone of dentary. Arrow marks layer of epithelium. Labial is to t h e right. H & E stain. X 365. 15 Coronal section through jaw bone a t level of tooth number 6. Arrow points to acellular layer. Labial is to the right. H & E stain. X 365. 16 Coronal section through jaw bone a t level of tooth number 8 showing wear facet in bone of dentary. Arrows point to limits of wear facet. labial is to t h e right. H & E stain. X 285.
EFFECT OF WEAR ON ACRODONT TEETH Gaylord S. Throckmorton
PLATE 4
207
ABSTRACT Serial coronal sections of the teeth and their surrounding tissues in the agamid lizard, Urornastix aegyptius, were examined with the light microscope in order to determine how these structures change as the teeth wear. Because new teeth are added only a t the posterior end of the tooth row and older teeth are not replaced, the series of sections included the youngest as well as the oldest teeth. Two types of changes occur as the teeth become older: bone under the teeth changes from cancellous to compact, and the pulp chamber of the tooth is obliterated. Although the labial surface of the dentary lacks a periosteal covering and some of the bone lacks any covering a t all, it remains functional throughout the life of the animal. Living reptiles exhibit a variety of methods ject to wear throughout the life of the animal. Several additional features characteristic of attaching the teeth to the jaw bones (Edmund, '69). In crocodilians, the teeth are in of acrodont teeth can be illustrated by exsockets formed in distinct alveolar bone and amining the lower jaw of Urornastix aegyptius, supported by a periodontal membrane (theco- a large herbivorous agamid (fig. 1). Posterior dont implantation). In squamates, the dentine to the single large incisiform tooth is a row of of t h e tooth is fused to t h e bone of t h e jaws via cheek teeth of increasing size. In Urornastix a special bone of attachment (Tomes, 1874- the incisor teeth are not replaced (Cooper and 1875). This fusion is termed ankylosis. The Poole, '73). As the animal grows, new teeth are tooth may be in a socket (subthecodont im- added a t the posterior end of the tooth row and plantation); the lingual wall of the socket the more anterior, older teeth are gradually may be reduced leaving the base of the tooth worn away. In Uromastix, the teeth must ocexposed (pleurodont implantation); or the clude in order to shear plant material and, tooth may be attached directly to the occlusal therefore, wear against each other to mainsurface of the jaws, and the tooth lacks a tain a cutting edge (Cooper and Poole, '73; root or base (acrodont implantation) (Ed- Robinson, '76; Throckmorton, '76). Wear facets develop on the labial surface of the mund,'69). Recently there has been increased interest lower teeth and on the lingual surface of the in the biology of acrodont dentitions (Cooper upper teeth. On the lower jaw, these wear et al., '70; Cooper and Poole, '73; Robinson, facets extend down into the dentary 2-3 mm '76). Acrodont implantation occurs in two re- below the bases of the teeth (Cooper and Poole, lated families of lizards, the Agamidae and '73). As the teeth age, the wear facet becomes Chameleontidae, and in Sphenodon puncta- more extensive, eventually covering the enturn (Rhynchocephalia). The dentition of tire occlusal surface of the tooth. The anterior agamid lizards has been most extensively teeth of old individuals may be completely studied (Cooper et al., '70; Cooper and Poole, worn away leaving the jaw bone to perform '73). In agamids the anterior incisiform teeth tooth function (Cooper et al., '70; Cooper and are pleurodont while the cheek teeth are acro- Poole, '73). Acrodont dentitions also are characterized dont. Acrodont teeth are of interest because, unlike the condition in a majority of reptiles, by a lack of soft tissue covering the teeth a t acrodont teeth are not replaced, and are sub- their junction with the jaw bone. This is parJ. MORPH. (1979) 160; 195-208.
195
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GAYLORD S. THROCKMORTON
ticularly noticeable on t h e labial aspect of t h e lower jaw when the lips a r e retracted (fig. 1 ) . Apparently t h e bone lacks any covering for a considerable space between the teeth and attachment of t h e lips. Whereas this “bare area” characterizes all other species of agamids examined (Amphibolurus barbatus, Calotes spp., and Liolepis belliana) i t is absent in nonagamids examined (Basiliscus uitatus, Crotaphytus collaris, Iguana iguana, Zguanidae; Cnemidophorus lemniscatus, Cnemidophorus sexlineatus, Teiidae; Lacerta muralis, Lacertidae). In the non-agamid species, a thick layer of mucous membrane surrounds each tooth and is attached to t h e jaw bone and the lips. In the agamid species, t h e mucous membrane does not extend between adjacent teeth and because i t is attached only to t h e lips i t is pulled away from t h e teeth when t h e lips are retracted. Another feature of t h e teeth of Uromastix is a bony core in the pulp chamber (fig. 2). This bony core appears in radiographs of t h e upper and lower cheek teeth of all four specimens of Uromastix examined but not in other species of agamids (Amphibolurus barbatus, Calotes spp., Liolepis belliana). In order to remain functional, there are two problems which acrodont teeth must overcome: (1) the teeth must be resistant to wear throughout a relatively long period of use; and (2) if they are to remain in occlusion the teeth must somehow alter their position as they wear and as t h e jaws grow. In most reptiles continuous replacement allows t h e dentition to grow with t h e jaws (Osborn, ’741, and because t h e teeth are regularly replaced they a r e subject to relatively little wear. The purpose of this study was to determine how t h e t e e t h a n d t h e i r surrounding tissues a r e modified as t h e teeth wear in Uromastix aegyptius. MATERIALS AND METHODS
An adult specimen of Uromastix aegyptius (specimen No. R-10) was perfused with normal saline followed by 10% formalin. The lower jaws were removed and immersed in 10%formalin for several weeks. The jaws were decalcified in formic acid and then cut into seven blocks: one contained t h e symphysis, two were cut from each tooth row, and a pair contained t h e mandibular joints. Each block was embedded in 14% celloidin and coronal sections were made at 12-15 p m . From each block every fifth section was stained with
hematoxylin and eosin. Thus, a series of sections was formed from t h e youngest tooth posteriorly to t h e oldest tooth anteriorly. Some of t h e other sections were stained with Mallory’s stain (Pantin and Picro Mallory methods), Gomori silver stain, Van Gieson stain, and PAS to clarify t h e nature of specific structures. The sections were examined with the light microscope. In t h e present study, it was more convenient to number t h e teeth from t h e posterior end of t h e tooth row. Excessive wear of t h e anterior teeth made i t difficult to determine the total number of teeth in t h e jaws. The specimen used in this study apparently had 12 teeth in each quadrant, 1 incisiform and 11 cheek teeth. RESULTS
There were two types of major changes observed in progressively older teeth. First, there was a gradual change from cancellous bone supporting t h e posterior-most tooth to completely compact bone supporting the anterior teeth. Secondly, there was gradual obliteration of t h e pulp chamber of the tooth by growth of secondary dentine.
Growth of bone under the teeth The posterior-most tooth in the tooth row, tooth number 1,is supported a t its base entirely by a layer of cancellous bone (fig. 3). The layer is relatively thin and blood vessels run through t h e interspaces. The interspaces open onto t h e lingual side of t h e jaw bone. In the more anterior teeth, bone gradually has grown into the cancellous spaces. This bone growth proceeds from t h e labial to t h e lingual side so t h a t the labial half of tooth number 3 (fig. 4)is supported by compact bone and t h e lingual half is supported by cancellous bone. By tooth number 6 (fig. 5 ) t h e process is complete, and t h e supporting tissue is entirely compact coarse-cancellous bone (Enlow, ’69). This corresponds to t h e bone of attachment of Tomes (1874-1875) and can be distinguished from the bone of t h e dentary by its complex pattern of resting lines which truncate t h e more laminar resting lines of t h e dentary. All of t h e more anterior teeth are supported by this type of compact bone. This process of bone compaction may be simply t h e result of t h e older bone h a v i n g more t i m e for bone deposition. Whether increasing t h e amount of compact bone serves a functional purpose is uncertain, especially because t h e posterior teeth are
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EFFECT OF WEAR ON ACRODONT TEETH
functional while supported by cancellous bone. Obliteration of the pulp chamber One unusual feature of the cheek teeth in Uromastix is the presence of a bony core within the pulp chamber. Only in tooth number 1 (fig. 3) was the bony core still developing. When completed, the bony core typically appears in coronal section as a roughly triangular process of laminar bone. However, there may be considerable variation in the shape of the core from section to section. For example, in a section near the posterior third of tooth number 2, the bony core appears dome-like, whereas in a section near the middle of the tooth, the core consists of two distinct peaks. Several sections show a channel through the bony core (fig. 6) which allows the entrance of blood vessels into the pulp chamber. The bony core is found in all of the teeth but apparently stops growing shortly after the tooth is ankylosed to the jaw. It does not seem to be smaller in the younger teeth, nor is there a layer of osteoblasts found on the outer surface of the bony core, which would indicate that the core is growing as the teeth wear. The pulp chambers of the more posterior teeth are cone-shaped with the apex of the cone a t the occlusal end of the tooth. As tooth wear occurs, primarily on the labial side of the lower teeth, the dentine becomes thinner. Presumably, this thinning stimulates the odontoblasts to begin formation of secondary dentine. By tooth number 6 (fig. 7), secondary dentine begins to develop a t the apex of the pulp chamber. The secondary dentine progressively fills the pulp chamber in the more anterior teeth. By tooth number 7 (fig. 81, the secondary dentine is in contact with the bony core. This contact increases (fig. 9) until by tooth number 10 (fig. 10) the pulp chamber is completely obliterated. Wear is primarily on the labial side of the tooth. In tooth number 10 (fig. 101, the dentine on the labial side is nearly worn away, while on the lingual side, the dentine is still substantially intact. Also, in tooth number 10, the enamel and dentine have been worn away sufficiently to expose the secondary dentine which is now being worn. Finally, in tooth number 11 (fig. ll),the dentine is entirely gone on the labial side, the cap of secondary dentine has been worn away, and the bony core is now subject to wear. At the extreme anterior end of the tooth row
sections occur in which no tooth tissue is found (fig. 12).This part of the jaw is triangular in coronal section and may play some role in shearing food. This bony structure comes to make up more and more of the functional surface of the jaw bone as the dentition wears. Relationship of soft tissues to the teeth A normal soft tissue covering is seen posterior to the tooth row (fig. 13). Here the bone is covered by a layer of periosteum which in turn is covered by a layer of epithelium. However, along the labial side of the tooth row these soft tissues rapidly retreat inferiorly and are found adjacent only to tooth number 1. In a section near the anterior edge of tooth number 1 (fig. 14) the soft tissue covering already is incomplete a t the base of the tooth. The two layers of soft tissue are found a t the line of a t tachment of the lips to the jaw bone, but above this line, they become progressively thinner until they disappear. First, the periosteal layer thins superiorly until the epithelium is in contact with the bone. The epithelial layer continues superiorly, but it also gradually thins and disappears. Superior to the epithelium is an acellular layer of uncertain composition (fig. 15). This layer covers the rest of the labial surface of the jaw bone except those areas which have wear facets formed by the upper teeth. The acellular layer apparently helps maintain the viability of the bone. Directly beneath this layer, the lacunae contain visible cell nuclei. Where there are wear facets (fig. 161, the bone is devoid of any covering. The lacunae directly beneath this surface are empty, but deeper bone remains viable. Bone which lacks any soft tissue covering also occurs a t the extreme anterior end of the tooth row (fig. 12). DISCUSSION
In organisms in which the teeth are not continuously replaced, mechanisms would be expected which increase the functional life of the individual teeth. In Uromastix there are three such mechanisms. First, the enamel and dentine layers are relatively thickened, thus the tooth is relatively more massive than those of other lizards and in a t least one species, Uromastix hardwickii, the enamel has a prismatic structure (Cooper and Poole, '73). It is not known whether this structural difference increases resistance to wear. Secondly, the growth of secondary dentine in the pulp chamber increases the amount of time in
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GAYLORD S . THROCKMORTON
which a functional dentine layer is available on the side of the tooth receiving the greatest amount of wear. Eventually, the secondary dentine obliterates the pulp chamber, but in doing so, the functional lifespan of the tooth is extended greatly. Thirdly, the presence of a bony core in the pulp chamber effectively decreases the volume of the pulp, thus facilitating eventual obliteration of the pulp chamber. These modifications may be especially important in Uromastix because of its herbivorous diet. Tooth wear is increased because of the fibrous nature of the plant material and because the teeth wear against each other to maintain a sharp shearing edge (Cooper and Poole, ' 7 3 ) . The presence of a bony core may be unique to Uromastix. Each of four specimens of Uromastix examined radiographically had bony cores in the more posterior teeth. Bony cores were not found in Amphibolurus barbatus, Calotes spp. or Leiolepis belliana. None of the previous histologic studies of acrodont teeth (Carlssen, 1896; Cooper et al., '70; Cooper and Poole, ' 7 3 ; Harrison, '01; Osawa, 1897; Rose, 18931, mentions bone in the pulp chamber. Bone or osteodentine has been reported in the pulp chambers of whales and sloths (Tomes, '14). Bone also can appear in the pulp chamber of mammalian teeth after trauma and reimplantation (Anderson et al., '68; Kaqueler and Massler, '69). But this bone is symptomatic of a pathological condition which leads to the eventual ankylosis of the tooth. The mechanism and functional reasons for bone appearing in the pulp chamber in mammals are not clearly understood. In addition to increasing the functional life of the teeth, the jaw bone is able to perform a shearing function once the teeth are completely worn away. Cooper and Poole ('73) described the development of a process of the premaxilla which replaces the upper incisors in Uromastix. This incisiform process is used to crop plant material (Throckmorton, '76). Similarly, the jaw bone is able to assume the function of the cheek teeth. I have observed feeding in one specimen of Uromastix in which nearly the entire dentition had been worn away. This specimen was able to feed on the same food as specimens with complete dentitions, although i t did require more chewing and twisting to bite through the food. Nonetheless, the jaw bone was able to shear through the food adequately.
The ability of jaw bone to perform tooth function is surprising in relation to some of our present concepts of bone biology. In the dental literature, it often is stated that bone must be protected from direct compressive forces (Orban, '66; Noble, '69; Shpiro, ' 7 5 ) . While a n evaluation of this concept is beyond the scope of the present paper, it is clear that in reptiles with acrodont dentitions, the jaw bones can survive when subjected to direct biting pressures. The ability of portions of the jaw bone to survive without a periosteal covering is unique to reptiles with acrodont dentitions (Donald H. Enlow, personal communication). Apparently t h e bone remains viable when covered by epithelium or the acellular layer. In areas deep to the wear facets, however, the lacunae are empty. The extent of these empty lacunae seems to be limited to particular areas bounded by the resting lines in the bone. The nature of the acellular layer remains uncertain. Although it may be a thin layer of acellular bone such as described by Harrison ('01) and Tomes ('14), in my preparations, it stains differently from adjacent bone. In a Van Gieson stain, this layer is the same yellow color as the epithelium, rather than the red of the bone. Permanently implanted dentitions must have some mechanism which allows repositioning of the teeth as the jaws grow, if precise occlusion is to be maintained. The presence of a peridontal ligament in mammals allows the teeth to move horizontally as the jaws grow to move vertically as they wear (Orban, '66; Noble, '69). This problem is more acute in reptiles than in mammals where the jaws may increase in size by as much as a factor of ten after implantation of the first set of teeth (Edmund, '62) compared to 15%to 20%increase in mammals (Crompton and Parker, '78). Although maintenance of occulusion is not important in most reptiles, it is essential to the "precision shear" mechanism in Uromastix (Robinson, '76). On the basis of growth patterns of the maxilla, she suggests remodeling of the maxilla to maintain the upper teeth in proper alignment. A similar mechanism may occur in the dentary; however, most of the remodeling seen in this study was associated with replacing of cancellous bone by compact bone (figs. 3-51 and the narrowing of channels for blood vessels (figs. 15, 16). Remodeling on the lateral side of the jaws also would seem to be prohibited because the labial
EFFECT OF WEAR ON ACRODONT TEETH
surface of the dentary and tooth-bearing parts of the maxilla are not covered by periosteum. Long term growth studies using bone markers are needed to understand the full extent of the remodeling. In reptiles with acrodont dentitions the continuous replacement of the teeth has been suppressed. Without replacement the teeth are subject to wear throughout the life of the animal and they must adjust their position as the jaws grow. In Uromastix the structure of the enamel has been modified and its thickness increased; as the teeth wear the bone supporting the teeth changes from cancellous to compact bone, the pulp chamber is obliterated, and finally the bone of the jaws is capable of shearing food. These changes ensure a functional shearing mechanism throughout the lifespan of the animal. ACKNOWLEDGMENTS
Special thanks are due Mr. K. V. Katele and Doctor T. C. Lakars for their help with this project. Mr. Katele and his staff sectioned the material and did the H & E staining. Doctor Lakars helped and advised on the other stains. Doctor Harry Hoogstraal, Doctor Jos Schall, and Doctor William Neaves supplied lizard specimens examined in this study. LITERATURE CITED Anderson, A. W., Y. Sharov and M. Massler 1968 Reparative dentine formation and pulp morphology. Oral Surg., 26: 837-847. Carlssen, A. 1896 Ueber den Zahnartz bei Agarna colonorurn. Anat. Anz., 1 1 : 758-766. Cooper, J. S., D. F. G. Poole and R. Lawson 1970 The dentition of agamid lizards with special reference to tooth replacement. J. Zool. Lond., 162; 85-98. Cooper, 3. S., and D. F. G. Poole 1973 The dentition and den-
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tal tissues of t h e agamid lizard Urornastix. J. Zool. Lond., 169: 85-100. Crompton, A. W., and P. Parker 1978 Evolution of the mammalian masticatory a p p a r a t u s . Am. Sci., 66: 192-201. Edmund, A. G. 1962 Sequence and fate of tooth replacement in the croccdilia. Contrib. Roy Ont. Mus., Life Sci. Div., 56: 1-41. 1969 Dentition. In: Biology of the Reptilia. Vol. I. C. Gans, A. Bellairs and T. Parsons, eds. Academic Press, London, New York, pp. 117-200. Enlow, D. H. 1969 The bone of reptiles. In: Biology of the Reptilia. Vol. I. C. Gans, A. Bellairs and T. Parsons, eds. Academic Press, London, New York, pp. 45-80. Harrison, H. S. 1901 The development and succession of teeth in Hatteria punctata. Quart. J. Microsc. Sci., 44: 161-219. Kaqueler, J. C., and M. Massler 1969 Healing following tooth replantation. J. Dent. Child., 36: 303-314. Noble, H. W. 1969 The evolution of the mammalian periodontium. In: Biology of the Periodontium. A. H. Melcher and W. H. Bowen, eds. Academic Press, New York, pp. 1-26. Orban, B. 1966 Oral Histology and Embryology. Sixth ed. H. Sicher, ed. Mosby, St. Louis, 176-196. Osawa, G. 1897 Beitrage zur Lehre von Eingeweiden der Hatteria punctata. Arch. Mikros. Anat., 49: 113-226. Osborn, J. W. 1974 On the control of tooth replacement in reptiles and its relationship to growth. J. Theor. Biol., 46: 509-527. Robinson, P. L. 1976 How Sphenodon and Urornastyx grow their teeth and use them. In: Morphology and Biology of Reptiles. A. d’A. Bellairs and C. B. Cox, eds. Linnean Society Symposium, Series No. 3. Academic Press, London, pp. 43-64. Rose, C. 1893 Ueber die Zahnentwicklung von Chamaeleon. Anat. Anz., 8: 566-577. Shpiro, P. 1975 The shape of implants in masticatory force distribution. J. Prosthet. Dent., 33: 567-570. Throckmorton, G. S. 1976 Oral food processing in two herbivorous lizards Iguana iguana (Iguanidae) and Urornastir aegyptius (Agamidae). J. Morph., 148: 363-390. Tomes, C. S. 1874-1875 Studies upon the attachment of teeth. Trans. Odont. SOC.Great Britain, 7: 41-66. 1914 A Manual of Dental Anatomy, Human and Comparative. Seventh ed. H. W. Marett-Tims and H. Smith, eds. P. Blakiston’s Son & Co., Philadelphia.
N 0 0
X
5.
dentary; a, cancellous bone of attachment; c, compact bone of attachment. Arrow marks resting line between the compact bone of the dentary and the bone of attachment. H & E stain. X 150.
4 Coronal section through tooth number 3 near middle of tooth. D, dentine; b, bony core; d, compact bone of
3 Coronal section through tooth number 1 near middle of tooth. D, dentine; b, bony core; p, pulp chamber; d, compact bone of dentary; a, cancellous bone of attachment. Labial is to the right. Arrow marks the resting line between t h e compact bone of the dentary and the bone of attachment. H & E stain. X 115.
pulp chamber.
2 Radiograph of right lower jaw of Urornastix aegyptius (specimen No. R-13). Arrow points to bony core in
covered by connective tissue, C, which joins the lip to t h e lower jaw. The anterior-most tooth is an incisor; the rest are cheek teeth. Arrow points to wear facet in dentary. X 3.
1 Right lower jaw of Urornastix aegyptius, (specimen No. R-12) labial view. The lip, L, has been reflected away from the jaw. The dentition is adjacent to apparently bare bone, B. More inferiorly the bone is
EXPLANATION OF FIGURES
PLATE 1
EFFECT OF WEAR ON ACRODONT TEETH Gaylord S. Throckmorton
PLATE 1
PLATE 2 EXPLANATION OF FIGURES
5 Coronal section through tooth number 6 near posterior one-third of tooth. D, den-
tine; b, bony core; p, pulp chamber; a, compact course-cancellous bone of attachment. Labial is to the right. H & E stain. X 150. 6 Coronal section through tooth number 2 near posterior one-third of tooth. D, den-
tine; b, bony core; p, pulp chamber; a, bone of attachment. Arrow points to blood vessel. Labial is to t h e right. H & E stain. X 115. 7 Coronal section through tooth number 6 near posterior one-fourth of tooth. D, dentine; b, bony core; p, pulp chamber, arrow marks position of secondary dentine a t apex of pulp chamber. Labial is to t h e right. H & E stain. X 285. 8 Coronal section through tooth number 7 near anterior one-third of tooth. D, dentine; b, bony core; p, pulp chamber: s, secondary dentine. Labial is to the right. H & E stain. X 285.
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EFFECT OF WEAR ON ACRODONT TEETH Gaylord S. Throckmorton
PLATE 2
203
PLATE 3 EXPLANATION OF FIGURES
9 Coronal section through tooth number 8 near middle of tooth. D, dentine; b, bony core; p, pulp chamber; s , secondary dentine. Labial is to t h e right. H & E stain. X 285. 10 Coronal section through tooth number 10, near middle of tooth. D, dentine; b, bony core; s, secondary dentine. Labial is to the right. H & E stain. X 365.
11 Coronal section through tooth number 11,near middle of tooth. D, dentine; b, bony core; s , secondary dentine; a, bone of attachment. The space between the bony core and the secondary dentine is an artifact. Labial is to the right. H & E stain. X 285. 12 Coronal section through jaw bone between teeth 10 and 11. Labial is to the right. H & E stain. X 285.
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ESFECT OF WEAR ON ACRODONT TEETH Caylord S. Throckmorton
PLATE 3
205
PLATE 4 EXPLANATION OF FIGURES
13 Coronal section through lower jaw posterior to the tooth row. e, epithelium; d, compact bone of dentary. Arrow points to layer of periosteum. Labial is to the right. H & E stain. X 285. 14 Coronal section through jaw a t level of anterior one-third of tooth number 1. d, compact bone of dentary. Arrow marks layer of epithelium. Labial is to t h e right. H & E stain. X 365. 15 Coronal section through jaw bone a t level of tooth number 6. Arrow points to acellular layer. Labial is to the right. H & E stain. X 365. 16 Coronal section through jaw bone a t level of tooth number 8 showing wear facet in bone of dentary. Arrows point to limits of wear facet. labial is to t h e right. H & E stain. X 285.
EFFECT OF WEAR ON ACRODONT TEETH Gaylord S. Throckmorton
PLATE 4
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