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Keywords:

  • Smilodon;
  • saber;
  • cementum;
  • gingiva;
  • maxillary canines

Abstract

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED

The maxillary canines of Smilodon californicus Bovard, 1907 have a deeply curved cementoenamel junction. The gingiva of modern cats is attached to the tooth at the cementoenamel junction and provides tactile and other dental information to the animal. The presence of cementum at the cervix of the maxillary canines, also called sabers, would indicate that the gingiva in Smilodon was attached in this region. Such an attachment would be advantageous, providing stability and sensory input for the large tooth. Also, gingiva at the cervix would impact the manner in which the teeth were used. Previous study using scanning electron microscopy of dental casts was indirect. The purpose of this study was to confirm by direct methods the presence of cementum at the cervix of Smilodon californicus sabers. Parts of three Smilodon californicus sabers were sectioned and examined with light and scanning electron microscopy (EDS). In addition, percent weight of calcium and phosphorus was measured in enamel, dentin, and cementum using electron dispersive spectroscopy. Cementum was identified in the cervical region of each saber. Spectroscopy confirmed that the tissue is calcified and the mineral is hydroxyapatite. Percent calcium and percent phosphorus of individual tissues were highly variable between specimens. However, the ratios of calcium to phosphorus were not significantly different from the hydroxyapatite standard. In the future, bite models will have to take the presence of soft tissues into account. © 2005 Wiley-Liss, Inc.

The canine teeth of modern cats consist of a core of dentin surrounding the pulp cavity. The dentin of the crown is covered with enamel and the root is covered with cementum. The tooth is held in the socket by fibers of the periodontal ligament, which extend from cementum to alveolar bone or from cementum to gingiva. The junction of the crown and root is fairly linear with a very slight curvature on the labial and lingual aspects toward the crown and away from the root. This line is called the cementoenamel junction (CEJ). Cementum may overlap the enamel for a few millimeters but no further. The gingiva is attached to the cementum along the CEJ by a specialized epithelium called the attachment epithelium. This epithelium produces and maintains its attachment, effectively separating the oral environment from the underlying connective tissues and thereby protecting them from bacterial invasion and damage. The cementum at the CEJ is acellular, while the cementum apically on the root is cellular (Hillson, 1986; Orsini and Hennet, 1992; Harvey and Emily, 1993; Schroeder and Listgarten, 1997; Ten Cate, 1998). The alveolar bone of the tooth socket and the periodontal ligament that holds the tooth in the socket lie inferior to the epithelial attachment of the gingiva. The region of the tooth just apical to the CEJ is called the neck or cervix of the tooth

The large saber-like maxillary canines of Smilodon (saber-toothed cat) are similar in construction to maxillary canines of modern cats. The core of dentin in the crown is covered with enamel and the root is thought to be covered with cementum (Riviere and Wheeler, 2001). The CEJ, however, is not linear but deeply curved toward the crown on the labial and lingual aspects (Figs. 1 and 2). The saber is embedded in alveolar bone up to a line drawn from just apical to the beginning of the enamel on the posterior surface to the anterior surface (Fig. 3) (Merriam and Stock, 1932; Akersten, 1985). A substantial amount of root lies between the alveolar crest and the cementoenamel junction. If the attachment of the gingiva of Smilodon is similar to extant cats, it should have covered the cervix of the tooth from the alveolar crest to the CEJ (Fig. 4A). If the gingiva was attached at the CEJ, then the functional surface, or clinical crown, of the tooth would be limited by that attachment. If the gingiva was attached inferior to the CEJ close to the alveolar crest, then a portion of the saber root would be exposed to the oral environment and the clinical crown of the tooth would be greater (Fig. 4B). Exposure of the root of a canine tooth to the oral environment in any extant mammal is considered pathologic. Such exposure occurs rarely in mammals in the wild and is usually in response to gingival recession, injury, or inflammation (Miles and Grigson, 1990).

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Figure 1. Labial and lingual views of an intact Smilodon saber. The enamel-covered crown is to the left. Arrows indicate the cementoenamel junction.

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Figure 2. Illustration of four views of a right Smilodon saber. From left to right, labial view, anterior view, lingual view, and posterior view.

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Figure 3. Illustration of the relationship of the alveolar margin to the cementoenamel junction of a Smilodon saber. The root is illustrated in black. A large portion of the root lies between the alveolar margin and the cementoenamel junction.

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Figure 4. Illustration of the extent of two possible gingival attachments. The gingiva follows the cementoenamel junction in A. The gingiva only covers the alveolar crest and a small portion of the root in B, leaving a large area of the root exposed.

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Cementum is the softest of the dental tissues. Exposed root cementum undergoes many changes, including bacterial contamination and invasion (Armatige and Christie, 1973a, 1973b; Bosshardt and Selvig, 1997). When located on the crowns of teeth, cementum is quickly worn away from functional surfaces, surviving only in lofts and folds of enamel not directly exposed to wear (Hillson, 1986). If Smilodon cementum is similar to modern cementum, exposed cementum on the smooth surface of the root of the sabers would be worn away by the abrasive action of food and the tongue. The subsequently exposed dentin would then be vulnerable to disease and wear.

If the gingiva was attached to the CEJ and covered the cervix of the tooth, there should be cementum on that surface extending up to the CEJ and possibly a short distance onto the enamel. Previous study indicated that cementum was indeed covering the area but the method was indirect, using casts of the surface. Scanning EM of the casts disclosed a material that appeared cementum-like compared to similar preparations of bobcat and cougar cementum but was probably altered by time and preservation methods. The purpose of this investigation was to demonstrate by direct methods that cementum is present on the cervix of the root of Smilodon sabers using sections of sabers, light, and scanning electron microscopy and electron dispersive spectroscopy (EDS).

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED

Three partial Smilodon californicus sabers were obtained from the George Page Museum of Discoveries (Los Angeles, CA; specimens 52094, 52093, and 52800). Each fragment consisted of some enamel, a relatively complete CEJ, and some root (Fig. 5). Each saber was soaked in several changes of acetone to remove all preservative materials. As preservative was removed, the specimens began to fragment. The location of the pieces was documented and the pieces were numbered. Fragments from the region of the CEJ of each saber were embedded in Bio-Plastic (Ward's Natural Science, San Luis Obispo, CA) according to instructions supplied with the plastic. Fragments from the distal portion of the root of each specimen were similarly prepared. Specimens varied in size and shape. Longitudinal sections approximately 300 μ thick were cut using a Buehler Isomet saw and diamond wafering blade (Buehler, 15 HC Series 10.3 cm × 0.3 mm). Sections were dehydrated in successive changes of 70%, 95%, and 100% ethyl alcohol and placed between two glass slides held together with clothes pins. They were allowed to dry on a slide drying table overnight. The dried sections were then mounted on clean slides and coverslipped using Permount mounting medium (Fischer Scientific). Slides were viewed with a Zeiss Photoscope and a Bio-Rad Radiance 2100 confocal system using a Nikon E800 microscope. Separate thicker sections (500 μ and larger) were dehydrated in ethyl alcohol, dried, and mounted on stubs for scanning electron microscopy (SEM). These sections were polished and coated with carbon and viewed with SEM (JEOL JXA-6400, Link Analytical model eXL). Calcium and phosphorus spectra were measured using energy dispersive spectroscopy (electron probe microanalyzer, 10 kv, 5 nanoamps, 35-sec lifetime). Probes were made of the enamel just incisal to the CEJ. Dentin and cementum probes were made in the tissues just inferior to the CEJ. Each probe covered an area of approximately 3–5 μ to a depth of approximately 1 μ. Spectral readings were converted to percent weight of calcium and phosphorus using the Quantitative Program for the microprobe and an apatite standard.

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Figure 5. Views of the labial and lingual aspects of the specimens used in this study. A and B are of specimen 52094, C and D of specimen 52093, and E and F of specimen 52800. Arrows indicate the cementoenamel junction. Enamel (e) and root (r) are indicated.

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RESULTS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED

Light Microscopy

The fossil specimens were very difficult to cut in thin sections. Three hundred micron sections could not be cut without crumbling. Small areas of some sections remained intact and could be mounted. Fragments from the CEJ refracted light from the microscope in patterns that obscured the image and made photography impossible. There appeared to be a layer of material that could be cementum in the area of interest but the layer was not resolvable with the standard light microscope. The specimens were viewed using confocal microscopy. The CEJ specimens were difficult to focus (Fig. 6A). Reverse image revealed a lamellar structure (Fig. 6B). The lamellae were parallel to the dentinocemental junction. The tissue in sections from the apical regions of roots was typical of mammalian cellular cementum (Fig. 7). While the specimen was thick, it did not refract light like the acellular specimens. Lacunae and fibers were present.

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Figure 6. Confocal micrographs of the surface of a saber near the cementoenamel junction. Dentin is visible in A but the surface is not resolvable. The reverse image shown in B reveals a thin surface layer, which appears itself to be layered (arrows). Magnification, 40×.

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Figure 7. Confocal microscopic views of a sample of apical root dentin with cementum. Dentin is to the right and layers of cellular cementum to the left of the dentinocemental junction (DCJ). Lacunae, appearing as black dots, and extrinsic fibers (arrows) are visible in A. Magnification, 10×. A higher-power view (B) at the DCJ reveals lacunae (short arrows) and intrinsic fibers (long arrows) in the cementum (c) and dentinal tubules in the dentin (d). Magnification, 40×.

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Scanning Electron Microscopy

Scanning electron microscopic images revealed clearly identifiable enamel and dentin at the CEJ of all fossil specimens (Fig. 8). Also present on the dentin surface just inferior to the CEJ was a thin layer of acellular cementum 40–45 μ thick (Fig. 9A and C). Cementum overlapped enamel in specimen 52093 (Fig. 9B). Acellular cementum in specimen 52800 was uneven in density, some areas appearing more electron-dense than others (Fig. 9A). This mottled appearance did not suggest any particular internal or histologic structure. No connective tissue fibers were apparent. Cementum in specimens 52093 and 52094 were very similar microscopically (Fig. 9B and C). They both had a fibrous appearance but no individual connective tissue fibers could be demonstrated. There were no lacunae. No debris and no bacteria were present in any of the specimens.

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Figure 8. Scanning electron micrographs of specimen 52800 (A), 52093 (B), and 52094 (C) at the dentinoenamel junction. Enamel (e) was clearly visible on all specimens, as was dentin (d). Magnification, 500×.

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Figure 9. Scanning electron micrographs of cementum (c) on the surface of the three specimens near the cementoenamel junction. Specimens 52800 (A), 52093 (B), and 52094 (C) all have a layer of cementum approximately 40–45 μ thick on their surface. The cementum in specimen 52093 overlapped the enamel (e). Cementum overlies dentin (d) in the other specimens. Magnification, 1,000×.

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Spectral Analysis

Spectral analysis of the enamel, dentin, and cementum confirmed that the tissues were calcified (Fig. 10). In all three fossil specimens, enamel contained more calcium and phosphorus by weight than dentin, and cementum was the least calcified tissue. All measurements of percent weight of calcium and phosphorus were lower than the standard (Table 1). The Ca/P ratios were, however, not significantly different from the standard Ca/P ratio (Table 2). The average Ca/P ratio for all tissues of all specimens was 2.1 ± 0.2 compared to the standard ratio of 2.1. Average percent weight calcium and phosphorus of dentin for the three specimens was not significantly different from the averages for enamel. This could be due to loss of mineral over time and/or loss of organic matrix, especially collagen, from dentin.

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Figure 10. Spectrographs of the cementum, enamel, and dentin of the three specimens. The left column represents specimen 52800. The center column represents specimen 52093. The right column represents specimen 52094. The top row spectra are of cementum, the middle row of enamel, and the bottom row of dentin.

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Table 1. Percent by weight of calcium and phosphorus in enamel, dentin, and cementum as determined by electron dispersive spectroscopy and Ca/P ratios for cementum, dentin, and enamel in each specimen
SampleWT % PWT % CaCa/P
52093 cementum2.04.72.4
52093 dentin8.517.52.1
52093 enamel9.919.72.0
52094 cementum3.78.12.2
52094 dentin11.523.22.0
52094 enamel13.426.01.9
52800 cementum5.512.62.3
52800 dentin11.225.82.3
52800 enamel12.726.92.1
Apatite standard18.639.62.1
Table 2. Average percent weight phosphorus and calcium in cementum, dentin and enamel from the three specimens and average calcium phosphorous ratios
TissueAV WT % PAV WT % CaAV Ca/P
Cementum3.7 ± 1.78.5 ± 3.92.3 ± .1
Dentin10.4 ± 1.622.2 ± 4.22.1 ± .2
Enamel12.0 ± 1.824.2 ± 3.92.0 ± .2
Apatite standard18.639.62.1

DISCUSSION

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED

This study demonstrated acellular cementum at the cervix of Smilodon sabers. This finding supports the presence of gingiva attached to the CEJ and covering the cervix, a condition typical of modern cats. The comparative morphology of teeth has been extensively described (Dahlberg, 1968; Butler and Joysey, 1974; Kurten, 1982; Hillson, 1986; Teaford et al., 2000). The individual tissues are variable in structure, as is the method of attachment to the jaw. The evolution of tooth attachment and morphology of attachment among extant and fossil species has been addressed by several investigators (Orvig, 1967; Shellis, 1982; Osborn, 1984; Gaengler and Metzler, 1992; Gaengler, 2000). Cementum itself can be classified according to composition and function (Bosshardt and Selvig, 1997; Ten Cate, 1998). Acellular extrinsic fiber cementum is found from the cervix to the apical third of teeth. Its function is anchorage of the tooth in the socket. Cellular mixed fiber cementum contains trapped cells and is found in the apical third and between the roots of multirooted teeth. Its function is adaptation of attachment to varying conditions. Acellular afibrillar cementum is found in patches on enamel. Its function is unknown. In addition, all placental mammalian teeth are thecodontal or socketed, meaning the roots are surrounded by and attached to alveolar bone. The periodontal attachment of teeth of thecodont mammals can be classified into one of six groups (Gaengler and Metzler, 1992; Gaengler, 2000): incisors and most canines of all omnivorous, carnivorous, and herbivorous dentitions are single-rooted teeth with a combination of acellular afibrillar cementum, acellular extrinsic fiber cementum, and cellular intrinsic fiber cementum. The sabers of Smilodon californicus conform to this group. The saber is single-rooted. The cementum at the CEJ on the enamel is acellular and may or may not be afibrillar. The cementum on the root surface at the CEJ is acellular and presumably extrinsic fiber in type, since acellular afibrillar cementum is found only on enamel (Bosshardt and Selvig, 1997; Ten Cate, 1998).

Similarly, four types of gingival epithelial attachment are described for thecodonts. The second type describes the epithelial attachment as being to enamel and/or to coronal cementum when it overlaps enamel. While this study could not demonstrate soft tissue attachment directly, the presence of acellular cementum at the cervix of the sabers and overlapping the enamel for a short distance is strong evidence for the location of the gingival attachment in this region.

Typical cellular mixed fiber cementum is located on the apical two-thirds of the root. Confocal images demonstrate extrinsic collagen fibers (Sharpy's fibers) in apical root cementum but not in the region of the CEJ. This may be due to the progressive destruction of the organic component in the thinner cervical tissues. However, the type of cementum and location of cementum observed in the present study are consistent with the thecodont classification of Gaengler (2000) and imply an epithelial attachment on the enamel or on the cementum at the CEJ.

Spectoral analysis confirmed that the tissue is cementum. It is a calcified tissue and consistently less calcified than the corresponding dentin or enamel. The layer is not museum-preservative, which contains no calcium. It is not dental plaque. It does not contain bacteria or debris characteristic of that material and it is smooth-surfaced and of constant thickness, also not characteristic of dental plaque. It is also not matrix. There was no indication of organic or inorganic material typical of the matrix in which the sabers were found. The actual percent weights of Ca and P vary between the sabers and tissues. Sabers 52093 and 52094 came from the same pit at La Brea. The pit origin of saber 52800 is unknown. Differences in conditions in the pits and age of the sabers could account for variation in the percent weight measurements. Water content of the specimens may have varied also. In addition, the type of apatite and crystallographic properties of dentin have been shown to vary from animal to animal (Sakae et al., 1994). This may be true for cementum as well. However, the average Ca/P ratios of the tissues were not significantly different from the hydroxyapatite standard, indicating that the measurements are accurate and that the mineral is hydroxyapatite.

The conclusion that the gingiva was attached to the CEJ has important implications for consideration of bite models for Smilodon. A number of studies have attempted to describe the manner in which Smilodon used the sabers and several bite models have been proposed (Simpson, 1911; Bohlin, 1947; Akersten, 1985; Biknevicius and van Valkenburgh, 1996). None of these, however, considered the location or extent of oral soft tissues and the manner in which such tissues might affect the bite. The extensive soft tissue attachment suggested by this study would limit the depth to which the sabers could be inserted without injury to the gingiva. Injury would result in gingival inflammation and recession and possible wear in the cementum and dentin on the lingual surface at the cervix as previously described. Such wear has been observed in approximately 1% of 838 sabers in the Page Museum collection (data not shown). This is consistent with the findings of Shermis (1984), who observed very low incidence of periodontally induced bone resorption in Smilodon maxillary splanchnocrania in the La Brea collection. Alveolar bone resorption is a universal response to periodontitis resulting from gingival injury and/or inflammation. A low incidence of bone resorption reflects a low incidence of gingival recession due to causes other than aging. Very few sabers should show the effects of wear resulting from gingival recession. Indeed, this is the case.

Finally, it would be of great functional advantage to have an extensive gingiva related to such a large tooth. Several important functions might be served. The gingival component of the periodontal ligament would provide greater attachment and stability for the large canine. The gingiva also acts as a tactile organ letting the animal know, among other things, when the tooth has reached its maximum functional penetration (Heyeraas et al., 1993; Jacobs and von Steenberghe, 1994; Kondo et al., 1995; Sugaya et al., 1995; Fristad, 1997; Shroeder and Listgarten, 1997). Additionally, the gingiva and periodontium may be involved in jaw-closing reflexes (Eriksson et al., 1998, 2000; Louca et al., 1998; Zafar et al., 2000). Smilodon, therefore, had better stability and a vast array of sensory input to help them use the sabers without damaging them. Hopefully, consideration of the location and extent of the gingiva in these animals will lead to a definitive bite model and a better understanding of how these animals utilized those large and impressive canine teeth.

Acknowledgements

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED

The authors thank the George Page Museum of Discoveries for their generous donation of three sabers for use in this study. They also thank Mr. Jerome Adey for help with the scanning electron microscopy and for the EDS measurements and analysis, as well as Dr. Michael Danilchik for the confocal microscope photographs.

LITERATURE CITED

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED
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