Journal of Vertebrate Paleontology The microstructure

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Journal of Vertebrate Paleontology

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The microstructure of enamel, dentine and cementum in advanced Taeniodonta (Mammalia) with comments on their dietary adaptations

Wighart Von Koenigswalda; Daniela C. Kalthoffb; Gina M. Semprebonc a Steinmann Institut (Paläontologie) der Universität Bonn, Bonn, Germany b Department of Paleozoology, Swedish Museum of Natural History, Stockholm, Sweden c Department of Biology, Bay Path College, Longmeadow, Massachusetts, U.S.A. Online publication date: 02 December 2010

To cite this Article Von Koenigswald, Wighart , Kalthoff, Daniela C. and Semprebon, Gina M.(2010) 'The microstructure of

enamel, dentine and cementum in advanced Taeniodonta (Mammalia) with comments on their dietary adaptations', Journal of Vertebrate Paleontology, 30: 6, 1797 — 1804 To link to this Article: DOI: 10.1080/02724634.2010.521931 URL: http://dx.doi.org/10.1080/02724634.2010.521931

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Journal of Vertebrate Paleontology 30(6):1797–1804, November 2010 © 2010 by the Society of Vertebrate Paleontology

ARTICLE

THE MICROSTRUCTURE OF ENAMEL, DENTINE AND CEMENTUM IN ADVANCED TAENIODONTA (MAMMALIA) WITH COMMENTS ON THEIR DIETARY ADAPTATIONS WIGHART VON KOENIGSWALD,*,1 DANIELA C. KALTHOFF,2 and GINA M. SEMPREBON3 ¨ ¨ Bonn, Nussallee 8, D–53115 Bonn, Germany, [email protected]; Steinmann Institut (Palaontologie) der Universitat 2 Swedish Museum of Natural History, Department of Paleozoology, Box 50007, SE–104 05 Stockholm, Sweden, [email protected]; 3 Department of Biology, Bay Path College, Longmeadow, Massachusetts 01106, U.S.A., [email protected]

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ABSTRACT—The cheek teeth of Ectoganus and Stylinodon, the most derived genera of Taeniodonta following recent phylogenies, show various morphological and microstructural characteristics that are unusual for herbivores of their size. Their continuously growing premolars and molars have blunt occlusal surfaces without shearing facets and enamel is restricted to the lingual and buccal sides of the teeth. The anterior and posterior walls of the teeth are covered with a thick layer of cementum to which the periodontal ligament is attached. The enamel band is relatively thin. The schmelzmuster is one-layered and features weakly developed Hunter-Schreger bands that are only recognizable in longitudinal section. In cross-section, the enamel prisms show a ‘keyhole pattern’ with an incomplete prism sheath. There is no interprismatic matrix. The microstructure of the dentine has the regular mammalian pattern and shows no special similarity to that of xenarthrans. Taeniodonts seem to have used their hypsodont cheek teeth almost exclusively for squeezing and some crushing of food and only to a minor degree for grinding. Weakly developed Hunter-Schreger bands indicate only light loading during mastication.

INTRODUCTION Taeniodonta are an enigmatic order of mammals that occurred in North America from the early Paleocene to the middle Eocene. Taeniodont remains are always very rare, but during the thermal maximum of the Wasatchian-0 faunal zone (between the Clarkforkian and the Wasatchian Land Mammal ages) fossils of Ectoganus are relatively abundant (Gingerich, 1989). They had a relatively clumsy body shape and later representatives show large, laterally compressed claws, indicating adaptations for digging. Compared with contemporary herbivores, taeniodonts attained a remarkably large body size in the Paleocene and evolved unusual dental adaptations during the Eocene (Fig. 1). The phylogeny of taeniodonts and their relationship to cimolestids was studied by Patterson (1949), Schoch (1986), and Eberle (1999). In the Paleocene, two groups occurred. The more conservative conoryctids of the early Paleocene were relatively small and are of significance here mainly because their lowcrowned molars retain some similarities to the tribosphenic pattern of primitive mammals. The rapidly evolving stylinodontid lineage extended from the Paleocene to the middle Eocene, including Wortmania in the Puercan and Psittacotherium in the Torrejonian. For its time, Psittacotherium was one of the largest mammals (Matthew, 1937; Schoch, 1986). These earlier stylinodontids are characterized as having lowcrowned premolars and molars but continuously growing canines with enamel only on the anterior surface. The incisors, especially the lower ones, became small and they formed a functional unit for cutting together with the canines and the first premolars (Coombs, 1983). During the subsequent stages (i.e., Tiffanian, Clarkforkian, and Wasatchian), two species of Ectoganus occur. Both have hypsodont but rooted molars with crown cementum. The latest known taeniodont genus is Stylinodon, which is known mainly from the late Wasatchian, Bridgerian, and Uintan (Schoch and Lucas, 1981; Schoch, 1986). The dentition of *Corresponding

author.

Stylinodon reached the highest degree of specialization. Instead of only the canines, all teeth became rootless and ever-growing (Fig. 1A). Thus an intensive abrasion of the teeth by a coarse diet was compensated by continuous growth. Taeniodonts are one of the first groups developing euhypsodont cheek teeth and crown cementum (White, 1959). In contrast to many herbivores of other orders, the morphology of taeniodont molars became simplified during evolution (Fig. 1E). Most mammals with distinctive molar and/or incisor morphologies show some specialization in their enamel microstructure. Thus we investigated taeniodont enamel, dentine, and cementum in the genera Ectoganus and Stylinodon. The aims of this study are (1) to describe the arrangement and microstructure of tooth tissues in comparison to those of other mammals; and (2) to discuss the functional aspects as well as the modifications during phylogeny. The specific tooth morphology and the possible mode of life of advanced taeniodonts (Eberle, 1999) have been compared with xenarthrans (Wortman, 1897), tubulidentates, and wombats (Schoch, 1986). Thus we will give some comments on the dental structures of these groups for comparison.

MATERIALS AND METHODS The analyzed specimens were generously made available from the collections of the Museum of Paleontology, University of Michigan (UM); the National Museum of Natural History, Smithsonian Institution; Department of Paleobiology, Washington, D.C. (USNM and USGS Denver collection at USNM); and of the Peabody Museum of Natural History, Yale University (YPM). Resulting preparations are deposited in the enamel collection (KOE) of the Steinmann Institute, Department of Palaeontology of the University of Bonn, Germany. Material Examined Ectoganus sp. (YPM 22870), tooth fragment, Wasatchian, Willwood Fm., Willwood locality 16, Big Horn County, Wyoming,

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FIGURE 1. Taeniodont dentition. A–C, Isolated tooth of Stylinodon mirus (USNM V 16664) from the Bridgerian in Wyoming. A, aspect of the cementum-covered anterior or posterior side. B, occlusal surface; and C, same tooth in enlarged oblique aspect showing the curved surface with the thin enamel band on the lingual and buccal side. Observe that there are multiple cracks in the dentine which should not be mistaken as structures or tissue junctions. D, sketch of a cross-section of an isolated tooth of S. mirus (KOE 4074), showing the distribution of the enamel on the buccal and lingual side and that of the cementum on the anterior and posterior inside. E, dentition of Stylinodon mirus, upper and lower dentition in occlusal view (modified from Turnbull, 2004). (c = cementum; d = dentine; e = enamel)

KOE 2778a and b; Ectoganus sp. (YPM 18618), tooth fragment, Wasatchian, Willwood Fm., S 16 T47N R91W, Washakie County, Wyoming, KOE 2779; and Ectoganus sp. (USGS 21966), various tooth fragments, Wasatchian, Willwood Fm., Willwood locality D-1710, Big Horn County, Wyoming, KOE 4101. Stylinodon mirus (UM 95698), molar fragment, Bridgerian, locality BB020, Lincoln County, Green River Basin, Wyoming, KOE 4074; and Stylinodon mirus (USNM V16664), three molars, Bridgerian, Bridger Basin, Wyoming. Abbreviations—EDJ, enamel-dentine junction; HSB, HunterSchreger bands; IPM, interprismatic matrix; OES, outer enamel surface; PLEX, prismless external enamel; SEM, scanning electron microscope.

Methods During the preparation of teeth for enamel microstructure analysis, an entire tooth or sometimes only a fragment is taken. For easier handling, the specimen is embedded in epoxy resin and, after hardening, cut in transverse and longitudinal sections. The next stages involve grinding and polishing with 1200 corundum powder and subsequently 2–5 seconds of etching with 2 N HCl to make the enamel details visible. After ultrasonic cleaning with distilled water, the specimen is mounted on an SEM stub and sputter coated with gold (ca. 3 minutes). The teeth were studied and digitally documented with a CAMSCAN MV 2300 and a Hitachi S-4300 at an acceleration voltage of 15 kV and at magnifications from 30× to 8000×. Throughout the text, we distinguish low-crowned (= brachydont) teeth from high-crowned ( = hypsodont) teeth and the lat-

ter from continuously growing (= euhypsodont or hypselodont) teeth (Mones, 1982). DESCRIPTION AND COMPARISON OF TOOTH MORPHOLOGY AND THE MICROSTRUCTURE OF THE TOOTH TISSUES Tooth Morphology and Distribution of Enamel and Cementum Paleocene-Eocene Taeniodonta are considered to be related to the Late Cretaceous cimolestid mammals (Eberle, 1999). In Paleocene taeniodonts, Onychodectes retained more or less a trituberculate and low-crowned tooth morphology. In the stylinodotines, Wortmania and later Psittacotherium have more hypsodont premolars and molars and a rather complicated morphology of the unworn occlusal surface (Schoch, 1986). The cheek teeth of advanced taeniodonts like those of Ectoganus and Stylinodon were subjected to intensive abrasive wear. During the late Paleocene and early Eocene, Ectoganus developed hypsodont molars with a complicated pattern of little cusps on the unworn occlusal surface. Turnbull (2004) assumed that the molars may have been bilophodont before hypsodonty was achieved. In slightly worn teeth of Ectoganus, the enamel band surrounds the entire tooth, but its lower margin is uneven, due to initial dentine tracts. Thus with progressive abrasion, dentine tracts occur on the anterior and the posterior side. Patterson (1949) described and figured an asymmetry of the enamel distribution in Ectoganus molars: the enamel reaches farther down towards the root on the buccal side of lower and on the lingual side of upper cheek teeth. Patterson (1949) and White (1959) mentioned that crown cementum was on the molars of Ectoganus.


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FIGURE 2. SEM images of the tooth enamel microstructure of Stylinodon mirus (KOE 4074) and Ectoganus sp. (KOE 2778). A, contact of dentine (bottom left) with enamel (right) and cementum (left). The cementum covers the enamel free area and overlaps the enamel only marginally in Stylinodon; B, cross-sections of enamel prisms in Stylinodon. Note the open prism sheath and the notch separating the prism into two fields; C, longitudinal section of the enamel of Stylinodon showing the prisms vanishing in the PLEX near the OES (right margin of image) and Retzius lines (R); D, cross-section of enamel prisms in Ectoganus. Prisms have the same morphology as those in Stylinodon but do not show a notch and are slightly larger.

Cementum covers the dentine tracts but overlaps the enamel only marginally. Stylinodon developed continuous growth at all tooth positions (Schoch, 1986). Thus the initial surface is functionally of minor significance, because it is worn away in euhypsodont dentitions. When an initial crown enamel cap is worn away, the enamel in Stylinodon is also restricted to lingual and buccal bands separated by wide dentine tracts on the anterior and posterior side (Fig. 1B–E). The enamel-free area is covered throughout the entire height by a thick layer of cementum overlapping the enamel only marginally (Figs. 1D, 2A). Enamel Prisms and the Lack of Interprismatic Matrix The enamel of Stylinodon and Ectoganus is prismatic (Fig. 2B, D). The prisms start near the EDJ, rise towards the occlusal plane, and disappear close to the OES in prismless external enamel (PLEX) (Fig. 2C). In Ectoganus, the cross-section of the prisms as seen in transverse sections is characterized by an incomplete prism sheath,

which opens in a cervical direction. The prisms are arranged as alternating in lateral rows as in Boyde’s Pattern 3 (Boyde, 1976; Martin and Boyde, 1984; Koenigswald and Sander, 1997). The space between neighboring prisms belongs to the tail-like appendix of the prism in the next row. Thus, no interprismatic matrix (IPM) can be identified. The prism size of Ectoganus (KOE 2778) is measured between 5 and 7 µm. Stylinodon shares its prism type with Ectoganus. But in our sections, almost all prisms show a distinct notch cutting axially into the prism body from the apex of the prism sheath almost to the base of the prism (Fig. 2B). Thus the prism body is separated into two fields of diverging crystallites. The notch seems to be related to the inclination of the crystallites rather than being an artifact from etching. The observed structure differs from the ‘seam’ as described by Lester and Koenigswald (1989), for the seam is on the tail side of the prism where the prism sheath is open. The enamel of Ectoganus lacks such a notch (Fig. 2D). The diameter of enamel prisms was measured in Stylinodon from transverse and longitudinal sections, and it varies between 4 and 6 µm.



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FIGURE 3. SEM images of enamel microstructure (A–C), dentine microstructure (D), and diagenesis (C, E–F) in the enamel in Stylinodon mirus (KOE 4074) and Ectoganus sp. (KOE 2778). A, longitudinal section through the enamel band of Stylinodon showing the weakly developed HSB; B, longitudinal section (close up) of another part of the enamel in Stylinodon showing HSB in more detail. The HSB are characterized by thick, alternating layers of prisms seen either more across sectioned or more in longitudinal aspect. C, longitudinal section through the enamel band of Ectoganus showing the weakly developed HSB. Note the slightly undulating diagenesis front in the outer half of the enamel; D, detail of the dentine microstructure in Ectoganus close to the EDJ. The longitudinal section shows dentine tubules with fossilized odontoblastic processes sticking out; the short collagen fibers of the dentine matrix are oriented roughly perpendicular to the long axis of the tubules. E–F, enamel modified by diagenesis in Stylinodon; E, prism sheath is well visible (black gap) but crystallites are fused due to re-crystallization; F, crystallites are well visible but the prisms sheath is indicated either by a gap (lower left corner) or preserved as a prominent rim (upper right area). The SEM image shows the narrow distances of different preservation states of minor details in the enamel.

KOENIGSWALD ET AL.—TOOTH MICROSTRUCTURES IN TAENIODONTS


The Schmelzmuster The possible combination of different enamel types, defined as schmelzmuster, can be investigated best from longitudinal sections. The molars of Ectoganus and Stylinodon have a onelayered schmelzmuster. In Ectoganus, the prisms rise from the EDJ initially with an angle of about 40◦ , but this angle is less with increasing distance from the EDJ. Prisms do not reach the OES but disappear near the outer surface in a prismless enamel (PLEX). The PLEX is not more than 10% of the enamel thickness, which varies between 700 and 800 µm (measured from cross-sections). The longitudinal sections show some groups of prisms in tangential aspect, others in oblique aspect. These groups form layers of different prism orientation stacked upon each other. Although this is not the most typical alternating pattern, it represents Hunter-Schreger bands (HSB) (Fig. 3A–C). They also become visible as light and dark bands when the outside of the tooth is illuminated very intensively from one side. The Stylinodon enamel is basically similar. The thickness of its enamel is between 390 and 500 µm. The prisms rise at an angle of about 35◦ from the EDJ. This angle becomes slightly lower with increasing distance from the EDJ. In the outermost 10% of the enamel thickness, the prisms irregularly fade out in a PLEX (Fig. 2C). Stylinodon shows similarly weak decussation between HSB as in Ectoganus. In some parts of the vertical sections, they can be differentiated only by the different gray scale. However, when well illuminated from the outside, the light and dark coloring becomes visible, indicating prism layers with different orientations. In contrast to the weak decussation in the HSB in Ectoganus and Stylinodon, the prism directions of adjacent bands in typical HSB often approach an angle of 90◦ , and thus the picture in the SEM is more obvious. Due to the low angle, the appearance of the HSB in Ectoganus and Stylinodon varies and often they are difficult to detect, even in longitudinal sections. The light and dark coloring, however, differentiates bands even when the angle of decussation is minor. Thus faint HSB are present in advanced taeniodont cheek teeth (Fig. 3A–C). The thickness of the HSB is quite large but varies greatly and is not easy to evaluate because the angle changes gradually between bands (Fig. 3A). From the SEM images, we counted a thickness of 10 to 20 prisms per band as a rough average. Despite the thin PLEX, the enamel of Stylinodon and Ectoganus is best described as a one-layered enamel with HSB. Teeth of Stylinodon and Ectoganus show slightly undulating perikymata on the enamel surface as a typical incremental structure. They are not related to the HSB, but show the same transverse orientation. The width of the perikymata is on average 146 µm (mean of 10 individual measurements on Ectoganus). The perikymata are related to steeply inclined striae of Retzius, which are visible in longitudinal sections close to the OES (Fig. 2C). The Dentine The hypsodont cheek teeth of Ectoganus, and particularly the euhypsodont teeth of Stylinodon, are characterized by high dentine tracts. As soon as the dental cap is worn off, enamel covers only the lingual and buccal side of the tooth. On the mesial and distal side, dentine and crown cementum make up the tooth walls (Fig. 1A–D). The dentine type in Ectoganus and Stylinodon is exclusively orthodentine that is also occurring in all other mammals including xenarthrans. Orthodentine is a dentine tissue showing dentinal tubules but no vascularization. It contains approximately 20 vol% of collagenous proteins (Carlson, 1990). In taeniodonts, the orthodentine shows the typical mammalian construction (Fig. 3D): its microstructure shows subparallel dentinal tubules in a more or less homogenous dentine matrix. Dentinal tubules are quite evenly distributed and measure between 2 and 3 µm in diameter.

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In the living tooth, the tubules contain among other things dentinal fluid and the odontoblastic process. In fossil teeth, the odontoblastic process is regularly preserved as a calcified, often empty tube sticking out from most tubules (Fig. 3D). The tube shows the former position, size, and morphology of the odontoblastic process and therefore allows us to study it also in fossil taxa. The odontoblastic process measures between 0.5 and 1 µm in diameter. The dentine matrix features abundant fibers, which are short and oriented roughly perpendicular to the long axis of the tubules. They most probably represent the former collagen fibers now mineralized during fossilization. Being a rather porous tissue, the orthodentine in both taxa is quite heavily affected by diagenesis. This results in an uneven and irregular to almost foamy microstructural appearance (Fig. 3D). After the animals’ death, the tubules often act as conduits for diagenetic fluids during fossilisation. A different investigation by one of the authors (D.K.) shows that the microstructure of the orthodentine is different in xenarthrans than in taeniodonts and other mammals. This provides additional and independent evidence that taeniodonts are not related to xenarthrans, a relationship, which was emphasized earlier by Wortman (1897), but rejected by later authors. The Cementum Patterson (1949) and White (1959) already noted the cementum in advanced Taeniodonta. It is restricted to the dentine tracks and overlaps the enamel only marginally. The cementum reaches a thickness of 470 µm in Ectoganus. Thus it is comparably thinner than the enamel band. The structure of the cementum is highly altered by diagenesis and thus cannot be described. In Stylinodon, cementum forms a thick layer on the mesial and distal side of the tooth covering the dentine tracts but not the enamel. The cementum measures between 500 and 760 µm and is thicker than the enamel band. There is only a slight overlap on the enamel at the margin (Figs. 1B, 2A). Only in Stylinodon can potential locations of typical features like cementocytes and passages for blood vessels be presumed. Some straight canals of about 20–30 µm in cross-section in more or less a radial direction were seen in the 3D Micro CT model of a Stylinodon tooth. No incremental lines could be detected. Diagenesis of Tooth Tissues in the Studied Taeniodonta Fossil enamel preserves structural details only when diagenesis is minor. In cases with severe diagenesis, all structures are eliminated, but no new misleading microstructures are generated. The tooth enamel of the studied specimen of Stylinodon shows some slight alteration due to postmortem diagenesis during fossilization (Fig. 3E–F). In most parts, the crystallites of the prisms are visible, but in some areas, the individual crystallites are fused together to a uniform matrix with a somewhat foamy appearance (Fig. 3E). We assume this is due to some kind of recrystallization. It is conspicuous that in these areas, the prism sheaths are well visible and occur (after etching) as gaps. In other parts of the same section, the prisms sheaths might have become more resistant to etching and thus form a distinct collar (Fig. 3F). The different preservation might occur in closely related regions, but we do not know the cause. The longitudinal section of Ectoganus shows similar diagenetic modifications of the enamel (Fig. 3C). The outer part is altered in a way highlighting the striae of Retzius and opening the prism sheaths. The altered area is surrounded by a seam of condensed enamel without structure. Areas with prism sheaths alternate occurring as gaps or as surrounding collars. Despite the diagenetic alterations, the tooth enamel microstructure can be reconstructed reliably down to the prism level in both taxa. The dentine and the cementum are also modified in their microstructure by diagenesis. The modifications are very obvious

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and much more profound than in the enamel. Dentine and cementum are generally prone to diagenetic alterations because they contain dentinal tubules and passages for blood vessels, respectively. A detailed investigation of the occlusal surfaces has indicated that these diagenetic alterations (e.g., recrystallization) might have affected surface micromorphology, leaving behind a complicated mixture of use wear traces and diagenetic modifications. This aspect is currently the subject of additional study by the authors in a separate paper. DISCUSSION


The Tooth Tissues Enamel—The enamel of Stylinodon shows some distinct characteristics on the prism level. An incomplete prism sheath occurs in many primitive mammals (Wood, 1992), especially when combined with plenty of IPM, e.g., in multituberculates (Carlson and Krause, 1985), in early primates, and in carnivores (Koenigswald, 1997). The prisms in Stylinodon are carefully arranged in regular lateral rows. The Pattern 3 in Boyde’s classification occurs in more derived primates and in proboscideans and is often called a ‘keyhole pattern’ or ‘ginkgo-tree-leaf-pattern’ (Kozawa, 1978; Koenigswald and Sander, 1997). Thus, this prism type was developed several times as a homoplasy. In Stylinodon, the apical incision of the prisms separates the prism body to some degree (Fig. 2B). This creates some superficial similarity to the bilobate prism cross-section in some proboscideans (Ferretti, 2003), but the proboscidean prisms are generally wider than deep. The densely packed prisms of Boyde’s Pattern 3 are not surrounded by an interprismatic matrix (IPM). This is an uncommon character and the lack of IPM is interpreted as a more derived stage. Prisms are surrounded by an IPM in most other mammalian taxa including many Mesozoic species (e.g., Carlson and Krause, 1985). There, the crystallites of the IPM usually form a large angle with the prisms and thus strengthen the enamel like a plywood structure (Koenigswald, 1997). The diameter of prisms as measured in Stylinodon of about 5 µm is regarded as average sized (Ten Cate, 1998), but in most small mammals, like rodents, common prism diameters are 2–3 µm and thus much smaller (Kalthoff, 2000). At the schmelzmuster level, the enamel of advanced taeniodonts is characterized by weakly developed Hunter-Schreger bands (HSB). HSB evolved multiple times among the various mammalian groups during the Paleocene and Eocene as reinforcement against cracking (Koenigswald, 1997). Their earliest occurrence so far has been found in the condylarthran Conacodon of the early Paleocene (Koenigswald et al., 1987). The occurrence of HSB seems to be linked to increasing body weight (Koenigswald et al., 1987), with HSB appearing at a body weight of roughly 2 kg. However, the dwarfed primates from South America and especially rodents are exceptions having welldeveloped HSB at much smaller body sizes. The presence of HSB in Ectoganus and Stylinodon fits into that scheme; however, the poor development of the HSB is exceptional for animals of such a large body size and stratigraphical age. The possible explanation might be the lack of shearing blades in the cheek teeth of Ectoganus and Stylinodon. This is in contrast to most other Eocene herbivores, and thus the enamel was not loaded in the same way during mastication. However, the properties of the enamel in taeniodonts were sufficient despite the large body size and presumable large food intake. No selective pressure required better developed HSB as in other mammals of the same size and age that developed shearing blades in their dentitions. Dentine—Dentine makes up the largest part of the tooth tissues. Microstructurally, it can be characterized as a regular mammalian orthodentine. Subparallel dentinal tubules are embedded

in a matrix consisting of intertubular dentine with fibers extending perpendicular to the long axis of the tubules. Inside the dentinal tubules another set of tubes can be seen. They represent the odontoblastic processes, which are preserved in the taeniodont teeth as thin, mineralized tubes of calcium phosphate. The preservation is that detailed that even the delicate side extensions of the odontoblastic process are visible. This is in contrast to the intertubular dentine matrix, which is partly highly altered by diagenesis. The dentine build-up shows no similarities to xenarthran orthodentine, which features a more complex internal structure. There is also no other dentinal tissue like vaso- or osteodentine present. Cementum—The crown cementum is well developed in taeniodonts and was listed as one of the earliest occurrences in mammalian dentitions (Patterson, 1949; White, 1959). Crown cementum occurs distinctly later such as in stem lagomorphs like the middle Eocene genus Gobiolagus (Meng et al., 2005). The main function of the cementum is assumed to provide a porous ground for the attachment of the periodontal ligament (Keil, 1966; Ten Cate, 1998). This is especially required in hypsodont teeth where the Sharpey’s fibers cannot attach on the shiny enamel. The distribution of cementum in Ectoganus and Stylinodon does not really match this simplified model. Cementum covers not the enamel but the enamel-free area, which is formed by the dentine tracts on the mesial and the distal sides of the teeth. Thus the possible area for the attachment of the periodontium is not enlarged by the presence of cementum. In contrast, the periodontal ligament would have had almost the same area for attachment without cementum. Thus the invention of the cementum did not have this specific adaptive value. Nevertheless, the cementum presumably indicates the position of the periodontal ligament holding the euhypsodont teeth in position. Mastication The special dentition of Stylinodon inspires a reconstruction of the mastication pattern. Schoch (1986:143) reconstructed the musculature and postulated a two-phase mastication pattern for this genus. A first phase in which the mandible moves slightly forward is followed by a second phase, in which the tooth row of the mandible crosses that of the upper dentition. Turnbull (2004:312) rejected this model and argued for an “orthal or weakly propalinal” power stroke in Stylinodon. He regards the enamel bands on the buccal and lingual sides as too thin to withstand a lateral phase of the power stroke. He compared this taeniodont with the modern tree sloth genera Bradypus and Choloepus. We agree that the alternating arrangement of mandibular and maxillary teeth resembles those in tree sloths (Naples, 1982, 1995) and both groups share the spacing of the cheek teeth. But in contrast, tree sloths show an anteromedially directed power stroke as well as distinct attrition facets (Naples, 1982). In the limited material we studied, we did not see facets indicating a lateral phase of the power stroke. On the enamel and the dentine, transversely oriented striae are visible, indicating somewhat transverse movement of the mandible. But this was certainly not very intensive because we observed smooth margins without any noteworthy step between enamel and dentine as well as between dentine to cementum. A more intensive and directed pressure would have caused a differentiated abrasion between dentine and enamel on the occlusal surface (Greaves, 1973). We therefore follow Turnbull (2004) in assuming a one-phase power stroke directed more or less orthally, at least for Stylinodon. This is a noteworthy functional difference compared to the dentition of most perissodactyls of that time and most of the later artiodactyls. Schoch (1986) stressed that Stylinodon is unisognath, which means the tooth rows of the mandible are closer together than those of the maxillae. Thus Stylinodon most probably chewed


KOENIGSWALD ET AL.—TOOTH MICROSTRUCTURES IN TAENIODONTS only on one side at a time, which is common in mammals. Thus we assume low bite pressure during the orthal power stroke. The poorly defined power stroke might have evolved early in the taeniodont lineage. Alveugena, a mammal related to early taenidontids from the transition from Lancian to Puercan as a sister group of Onychodectes (Eberle, 1999), has flat worn cusps in the tribosphenic upper molars and premolars. The assumed mastication pattern for Ectoganus and Stylinodon differs distinctly from that in the marsupial Vombatus. The wombat shares the euhypsodont cheek teeth with these taeniodonts but has thick enamel on the buccal side in lower check teeth and the lingual side in uppers. This resembles to some degree the enamel distribution in old individuals of Ectoganus, as described and figured by Patterson (1949:fig. 3F). But in contrast to stylinodontids, this one-sided enamel was preserved in vombatids and extended in the euhypsodont teeth. Striations show clearly, that the thick enamel acts during a powerful lateral movement of the jaw as a shearing blade. The position of the antagonistic blades is a good example for the pattern of functional symmetry (Koenigswald et al., 1994) not present in any taeniodont. Paleodiet The diet of the stylinodontids has been interpreted in various ways by previous workers. Based on the peculiar tooth morphology and the large claws, Patterson (1949) was among the first proposing hard object feeding (e.g., nuts, hardshelled fruits) for advanced Taeniodonta. On the other hand, McKenna (1980) compared taeniodonts to aardvarks. Coombs (1983:73) concluded that taeniodonts have a large number of digging and tearing adaptations and relatively few adaptations associated with bipedal browsing. The dentition and skull suggest that the diet consisted probably of tough and/or fibrous food. More complete fossil material was available to Schoch. He (1986:193) summarized the lifestyle of stylinodontids as “fossorial to subfossorial rooters and grubbers, feeding on vegetable matter much of which took the form of underground roots and tubers.” Recently Turnbull (2004) assumed that the large claws of taeniodonts were used for digging burrows. He (2004:331) interpreted the peculiar arrangement of the lower canine and the lower first premolar (Fig. 1E) as a “unique leaf stripping mechanism.” Based on this and the smoothly worn occlusal surfaces, he suggested that stylinodontids fed on “leaves, bark and berries” and more general “fleshy, pulpy and fibrous foods.” We cannot assume that the type of vegetation that was available for taeniodonts in the Eocene is necessarily the same as what is available to ungulates today. Although a detailed dental microwear analysis is not possible at this time due to the above-described diagenetic modifications of the enamel surface, some conclusions can be drawn from the analysis of the occlusal surface morphology. Most browsers among extant artiodactyls and perissodactyls show distinct wear facets (due to toothon-tooth contact when cheek teeth cut completely through soft foods) and well-defined jaw movements during the mastication cycle. Also, the dentitions of browsers are typically characterized by low-crowned teeth because abrasion is limited. Thus, the relatively hypsodont dentition (euhypsodont in Stylinodon), which lacks attritional wear facets, does not fit into the traditional interpretation. Also, an increasing crown height in stratigraphically younger or recent taxa is often taken as a proxy for an increasingly abrasive diet, meaning that the transition from brachyodont to hypsodont dentition is often assumed to indicate an increasing amount of grazing in the diet (e.g., Janis et al., 2000). However, it has become increasingly clear lately that this correlation between hypsodonty and grazing is too simplistic. For example, dust and grit-contaminated food is regarded as a major factor in the evolution of high-crowned teeth (e.g., in horse evolution—Solounias and Semprebon, 2002; in oreodont

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evolution— Mihlbachler and Solounias, 2006; Semprebon and Drewniak, 2008; in camel evolution—Semprebon and Rivals, 2010; and in biomechanical studies of the hardness index of grass phytoliths in relation to dental enamel—Sanson et al., 2007). Taeniodonts evolved during the Paleocene-Eocene when the climate was much warmer and more humid than today and tropical rainforest with low seasonality was the predominant ecosystem (Rose, 2006). Thus, neither grasses nor a great amount of dust correlates with the evolution of the (eu)hypsodont dentition in advanced taeniodonts and the trigger for this evolution remains unsolved. Nevertheless, the hypsodont dentition in Ectoganus and the euhypsodont dentition in Stylinodon, as well as the manner of toothwear indicate a very high abrasion diet in taeniodonts. One theoretical solution would be that the intensive abrasion might be caused by grit intake when feeding on roots or tubers as proposed by Schoch (1986). Large, massive claws and other postcranial specializations argue for digging activities at least in Stylinodon (Coombs, 1983; Turnbull, 2004). Root feeding was already discussed (and rejected) by the latter author with whom we agree according to the analysis of the molar occlusal surfaces. The enamel surfaces of Ectoganus and Stylinodon are very smooth and pristine and lack the rather chewed up and gouged surface topography noted by Solounias and Semprebon (2002) in rooting pigs as well as the large pits, gouging, and coarse scratching seen in heavy grit consumers. The rounded edges of the enamel band would indicate a very coarse type of browse as well as a fair degree of crushing during mastication. Another cause for the intensive wear seen in taeniodonts might be the quality of the teeth themselves. The enamel is fairly thin and seems to become even somewhat thinner during evolution between Ectoganus and Stylinodon. Euhypsodonty means an increasing tooth eruption and a greater abrasion. Thus the dentine carries the main load of breaking down the food particles. The functionality of the taeniodont dentition shows that there was an efficient equilibrium between amount and quality of tooth materials and the abrasion—at least in Paleocene and Eocene environments. However, in taeniodonts, no indication of a trend becomes visible for a differentiation of the dentine, as in toothed xenarthrans or in the tillodont Chungchienia (Chow et al., 1996). Although the exact nature of the type of abrasive browse remains unknown, an analysis of the molar surfaces does reveal certain aspects regarding paleodietary habits; however, results are preliminary and further study is planned. The analysis reveals that at least some taeniodonts most likely engaged in some hard object feeding. One of the three specimens of Ectoganus sp. displays very large (between 0.03 and 0.1 mm in diameter) and symmetrical puncture-like pits seen thus far only in extant hard fruit and/or seed consumers (Solounias and Semprebon, 2002; Semprebon et al., 2004). With their relatively low-slung bodies and large claws and digging adaptations, it is probable that any fruits consumed would be either fallen fruits or underground fruits such as those consumed regularly by the aardvark for their water content. One thing is clear—taeniodonts clearly had an unusual diet and most likely one with more variability than most ungulates analyzed thus far. CONCLUSION The teeth in the advanced taeniodont genera Ectoganus and Stylinodon show some interesting combination of opposing features. The euhypsodonty of the entire dentition in Stylinodon indicates a diet causing intensive abrasion and possible hard object feeding. This is in contrast to the more soft browse feeding interpretation of Turnbull (2004) deduced from dental morphology. The teeth are blunt and show no attritional facets. This means that the jaw movement was not well defined, which is supported by the high number of cross-scratches on the enamel band. The

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enamel is limited to the buccal and lingual side but seems not to function as a shearing blade. The enamel is thin and HunterSchreger bands are only weakly developed. Thus, despite the high abrasion, the loading of the enamel during mastication was quite low.


ACKNOWLEDGMENTS We are deeply indebted to P. D. Gingerich for his valuable comments on an earlier draft of the manuscript. He and G. Gunnell (both UM, Ann Arbor), K. D. Rose (Johns Hopkins University School of Medicine, Baltimore), A. K. Gishlick (YPM, New Haven), and M. K. Brett-Surman (USMN) kindly supplied us with the valuable taeniodontid material to be studied. We thank T. Kaiser and E. Schulz (Biocenter Grindel and Zoological Museum, University of Hamburg) for help with microtexture analysis. We appreciate the helpful comments of R. Asher as the responsible editor of JVP and those of the reviewers M. T. Silcox and an anonymous one. This research was supported by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) for WvK and DK. It is publication no. 18 of the DFG Research Unit 771 ‘Function and performance enhancement in the mammalian dentition—phylogenetic and ontogenetic impact on the masticatory apparatus’ at the University of Bonn, Germany.

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