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Journal of Vertebrate Paleontology 23(3):622–630, September 2003 q 2003 by the Society of Vertebrate Paleontology

HISTOLOGY OF TOOTH ATTACHMENT TISSUES IN THE LATE CRETACEOUS MOSASAURID PLATECARPUS M. W. CALDWELL1,*, L. A. BUDNEY1,*, and D. O. LAMOUREUX2 Paleobiology, Research Division, Canadian Museum of Nature, P.O. Box 3443, Station ‘D’, Ottawa, Ontario, K1P 6P4, Canada, mw.caldwell@ualberta.ca; 2 Department of Oral and Health Sciences, Faculty of Medicine and Oral Health Science, Dentistry/Pharmacy Centre, University of Alberta, Edmonton, Alberta, T6G 2N8, Canada

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ABSTRACT—We present new data on the tooth attachment histology of the Late Cretaceous marine lizard Platecarpus (Mosasauridae). Examination of thin sections of a right dentary reveals the presence of a woven-fiber bone matrix that forms the margins and floor of the tooth alveolus; this bony matrix is traditionally identified as bone of attachment. We identify it as alveolar bone based on its histologic and topologic similarities to archosaurian and mammalian alveolar bone. We also identify a cribiform plate, a structure usually associated with the periodontal ligament. Parallel fibers present in multiple, non-resorbed generations of alveolar bone are tentatively identified as remnants of mineralized portions of collagen fiber bundles, or Sharpey’s fibers. Along the sides of the dentine root we identify a thin layer of acellular cementum. The acellular cementum is surrounded by an enormous mass of cellular cementum tissue that fills the alveolus. This cementum mass is composed of two histologically distinct forms: (1) a loosely organized cellular cementum ground matrix; (2) a laminar form surrounding the vascularization (cementeons) that we term osteocementum. Mosasaurs possess the attachment tissues that are used to diagnose thecodont ankylosis. Mosasaur thecodonty is derived within the Mosasauroidea (aigialosaurs 1 mosasaurs).

INTRODUCTION The Late Cretaceous marine lizards known as mosasaurids (Mosasauridae) achieved gigantic proportions and evolved a number of specializations for living in aquatic environments. The dentition of mosasaurids, when compared to other squamates, is also highly modified. The teeth are set in deep sockets, anchored in place by massive amounts of bony tissue. Numerous authors have characterized the type of mosasaur tooth implantation and attachment with categories ranging from a modified form of acrodont-pleurodont attachment (Owen, 1840) to a modified form of thecodont attachment (Leidy, 1865; Edmund, 1960; Shellis, 1982). Most recently, Lee (1997) followed Leidy (1865) by identifying the tooth attachment in mosasaurids (Mosasauridae) as sub-thecodont, while Zaher and Rieppel (1999), in a critical review of Lee (1997), identified the mode of tooth attachment as sub-pleurodont, thus following Owen (1840). Zaher and Rieppel (1999), continuing their critique of Lee (1997), also argued that mosasaur tooth sockets are not real sockets as compared to the sockets present in vertebrates fitting their definition of thecodonty (see below). For Zaher and Rieppel (1999), mosasaur tooth sockets were merely apparent sockets formed by large amounts of bone of attachment. Conversely, Lee (1997) argued that the mosasaurian socket wall is true bone and not a dental tissue like bone of attachment. Lee (1997) and Zaher and Rieppel (1999) followed a precedent in zoological studies that identifies thecodonty in fossil taxa by verifying the presence or absence of socket walls. This means the geometry of the attachment site, i.e., a fully-sided socket, constitutes the only significant feature used to identify thecodonty. Diagnosing a single category such as thecodonty in squamates based purely on the geometry of the attachment site is extremely difficult

* Present Address: Departments of Earth and Atmospheric Sciences and of Biological Sciences, University of Alberta, Edmonton, Alberta, T6G 2E3, Canada.

because of the degree of morphological variation in squamate tooth attachment. The conflicting interpretations of mosasaur dental anatomy as given by Zaher and Rieppel (1999) and by Lee (1997) reflect the difficulties of describing tooth attachment types by examining gross morphology. For example, Zaher and Rieppel (1999) examined many of the same specimens as Lee (1997) but produced very different interpretations of the mode of tooth implantation and attachment. To address the conflicting descriptions of tooth attachment given by these authors we undertook a histological investigation of the tissues of tooth attachment. In this paper we report new data on the histology of tooth attachment for the mosasaurid Platecarpus that challenge the characters used to define the traditional attachment categories of pleurodonty and thecodonty. We present a review of tooth attachments and attachment tissues, follow with the results of our histological study, and finally, discuss our findings relative to the conclusions of Lee (1997) and Zaher and Rieppel (1999). We conclude with a discussion of the limitations of the traditional categories of acrodonty, pleurodonty, and thecodonty to classify the variety of tooth attachments observed in squamates specifically, and in amniotes generally. TOOTH ATTACHMENT TYPES In his review of the evolution of amniote tooth replacement and attachment, Osborn (1984:556–557) noted that vertebrate teeth are ‘‘. . . somewhat immovably attached to the jaw bone by mineralized tissue (ankylosis) or attached by unmineralized fibres embedded into the root surface and the adjacent bone (fibrous attachment). . . .’’ Osborn (1984) identified the mineralized tissue as ‘bone of attachment’; this tissue is resorbed when a tooth is shed and re-develops during the maturation of the replacement tooth. Osborn (1984) distinguished four categories of ankylosis. Acrodont ankylosis is when the tooth is attached to the apex of the tooth-bearing element (TBE). Pleurodont ankylosis is when the tooth is attached to the lingual side of the TBE. Protothe-

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CALDWELL ET AL.—MOSASAUR ALVEOLAR BONE codont ankylosis is when teeth are attached in a gutter created by the lingual and labial walls of the TBE. Thecodont ankylosis is when the tooth root is embedded in a socket on the TBE. Osborn (1984) distinguished between a gomphosis and an ankylosis such that a gomphosis is recognized if teeth are embedded in a socket and attached by fibres. Gaengler (2000) reviewed the traditional categories of acrodonty, pleurodonty and thecodonty. He noted that these three categories do not acknowledge the diversity of tooth attachment modes in nature. Gaengler (2000) introduced a new set of categories for tooth attachment. Acrodonty is identified when teeth are ankylosed or attached by fibers to the apex of the jaw (e.g., acanthodians, and early Silurian osteichthyans). Acro-protothecodonty is identified when teeth are attached by a complex fiber apparatus to the apex of the jaw (e.g., most fishes); a pedicel of bone mediating the attachment may be present. Gaengler (2000) subdivided acro-protothecodonty into six sub-categories. Pleurodonty is identified when teeth are attached by fibres or bone to the lingual wall of the jaw (e.g., Recent amphibians and lizards). Gaengler (2000) identified thecodonty as present when teeth are attached within a socket by a complex of tissues including cementum, a periodontal ligament, and alveolar bone. From our initial survey of squamate dentitions we noted a wide range of tooth-attachment morphologies. We found four attachment morphologies that loosely parallel Osborn’s (1984) categories of ankylosis: (1) deep, four-sided ‘alveoli’ (mosasaurids and many snakes); (2) deep to shallow, three-sided ‘alveoli’ formed by mesial, distal, and labial walls (some snakes [Zaher and Rieppel, 1999] and most lizards including basal mosasauroids [Caldwell, 1999; Caldwell and Cooper, 1999]); (3) very shallow attachment sites with slight rugosities for tooth attachment (e.g., varanoid lizards); (4) no obvious attachment site/alveolus as the teeth are anchored to the apex of the TBE (e.g., acrodont lizards). The problem then, relative to squamate tooth attachment, is not one of gross morphological similarities, but rather one of histological similarity. What type of tissue forms the alveolus and how is the tooth anchored to this tissue? ATTACHMENT TISSUES Osborn (1984) and Gaengler (2000) presented histological data on the quality and quantity of the differing dental attachment tissues. The tissue histology, development, and function of mammalian alveolar bone, cementum, and periodontal ligaments are extremely well known (e.g., Tomes, 1898; Peyer, 1968; Osborn, 1984; Ten Cate, 1989; Carlson, 1990; Berkovitz et al., 1992; Reid, 1996). Because crocodilian tooth attachment is recognized as a thecodont gomphosis different from the mammalian type, it too has been studied in some detail (e.g., Berkovitz and Sloan, 1979). Alveolar bone, periodontal ligaments, and cementum are recognized as present in living crocodilians; similar tissues are described for other fossil archosaurs such as birds and dinosaurs (Peyer, 1968; Reid, 1996). Differences between mammalian and crocodilian gomphoses are recognized at the histological level: (1) the type, amount, and point of attachment of acellular and cellular cementum; (2) the alignment of periodontal ligament fibers relative to the tooth root; (3) the size of ligament fibers; (4) the persistence of the alveolus in crocodilans between tooth generations. The following characterization of mammalian attachment tissues is intended to create a baseline of comparison to those of crocodilians (Berkovitz and Sloan, 1979), and the mosasaurid Platecarpus (to be described below). Alveolar Bone The alveolar process of mammals consists of an outer cortical plate, a central spongiosa, and the bone lining the socket. The lining bone is referred to as bundle bone and provides the attachment surface for calcified and non-calcified periodontal ligament fibers; the bundle bone layer is also

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referred to as the cribiform plate. The cribiform plate has numerous perforations allowing blood vessels and nerves passage from the alveolus, through the periodontal ligament, to the cementum layer next to the tooth root. Histologically, the bone of the alveolar process (alveolar bone) is composed of coarsefibered woven bone (WFB). A WFB matrix is formed by randomly distributed, loosely packed collagen fibers of varying sizes that create a woven, mesh-like structure. Developmentally, WFB of the alveolar process is derived from the basal portion of the dental follicle (for a review see Ten Cate, 1989). Periodontal Ligaments These ligaments originate in the bundle bone layer (cribiform plate) and penetrate the layer of cementum (cellular cementum) coating the tooth root. In general, the tooth root of mammals and archosaurs is considered to be the dentine portion of the tooth that is coated with cementum and secured in the alveolus by mineralized and unmineralized fibers of the periodontal ligament. Cementum Cementum is a calcified connective tissue coating the tooth root in thecodont animals. Its primary function is to provide an attachment site for the fibers of the periodontal ligament. Histologically, cementum is similar to bone but avascular. Two types of cementum are recognized. The first, acellular cementum, is generally lamellar in structure and forms a thin coating around the outer surface of the dentine of the root. The second type, cellular cementum, contains cementoblasts that were trapped during cementum formation. The trapped cementoblasts (cementocytes) sustain the periodontal ligament fibers anchored in the cementum. In most mammals, both acellular and cellular cementum form a relatively thin layer of bony tissue around the root. In terms of development, all the tooth tissues, including the enamel, dentine, cementum, periodontal ligament fibers (calcified and uncalcified), and alveolar bone, are produced by various specialized layers of the developing tooth germ bud, and are not derived from the periosteum of the TBE. Ten Cate and Mills (1972), Freeman et al. (1975), and Ten Cate (1976) discovered the developmental origin of these tissues through experiments involving the excision and re-implantation of oneday-old tooth germs to non-tooth-bearing dermal bones, e.g., the parietal. The transplanted tooth germs developed normally with the formation of enamel, dentine, cementum, periodontal ligament, and a socket of alveolar bone. Tooth attachment is often referred to as tooth implantation. The aforementioned experiments indicate that tooth implantation is a developmental artifact of the complex interactions between the developing tooth bud and the development of the TBE; implantation is thus not a feature unique to the TBE. MATERIALS AND METHODS Vertical and horizontal sections of a left dentary of the plioplatecarpine mosasaur, Platecarpus sp., were cut using a Buehler Diamond Wafering Blade (11-4245) mounted on a Buehler Isomet Low Speed Saw (11-1180). Vertical sections were cut sequentially through a tooth-bearing alveolus beginning in the mesial portion of the alveolar bone and ending in the distal portion of the alveolar bone; sections ranged in thickness from two millimeters to four millimeters. Horizontal sections of a tooth-bearing alveolus were made beginning at the remnant tooth crown apex and ending at approximately one-half of the socket height; cut sections were two millimeters thick. All vertical sections, except those used to make thin sections, were embedded in epoxy and manually polished on 400 and 600 grit emery paper, and then mechanically polished on a rotating stage polisher using one micron and half micron alumina solutions. A vertical section of an alveolus of a right maxilla of the fossil snake Dinilysia (Estes et al., 1970) was obtained by polishing the fractured mesial face of the fourth alveolus. The


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specimen was not embedded in epoxy due to the rarity of toothbearing bones for this fossil snake. The right maxilla was polished manually on 400 and 600 grit emery paper, and then mechanically on a rotating stage polisher using one micron and half micron alumina solutions. Specimens studied for bone histology include: Dinilysia patagonica (UALVP unnumbered specimen); Platecarpus (NMC 40957). Specimens examined for gross morphology include: Varanus rudicollis (FMNH 145710), Cylindrophis rufus (USNM 297456), Xenopeltis unicolor (USNM 287277), Leptotyphlops humilis (USNM 222795), Typhlops punctatus (USNM 320904), Mosasaurus mokoroa (CM ZFR1), Platecarpus sp. (NMC 40969). Abbreviations CM ZFR, Canterbury Museum, Christchurch, New Zealand; FMNH, Field Museum, Chicago, Illinois; NMC, Canadian Museum of Nature, Ottawa, Canada; UALVP, University of Alberta, Laboratory for Vertebrate Paleontology, Edmonton, Canada; USNM, Smithsonian Institution, United States National Museum, Washington, D.C., U.S.A. RESULTS Gross Morphology Mosasaur teeth have a sharply pointed, recurved, enameldentine crown, and may be fluted along one side or possess lateral carinae (Fig. 1). There is a large bulbous mass of ossified tissue at the base of the tooth, below the crown. The bony tissue mass is attached at its base to the bottom of an alveolar groove in the TBE. This bony tissue mass is often large enough to project above the margins of the alveolar groove of the TBE (Fig. 1); it is clear that this bony tissue is involved in anchoring the tooth to the TBE. Close observation indicates that the tooth-attachment sites appear to be distinct sockets. The sockets surround the entire tooth base (described in the previous paragraph) and are formed of bony tissue (Fig. 1). Conventionally, the mesial and distal socket walls have been referred to as interdental plates (see Zaher and Rieppel, 1999); however, we recommend abandoning this term as the mesial and distal socket borders are not independent plates of bone. Clarification of the above features of gross morphology are assisted by the following histological observations of mosasaur tooth-attachment tissues. We therefore utilize the terminology applied to mammalian and crocodilian attachment tissues (see Introduction) for our histological characterizations of mosasaurid attachment tissues. Histology Alveolar Bone In the mosasaur Platecarpus, the walls and floor of the socket are formed by a woven-fiber bone (WFB) tissue distinct from the lamellar bone of the TBE (Figs. 1B, 2, 3); this WFB tissue is typical of alveolar bone in other vertebrates (Peyer, 1968; Ten Cate, 1989; Carlson, 1990; Berkovitz et al., 1992). The alveolar bone closest to the tooth base is formed of primary woven bone, composed of primary osteons (Zone 2 bone, Fig. 2B–B9). Alveolar bone from the outer region of the socket (distal to the tooth base) is remodeled (secondary osteons) (Zone 1 bone, Fig. 2B–B9). The difference in osteon type between the inner and outer regions of the socket is interpreted as having been caused by multiple waves of tooth replacement and tooth attachment. The alveolar bone closest to the tooth is resorbed and replaced with every replacement event. Primary osteons are therefore observed in the alveolar bone closest to the tooth base. Secondary osteons, indicating older, more mature bone, are found where alveolar bone is not resorbed or replaced, i.e., near the outer edge of the socket wall. Cementum Platecarpus sp. shows two types of cementum,

a typical acellular cementum, and a new type of cellular cementum that we term osteocementum. The osteocementum of Platecarpus forms the massive tooth base surrounding the tooth root and extending down into the alveolus. The basal mass of dental tissue, the conventional tooth base of mosasaurids, is more appropriately termed the tooth root because the cellular cementum fibers originate in the tooth root (the dentinous portion of the tooth not covered by enamel). In horizontal and vertical section we see cellular cementum composed of cementeons, analogous to bone osteons, within a generalized, cellular, cementum ground matrix. The cementeons are thin, centripetally deposited osseous laminae, which surround the blood vessels (Figs. 2–4). The ground matrix of the cellular cementum forms globular to columnar bodies (Fig. 3B). Collectively, the cementeons and cellular cementum ground matrix create a massive cementum coating around the dentine portion of the tooth root. This mass also shows incremental growth lines (Lines of Salter) aligned parallel to the long axis of the tooth. The large mass of cellular cementum greatly increases the surface area for tooth attachment to the alveolar bone. Dense fields of probable Sharpey’s fiber traces are present at the cellular cementum–alveolar bone contact. Multiple layers of partially resorbed Sharpey’s fibers, possible Lines of Salter, cementum, and alveolar bone are observed in histological sections at the contact between alveolar bone and cementum (Fig. 3D). An acellular cementum matrix forms a thin, dense band around the ventral extension of the orthodentine portion of the crown; this matrix is an osseous tissue that has neither cell lacunae nor vascularization (Fig. 4). Periodontal Ligament/Sharpey’s Fibers The only tissue type unrecognizable in fossil squamates is the non-ossified component of the periodontal ligament. However, the morphology of a cribiform plate-like structure and the remnants of Sharpey’s Fibers indicates the presence of a periodontal membrane (Fig. 3D). DISCUSSION Because the majority of squamates show neither obvious dental alveoli nor obvious tooth roots it has been concluded that squamate tooth attachment was not of the thecodont type (Tomes, 1898; Peyer, 1968; Osborn, 1984; Carlson, 1990; Zaher and Rieppel, 1999). This conclusion is reached because at one diagnostic level, e.g., as a category for character construction in phylogenetic analysis, thecodonty has been understood as a form of implantation where a root sits in a complete socket (see above). The difficulty of diagnosing tooth-attachment tissues, and thus thecodonty, is illustrated by Tomes’ (1898:229–230) description of bone of attachment, the supposed non-thecodont, amniote, tooth-attachment tissue. ‘‘. . . it seldom, perhaps never, happens that a tooth is attached directly to a plane surface of the jaw which has been formed previously; but the union takes place through the medium of a portion of bone (which may be large or small in amount) which is specially developed to give attachment to that one particular tooth, and after the fall of that tooth is itself removed. For this bone I have proposed the name of ‘‘bone of attachment’’, and it is well exemplified in the Ophidia. . . ’’ (p. 229). ‘‘But the ‘‘bone of attachment,’’ is very coarse in texture, full of irregular spaces, very different from the regular lacunae, and its lamination is roughly parallel with the base of the tooth.’’ (p. 230)


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FIGURE 1. Gross morphology of the tooth-bearing elements of two mosasaurs. A, Anterior portion of the left dentary of Platecarpus sp. (NMC 40969) in lingual view. Four tooth positions are preserved on this anterior segment. Section lines show placement and position of vertical and horizontal thin-sections examined in Figures 2–4 from jaw fragment sacrificed for this study (CMN 40967). B, Posterior portion of the left maxilla, in oblique inferior view, of the mosasaur Mosasaurus mokoroa (CM ZFR1). Interdental plates are composed of alveolar bone, are distinct from the cementum forming tooth root and the fibrolamellar bone of the TBE, and remain between generations of replacement teeth. Similar features are observed in the toothed pterygoid elements (not figured). Abbreviations: pc, pulp cavity; r.p., resorption pit; TBE, tooth-bearing element.

We can find no comparative histological description of Tomes’ (1898) ‘‘bone of attachment’’ indicating how it differs from alveolar bone. We note as well that Osborn (1984) considered that bone of attachment might be the homolog of alveolar bone. This raises the question of how to distinguish histologically between the two attachment tissues other than the

illogical application of taxonomic criteria, i.e., in non-crocodilian reptiles alveolar bone is referred to as bone of attachment. Such criteria are akin to referring to a bird wing as a structure different than a human forearm (and hand). We find that mosasaurid bone of attachment is ontogenetically, compositionally, and topologically indistinguishable from alveolar bone. As in


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FIGURE 2. Platecarpus sp. (NMC 40967), horizontal sections, light microscopy of mosasaur tooth attachment tissues. A (340), A9 (3100), thin sections showing fibrolamellar and woven-fiber bone. B (340), thin-sections of alveolus showing zones 1–2 of alveolar bone at contact with cementum. B9 (3100), detail of zone 1 and 2 alveolar bone. C–C9 (340 & 3200), thin-sections of cementum portion of tooth root showing details of the cementeons and cementum ground matrix. Abbreviations: FLB, fibrolamellar bone; pc, pulp cavity; r.p., resorption pit; R-L, resorption lacunae; V-L, vascular lacunae; WFB, woven fiber bone; Z-1, zone 1 alveolar bone; Z-2, zone 2 alveolar bone.


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FIGURE 3. Platecarpus sp. (NMC 40967), vertical sections, light microscopy of mosasaur tooth attachment tissues. A, thin section showing fibrolamellar bone of dentary (340), with A9, detail of secondary osteon development (3100). B, thin-section of tooth root showing vertical orientation of cementum fibers (340). B9, details of cellular cementum, cementeons, cementocytes (3400). C, thin sections showing fibrolamellar and woven-fiber bone (340). C9, at base of alveolus (3200) (note secondary osteon development within primary bone matrix). D, thin-section detail (3200), at base of alveolus showing Sharpey’s fibers and multiple generations of alveolar bone with remnant Sharpey’s Fibers. Abbreviations: FLB, fibrolamellar bone; Gen. 1, first preserved generation of Sharpey’s fibers; S.F. G-2, Sharpey’s Fibers, second generation;V-L, vascular lacunae; WFB, woven-fiber bone.


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FIGURE 4. Platecarpus sp. (NMC 40967), vertical sections, light microscopy of mosasaur tooth attachment tissues. A, thin-section of lingual side of tooth wall and root showing orthodentine portion of tooth terminus within pulp cavity; pulp cavity continues to base of root (340). A9, thin-section detail of dentine margin and pulp cavity showing dentine tubules (3400). A0, thin-section detail showing cellular cementum, orthodentine, and very thin band of acellular cementum (3400). Abbreviations: acell. cementum, acellular cementum; alv. bone, alveolar bone; FLB, fibrolamellar bone; pc, pulp cavity.

mosasaurids, the alveolar bone of mammals and archosaurs directly contacts the TBE, serves as the attachment point for periodontal ligament fibers via the cribiform plate, forms a point of attachment for the tooth root (socket-shaped attachment point in non-squamates, and develops from the basal membranes of the tooth bud. Therefore, we suggest applying the term alveolar bone to any and all future descriptions of the tissue previously identified as squamate bone of attachment. A phylogenetic argument for our suggestion is made as follows. Reference to amniote phylogenetic patterns, and more specifically, diapsid phylogenies, would predict that if synapsids and archosauromorphs are thecodont in tooth implantation, and possess the relevant attachment tissues, then those similar tissues should be present in some form within lepidosauromorphs, i.e., squamates. Therefore, alterations to the geometry

of the attachment site need not presume the evolution of a suite of new attachment tissues. The dental histology of those tissues must be shown to differ from the more plesiomorphic form before such a statement can be made. If attachment tissues are integral to understanding mammalian and archosaurian tooth attachment modes and evolution, then the same must hold true for squamates, diapsids, and potentially, for all amniotes. The problem of understanding squamate tooth attachment variability, pleurodonty, acrodonty, and thecodonty, can only be resolved by studying tooth-attachment tissues. Comparing the histology of mosasaur tooth-attachment tissues to their tooth gross morphology, we find that certain histologies equate roughly to certain gross morphologies. Applying this observation to the dentitions of squamates not yet ex-


CALDWELL ET AL.—MOSASAUR ALVEOLAR BONE amined histologically allows us to speculate on their dental histology. A cribiform plate-like structure indicating the probable presence of a woven-fiber attachment bone and periodontal ligament is noted in other squamates examined such as aigialosaurs and coniasaurs (Caldwell, 1999; Caldwell and Cooper, 1999). We also note, from a polished face of a right maxilla of the Late Cretaceous snake Dinilysia patagonica (Estes et al., 1970), that bony tissues forming the mesial and distal walls of the alveolus show a woven-fiber bone histology, and cribiform plate-like gross morphology. These characteristics are identical to those identified as alveolar bone tissues in mosasaurs and other thecodont amniotes. We note that alveolar bone in basal snakes and basal mosasauroids (aigialosaurs, dolichosaurs, coniasaurs) forms a three-sided dental alveolus lined with a partial cribiform plate, i.e., the lingual wall is incomplete (see Pseudotyphlops, a uropeltine snake, as illustrated by Zaher and Rieppel, 1999:fig. 7). Zaher and Rieppel’s (1999) assertion that the mode of attachment in snakes and mosasaurs is fundamentally different is inaccurate; there may not be particular phylogenetic significance to the similarities, but tooth attachment is certainly not different in the sense implied by Zaher and Rieppel (1999). They describe primitive snake tooth-attachment morphology, exemplified by Pseudotyphlops, as a three-sided socket. However, this same alveolar morphology is present in a number of snakes such as Dinilysia, Xenopeltis, basal mosasauroids, and in many other squamates. The gross anatomy of tooth attachment is very similar, particularly as concerns the amount of alveolar bone deposited and the 3-sided construction of the alveolus, between basal snakes and basal mosasauroids (3-sided alveoli are also common in many other squamates). Further, we reject Zaher and Rieppel’s (1999) strict definitions of acrodonty, pleurodonty, and thecodonty as they do not account for relevant attachment tissues (i.e., mineralized and non-mineralized periodontal ligaments). These tissues are illustrated by Gaengler (2000) in Lacerta and noted by other authors (Shellis, 1982; Osborn, 1984). Additionally, in their definition of thecodonty, Zaher and Rieppel (1999) require the presence of a discontinuous dental lamina, and that tooth replacement be continuous throughout the life of a thecodont amniote. Zaher and Rieppel’s (1999) definition is inconsistent and erroneous as neither condition occurs in mammals (diphyodont and thecodont). Crocodilian thecodonty differs from mammalian thecodonty in many respects (Shellis, 1982; Osborn, 1984) not the least of which is the possible discontinuous nature of the dental lamina; therefore, this tissue is inconsequential to a definition of thecodonty as it is autapomorphic if it exists at all (contra Zaher and Rieppel, 1999). Phylogenetically, we recognize squamate ‘‘pleurodonty’’ as a modification of the primitive pattern of diapsid thecodonty accomplished by varying the quantity, but not the presence or absence, of the tissues of attachment. Thecodont attachment tissues are primitive for, and present in, squamates and likely all lepidosaurs. Socket development can be studied in relation to phylogeny by studying the modifications and specializations of attachment tissues and not simply on the basis of the presence/absence of a socket. For example, mosasaurs are a derived clade of thecodont squamates, nested in the clade Mosasauroidea, whose basal members (i.e., dolichosaurs; see Caldwell, 1999; Caldwell and Cooper, 1999) have reduced sockets and thus smaller amounts of alveolar bone. CONCLUSIONS Our data show that mosasaurids possess real sockets into which rooted teeth are attached, and that they possess bony tissues that are histologically consistent with tissues seen in thecodont reptiles (e.g., crocodilians). Like crocodilians, the

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mosasaurian alveolus remains in place through multiple replacement events, evidenced by the partial resorption of alveolar bone and the remodeled mesial and distal alveolar walls. For systematists constructing characters for phylogenetic analysis, primary homologies should not be sought at the level of presence/absence of a socket, but rather at the level of shared features of attachment tissue histology, and the topological relations of those tissues at the gross morphological level. Implantation (root in a socket) is a developmental phenomenon resulting from the amount of alveolar bone (homologized with bone of attachment as per Osborn, 1984) produced during socket ontogeny. We suggest considering acrodont and pleurodont dentitions as highly modified thecodont attachment geometries, with these geometries resulting from qualitative and quantitative modifications of the primitive condition of thecodont attachment tissues. Conceptualizing squamate dentitions in this manner becomes a more useful and informative explanation of the apparently homoplastic distribution of squamate acrodonty and pleurodonty. We find we are in agreement with Gaengler (2000: 173) who notes that, ‘‘. . . the traditional classification of tooth attachment into three types (acrodont, pleurodont, and thecodont) does not fully reflect the biological variations encountered. A great variety of direct union of tooth to bone (ankylosis) and fibrous tooth attachments is detectable in the classes of agnatha, chondricthyes, osteichthyes, amphibia, reptila, and mammalia [sic].’’ ACKNOWLEDGMENTS For consultation, technical assistance, and reading various drafts of manuscripts, we thank R. Day, R. Gault, the late J. van Velthuizen, E. Peters, M. Eggert, G. Hanke, D. Carmel, M. Lee, J. Scanlon, N. Hiller, R. Holmes, S. Cumbaa, A. Murray, A. Nicholson, R. Nydam, K. Shepherd. We acknowledge financial support from a Canadian Museum of Nature, Research Advisory Council Grant and from an NSERC Operating Grant 238458-01 to MWC. LITERATURE CITED Berkovitz, B. K. B., and P. Sloan. 1979. Attachment tissues of the teeth in Caiman sclerops (Crocodilia). Journal of Zoology, London 187: 179–194. ———, G. R. Holland, and B. J. Moxham. 1992. A Color Atlas and Textbook of Oral Anatomy, 2nd ed. Mosby Year Book, St. Louis, 247 pp. Caldwell, M. W. 1999. Description and phylogenetic relationships of a new species of Coniasaurus Owen, 1850 (Squamata). Journal of Vertebrate Paleontology 19:438–455. ———, and J. Cooper. 1999. Redescription, palaeobiogeography, and palaeoecology of Coniasaurus crassidens Owen, 1850 (Squamata) from the English Chalk (Cretaceous; Cenomanian). Zoological Journal of the Linnean Society 127:423–452. Carlson, S. 1990. Vertebrate dental structures; pp. 531–554 in J. G. Carter (ed.), Skeletal Biomineralization: Patterns, Processes and Evolutionary Trends. Van Nostrand Reinhold, New York. Edmund, A. G. 1960. Tooth replacement phenomena in the lower vertebrates. Royal Ontario Museum, Life Sciences Contributions 52: 1–190. Estes, R., T. H. Frazzetta, and E. E. Williams. 1970. Studies on the fossil snake Dinilysia patagonica Woodward: Part 1. Cranial morphology. Bulletin of the Museum of Comparative Zoology, Harvard 140:25–74. Freeman, E., A. R. Ten Cate, and H. R. Mills. 1975. Development of a gomphosis by tooth germ implants in the parietal bone of the mouse. Archives of Oral Biology 20:139–140. Gaengler, P. 2000. Evolution of tooth attachment in lower vertebrates to tetrapods; pp. 173–185 in M. F. Teaford, M. M. Smith, and M. W. J. Ferguson (eds.), Development, Function and Evolution of Teeth. Cambridge University Press, Cambridge.


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Lee, M. S. Y. 1997. On snake-like dentition in mosasaurian lizards. Journal of Natural History 31:303–314. Leidy, J. 1865. Cretaceous reptiles of the United States. Smithsonian Contributions to Knowledge 192:1–135. Osborn, J. W. 1984. From reptile to mammal: evolutionary considerations of the dentition with emphasis on tooth attachment. Symposium of the Zoological Society of London 52:549–574. Owen, R. 1840. Ondontography. Bailliere, London, 655 pp. Peyer, B. 1968. Comparative Odontology. The University of Chicago Press, Chicago, 347 pp. Reid, R. E. H. 1996. Bone histology of the Cleveland-Lloyd dinosaurs and of dinosaurs in general, part 1: Introduction: Introduction to bone tissues. Brigham Young University, Geological Studies 41: 25–71. Shellis, R. P. 1982. Comparative anatomy of tooth attachment; pp. 3– 24 in B. K. B. Berkovitz, B. J. Moxham, and H. N. Newman (eds.), The Periodontal Ligament in Health and Disease. Pergamon Press, Oxford.

Ten Cate, A. R. 1976. Development of the periodontal membrane and collagen turnover; pp. 281–289 in D. F. G. Pode and M. V. Stack (eds.), The Eruption and Occlusion of Teeth. Butterworths, London. ——— 1989. Oral Histology: Development, Structure, and Function, 3rd ed. The C.V. Mosby Company, St. Louis, 497 pp. ———, and H. R. Mills. 1972. The development of the periodontium: the origin of alveolar bone. Anatomical Records 173:69–77. Tomes, C. S. 1898. A Manual of Dental Anatomy: Human and Comparative, 5th ed. J. and A. Churchill, London, 596 pp. Zaher, H., and O. Rieppel. 1999. Tooth implantation and replacement in squamates, with special reference to mosasaurs lizards and snakes. American Museum Novitates 3271:1–19. ———, and ——— 2002. On the phylogenetic relationships of the Cretaceous snakes with legs, with special reference to Pachyrhachis problematicus (Squamata, Serpentes). Journal of Vertebrate Paleontoogy 22:104–109. Received 27 April 2001; accepted 17 June 2002.


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