The development and structure of the chimpanzee mandible

J. Anat. (1976), 122, 2, pp. 467-477 467With 6 figuresPrinted in Great Britain

The development and structure of the chimpanzee mandible

P. A. JOHNSON, P. J. ATKINSON AND W. J. MOORE

Departments ofAnatomy and Oral Biology, University ofLeeds

(Accepted 19 November 1975)

INTRODUCTION

Man is distinguished from other extant hominoids in having a mandible which(1) is generally less robust, (2) is much smaller relative to body size, (3) has arounded, rather than a U-shaped dental arch and (4) has a pronounced chin butno lingual shelf. Since the lower jaw comprises a large and often a principal partof the fossil record (e.g. Dryopithecus, Simons, 1964), these marked differences inmandibular morphology have frequently been used as a basis for comparison inassessing the taxonomic status of fossil hominoids.The ontogenetic processes underlying these differences are poorly understood,

mainly because there is insufficient information about the sites of growth and re-modelling in the mandible of any hominoid other than Man. Early studies of growthin the human mandible (beginning with those of Hunter, 1771) showed that themajor sites of growth are located in the ramus (e.g. Brash, 1934; Rushton, 1944;Wilson, 1925). Recently, Enlow & Harris (1964) have provided more detailed in-formation about the remodelling which accompanies these major growth changes.Their findings, based on the identification of areas of bone deposition and resorptionin serial sections of the mandible, are illustrated in Figure 1. Condylar growth in apostero-superior direction increases both the total antero-posterior dimension(depth) of the mandible and the height of the ramus. Bone is also added along theposterior border of the ramus, but resorbed from its anterior border. These changesprogress at rates proportional to the posterior component of condylar growth andserve to increase the depth of the body and, since the rate of posterior depositionexceeds that of anterior resorption, also the depth of the ramus.The only other sub-human primate for which comparable information is available

is the macaque monkey (Macaca mulatta). For this species, Enlow (1966) andTurpin (1968) have provided an account of mandibular remodelling, while Duterloo,Atkinson, Woodhead & Strong (1974) have compared remodelling processes andcortical bone structure in Man and macaque. Areas of deposition and resorption inthe macaque mandible are similar in their general topography to those in the humanmandible, except in the anterior part of the body. In this region, the entire labialperiosteal surface in the macaque is depository, while in Man the labial surface ofthe alveolar process is resorptive and only the mental protuberance is depository.Yet the porosity of the cortical bone structure, assessed from the distribution ofdensity, is similar in both species. These differences in surface remodelling andsimilarities in compactness of structure underlie the contrasts to be seen between thetwo species in the morphology of the anterior region of the mandible, the adult

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Fig. 1. The distribution of resorptive and depository periosteal surfaces in the human mandible.Depository surfaces in light stipple, resorptive surfaces in dark stipple. (Reproduced by per-mission of Enlow, 1968.)

macaque mandible being generally more prognathous but lacking the protuberantchin of the human mandible.The relevance of these observations to the interpretation of evolutionary changes

which have produced the orthognathous human face is limited by the phylogeneticremoteness of Homo and Macaca. The present study of remodelling and bone struc-ture in the chimpanzee mandible (chosen because of the availability of the skulls)was made in order to obtain a comparison of the process of mandibular growth inMan with that in another member of the Hominoidea.

MATERIALS AND METHODS

SkullsThe skulls of six chimpanzees (Pan sp. indet.) were available. One of these was a

young adult male (full permanent dentition erupted, minimal attrition). The re-maining five were immature and of unknown sex. They were allocated to the fol-lowing dental age groups (approximate chronological ages from Schultz, 1935):

(1) deciduous dentition erupting (0-3 years) - 2 specimens;(2) deciduous dentition erupted with first permanent molars erupting or erupted

(3-5 years) - 3 specimens.Microradiography

Multiple ground sections were prepared from the left half of each mandible.The number of sections varied with the size of the mandible, the average being 10.The location of the sections is given in Figure 2.The sections were cut with a rotary diamond wheel and then ground down by

hand to a thickness of 100,um. Contact microradiographs of each section wereprepared on Kodak ultrafiat high resolution plates (grain size, 0-5 pm; X-raysource, 17-5 kV, 4 mA; exposure, 30 minutes; anode-film distance, 18 cm) and

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Mandibular development 469

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Fig. 2 (A). Lateral view of mandible to show approximate position of sections (2-10) preparedfor microradiography. Section 1 was in the median plane of the symphyseal region and cannotbe seen in lateral view. (B). The segment between sections 5 and 6 to show the position of the6 blocks (a-f) prepared for pyknometry.

then examined under a dissecting microscope (magnification x50) to identifysurfaces undergoing deposition and resorption. Following Enlow (1963, 1968), theprincipal criterion used in making this identification was the lamellar arrangementof the bone adjacent to the periosteal surface. Lamellae arranged in a regular fashionparallel to a smooth unbroken surface were assumed to be of periosteal origin andthe surface was classed as depository (Fig. 3 A). Convoluted lamellae were judged tobe formed by the in-filling of cancellous bone as a result of endosteal deposition andsubsequently brought to the surface by periosteal resorption (Fig. 3 B). The presenceof Howship's lacunae was taken to indicate a resorptive surface.These lamellar arrangements were considerably easier to study on microradio-

graphs than on ground or decalcified sections.

PyknometryThe essence of this method of measuring bone density is to distinguish bone of

high porosity (i.e. low density) from bone of low porosity (high density). It providesa general indication of the degree of compactness of structure in a much largervolume of bone than can readily be obtained from single sections.Three buccal and three lingual blocks were taken from between each pair of

sections used for microradiography (Fig. 2). Cancellous bone was removed fromthe blocks using a dental burr, leaving only the compact bone of the cortex. Themore solid texture at the division between cancellous and cortical bonewas identifiedby the increasing whiteness and smoothness of the surface as the cancellum wasremoved.Each block was dehydrated in absolute alcohol, defatted using ether in a Soxhlet

apparatus, dried over phosphorous pentoxide in vacuo for 12 days and then weighed.The blocks were immersed in wax in vacuo to seal the spaces on the surface of the

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. ,fa,. .iu - '.u mwFig. 3. Microradiographs showing (A) periosteal lamellar bone formation, (B) resorption on aperiosteal surface, (C) porous plexiform bone and (D) dense 'in-filled' plexiform bone x 120.

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Mandibular development

B

Fig. 4. Areas of deposition (light stipple) and resorption (dark stipple) in the mandible of agegroup 1. (A) buccal view; (B) lingual view.

bone. When the surplus was scraped away under a dissecting microscope until thebone surface was exposed, the specimen remained waterproof. The volume of eachspecimen was found by measuring its water displacement in a small pyknometer(Strong, 1963). Its density was then calculated by dividing the dry weight by thevolume.

RESULTS

MicroradiographySurface remodelling was assessed from the microradiographs of all the sections

from each jaw, each age group being considered separately.Age group 1The buccal periosteal surface of the ramus was found to be depository in its

inferior part but resorptive superiorly (Fig. 4A). These two zones were separatedby an oblique line of reversal which ran antero-inferiorly from the posterior buccalaspect of the mandibular neck to the anterior border of the ramus at its junctionwith the body of the mandible. The resorptive area above this line covered thebuccal surface of the neck and coronoid process but finished short of the mandibularnotch where the buccal margin was depository. The zone of deposition includedthe posterior border of the ramus, where the bone was plexiform in nature (Fig. 3 C)consisting of incomplete lamellae separated by large vascular spaces and indicatinga very rapid rate of periosteal bone formation (Spurrell, Felts & Baudin, 1965).The lingual periosteal surface of the ramus possessed a large resorptive area in its

posterior part (Fig. 4B). This area extended superiorly on to the lingual surface ofthe neck and inferiorly down to the lower edge of the ramus but, along the posteriorborder of the ramus, resorption gave way to bone deposition. An oblique line ofreversal, running from the anterior lingual surface of the mandibular neck to the

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Fig. 5. Areas of deposition (light stipple) and resorption (dark stipple) in the mandible of agegroup 2 (A) and the adult (B), both buccal views. Not to scale.

masseteric notch, separated this resorptive zone from a depository zone whichcovered the anterior part of the ramus and the lingual aspect of the coronoid processwhere the bone was plexiform in nature. A further reversal line coincided with thetemporal crest, the surface anterior to which was resorptive in nature. This wascontinuous with the resorptive area on the buccal aspect of the coronoid process.As already described, both buccal and lingual surfaces of the mandibular neck

were resorptive. The anterior and posterior surfaces, however, indicated periostealdeposition, the bone at both sites being plexiform.The buccal periosteal surface of the mandibular body was entirely depository.

On the lingual surface, there was a small area of resorption located just above theinferior border in the symphyseal region and extending laterally to the canineregion. Apart from this, the lingual surface also was depository.

Age group 2The pattern of remodelling in the rami of the three jaws comprising this group

was in general similar to that described for age group 1.In the body of one of the mandibles, the pattern was identical to that seen in age

group 1. However, in the remaining two mandibles, there was an additional area ofresorption along the inferior border of the labial surface of the symphyseal region,reaching posteriorly to the canine or premolar region (Fig. 5A).

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Mandibular development

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<1 5 g ml

1 5-1 7 g;ml

E 1 7-1 9g ml

> 1 9g ml

Fig. 6. Cortical densities in the mandible. (A) age group 1; (B) age group 2; (C) adult.Buccal views to left, lingual views to right. Not to scale.

Adult mandibleThe ramus of the single young adult mandible showed the same basic pattern of

remodelling as the other jaws (Fig. 5 B). In this jaw, however, the areas of plexiformbone found in the younger mandibles had become in-filled (Fig. 3 D).Although the greater part of the bucco-labial surface of the body of the mandible

was depository, an area of resorption occurred on the lower border, just lateral tothe symphysis, and extending laterally along the inferior mandibular border as faras the second molar tooth. A larger area of resorption was found on the labialsurface immediately below the incisor and canine teeth overlying the symphysis andextending as far as the first premolar tooth.

PyknometryThe results of the pyknometric investigation of cortical density are illustrated in

Figure 6. Density distribution followed a fairly constant pattern in all six jaws.In the body, density was greatest in the basal region and diminished towards thealveolar process. Density increased with age but followed the same pattern. The

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ramus was of lower density than the body, but within this region no consistentpattern was seen apart from areas of very low density in the coronoid and condylarprocesses, and along the posterior border of the ramus, due to the presence in thesesites of large amounts of plexiform bone.

DISCUSSION

This investigation has shown that the major sites of growth in the mandible ofthe chimpanzee are located, as in other mammals, in the condyle and along theposterior border of the ramus (e.g. Bhaskar, 1953; Brash, 1934; McNamara &Graber, 1975). These sites are characterized in the chimpanzee by the presence oflarge amounts of plexiform bone which is indicative of very rapid growth. Plexiformbone is also found in the macaque (Duterloo et al. 1974) but does not occur in thehuman mandible (Atkinson & Woodhead, 1968), presumably reflecting its muchslower rate of growth.The modelling of the ramus that accompanies growth at these major sites in the

chimpanzee was found to resemble closely that previously demonstrated in Man(Enlow & Harris, 1964, Fig. 1) and Macaca (Enlow, 1966). Both lingual and buccalperiosteal surfaces of the mandibular neck are resorptive in all three species, servingsuccessively to remove condylar bone and form the narrower regions of the neckas the condyle grows. Similarly, the three.species show resorption along the anteriorborder of the coronoid process which, as a concomitant of the rapid depositionalong the posterior border of the ramus, produces an increase in the depth of thebody of the mandible. Remodelling patterns on the periosteal surfaces of the mainpart of the ramus are also similar, the distribution of formation and resorptionhelping to preserve the lateral convexity usually present in the superior half of theramus in all three species by re-locating regions formed posteriorly, first antero-laterally and then antero-medially. The depository nature of the lingual surface ofthe coronoid process produces two other important effects. First, since this surfacefaces medially, superiorly and posteriorly, bone additions, combined with resorptionalong the anterior border and buccal surface of the coronoid process, result in theprocess growing upwards and backwards. Secondly, lingual deposition re-locatesthe inferior part of the coronoid process into line with the more medially placedalveolar process, as both the depth of the body and the length of the dental archare increased by resorption from the anterior border of the coronoid process.

In contrast to the similarity of the changes occurring in the ramus, remodellingin the body shows a number of marked species differences between Man, macaqueand chimpanzee. In Man (Fig. 1), although both buccal and lingual periostealsurfaces are predominantly depository, important areas of resorption occur in thesublingual fossa and on the labial surface of the alveolar process below the incisorteeth (Enlow & Harris, 1964). The resorptive area in the sublingual fossa is ananterior extension of the resorptive zone on the lingual aspect of the ramus. Togetherwith deposition on the opposed buccal surface of the body, this resorption producesa lateral shift of the basal part of the body, so increasing the width of the mandi-bular arch. The alveolar arch, surmounting the mandibular arch, is depositoryaround its entire lingual surface. This, coupled with resorption in the sublingual

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Mandibular developmentfossa, results in the mandibular arch increasing in width more rapidly than thealveolar arch and thus in an increasing overhang of the alveolar process as growthproceeds. In the macaque mandible, the area of resorption in the sublingual regionis limited to the area of a small depression just inferior to the first and second molarteeth and the overhang is not as pronounced as in Man (Enlow, 1966). In the chim-panzee the bone in this region was found to be entirely depository in nature, so thatthe lingual surface is smoothly rounded with little or no overhang of the posteriorpart of the alveolar arch.

Contrasts between the three species were also observed in the symphyseal region.In the human mandible, the lingual periosteal surface is depository over its wholeextent. On the labial surface, the changes are variable, the commonest pattern beingone in which the mental prominence is depository but the region between this andthe incisor and canine teeth is resorptive (Enlow & Harris, 1964, Fig. 1). Hence,as growth proceeds the chin becomes increasingly more prominent. The prognathousmacaque mandible, on the other hand, has an entirely depository labial surface andthe lingual surface is resorptive except in its basal part where deposition producesthe lingual shelf. Finally, in the chimpanzee, while the labial surface was found tobe entirely depository in the youngest age group, in the older mandibles of age group2 an area of resorption was observed along the inferior border of this surface in thesymphyseal region. Resorption was also present in this region of the young adultmandible, although more extensive posteriorly and separated into two halves by amedian zone of deposition. Of particular interest was the finding, in the adultmandible, of an area of resorption immediately inferior to the anterior teeth, similarin its distribution to that seen in the growing human mandible. Since this observa-tion was based on a single specimen, it may represent merely an individual variation,but if this should prove to be a general finding, it would suggest that, during thelater stages of mandibular growth in the chimpanzee, resorption occurs anteriorly,reducing the forward movement of the symphyseal region produced by growth ofthe ramus. Such a mechanism apparently operates throughout the growth period inMan (Enlow & Harris, 1964). The lingual surface of the symphyseal region of allthe chimpanzee mandibles studied was found to have a resorptive area located ashort distance above the inferior border which was, itself, strongly depository.Although not identical, this arrangement is similar to that seen in the mandible ofthe macaque and, as in that species, serves to produce a lingual shelf.The pattern of distribution of cortical density also showed a repeating pattern

but this differed from that of surface remodelling. This is not unexpected sincedensity reflects variations in bone structure throughout the full width of the cortex.Correspondence between the patterns of density and remodelling would occur onlywhen surface remodelling remains the same throughout growth. For instance, thedensest regions of bone were found in the basal part of the mandible, which was thesite of most consistent lamellar deposition. The least dense regions were those withthe most marked deposition of porous plexiform bone. Areas where active remodel-ling led to the greatest reorientation of bone tissue, as in the ramus, showed theleast similarity between the two patterns. The two patterns are thus complementary,giving information related to the mode of growth of the bone.The consistent distribution of dense bone along the inferior border of the

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mandibular body might be related to mechanical stress. During mastication, theorientation of the pressures exerted on the teeth, and the tension developed in themasseter and medial pterygoid muscles, would probably lead to a zone of highcompression along the lower border of the mandible. It is, however, still uncertainwhether mechanical stress or genetic mechanisms are the dominant influences on bonegrowth (Moore & Lavelle, 1974). If mechanical factors are the prime influence onremodelling, species differences in remodelling patterns might merely indicatevariations in the mechanism of mastication. That this is not so, and that geneticinfluences play a major role in controlling bone growth, is indicated by the presentfindings of: (1) a consistent distribution of remodelling and density patterns in jawsof different ages; (2) the occurrence of similar patterns in different primate species;and (3) the position in the ramus of reversal lines related to bone growth rather thanto muscle attachment.These findings suggest therefore a basis for the study of mandibular bone structure

in the chimpanzee and other great apes as further skeletal material becomes avail-able. Of particular interest is the chin region where, from the single adult chimpanzeespecimen available to us, it appears that an anterior area of resorption, similar tothat seen in Man, becomes instituted in the later growth stages.

SUMMARY

The sites of growth and remodelling, and the associated changes in cortical bonestructure, have been studied in the chimpanzee mandible and compared with thosepreviously reported in the human and macaque mandibles. The location of theprincipal sites of growth, and the distribution of the areas of deposition and re-sorption in the ramus, were found to be similar in all three species. In the chim-panzee, unlike Man, the bone being deposited at the condyle, posterior border ofthe ramus and coronoid process was plexiform in nature, indicating very rapidgrowth. The pattern of remodelling in the mandibular body, on the other hand,showed marked species differences at the chin and on the submandibular lingualsurface, which account for the contrasts seen in the adult morphology of theseregions.Although the pattern of distribution of cortical densities differed from that of

surface remodelling, the information they give is complementary in analysing bonegrowth. The densest regions were found to coincide with sites of consistent lamellardeposition, while the least dense regions were those where plexiform bone wasformed. Areas where remodelling led to the greatest reorientation of bone tissuewithin the cortex showed the greatest disparity between the two patterns.

We should like to thank Professor Donald H. Enlow and Harper and Row,Publishers Incorporated, for their permission to publish Figure 1.

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REFERENCES

ATKINSON, P. J. & WOODHEAD, C. (1968). Changes in human mandibular structure with age. Archives ofOral Biology 13, 1453-1463.

BHASKAR, S. N. (1953). Growth pattern of the rat mandible from 13 days insemination age to 30 daysafter birth. American Journal ofAnatomy 92, 1-53.

BRASH, J. C. (1934). Some problems in the growth and developmental mechanics of bone. EdinburghMedical Journal 41, 363-387.

DUTERLOO, H. S., ATKINSON, P. J., WOODHEAD, C. & STRONG, M. (1974). Bone density changes in themandibular cortex of Macaca mulatta. Archives of Oral Biology 19, 241-248.

ENLow, D. H. (1963). Principles ofBone Remodelling. Springfield: Charles C. Thomas.ENLOW, D. H. (1966). A comparative study of facial growth in Homo and Macaca. American Journal of

Physical Anthropology 24, 293-308.ENLOW, D. H. (1968). The Human Face. New York: Harper and Row.ENLOW, D. H. & HARRIS, D. R. (1964). A study of the postnatal growth of the human mandible. American

Journal of Orthodontics 50, 25-50.HUNTER, J. (1771). Natural History of the Human Teeth. London: John Johnson.MCNAMARA, J. A. & GRABER, L. W. (1975). Mandibular growth in the rhesus monkey (Macaca mulatta).American Journal ofPhysical Anthropology 42, 15-24.

MOORE, W. J. & LAVELLE, C. L. B. (1974). Growth of the Facial Skeleton in the Hominoidea. London:Academic Press.

RUSHTON, M. A. (1944). Growth at the mandibular condyle in relation to some deformities. British DentalJournal 76, 57-68.

SCHULTZ, A. H. (1935). Eruption and decay of the permanent dentition in primates. American Journal ofPhysical Anthropology 19, 489-581.

SIMONS, E. L. (1964). The early relatives of Man. Scientific American 211, 50-65.SPURRELL, F. A., FELTS, W. J. L. & BAUDIN, L. V. (1965). Osteon development in swine. In Swine in

Biomedical Research (ed. L. K. Bustard & R. 0. McClellan with M. P. Burns), pp. 173-192. BatelleMemorial Institute (Pacific N.W. Laboratories Division).

STRONG, M. (1963). A method for the determination of the specific gravity or density of small volumesof liquids and small solid objects. American Journal ofPathology 40, 48-49.

TURPIN, D. L. (1968). Growth and remodelling of mandible in the Macaca mulatta monkey. AmericanJournal of Orthodontics 54, 251-271.

WILSON, CHARLES S. (1925). The temporo-mandibular joint and its influence on the growth of the man-dible. British Dental Journal 46, 845-855.

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The development and structure of the chimpanzee mandible