Growth changes in measurements of upper facial positioning

Growth Changes in Measurements of Upper Facial PositioningRICHARD MAY1,2* AND DANIEL B. SHEFFER3

1Biology Department, Morningside College, Sioux City, Iowa 511062Biological Anthropology Program, School of Biomedical Sciences,Kent State, University, Kent, Ohio 442423Department of Biomedical Engineering, College of Engineering,The University of Akron, Akron, Ohio 44242

KEY WORDS facial growth; extant hominoids; fossil hominids

ABSTRACT Growth changes in the position of the midline upper face areexamined for samples of Pan troglodytes, Gorilla gorilla, and modern hu-mans. Horizontal and vertical distances between nasion and the anterior endof the cribriform plate are plotted against stage of dental development.Kendall’s nonparametric correlations between facial positioning and stage ofdental development are tested for significance.

In African apes, the upper face becomes more projecting and positionedhigher relative to the anterior cranial base. The extent of this horizontal andvertical separation reflects primarily facial size. In modern humans, theupper face becomes more projecting but is relatively stable in its verticalposition. Comparison of Pan and modern human crania in the youngestdental age category indicates that the upper face of modern humans ispositioned lower early in postnatal life.

The position of the upper face (glabella) relative to the anterior andposterior cranial base is presented for several fossil hominid crania. The fossilcrania are similar to Pan and modern humans in facial projection relative tothe anterior cranial base. However, glabella is positioned low in the fossilcrania. Total facial projection (relative to hormion) for Sts 5 is similar to themean for Gorilla. Fossil Homo and robust australopithecine crania displayvery projecting upper faces. We suggest that the upper face of Homo isprojecting due to the length of the anterior cranial fossa, while robustaustralopithecines possess a thick frontal bone. Am J Phys Anthropol108:269–280, 1999. r 1999 Wiley-Liss, Inc.

The craniofacial relationship is a criticalfeature of the mammalian skull since itinvolves juxtaposition of cranial componentswith distinct functional roles and develop-mental histories (Kohn, 1991). The positionof the upper face relative to the neurocra-nium varies considerably among early homi-nid crania, and recent ontogenetic studieshave provided a useful perspective for theanalysis of taxonomic variation in facial posi-tioning (Bromage, 1992; McCollum, 1997).

Previous studies have focused on separateaspects of facial positioning. The verticalposition of the upper face is often referred toas facial hafting (McCollum, 1994), while

the horizontal separation between the faceand neurocranium is termed facial projec-tion. Most measurements of facial position-ing have been made relative to externalneurocranial landmarks (Bilsborough andWood, 1988; Schultz, 1955; Tobias, 1967). Aproblem encountered when using externallandmarks is that measurements of facialpositioning may be influenced by variationin the size and shape of the brain.

Grant sponsor: National Science Foundation; Grant number:SBR 9634155.

*Correspondence to: Richard May, Biology Department, Morn-ingside College, 1501 Morningside Avenue, Sioux City, IA 51106–1751. E-mail: [email protected]

Received 16 August 1996; accepted 23 November 1998.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 108:269–280 (1999)

r 1999 WILEY-LISS, INC.

In this study, distances between land-marks of the midline upper face and ante-rior cranial base are used to characterize thecraniofacial relationship. Basic growthchanges in these dimensions remain poorlydocumented for extant hominoids.An advan-tage of our measurements is that they reflectthe craniofacial relationship without includingbrain size as part of the measurement.

We document and discuss growth changesin upper facial positioning for Pan tro-glodytes, Gorilla gorilla, and modern hu-mans. The main objective of this study is todescribe growth changes in upper facialpositioning relative to the internal cranialbase. Growth changes are assessed usingthe stage of dental development as a base-line. Of particular interest is the develop-ment of species differences in upper facialpositioning. The three extant species shouldbe similar in the youngest dental age cat-egory if differences in facial positioning areentirely postnatal in origin. We also presentfacial positioning measurements for fossilhominid crania and interpret species differ-ences as they relate to the results of thegrowth study.

MATERIALS AND METHODS

The sample consists of postnatal growthseries of Pan troglodytes, Gorilla gorilla,and modern human crania which are part ofthe Hamann-Todd collection housed at theCleveland Museum of Natural History. Addi-tional juvenile human crania housed at theArmed Forces Institute of Pathology are alsoincluded. For this analysis, each cranium isassigned a score (DENTAGE) which indi-

cates the number of permanent maxillarymolars in occlusion. DENTAGE is coded asfollows: 0, deciduous molars; 1, first perma-nent molars; 2, second permanent molars; 3,third permanent molars. The stage of dentaldevelopment is a useful baseline for exami-nation of growth changes (Ashton, 1957;Laitman et al., 1978), and our classificationsystem provided sufficient discriminationamong crania to detect growth changes.

Measurements of the position of nasionrelative to the anterior cranial base areshown in Figures 1 and 2. On tracings fromlateral radiographs, a perpendicular fromnasion is projected onto a line defined bytuberculum sella and the anterior end of thecribriform plate (at the intersection with theinternal contour of the frontal bone). Thelatter point is designated the anterior basepoint (abp). Vertical (NAVERT) and horizon-tal (NAHOR) distances between nasion andthe anterior base point were measured us-ing Mitutoyo digimatic calipers. Radio-graphic measurements are corrected for en-largement using the distance between themedian plane of the cranium and the radio-graphic film. The correction was found to bequite accurate; mean differences betweencorrected radiographic measurements andcorresponding caliper measurements are lessthan 1 mm. As illustrated in Figure 1,projection of nasion beyond the anterior endof the cribriform plate (NAHOR) reflects inlarge part the thickness of the frontal bone.The vertical separation between these points(NAVERT) (Fig. 2) may be primarily a reflec-tion of total facial height (see below).

Fig. 1. Measurements of upperfacial projection. NAHOR andGABHOR are horizontal distancesbetween the upper face and theanterior base point. These dis-tances are measured along a linedefined by tuberculum sella andthe anterior base point. GHHOR isthe horizontal distance between theupper face and hormion taken alongthe opisthion-hormion line.

270 R. MAY AND D.B. SHEFFER

The two measurements of facial position-ing are plotted against DENTAGE. Correla-tions between facial positioning measure-ments and DENTAGE are calculated foreach species. Since one of the variables isonly ordinal in scale, a nonparametric corre-lation coefficient (Kendall’s tau) is tested forsignificance. Correlations are tested for totaland single-sex samples.

Facial positioning measurements were col-lected for several early hominid crania. Sincethe front-nasal suture at nasion is fre-quently obliterated in adult crania, glabellawas used instead to indicate the midlineposition of the upper face. Glabella is notintended as a surrogate landmark for nasionsince the relationship between nasion andglabella is not constant. To describe therelationship between nasion and glabella,we calculated vertical and horizontal dis-tances between these landmarks (relative tothe anterior cranial base line) for adult samplesof our three species. For every individual ineach species, glabella is positioned superiorand anterior to nasion. The vertical separa-tion between these landmarks is greaterthan the horizontal. Thus, there is at least aconsistent relationship between glabella andnasion in our extant groups, and we suggestthat the results of our growth study may beused to interpret variation in upper facialpositioning using glabella.1

The horizontal (GABHOR) and vertical(GABVERT) position of glabella relative tothe anterior cranial base was calculatedusing coordinate data for original specimensattributed to Australopithecus africanus (Sts5, housed at the Transvaal Museum) and forA. aethiopicus (KNM WT 17000, housed atthe Kenya National Museum). These mea-surements were also calculated for a digi-tized cast of a specimen attributed to archaicHomo sapiens (Arago). These measurementswere calculated trigonometrically from coor-dinate data using an angle (tuberculumsella–anterior base point–glabella) and adistance (anterior base point–glabella).

Since internal landmarks are often inac-cessible in fossil crania, the position of gla-bella was also assessed relative to the poste-rior cranial base. These measurements werederived from coordinate data collected fromoriginal fossil crania. Vertical (GHVERT)and horizontal (GHHOR) distances betweenglabella and hormion were derived fromcoordinate data collected for each skull (Figs.1, 2). Using an angle (nasion–hormion–opisthion) and a distance (nasion–hormion),a perpendicular from nasion is projected tothe opisthion-hormion line and distancescalculated trigonometrically. Measurementsrelative to hormion were calculated for fossilcrania attributed to A. africanus (Sts 5), A.boisei (KNM ER 406), and Homo erectus(KNM ER 3733). Coordinates were also col-lected from a cast of a specimen attributed toarchaic Homo sapiens (Kabwe). These mea-surements are compared to adult means for

1For adult Pan, the mean vertical distance between glabellaand nasion is 9.3 mm (S 5 2.8, n 5 21), and the mean horizontaldistance is 3.0 mm (S 5 1.4). Distances for adult Gorilla weresimilar to those for Pan. In modern humans, the mean verticaldistance is 12.4 mm (S 5 3.1, n 5 38), and the mean horizontaldistance is 4.3 mm. (S 5 1.5).

Fig. 2. Measurements of verti-cal facial positioning. NAVERT andGABVERT are vertical distancesbetween the upper face and theanterior base point. GHVERT isthe vertical distance between theupper face and hormion.

271GROWTH CHANGES IN FACIAL POSITIONING

African apes and modern humans, and spe-cies differences are discussed in relation tothe growth study.

RESULTS

Table 1 lists summary statistics forNAHOR and NAVERT by DENTAGE andsex for Pan. Table 2 lists Kendall’s taucoefficients for correlations between facialpositioning measurements and DENTAGEfor all three species. In Pan, upper facialprojection increases from the dm to M3stage in the total and single-sex samples(Fig. 3a). Males ultimately attain a moreprojecting face than females. NAVERT in-creases from dm to M3 stage (Tables 1, 2).

While the t-test for sex differences in adultsindicated that males have a face positionedhigher relative to the cribriform plate, thedifference is not as large as for facial projec-tion. In the youngest age category, Pan andmodern humans are not significantly differ-ent in the degree of upper facial projection.

Table 3 presents summary statistics forfacial positioning measurements in Gorilla.Facial projection increases significantly fortotal and single-sex samples. Males attain amore projecting upper face than females,and divergence between males and femalesseems to occur after the M2 stage (Table 3;Fig. 3b). NAVERT also increases in total andmales-only samples (Table 3; Fig. 4b). Wedid not detect a significant increase inNAVERT for female gorillas. This is prob-ably due to small sample size for this sub-group since total facial height does increasein female gorillas during postnatal growth(Moore and Lavelle, 1974). The upper face ofadult males is positioned higher than that offemales. At the M1 stage, nasion in Gorillais higher relative to the anterior base seg-ment than in Pan at the same stage.

Table 4 lists summary statistics for facialpositioning measurements in modern hu-mans. Upper facial projection increases inmodern humans in the total and single-sexsamples. The greatest increase occurs be-tween the dm and M1 stage (Table 4; Fig.3c). NAVERT increases slightly in the totaland males-only samples. The t-test indicatesthat the upper face of modern humans ispositioned lower than that of Pan in theyoungest dental age category.

Variation among fossil hominid crania

Table 5 lists measurements of upper facialpositioning (relative to both cranial basepoints) for selected fossil hominid crania.Figure 5 plots measurements of facial posi-tioning relative to the anterior base point forAfrican apes, modern humans, and fossilhominids. The fossil crania are quite uni-form in the degree of facial projection andare most similar to Pan and modern humanmales (Fig. 5a). The upper face of the fossilcrania is positioned lower than that of Afri-can apes, and all three fossil crania are atthe low end of the modern human range forthis measurement (Fig. 5b).

TABLE 1. Mean and standard error of the meanfor (NAHOR) and (NAVERT) in Pan1

DENTAGE

NAHOR NAVERT

Mean SEM Mean SEM

0 (U) 10.7 (5) 0.3 7.2 1.21 (T) 14.6 (12) 0.9 8.4 1.2

(M) 12.2 (1) — 5.1 —(F) 16.9 (5) 1.2 11.2 0.9(U) 13.0 (6) 1.1 6.7 1.9

2 (T) 17.5 (14) 0.6 10.7 1.1(M) 18.3 (4) 1.8 10.1 2.7(F) 17.2 (7) 0.5 11.2 1.5(U) 17.1 (3) 0.8 10.4 2.1

3 (T) 22.4 (22) 0.7 14.2 0.7(M) 23.8 (11) 1.1 14.5 1.0(F) 20.9 (11) 0.6 14.0 0.9

1 All measurements are in millimeters. Sample sizes are inparentheses next to the mean values. NAHOR, horizontaldistance between nasion and the anterior base point; NAVERT,vertical distance between nasion and the anterior base point; T,total sample; M, males; F, females; U, sex unknown.

TABLE 2. Correlations between measurementsof facial positioning and DENTAGE1

NAHOR NAVERT

PanT .72** (53) .49**M .56** (16) .44*F .61** (23) .33*

GorillaT .75** (44) .37**M .81** (18) .58**F .67** (21) .27

Modern humansT .55** (61) .27**M .30* (39) .29*F .67** (18) .24

1 Sample sizes for each correlation are in parentheses next tomeans for NAHOR. DENTAGE, score that indicates the numberof permanent maxillary molars in occlusion; NAHOR, verticaldistance between nasion and the anterior base point; T, totalsample; M, males only; F, females only.* P , .05.** P , .01.


Fig. 3. NAHOR plotted againstDENTAGE for Pan (a), Gorilla (b)and modern humans (c).

Figure 6 compares horizontal and verticaldistances between glabella and hormion.The upper face of Sts 5 is more projectingthan that of Pan and is most similar to themean for female Gorilla (Fig. 6a). The upperface of KNM ER 406 is closest to the meanfor modern human males. The archaic Homosapiens specimen (Kabwe) and KNM ER3733 are at the upper end of the modernhuman range in terms of upper facial projec-tion.

The upper faces of the two australopithe-cine crania (Sts 5 and KNM ER 406) arepositioned lower than those of African apesbut higher than in modern humans. In thetwo genus Homo crania (Kabwe and KNMER 3733), the upper face is positionedslightly higher than that of modern humans.

DISCUSSION

The pattern of growth changes in theupper face relative to the cranial base inAfrican apes has not been well documentedin previous studies. The growth pattern oftheir middle and lower face is generallycharacterized as downward and forward(Krogman, 1931a,b). Krogman used superim-posed tracings of growth series of apes todocument the growth pattern of the cra-nium. However, the skulls were orientedalong a nasion-porion registration line, thusobscuring changes in the position of theupper face relative to the cranial base.

In this study, upper facial projection wasfound to increase in African apes, with Go-rilla ultimately attaining the most project-ing upper face. By the eruption of the firstpermanent molar, the upper face of Gorillais positioned much higher than that of Pan.Growth changes in these measurements offacial positioning inAfrican apes are presum-ably secondary to a general increase in thedimensions of the upper face. Supero-infe-rior and antero-posterior expansion of theupper facial skeleton leads to horizontalseparation between the inner and outertables of the frontal bone and to verticalseparation between nasion and the plane ofthe anterior cranial base (see below). Thus,we suggest that differences in upper facialpositioning between Pan and Gorilla arelargely the result of differences in facial size.

Previous experimental studies have docu-mented a different growth pattern for su-tural landmarks of the middle and lowerface. In a longitudinal implant study, Sarnat(1976) found that these sutural landmarksmoved anteriorly and inferiorly relative tothe floor of the anterior cranial fossa.

Although sample sizes are small, thisstudy reveals sex differences in the ontogenyof facial positioning in Gorilla. Sex differ-ences in facial projection seem to arise afterthe M2 stage, while differences in the verti-cal position are already evident at the M2stage. We detect little change in verticalfacial positioning in female gorillas betweenthe M1 and M3 stages.

Previous studies have attempted to ex-plain underlying mechanisms of sexual di-morphism in anthropoids. Sirianni and VanNess (1978) suggested that sex differencesin adult macaque cranial base dimensionswere the result of the increased rate andduration of growth in males. In a recentstudy (Leigh and Shea, 1996), adult bodysize dimorphism in Gorilla was found toresult from a combination of sex differencesin the rate and duration of somatic growth.Since systemic growth exerts a greater effecton facial dimensions than on other skullcomponents (Ravosa, 1991), sex differencesin facial positioning may be the result ofsimilar ontogenetic mechanisms.

Leigh and Shea (1996) also concludedthat, in Gorilla, male and female somatic

TABLE 3. Mean and standard error of the meanfor NAHOR and NAVERT in Gorilla1

DENTAGE

NAHOR NAVERT

Mean SEM Mean SEM

0 (T) 15.2 (6) 0.8 13.8 1.8(M) 18.1 (1) — 15.1 —(F) 13.2 (1) — 10.8 —(U) 14.9 (4) 0.5 14.3 2.6

1 (T) 22.2 (9) 1.1 18.1 1.4(M) 22.0 (4) 1.2 18.6 1.6(F) 22.4 (5) 1.8 17.8 2.3

2 (T) 26.7 (15) 0.8 23.1 1.6(M) 27.8 (8) 0.9 26.5 2.2(F) 26.2 (6) 1.4 18.9 1.4(U) 20.7 (1) — 20.5 —

3 (T) 34.5 (14) 1.9 24.2 2.0(M) 40.2 (5) 4.0 31.2 2.6(F) 31.3 (9) 0.8 20.4 1.9

1 All measurements are in millimeters. Sample sizes are inparentheses next to the mean values. F, females; M, males;NAHOR, vertical distance between nasion and the anterior basepoint; NAVERT, horizontal distance between nasion and theanterior base point; T, total sample; U, sex unknown.


Fig. 4. NAVERT plotted againstDENTAGE for Pan (a), Gorilla (b)and modern humans (c).

growth trajectories diverge approximatelybetween 6 and 7 postnatal years. The timingof ontogenetic divergence in general somaticgrowth trajectories is at least consistentwith the divergence in our measurements offacial positioning. In the present study, sexdifferences in facial positioning were evidentafter the eruption of the first permanentmolar, which is largely complete by 4 yearsof age (Aiello and Dean, 1990).

Growth changes in upper facial projectionhave been described for modern humans.Knott (1971) measured frontal bone thick-ness (nasion to posterior wall of frontalsinus) in a longitudinal sample of modernhumans aged 5 to adult. Upper facial projec-tion increased gradually in both sexes, andon average the increase was greater in malesthan in females. Scott (1958) documented anincrease in the distance between nasion and

foramen cecum from birth to adulthood.Early, rapid increase in this dimension wasfollowed by stability during early adoles-cence and then a regular increase to adult-hood. This pattern of change is similar to theone documented in the present study. Al-though there appears to be no increase inthe facial projection from the M1 to M2 stage(Fig. 3), four of the five M2 individuals arefemales. As sex differences in facial position-ing are evident by this stage (Knott, 1971),overall increase in this dimension may beobscured.

The vertical position of the face has beenfound to be relatively stable in modern hu-mans during postnatal development. Ford(1958) examined growth changes in theheight of nasion above the cribriform planein modern humans aged neonatal to adult.As in the present study, no regular increase

TABLE 4. Mean and standard error of the meanfor NAHOR and NAVERT in modern humans1

DENTAGE

NAHOR NAVERT

Mean SEM Mean SEM

0 (T) 9.5 (9) 1.0 1.4 0.3(M) 10.0 (3) 2.0 0.8 0.2(F) 9.8 (5) 1.3 1.3 0.4(U) 6.4 (1) — 3.1 —

1 (T) 17.3 (3) 1.7 2.5 0.6(M) 20.5 (1) — 3.7 —(U) 15.7 (2) — 1.9 0.4

2 (T) 15.0 (5) 1.2 3.8 0.6(F) 15.3 (4) 1.0 3.6 0.8(U) 13.6 (1) — 4.4 —

3 (T) 19.4 (44) 0.5 4.0 0.4(M) 20.1 (35) 0.5 4.1 0.5(F) 16.8 (9) 0.3 3.3 0.9

1 All measurements are in millimeters. Sample sizes are inparentheses next to the mean values. F, females; M, males;NAHOR, vertical distance between nasion and the anterior basepoint; NAVERT, horizontal distance between nasion and theanterior base point; T, total sample; U, sex unknown.

TABLE 5. Measurements of upper facial positioningfor fossil hominid crania1

GABHOR GABVERT GHHOR GHVERT

KNM WT17000 24.9 7.7 — —

KNM ER406 — — 72.5 50.3

Sts 5 27.2 9.5 58.9 48.1KNM ER

3733 — — 79.2 28.8Arago 26.3 9.8 — —Kabwe — — 85.8 28.61 GABHOR and GABVERT are distances (in millimeters)between glabella and the anterior base point. GHHOR andGHVERT are distances between glabella and hormion.

Fig. 5. Boxplots of GABHOR (a) and GABVERT (b)for African ape, modern human, and several fossilhominid crania. The vertical line in the box is themedian, and the limits of the box represent the 50%range. The whiskers indicate the maximum and mini-mum values.


in this dimension was found. Adult dimen-sions for his measurement are slightly higherthan reported here, probably owing to theslight difference in the reference line.

The results of this study indicate thatdifferences between African apes and mod-ern humans in the vertical position of nasionare established during prenatal or earlypostnatal development. Compared to Pancrania in the deciduous molar category, mod-ern human crania have an upper face posi-tioned significantly lower relative to theanterior base segment. However, Pan andmodern humans are initially quite similarin the projection of the upper face. Theseearly differences in vertical facial positionmay relate to species differences in thepattern of early brain growth.

Possible mechanisms of changein facial positioning

Depending upon which cranial base refer-ence point is used, measurements of upper

facial positioning may reflect growthprogress of somatic and neural functionalmatrices contiguous with the cranial baseand face. Measurements of facial projectionrelative to the anterior end of the cribriformplate reflect separation between inner andouter tables of the frontal bone. Corticaldrift of the external table of the frontal boneleads to an increase in upper facial projec-tion (Enlow, 1990). Growth of the facialaspect of the frontal bone is a compromisebetween the demands of functional matricessuch as orbital contents, respiratory mu-cosa, and hematopoietic diploe within thebone (Moss and Young, 1960). Antero-poste-rior growth of the upper facial complex mayalso reflect growth of nasal, pharyngeal, andeven oral matrices (Moss, 1962). The factthat experimental hydrocephaly in rats hadminimal effect on the morphology of theupper facial skeleton (Moss and Young, 1960)suggests that separation between inner andouter tables of the frontal bone is not di-rectly related to neural expansion.

Ontogenetic changes in the vertical posi-tion of nasion relative to the anterior basesegment reflect compensatory growth at thefrontonasal suture. Superior displacementof the upper face relative to the anteriorcranial base in apes is possible given thespatial relationship between the face andthe anterior pole of the brain. Superiorgrowth of the upper face in prevented inmodern humans by the presence of the over-lying neural mass.

Gross spatial relationships between bonesof the neurocranial and facial skeleton maybe established during fetal life in humans(Moss et al., 1956). Minor adjustments offacial position (mostly projection) occur dur-ing postnatal development. The fact that, inthe youngest age category, the upper face ofmodern humans is positioned lower than inPan suggests that differences in facial posi-tioning extend to the prenatal period. Thesedifferences in vertical facial positioning mayrelate to prenatal differences in the rate ofcerebral expansion. Cerebral expansion inmodern humans has been linked to reposi-tioning of the upper facial skeleton (Biegert,1963; Weidenreich, 1941).

Pan and modern human crania are simi-lar in the measurement of frontal bone

Fig. 6. Boxplots of GHHOR (a) and GHVERT (b) forAfrican ape, modern human, and several fossil hominidcrania.


thickness (GABHOR) (Fig. 5). However,when upper facial projection is assessedrelative to hormion (GHHOR) (Fig. 6), mod-ern humans have very projecting upper faces.This difference reflects species differences inthe length of the anterior cranial fossa.Measurements of upper facial projection rela-tive to points along the posterior cranialbase (e.g., hormion) reflect both frontal bonethickness and the length of the anteriorcranial fossa. The length of the anteriorcranial fossa in turn is influenced in largepart by the length of the frontal lobes of thebrain. Thus, the relatively large frontal lobesof modern humans contribute greatly to themeasurement of total facial projection.

In humans, growth at the fronto-ethmoi-dal suture until about 7 years of age facili-tates expansion of the frontal lobes of thebrain (Bjork, 1955; Scott, 1958). After thistime, any increase in total facial projection(GHHOR) must be accomplished primarilyby bone deposition at nasion. Given therelatively small frontal lobes of Gorilla com-pared to modern humans, upper facial projec-tion in Gorilla is strongly influenced by thethickness of the frontal bone.

Variation among fossil hominid crania

Comparison of facial positioning relativeto the anterior and posterior cranial basereveals an interesting pattern of interspe-cific variation. Although these dimensionsare partly a function of cranial size, thepattern of variation suggests fundamentalspecies differences in both aspects (verticaland horizontal) of the craniofacial relation-ship which are unrelated to cranial size.Relative to the anterior cranial base, austra-lopithecine crania are similar to Africanapes in the degree of facial projection. How-ever, measurements from hormion indicatethat the upper face of Sts 5 is more project-ing than that of Pan and that that of KNMER 406 is similar to modern humans. Sincethe anterior component of facial projection(GABHOR) in Sts 5 is very similar to Pan,the greater degree of projection relative tohormion may reflect a long anterior cranialfossa.

It is unlikely that extreme facial projec-tion in the A. boisei specimen is related tothe length of the anterior cranial fossa. As

noted earlier, facial projection from hormionreflects both the length of the frontal lobesand the separation between the face andanterior cranial base. Since the frontal lobesof robust australopithecines seem to havebeen small (Holloway, 1988), extreme facialprojection in KNM ER 406 probably indi-cates considerable separation between theupper face and the anterior terminus of thecranial base.

The crania attributed to Homo erectus(KNM ER 3733) and archaic Homo sapiens(Kabwe) are most similar to modern hu-mans in upper facial positioning. These speci-mens have quite projecting upper faces rela-tive to hormion. The anterior component offacial projection (GABHOR) could not bemeasured for these specimens. Thus, theirextreme facial projection could reflect a longanterior cranial fossa and a thick frontalbone.

Relative to the anterior cranial base, theupper face of australopithecines and archaicHomo sapiens is positioned quite inferiorly.This measurement of facial positioning inSts 5 is consistent with previous descrip-tions. Ashton and Zuckerman (1951) andTobias (1967) found that, according to thesupraorbital height index, Sts 5 was similarto modern humans in the vertical position ofthe upper face. The inferior position of theupper face in KNM WT 17000 is surprising,given the generally primitive nature of thisspecimen. However, specialized enlarge-ment of the masticatory apparatus whichcharacterizes this specimen might also alterthe growth pattern of the upper face. Unfor-tunately, it was not possible to collect thismeasurement for later robust australopithe-cine crania.

Relative to hormion, the australopithe-cine upper face is positioned lower than thatof Gorilla and Pan but higher than that ofmodern humans. Using a supraorbital heightindex developed by Le Gros Clark (1950),previous studies have found that the robustaustralopithecine face is hafted high rela-tive to the top of the neurocranium (Ashtonand Zuckerman, 1951; Tobias, 1967). Usinga different measurement of facial position-ing, McCollum (1994) also concluded thatthe Paranthropus upper face is positionedhigh relative to the cranial base. Measure-


ments of facial positioning relative to theanterior cranial base would improve ourunderstanding of the craniofacial relation-ship in robust australopithecines.

The inferior position of the face in speci-mens attributed to archaic Homo sapiens isconsistent with the large anterior cranialfossae in these specimens. Expansion of thefrontal lobes of the brain may have alteredthe craniofacial relationship early in devel-opment, restricting superior growth of theface.

CONCLUSIONS

We have documented growth changes inthe craniofacial relationship for Pan, Go-rilla, and modern humans. Measurement ofupper facial positioning relative to the inter-nal cranial base is preferable to previousmethods because the influence of brain sizeand shape is minimized. Although only onelandmark of the upper face was utilized inthis study, we feel that this is an importantstep toward better characterization of thecraniofacial relationship.

Further work on the influence of prenataland early postnatal brain growth on thefacial growth pattern is needed to interpretspecies differences in facial positioning. Inaddition, growth of the entire facial skeletonrelative to the internal cranial base shouldbe better characterized.

Variation in upper facial positioningamong fossil hominid crania reflects speciesdifferences in the relative size of endocranialand facial dimensions. We suggest that fron-tal lobe expansion increased total facial pro-jection in Homo erectus and archaic Homosapiens crania and may have limited supe-rior facial growth. Expansion of the mastica-tory apparatus may relate to upper facialpositioning in robust australopithecine cra-nia. However, further research in this areais needed to clarify the effects of masticatoryexpansion on the facial growth pattern. As-sessments of facial position in fossils shouldbe made relative to the internal and exter-nal cranial base to evaluate the relativeimportance of neural and nonneural softtissue influences on the position of the upperface.

ACKNOWLEDGMENTS

We thank Dr. Bruce Latimer for permis-sion to examine extant hominoid crania atthe Cleveland Museum of Natural Historyand Lyman Jellima (CMNH) for assistancein data collection. We also thank Drs. MeaveLeakey, Francis Thackeray, and Lee Bergerfor permission to examine fossil hominidcrania in their care. Three reviewers offereduseful advice. This project was supported bya National Science Foundation dissertationimprovement grant (SBR 9634155) to R.L.M.

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Growth changes in measurements of upper facial positioning

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