Anat Embryol (1992) 186:319-326
Anatomyand Embryology 9 Springer-Verlag1992
A scanning electron microscopic study on the distribution of peritubular dentine in cheek teeth of Cervidae and Suidae (Mammalia, Artiodactyla) Horst Kierdorf 1 and Uwe Kierdorf 2
1 ZoologischesInstitut der UniverstitS.tzu K61n, Weyertal 119, W-5000 K61n4I, Federal Republic of Germany 2 I. ZoologischesInstitut der UniversitS.tG6ttingen, Berliner Strasse 28, W-3400 G6ttingen, Federal Republic of Germany Accepted July 2, 1992
Summary. Distribution of peritubular, dentine was studied in cheek teeth of fallow deer (Dama dama), roe deer (Capreolus capreolus) and wild boar (Sus scrofa). In the two cervid species, especially intense peritubular dentine formation was found in the outer regions of mid and cuspal coronal dentine. In these areas a marked asymmetry occurred, peritubular dentine being predominantly secreted onto the side of the dentinal tubule walls nearest to the dentinoenamel junction. Intensity and asymmetry of peritubular dentine formation decreased cervically. In root dentine, the walls of the dentinal tubules were covered with only a thin peritubular dentine layer of even thickness. Here, in contrast to peripheral coronal dentine, the volume of intertubular dentine far exceeded that of peritubular dentine. In porcine coronal dentine, PTD asymmetry, being of lesser extent than in cervids, was observed only in peripheral areas ofcuspal and flank regions of the cheek teeth. Because peritubular is more highly mineralized than intertubular dentine, the relative volume of dentine made up from the two components has an important influence on dentinal wear resistance. The significance of variations in volume and distribution of peritubular dentine between different dentinal regions for achieving and maintaining a functional occlusal surface is shown for cervid cheek teeth. Our results suggest that dentinal structure (in addition to enamel structure) should be taken more into consideration when discussing occlusal surface morphology in herbi- and omnivores from a functional point of view. Key words: Artiodactyla - Cheek teeth - Peritubular
dentine - Occlusal morphology - SEM
Abbreviations: DEJ, dentinoenameljunction; DPI, dentine-pulp interface; ITD, intertubular dentine; PTD, peritnbular dentine Correspondence to: H. Kierdorf
Introduction
Up to now, studies of the structure of the dental hard tissues with regard to taxonomic questions or functional aspects have almost completely focused on dental enamel (Boyde 1965, 1967; v. Koenigswald 1980, J985; Boyde and Martin 1982; Fortelius 1985; Boyde and Fortelius 1986; Flynn et al. 1987; v. Koenigswald and Pfretzschner 1987; v. Koenigswald et al. 1987; Janis and Fortelius 1988; Stern et al. 1989). The uniform ultrastructure of tooth enamel found within certain mammalian taxa is regarded as an adaptation to the specific mechanical stress to which the teeth are exposed during food uptake and comminution in these groups (v. Koenigswald 1980; Rensberger and v. Koenigswald 1980; Boyde and Fortelius 1986; Flynn et al. 1987; v. Koenigswald et al. 1987; Kierdorf et al. 1991). From a functional point of view, enamel and dentine can be regarded as a unity, because, in contrast to enamel, dentine is elastic and to some extent deformable (Schroeder 1987) and thus forms a supportive structure for the harder but brittle enamel. The presence of taxon-specific structures in the orthodentine (primary dentine) of mammalian teeth has been described by Bradford (1967). In a large number of Eutherian orders he studied the existence of the so-called peritubular dentine (PTD), which in greater detail had first been examined in human teeth (Bradford 1955; Frank 1959). PTD delimits the walls of the dentinal tubules. As shown by microradiography (Miller 1954; Baud and Held 1956; Blake 1958; Dreyfuss et al. 1964; Eda and Takuma 1965), transmission electron microscopy (Frank 1959; Plackova and Stepanek 1960; Takuma 1960; Johanson and Parks 1962; Eda and Takuma 1965; Schroeder and Frank 1985) and microanalysis (Takuma et al. 1966), the mineral content of PTD is higher than that of intertubular dentine (ITD). Whereas ITD contains large amounts of collagen, for human teeth it is a matter of controversy, if PTD is free of collagen (Schroeder 1987) or contains a few collagen fibers believed to be continuous with those of ITD (Mj6r 1986).
320 By studying thin ground sections, Bradford (1967) demonstrated the existence o f P T D in teeth of representatives of the orders Primates, Carnivora, Hyracoidea, Perissodactyla, Artiodactyla, Cetacea, Sirenia and Proboscidea. No P T D was found in members of the orders Insectivora, Chiroptera, L a g o m o r p h a and Rodentia. According to Bradford (1967), differences with respect to the relative volumes of orthodentine formed by either I T D or P T D were observed when comparing teeth from different orders within the first group. Highest relative volumes of P T D were found in representatives of the Artio- and Perissodactyla. Because P T D is more highly mineralized than I T D , the volume relation of the two tissue types has an effect on hardness and, thus, wear resistance o f the dentine. In summarizing his results, Bradford (1967, p. 31) states t h a t " t h e greatest development of the peritubular dentine is to be found in the Perissodactyla and the Artiodactyla, in which teeth of limited growth withstand considerable attrition. Conversely, in those animals in which wear caused by attrition is made good by continued tooth growth, the proportion of peritubular dentine is at a m i n i m u m . " Neither in the aforementioned study, nor in those of Lester and Boyde (1968), Boyde (1971) and Boyde and Jones (1972) were teeth from cervid species examined. C r o w n height in the b r a c h y o d o n t (e.g., Capreolus capreolus L., Alces alces L., and Rangifer tarandus L.) to subhypsodont (e.g., Cervus elaphus L. and Dama dama L.) cheek teeth of cervids (Thenius 1989) is m a r k edly lower than in the hypsodont premolars and molars of m a n y bovid species. Because in both cervids and bovids the teeth are exposed to severe masticatory stress, according to the view expressed by Bradford (1967), a massive formation of P T D in cervid cheek teeth can be expected. At present, no detailed description of the distribution of P T D exists for the teeth of cervids or other families within the Artiodactyla. The present study is mainly aimed at filling this gap for the Cervidae. Moreover, functional aspects of P T D formation will be discussed with special regard to the adaptive value of orthodentine structure.
(DPI) to the dentinoenamel junction (DE J). On step-like fracture surfaces, dentinal tubules were cut in a transverse direction. After cutting, teeth were dehydrated in a graded series of acetone, and critical-point dried from liquid CO2. All specimens were then mounted on aluminium stubs, sputter-coated with gold, and examined in a Cambridge Stere0scan 180 or a Hitachi S 520 scanning electron microscope.
Results
Cervidteeth As shown schematically in Fig. 1, the course followed by the dentinal tubules in the orthodentine of cervid cheek teeth varied according to the region of the tooth. Over the tips of the pulp chambers and below the b o t t o m of the infundibulum the tubules ran nearly straight f r o m the D E J to the DPI. In cuspal and mid-flank regions of the tooth crowns, and in the cuspal part of the dentine lining the infundibulum, the tubules were oriented perpendicular to the D E J up to a distance of about 100 to 200 ~tm f r o m the dentine-enamel interface. Then they bent into a more vertical direction and thus reached the D P I at a sharp angle (Fig. 1). In more cervical regions of coronal dentine, the vertical inclination of the tubules observed at this distance from the D E J became progressively reduced, the tubules therefore reaching the D P I at a more and more obtuse angle. In root dentine, a distinct bending in the course of the dentinal tubules was no longer discernible, the tubules following a straight and in most regions nearly horizontal course f r o m the dentinocemental junction to the DPI. Because in the tooth crown the surface area of the D E J was 2.5 to 5 times that of the DPI, a progres-
Materials and methods
In total 13 teeth of fallow deer (Dama dama), subfamily Cervinae, and roe deer (Capreolus capreolus), subfamily Odocoileinae, from individuals of different postnatal age were studied (Dama dama." ] P4, 2M1, 1 M 1, 2M2, 1 M3; Capreolus capreolus. 1 P4, 1M 1, 4M3). Teeth were extracted from either dried skulls and mandibles or from material fixed in 4% phosphate-buffered formaldehyde (pH 7.4). For comparison, also three teeth (1 M~, 1 M 1, I M2) of wild boars (Sus scrofa L.), a non-ruminating artiodactyi species, were examined. Crown form of the bunododont molars of the latter species deviates very much from that of the selenodont cervid molars. In all of the extracted teeth, organic remnants were removed under a dissecting microscope. Afterwards the teeth were cut in corono-cervical direction using a hammer and a pointed steel blade, the plane of section running through the tip of the pulp chamber. In these specimens the course of individual, longitudinally cut dentinal tubules could be followed from the dentine-pulp interface
li
bu
Fig. 1. Schematic illustration of an unworn mandibular cervid molar showing the course followed by the dentinal tubules in orthodentine. C, cementum; D orthodentine; E, enamel; I, infundibulum; P, pulp chamber; li, lingual; bu, buccal. Not to scale
321
Fig. 2. PTD (*) and ITD (arrow) in peripheral regions of coronal orthodentine, roe deer M3; cuspal to the top, pulp chamber to the right, x 5,000 Fig. 3. Mineralized collagen fibers (arrow) in ITD of inner part of cervical orthodentine; even distribution of PTD, roe deer M3; pulp chamber to the left. x 10,000 Fig. 4. Thin layer of evenly distributed PTD (arrow) in juxtapulpal dentine, roe deer M3 ; pulp chamber to the left, x 5,000
Fig. 5. Juxtapulpal orthodentine of fallow deer MI; PTD present only as a thin layer (*) or absent (arrow); cuspal to the top. x 5,500 Fig. 6. Asymmetrical PTD distribution in outer third of coronal flank dentine, roe deer M3; cuspal to the top, DEJ to the right. x 4,800 Fig. 7. Pronounced PTD asymmetry in coronal flank dentine of fallow deer M1 ; cuspal to the top, DEJ to the left. x 5,500
322
Fig. 8. Volume of PTD (*) exceeding that of ITD in the region where the course of the dentinal tubules changes from perpendicular to the DEJ to a more vertical orientation; roe deer M3; cuspal to the top, DEJ to the right, x 1,900
Fig. 11. Central root dentine, only thin layer of PTD (arrow); dentinocemental junction to the right; roe deer M3. x 3,900
Fig. 9. Decreasing diameter of dentinal tubules at DE J; roe deer M3 ; E, enamel, x 1,900
Fig. 13. Outer region of coronal flank dentine of wild boar M1; evenly distributed PTD; cuspal to the top. x 6,300
Fig. 10. Dentinal tubules over the tip of the pulp chamber near the DEJ (to the top), evenly distributed P T D ; arrow, remnant of odontoblast process; roe deer M3. x 4,500
Fig. 12. Intense branching of dentinal tubules in root dentine near the dentinocementaljunction (to the bottom); roe deer M3. x 3,600
323 sive crowding of the dentinal tubules occurred in pulpal direction, i.e., the intertubular distances decreased towards the DPI. On fracture planes, ITD and P T D could easily be distinguished. ITD exhibited a coarse texture and a rough surface structure (Fig. 2). At higher magnifications, mineralized collagen fibers were discernible (Fig. 3). In contrast to this, P T D showed a finer texture and smooth surface structure (Fig. 3). No mineralized collagen fibers were seen in P T D of fractured teeth. Differences with respect to P T D formation were observed between root dentine and coronal dentine as well as between different segments of the dentinal tubules within the latter. In coronal dentine, mineralization of P T D commenced at the same time as that of ITD. Circumpulpally, i.e., in the most recently formed dentine, only a little P T D was found; this evenly covered the dentinal tubule walls as a thin layer (Fig. 4). Only sporadically were collagen fibers of ITD seen, due to a local lack of P T D covering (Fig. 5). Towards the D E J, P T D formation varied in a predictable manner. In cuspal and mid flank regions of coronal dentine, in which the tubules ascended at a steep angle from the DPI, a distinct asymmetry o f P T D formation was observed. This asymmetry, which began at a short distance from the pulp, became accentuated towards the DEJ. P T D was mainly secreted onto the side of the tubule wall nearest to the DEJ (Fig. 6), the asymmetry being most pronounced in the region where the tubules changed from a course perpendicular to the DEJ to a vertical one (Fig. 7). Here the volume occupied by P T D equalled or often even exceeded that of ITD (Fig. 8). The walls of the dentinal tubules were perforated by numerous small pores, through which branchings of the odontoblast process had entered the dentine (Figs. 3, 6, 7). In mantle dentine (peripheral dentine), the diameter of the tubules, oriented perpendicular to the D E J, decreased continuously. In this region an almost symmetrical distribution of P T D was observed (Fig. 9). In more cervically located coronal dentine, where the tubules followed a less steep course, P T D asymmetry was less pronounced, and began at a greater distance from the DPI than in more cuspal regions. In the inner part of cervical orthodentine a nearly symmetrical P T D distribution was observed (Fig. 3). Over the tip of the pulp horns (Fig. 10) and below the b o t t o m of the infundibulum, i.e., in the regions where the dentinal tubules followed a straight course from the DEJ to the DPI, a nearly symmetrical distribution of P T D was found along the whole tubule. There was markedly less than in more peripheral regions, with a minimum of P T D ~brmation again seen in juxtapulpal dentine. Towards the infundibulum and the tooth flank region P T D asymmetry gradually increased. In root dentine, ITD volume far exceeded that of PTD, which as a thin layer of even thickness covered the tubule walls (Fig. 11). An especially intense branching of the dentinal tubules was seen near the dentinocemental junction (Fig. 12). Because in the root region the surface area of the DPI more or less equalled that of the dentinocemental junction, the tubules did not become crowded towards the pulp.
No differences with respect to primary dentine structure were observed between teeth of fallow and roe deer. Except for obliteration of peripheral tubule regions, also no differences were observed between teeth not previously exposed to masticatory stress and teeth already abraded to different extents. Furthermore, the structure of primary dentine in maxillary teeth did not differ from that of their mandibular counterparts.
Pig teeth In the pig molars examined for comparison, the course followed by the dentinal tubules resembled that described for cervid teeth. Starting from the DEJ, the tubules of mid and cuspal porcine coronal dentine first followed a nearly horizontal course for about 200 to 250 gin, then bent into a vertical direction. P T D distribution in the pig teeth however differed significantly from the situation in the two cervid species. First, a symmetrical arrangement of P T D was found not only in circumpulpal dentine of the crown flanks of pigs, but also along 50% to 60% of the distance between DPI and DEJ (Fig. 13). Secondly, in these areas the volume of ITD always far exceeded that of PTD. Asymmetric PTD formation in porcine coronal dentine was observed only in more peripheral areas of cuspal and flank tooth regions. The asymmetry, which as a rule was less pronounced than in cervid teeth, became progressively accentuated towards the DEJ. As in cervid teeth, in the areas of asymmetry P T D was preferentially secreted onto the side of the tubule walls nearest to the DEJ. But also in these regions, ITD volume always exceeded that of PTD.
Discussion
To the knowledge of the authors no other study has dealt with P T D of cervid teeth. However, for some other (domestic) artiodactyls (cattle, sheep and pig) information on P T D structure and distribution already exists (Lester and Boyde 1968; Boyde 1971; Boyde and Jones 1972). In these species, P T D formation was found to occur at the same time as that of ITD. As stated by the abovementioned authors, the amount of P T D secretion onto the walls of the dentinal tubules relates to their angle of incidence upon the DPI. In tubules ending perpendicular to the DPI, which is the situation also found in human cheek teeth (Lester and Boyde 1968; Schroeder 1987), P T D is either evenly distributed or, if an asymmetry exists, there is no preference for either side of the tubule wall. In tubules ending obliquely to the DPI, P T D is preferentially secreted onto the tubule wall nearest to the DEJ. In general, these findings correspond well with those of the present study. Our results, however, allow a more precise description of the mode of P T D formation in cervid and pig teeth than was previously given for any other artiodactyl species. In cervid teeth, a marked P T D asymmetry was first seen at a certain distance from the DPI, which proves that side-specific differences in secre-
324 tion rates appear only some time after the start of PTD formation by the odontoblasts. Furthermore it was noted that the degree of asymmetry in PTD covering of the tubule walls was not uniform, but most pronounced in the peripheral areas of mid and cuspal coronal dentine. Comparing cervids and pigs, it can be stated that in both groups asymmetric PTD distribution was found in certain regions of the teeth, but that the degree of asymmetry found in pig teeth was always less than that in cervid teeth. With respect to PTD formation it therefore seems necessary to differentiate at least between ruminating and non-ruminating artiodactyl species. The fact that corresponding PTD structures were seen in both worn and unworn cervid teeth, the latter not previously exposed to masticatory forces, clearly demonstrates that PTD formation is not the result of an individual adaptation to the specific stress on the teeth during food processing, but that PTD structure, like that of dental enamel, is genetically determined. This can also be concluded from the fact that primary dentine secretion only occurs until the end of root formation, i.e., before the tooth reaches its definite occlusal position, and is to a significant extent exposed to mechanical stress. Secondary and tertiary dentine on the other hand are formed as a consequence of dental wear and unphysiologic irritation of dentine throughout the life of a tooth (Seltzer and Bender 1984). Primary dentine structure, therefore, has to be regarded as the outcome of a selective process in the course of evolution. This raises the question of its adaptive value. The cervid dentition is characterized by the anisognathy typical of all ruminants. During central occlusion, only a narrow buccal region of the crowns of the mandibular cheek teeth is covered by an equally narrow palatinal seam of their maxillary antagonists. During mastication, proceeding in the form of lateral (transverse) jaw movements, the mandibular cheek teeth, whose occlusal surfaces are inclined buccally (Fig. 1), slide over their maxillary antagonists, the occlusal surfaces of which are sloped in the opposite direction. According to Fortelius (1985), the nearly horizontal jaw movements of ruminants consist of a single phase power stroke, allowing great overlap in muscular activity, thus leading to high load and shear forces. Full functionality of cervid cheek teeth is reached only after abrasion of cuspal enamel, the occlusal surface then being formed by both enamel and dentine. Functional occlusal surfaces of cervid cheek teeth are thus characterized by thin enamel ridges that surround valleys made of dentine. The slope of these troughs is highest in dentine near the DE J, and gradually decreases in a centripetal direction, i.e,, towards the deepest point of the dentinal valley located over the top of the pulp chamber (Fig. 14a). This acquired occlusal morphology, consisting of enamel ridges, mostly running perpendicular to the direction of jaw movement, and larger areas of less resistant dentine, constitutes an excellent adaptation to comminution of plant material by lateral jaw movements (Fortelius 1985; Janis and Fortelius 1988). Due to the differences in mineralization, and thus also resistance, between enamel and dentine, functionality of the occlu-
9 PTD Fig. 14 a-c. Schematicillustrationof the occlusal surfaceof a worn
cervid cheek tooth (a). In central dentine, tubules showingsymmetrical PTD formation are cut transversely(b); in peripheral dentine the tangentially cut tubules show asymmetric PTD distribution and higher PTD content (c). D, orthodentine;E, enamel; I infundibulum; P, pulp chamber. Secondarydentine omitted. Not to scale
sal surface is maintained for most of the tooth's life. Only after total abrasion of the infundibular area, a drastic change in the form of the occlusal surface occurs concomitant with a reduced ability for proper comminution of the diet. In order to maintain a functional occlusal surface, hardness, and thus also resistance of enamel and dentine, must be adjusted to each other. Of course dental enamel is the most important tissue regarding tempo and mode of dental wear, but also dentinal hardness is an essential factor. If, for instance, dentine and enamel were of equal hardness, or if the difference in hardness were low, enamel ridges could not develop on the occlusal surfaces, and comminution of food would be ineffective. Impairment of masticatory function is seen in (pathological) cases of greatly decreased enamel hardness, and normal, or nearly normal dentinal hardness, e.g., in fluorosed roe deer teeth (Kierdorf 1988; Kierdorf and Kierdorf ]989). On the other hand, a reduction in the hardness of dentine would lead to its rapid erosion. As a result, deep troughs would develop between the enamel ridges and, because of food impaction into these troughs, proper comminution would no longer be possible. Furthermore, the enamel ridges would loose their support by adjacent dentine, and therefore eventually break away. As can be seen in cases of pathologically altered dentinal structure leading to reduced dentinal hardness, e.g., in dentinogenesis imperfecta, such teeth are rapidly worn (Schroeder 1991).
325 Because P T D is more highly mineralized than ITD, P T D formation increases dentinal resistance (Bradford 1967). Variation in the amount of P T D formation between different mammalian taxa can therefore be regarded as an adaptation to specific functional demands occurring in these groups. So the high P T D content of cervid teeth can, in accordance with Bradford (1967), be interpreted as an adaptive trait increasing dentinal resistance. F r o m our observations it can further be deduced that in cervid cheek teeth variations in amount and distribution of P T D between different dentinal regions are definitely important for achieving and maintaining a functional occlusal surface. After abrasion of cuspal enamel, dentinal tubules in peripheral dentine are tangentially cut by the occlusal surface, whereas in more central regions the tubules, running a nearly vertical course, are cut transversely (Fig. 14). As a consequence of this, and due to the fact that in peripheral dentinal regions more P T D is formed than in central ones, in the former a larger area of the occlusal surface is made up of the more resistant P T D than in the latter (Fig. 14b, c). This is one of the reasons for the less intense abrasion of peripheral dentine when compared with the dentine over the tip of the pulp chamber, leading to the differences in the slope of the dentinal coronal surface mentioned above. The other main reason probably is the protective effect on peripheral dentine exercised by the adjacent enamel ridges. At present it is speculative to suggest that the differences in primary dentine structure observed between cervids and pigs might relate to the morphology of the occlusal surface and the particular mode of jaw movement (transverse in cervids, orthal in pigs) of the two groups, as has already been assumed for overall morphology of the cheek teeth by Fortelius (1985). Information on P T D occurrence in the course of ungulate phylogeny is scarce. Frank et al. (1987) studied P T D in Protungulatum, a late cretaceous member of the family Arctocyonidae, and in various paleocene perissodactyls, by inspecting sections through various tooth regions oriented planoparallel to the occlusal surfaces. Whereas no P T D was found in specimens from the genera Phenacodus, Hyracotherium and Homogalax, P T D formation occurred in Protungulatum, Tetraclaenodon, Propachynolophus and Hyrachus. Because the Arctocyonidae are thought to include the ultimate ancestor of all later ungulates (Carroll 1988), the fact that P T D is present in Protungulatum while it is lacking in Hyracotherium, Homogalax and Phenacoduscalls for explanation. Summing up their results, Frank etal. (1987, p. 150) state that " t h e presence of peritubular dentine as early as in the Protungulatum stage and its meager growth in the paleocene forms, testifies that this structure remained for a long time weak and fluctuating and increased only in those lineages and in those conditions where this character was of selective interest". When evaluating the results of Frank et al. (1987), it has to be considered that they studied only one tooth per taxon. Thus, P T D formation only in certain elements of the dentition, or minor amounts of P T D within their material not lying in the plane of section, could have
escaped their attention. Furthermore it must be clearly stated that at present ungulate phylogeny is still rather obscure, and ungulate taxonomy not satisfactorily resolved. While the monophyly of different groups (e.g. Artiodactyla, Proboscidea) commonly united in the taxon Ungulata is widely accepted, this is not the case for the Ungulata itself (Fischer 1991). To the knowledge of the authors, at present no information is available on P T D formation in early artiodactyls. Regardless of the question if the Ungulata really form a monophyletic group, it is accepted that Artioand Perissodactyla evolved separately at least since the paleocene (Thenius 1979; Carroll 1988). Therefore, similarities in P T D formation between the two groups (Boyde 1968; Boyde and Jones 1972) can (at least to a large extent) be regarded as the result of parallel evolution or convergence (if Perisso- and Artiodactyla are of diphyletic origin) due to the action of comparable selective pressures, as earlier stated for certain adaptive traits of enamel structure (Kierdorf et al. 1991). We are now just beginning to consider dentinal structure from phylogenetic and functional points of view (Hildeboldt et al. 1986). In the present study we could demonstrate an adaptive relation between masticatory stressing of cervid cheek teeth, shape of their occlusal surfaces and P T D distribution in orthodentine. From this it can be concluded that in addition to enamel micromorphology, certain aspects of dentinal structure should be regarded as the outcome of a selective process in the course of evolution. For a more comprehensive approach to the question of the adaptive value of dentinal structure in mammals, further studies on a wide variety of species with different types of tooth shape and mastication are necessary. On the basis of our results, it seems especially promising to start with the study of species whose cheek teeth achieve full functionality only after abrasion of cuspal enamel, and whose occlusal surfaces are in consequence made up of enamel and dentine, as is the case in most herbivores and many omnivores. References Baud CA, Held AJ (1956) Silberffirbung, R6ntgenmikrographie und Mineralgehalt der Zahnhartgewebe. Dtsch Zahn/irztl Z 11:309 314 Blake GC (1958) The peritubular translucent zones in human dentine. Br Dent J 104:57-64 Boyde A (1965) The structure of developing mammalian enamel. In: Stack MV, Fearnhead RW (eds) Tooth enamel. Wright, Bristol, pp 163-167 Boyde A (1967) The development of enamel structure. Proc R Soc Med 60 : 923-928 Boyde A (1971) Comparative histology of mammalian teeth. In: Dahlberg AA (ed) Dental morphology and evolution. University of Chicago Press, Chicago London, pp 81 94 Boyde A, Fortelius M (1986) Development, structure and function of rhinoceros enamel. Zool J Linnean Soc 87:181-214 Boyde A, Jones SJ (1972) Scanning electron microscopic studies on the formation of mineralized tissues. In: Slavkin HC, Bavetta LA (eds) Developmental aspects of oral biology. Academic Press, New York London, pp 243-274 Boyde A, Martin L (1982) Enamel microstructure determination in hominoid and cercopithecoid primates. Anat Embryol 165:193-212
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