Taylor AB, 2002. Masticatory form and function in the African apes. Am J Phys Anthropol. 117,...

Masticatory Form and Function in the African ApesAndrea B. Taylor*

Departments of Community and Family Medicine/Division of Physical Therapy and Biological Anthropology andAnatomy, Duke University Medical Center, Durham, North Carolina 27710

KEY WORDS African apes; masticatory form; biomechanics; ontogeny; allometry; evolution

ABSTRACT This study examines variability in masti-catory morphology as a function of dietary preferenceamong the African apes. The African apes differ in thedegree to which they consume leaves and other fibrousvegetation. Gorilla gorilla beringei, the eastern mountaingorilla, consumes the most restricted diet comprised ofmechanically resistant foods such as leaves, pith, bark,and bamboo. Gorilla gorilla gorilla, the western lowlandgorilla subspecies, consumes leaves and other terrestrialherbaceous vegetation (THV) but also consumes a fairamount of ripe, fleshy fruit. In contrast to gorillas, chim-panzees are frugivores and rely on vegetation primarily asfallback foods. However, there has been a long-standingdebate regarding whether Pan paniscus, the pygmy chim-panzee (or bonobo), consumes greater quantities of THVas compared to Pan troglodytes, the common chimpanzee.Because consumption of resistant foods involves moredaily chewing cycles and may require larger average biteforce, the mechanical demands placed on the masticatorysystem are expected to be greater in folivores as comparedto primates that consume large quantities of fleshy fruit.Therefore, more folivorous taxa are predicted to exhibitfeatures that improve load-resistance capabilities and in-crease force production.

To test this hypothesis, jaw and skull dimensions werecompared in ontogenetic series of G. g. beringei, G. g.gorilla, P. t. troglodytes, and P. paniscus. Controlling for

the influence of allometry, results show that compared toboth chimpanzees and bonobos, gorillas exhibit some fea-tures of the jaw complex that are suggestive of improvedmasticatory efficiency. For example, compared to all othertaxa, G. g. beringei has a significantly wider mandibularcorpus and symphysis, larger area for the masseter mus-cle, higher mandibular ramus, and higher mandibularcondyle relative to the occlusal plane of the mandible.However, the significantly wider mandibular symphysismay be an architectural response to increasing symphy-seal curvature with interspecific increase in size. More-over, Gorilla and Pan do not vary consistently in all fea-tures, and some differences run counter to predictionsbased on dietary variation. Thus, the morphological re-sponses are not entirely consonant with predictions basedon hypothesized loading regimes. Finally, despite morpho-logical differences between bonobos and chimpanzees,there is no systematic pattern of differentiation that canbe clearly linked to differences in diet. Results indicatethat while some features may be linked to differences indiet among the African apes, diet alone cannot account forthe patterns of morphological variation demonstrated inthis study. Allometric constraints and dental developmentalso appear to play a role in morphological differentiationamong the African apes. Am J Phys Anthropol 117:133–156, 2002. © 2002 Wiley-Liss, Inc.

The African apes vary in craniodental form inways that may reflect dietary differences related todegree of frugivory vs. folivory (Krogman, 1931a,b;Giles, 1956; Schultz, 1969; Jolly, 1970; Shea, 1983a;Kinzey, 1984; Spears and Crompton, 1996; Uchida,1996, 1998). For example, several investigators haveshown that chimpanzees are characterized by largeincisors relative to both body mass (Hylander, 1975)and skull size (Shea, 1983a), a dental pattern thathas been linked adaptively to extensive incisal prep-aration of large, resistant fruits (Jolly, 1970; Hy-lander, 1975; Shea, 1983a). By contrast, gorillashave relatively smaller incisors coupled with a rel-atively enlarged and sharper-cusped postcaninedentition (Shea, 1983a; Uchida, 1996; Spears andCrompton, 1996), all of which suggest an efficientshearing mechanism that appears to reflect theirfolivorous diet (Kay, 1975; Kay and Covert, 1984).Differences in dental morphology between chimpan-zees and bonobos (Kinzey, 1984; cf. Uchida, 1996)

and among subspecies of Gorilla (Groves, 1970;Uchida, 1998; Taylor, 1998) have also been associ-ated with dietary variation and the extent to whichthese taxa consume a diet of herbaceous vegetationvs. fruits.

Shea (1983a,b, 1985a,b), in his landmark studiesof skull form in the African apes, additionally re-veals a number of departures from common patternsof relative growth, some of which may representmorphological adaptations to dietary variation. Forexample, Shea (1983a) noted that the nasal aperture

Grant sponsor: L.S.B. Leakey Foundation; Grant sponsor: SamuelMerritt College.

*Corespondence to: Andrea B. Taylor, Doctor of Physical TherapyProgram, Duke University Medical Center, Box 3965, Durham, NC27710. E-mail: [email protected]

Received 9 March 2000; accepted 9 August 2001.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 117:133–156 (2002)

© 2002 WILEY-LISS, INC.DOI 10.1002/ajpa.10013

is positioned relatively more inferiorly in gorillas ascompared to chimpanzees, a feature he suggestedmight be diet-related, in the sense that the position-ing of the aperture may reflect the relatively smallerincisors of gorillas. He also noted allometric differ-ences associated with the extreme development ingorillas of sagittal cresting produced by the relativeenlargement of the temporal musculature. Adult dif-ferences between G. g. gorilla and G. g. beringei incertain aspects of the lower jaw (Vogel, 1961;Groves, 1970) have also been observed, and Groves(1970) explicitly proposed that the jaw morphologyof G. g. beringei reflects an intensification of differ-ences between chimpanzees and gorillas as a func-tion of the mountain gorilla’s highly specialized dietof fibrous vegetation.

Variation in African ape craniodental morphologysuggests that these taxa may exhibit features of thejaw complex that represent adaptive responses tomastication and diet, yet surprisingly jaw form inthe African apes has been relatively ignored. Dae-gling (1989, 1990) provides a detailed evaluation ofthe internal geometry of adult mandibles, and ananalysis of mandibular growth using an outline ap-proach (Daegling, 1996), in G. g. gorilla and Pantroglodytes. Apart from these studies, there has beenno comprehensive morphometric analysis of man-dibular form among the African apes, particularly ina comparative context including G. g. beringei, ar-guably the most specialized towards a diet of herba-ceous vegetation. Further, no one has attempted totease apart the effects of size variation from nonal-lometric differences in identifying adaptations of themasticatory complex based on standard morphomet-ric measurements. Therefore, I use ontogenetic al-lometry to investigate masticatory morphologyamong the African apes and to evaluate whethermorphological differences are the predictable conse-quences of dietary variation. In this investigation,results of prior comparative studies are integratedwith in vivo experimental data on patterns of stressin the mandibular corpus during mastication (Hy-lander, 1979a,b, 1984, 1985a), to test predictions ofhow the African ape masticatory apparatus shouldbe expected to vary as a function of dietary prefer-ence.

AFRICAN APE DIET

Studies of African ape feeding ecology reveal dif-ferences in the types of foods consumed and howfoods are prepared, both within and among species.Gorilla subspecies and even local populations arecharacterized by seasonal differences in food avail-ability and in dietary composition (Williamson et al.,1990; Tutin and Fernandez, 1993; Yamagiwa et al.,1996; Remis, 1997). G. g. beringei has the most re-stricted diet, consuming only leaves, pith, bark, andother terrestrial herbaceous vegetation (THV), andbamboo when seasonally present (Watts, 1984). Bycontrast, the diet of G. g. gorilla is considerablymore diverse, the latter demonstrating a manifest

preference for ripe, fleshy fruit whenever available(Tutin et al., 1997). Nevertheless, while westernlowland gorillas may be the “frugivores” of gorillas(Tutin, 1996), G. g. gorilla is not an obligate frugi-vore, and gorillas as a group are more folivorousthan chimpanzees. Gorillas consume less fruit thanchimpanzees, particularly during poor fruit seasons(Remis, 1997; Tutin et al., 1997), and depend onTHV, including leaves, pith, bark, and seeds whenfruit is unavailable (Kuroda et al., 1996; Tutin et al.,1997). While gorillas and chimpanzees overlap inmuch of their fruit consumption, there appears to beminimal overlap in herbaceous foods (Kuroda et al.,1996). During the dry season, gorillas also eat fi-brous fruits that chimpanzees do not eat, althoughsuch fruits are equally available to both (Tutin et al.,1997). Access to some fibrous vegetation requiresthat gorillas strip the fibrous outer layers fromstems, bark, and bamboo, suggesting that thesefoods are particularly mechanically difficult to pro-cess (Tutin et al., 1997). In addition, western low-land gorillas masticate fruit seeds, many of whichcontain tannins or toxins (Williamson et al., 1990;Rogers et al., 1990; Kuroda et al., 1996), and G. g.gorilla is reportedly the only species (other thanadult male mandrills) strong enough to breakthrough the hard protective shell of the Detariummacrocarpum seed (Tutin et al., 1997), which theyprocess for the inner fibrous fruit as well as ingest.

By contrast, chimpanzees rely on a diet dominatedby fruit and, unlike even the most frugivorous ofgorillas, maintain a fruit-dominated diet even intimes of fruit scarcity (Tutin et al., 1997). Like go-rillas, however, chimpanzees are also characterizedby a pattern of local variation in foraging and di-etary behavior. In particular, there has been a long-standing debate over whether bonobos consumemore THV than chimpanzees (Badrian andMalenky, 1984; Kano and Mulavwa, 1984; Wrang-ham, 1986; Malenky and Stiles, 1991; Malenky andWrangham, 1994; Malenky et al., 1994). Bonoboshave been noted to closely parallel gorillas in theirpreference for, and consumption of, herbaceousfoods (Malenky and Wrangham, 1994). In fact, agreater reliance on THV has been used to explainthe relaxed feeding competition observed in bonoboscompared to chimpanzees (Chapman et al., 1994;White, 1996; Wrangham et al., 1996). The evidencefor a greater degree of THV consumption by bono-bos, however, is far from clear, particularly in lightof the fact that the greater availability of THV insome chimpanzee populations has not resulted inthe predicted differences in party size, food prefer-ence, and feeding competition (Wrangham et al.,1996). Furthermore, Wrangham et al. (1996) refinedthe THV hypothesis to more accurately reflect thebonobo’s preference for high-quality THV, which in-cludes foods rich in protein but low in cellulose con-tent. In addition to ecological data, cranial (Cramer,1977) and dental (Johanson, 1974a,b; Kinzey, 1984;McCollum and McGrew, 2001) differences have been

134 A.B. TAYLOR

used as indicators of a more herbaceous diet in bo-nobos, although these data appear no more conclu-sive than dietary data in resolving this debate (cf.Kinzey, 1984; Uchida, 1996).

There is little in the way of data to directly ad-dress the hypothesis that foods consumed by someAfrican apes are mechanically tougher to processthan foods consumed by other species. The only pub-lished data quantifying the physical properties offoods consumed by any of the African apes are pre-liminary, and indicate that Virunga mountain goril-las consume tougher leaves than do Bwindi moun-tain gorillas (Elgart, 1999). Among the foods tested,leaves reportedly had relatively lower toughnessvalues than other foods consumed by these two taxa.Unfortunately, these results are not particularly in-formative in terms of the specific mechanical prop-erties of foods eaten among the African apes, or evenbetween gorilla populations that vary in diet. Giventhe specialized nature of the mountain gorilla diet, itis certainly reasonable to conclude that differencesin the mechanical properties of foods consumed bythese two local populations of mountain gorillas donot reflect mechanical differences between frugivoryand folivory.

What is well-established is that plants and leavesare protected against herbivory primarily throughthe structural complexities of the cell walls (Choonget al., 1992; Choong, 1996; Lucas et al., 2000).Woody plants in particular, which include bark andbamboo, are characterized by an effective plasticintracellular collapsing mechanism in their second-ary cell walls, rendering these plants exceptionallytough (Lucas et al., 2000). Moreover, the nutritionalcontent of leaves in particular is very low (Bauchop,1978; Demment and van Soest, 1985), which sug-gests that the nutritional needs of folivores can beadequately met only if large quantities of leaves arewell-masticated.

Results of experimental and comparative studiesare informative and serve to guide our expectationsregarding variation in jaw form and masticatorybiomechanics in the African apes. For example, elec-tromyographical studies in papionins reveal intra-muscular variation in unloading times of jaw mus-cles as a function of food type, with significantlylonger unloading times associated with the mastica-tion of mechanically tougher foods (Hylander andJohnson, 1994). As evidenced by experimental datafor several anthropoid primate taxa, the masticationof tougher foods involves the recruitment of rela-tively greater amounts of balancing-side muscleforce, particularly the balancing-side deep massetermuscle (Luschei and Goodwin, 1974; Hylander andJohnson, 1985, 1994; Hylander and Crompton, 1986;Hylander et al., 1992, 2000). Furthermore, and ofparticular relevance to folivores, primates that con-sume large amounts of folivorous material risk fa-tigue failure of the corpus and symphysis from re-petitive loading of the jaws during mastication(Hylander, 1979a, 1985a). Thus, there is experimen-

tal and morphological evidence to support the hy-pothesis that mastication of resistant foods involvesmore daily chewing cycles and requires larger aver-age bite forces than the mastication of soft, pulpyfruits (Walker and Murray, 1975; Beecher, 1977;Hylander, 1979a,b; Lucas et al., 2000).

In the absence of experimental data for Africanapes, I draw on results of comparative studies whichhave collectively demonstrated mechanical differ-ences associated with the mastication of tough foods,and a more robust jaw apparatus in primates whomasticate a tougher diet as compared to closely re-lated congeners with softer diets (DuBrul, 1977; Hy-lander, 1979a–c, 1985a,b; Bouvier, 1986a,b; Dae-gling, 1992; Ravosa, 1990, 1991, 1996a,b; Takahashiand Pan, 1994; Pan et al., 1995; Anton, 1996a; Tay-lor, in press). Chimpanzees are frugivores, whereaswestern lowland gorillas are opportunistic fruit eat-ers. Thus, I assume that reliance on fruit by chim-panzees, even during times of fruit scarcity, is acritical ecological difference that provides a biome-chanical basis for predicting morphological distinc-tions between gorillas and chimpanzees. As G. g.beringei is restricted to a nonfruit diet comprisedentirely of herbaceous vegetation and other resis-tant foods, I further assume that such extreme her-bivory predicts morphological distinctions betweenG. g. beringei and the other African apes. While thequestion of dietary differences between bonobos andchimpanzees remains open to debate, I predict howthe bonobo masticatory apparatus should look if,indeed, evidence in support of a tougher, more fi-brous diet in bonobos holds up under further scru-tiny (Table 2).

IN VIVO MODELS OF STRESS AND STRAINAND STRUCTURAL CORRELATES

Experimental investigations have yielded criticalinsights into how the anthropoid mandible is rou-tinely stressed and strained during mastication andincision (Hylander, 1979a,b, 1981, 1984, 1985a). Iuse these experimental data to draw functional in-ferences about differences in masticatory formamong the African apes. It should be stated clearlyat the outset that in assessing the functional conse-quences of changes in masticatory form, I assumethat differences are associated with improving resis-tance to relatively greater masticatory loads in orderto maintain similar levels of stress and strain (Hy-lander, 1985a). There is evidence of dynamic simi-larity in peak strain magnitudes in the postcraniumacross diversity of taxa (Biewener, 1982; Rubin andLanyon, 1984), and of preservation of functionalequivalence in jaw stress and strain levels ontoge-netically and interspecifically in primates (Vinyardand Ravosa, 1998).

Experimental data demonstrate that during thepower stroke of mastication, the balancing-sidemandibular corpus is bent in the parasagittal plane(Fig. 1A) (Hylander, 1979a,b). The amount of para-sagittal bending is directly proportional to the level

AFRICAN APE MASTICATORY FORM 135

of balancing-side jaw muscle force. Elevated bendingloads are most efficiently resisted by increasing thedepth of the mandibular corpus.

Parasagittal bending of the mandibular corpuscauses dorsoventral shear stress at the mandibular

symphysis (Fig. 1B) (Hylander, 1979a,b). Dorsoven-tral shear stress derives from the increase in balanc-ing-side muscle force coupled with the bite pointreaction forces that occur during unilateral mastica-tion. Increasing the depth of the mandibular sym-

Fig. 1.

136 A.B. TAYLOR

physis, or overall area of cortical bone, will theoret-ically serve to best resist elevated loads associatedwith dorsoventral shear stresses.

During unilateral mastication, the anthropoidmandibular corpus and symphysis experience lat-eral transverse bending, or “wishboning” stress (Fig.1C) (Hylander, 1984, 1985a). In anthropoid pri-mates, wishboning stress derives from high levels ofactivity of the balancing-side deep masseter muscleduring the late phase of the power stroke of masti-cation, coupled with the decline in activity of boththe balancing-side superficial masseter muscle andworking-side deep and superficial masseter muscles(Hylander, 1986; Hylander et al., 1987, 1996, 2000;Hylander and Johnson, 1994). Because the mandi-ble is bent in the plane of curvature during wishbon-ing, it functions as a curved beam, resulting in par-ticularly high levels of tensile stress along thelingual surface of the symphysis (Fig. 1C). In pri-mates with fused mandibular symphyses, increas-ing the labiolingual thickness or orienting the longaxis of the symphysis more horizontally have beenhypothesized to best counter elevated wishboningloads. Irrespective of dietary variation, wishboningstress intensifies with an increase in symphysealcurvature, simply because the symphysis functionsas a curved beam. Because symphyseal curvaturehas been shown to increase with ontogenetic andinterspecific size increase in some primate taxa (Hy-lander, 1985a; Ravosa, 1996a,b; Vinyard and Ra-vosa, 1998), larger primates with fused symphysesmay experience greater wishboning forces as a func-tion of scale.

Lastly, experimental studies demonstrate thatthe mandibular corpora experience twisting abouttheir long axes during unilateral mastication andincision; axial torsion has been argued to be themost important loading regime in the molar regionof the working-side mandibular corpus (Hylander,1979a,b, 1981) (Fig. 1D). Axial torsion is producedprimarily by the masseter muscle force resultants,which are positioned lateral to the mandible, and bythe bite force associated with the working-side cor-pus (Hylander, 1979a,b, 1984). The forces that com-bine to produce axial torsion evert the basilar corpusand invert the alveolar corpus, with the net effect

that the mandibular symphysis is bent in the verti-cal plane (Hylander, 1979a,b, 1981). Magnitude ofthe muscle force, orientation of the superficial anddeep masseter muscles, and timing of muscle re-cruitment influence the degree of axial torsion (Hy-lander, 1985a; Hylander and Johnson, 1994). Tor-sional loads are best resisted by redistributingcortical bone more evenly about the neutral axis ofthe mandible to increase buccolingual thickness ofthe premolar and molar corpus (Hylander, 1979a,b,1985a; Demes et al., 1984). The optimal biomechani-cal response to symphyseal bending is to increasethe depth of the symphysis.

A number of structural features have been hy-pothesized to confer a mechanical advantage andimprove masticatory efficiency, particularly amongprimates characterized by highly fibrous diets. Forexample, comparative data reveal that folivores ex-hibit larger masseter, medial pterygoid, and tempo-ralis muscles and attendant alterations in the gonialangle of the mandible (Turnbull, 1970; Herring andHerring, 1974; Ravosa, 1990; Anton, 1996a,b). An-teroposterior shortening and vertical deepening ofthe face, and more anteriorly positioned masticatorymuscles, should confer a mechanical advantage bypositioning the masticatory musculature closer tothe bite points (i.e., improving the load-to-lever armratio) and reducing the bending moments in the face(Dubrul, 1977; Hylander, 1977, 1979a; Ravosa,1990; Spencer and Demes, 1993; Anton, 1996a). Asbite force is inversely proportional to jaw length(Hylander, 1985a; Spencer and Demes, 1993), rela-tive shortening of the jaw provides for an increase inthe amount of muscle force that may be convertedinto usable bite force, particularly at M1 (Hylander,1979a; Spencer, 1998). A condyle elevated furtherabove the occlusal plane may reduce the fatiguefailure associated with frequent chewing cycles bydistributing occlusal loads more evenly along thepostcanine teeth (Herring and Herring, 1974; Wardand Molnar, 1980). Finally, folivores exhibit widermandibular condyles (expanded mediolaterally),which have been associated with enhanced use ofthe postcanine dentition (Smith et al., 1983; Bou-vier, 1986a; Takahashi and Pan, 1994) and the dis-tribution of loads on the lateral condyle during uni-

Fig. 1. Adult male gorilla mandible. A: Lateral view, left side. During the power stroke of mastication, the balancing-sidemandibular corpus is bent in the parasagittal plane. Fc, vertical component of condylear reaction force; Fm, vertical component of jawadductor muscle force; Fi, vertical component of internal force transmitted across symphysis from balancing to working side. Thisresults in tension (T) along the alveolar corpus, and compression (C) along the basal corpus. Parasagittal bending loads are efficientlyresisted by an increase in corpus depth. B: Frontal view. Parasagittal bending of the balancing-side mandibular corpus producesdorsoventral shear stress at the symphysis. Fb, vertical component of molar force; Fm, vertical component of jaw muscle force.Dorsoventral shear stress results from the vertical component of the balancing-side muscle force. In primates with fused symphyses,dorsoventral shear is efficiently countered by an increase in symphysis depth. C: Superior view. During mastication, the transversecomponent of bite force (Fbp) on the working-side corpus (Fwsm), and the transverse component of the adductor muscle force on thebalancing-side corpus (Fbdm), together result in lateral transverse bending, or “wishboning,” at the symphysis. During wishboning, themandible functions as a curved beam, such that the labial aspect of the symphysis experiences relatively high tensile (t) stresses andrelatively low compressive (c) stresses. Wishboning loads are best resisted by increasing the labiolingual thickness of the mandibularsymphysis. D: Frontal view. During the power stroke of mastication, the mandibular corpora are twisted about their long axes. Axialtorsion results in eversion of the basal corpus and inversion of the alveolar corpus, from the muscle force (M); the bite force (B) hasthe opposite effect. Resistance to axial torsion is most effectively achieved by increasing the transverse thickness of the postcaninemandibular corpus (adapted from Hylander, 1988).


lateral mastication (Hylander and Bays, 1979). Bycontrast, anteroposteriorly longer condyles havebeen associated with anterior tooth function (Smithet al., 1983; Bouvier, 1986a).

From the in vivo models of mandibular stress andstrain, in combination with results of comparativestudies of masticatory form and function, a numberof predictions follow regarding how the masticatoryapparatus of the African apes should be expected tovary as a function of dietary preference. Specifically,the more folivorous gorillas should exhibit relativelythicker and deeper mandibular corpora and sym-physes, longer lever arms for the masticatory mus-cles and/or shorter faces, higher mandibular ramiand temporomandibular joints, smaller gonial an-gles, and mediolaterally wider mandibular condyles.Assuming biologically meaningful dietary differ-ences between chimpanzees and bonobos, bonoboswould be predicted to parallel gorillas in exhibitingmusculoskeletal adaptations that reflect a more fo-livorous diet.

MATERIALS AND METHODS

Methodological approach

In this study, an ontogenetic allometric approachis used to investigate variation in masticatory formamong the African apes. Surprisingly few studieshave focused on African ape masticatory form(Groves, 1970; Daegling, 1989, 1990), and only one ofthese examined jaw form and function in the Africanapes from a developmental perspective (Daegling,1996). This is unfortunate, since an ontogenetic al-lometric approach serves to distinguish betweenstructural differences that result from ontogeneticscaling, or the differential extension or truncation ofcommon patterns of relative growth, and thosewhich result independent of the effects of size(Gould, 1966, 1975; Shea, 1984, 1985a,b). When apattern of divergence emerges, it is indicative ofderived dissociations of shared allometries that sug-gest novel transformations; at a minimum, we areobliged to explain the observed departures in termsother than the correlated effect of size change(Gould, 1966, 1975; Martin, 1989; Lauder andReilly, 1990; Reilly and Lauder, 1990; Harvey andPagel, 1991). It has been well-argued that an onto-genetic allometric approach provides the appropri-ate “criterion of subtraction” for distinguishing be-tween allometric-based trends and evolutionarynovelties that reflect transitions into new morpho-space (Gould, 1966, 1971; Shea, 1983a, 1985a, 1995;Emerson and Bramble, 1993). As ontogeny can havea significant influence on adult form, the approachtaken here serves to highlight patterns of allometricchange during growth as well as clarify results ofprevious size and shape comparisons between adults(e.g., Groves, 1970; Daegling, 1990).

The focus of this paper is explicitly on novel shapechanges that suggest additional selection pressuresbeyond those linked to size change that may be

associated with the maintenance of functionalequivalence (Jungers and Fleagle, 1980; Cheverud,1984; Shea, 1983a,b, 1988; Atchley, 1987; Mueller,1990; Atchley and Hall, 1991). This is because de-partures from common ontogenetic allometries im-prove the chances that shape differences reflect no-table dissociations in the shared patterns ofstructured covariance. I emphasize that ontogeneticscaling of allometries should in no way be taken asprima facie evidence that such alterations are func-tionally unimportant (cf. Godfrey et al., 1998). Onthe contrary, the study of size and its consequenceshas a long history, culminating in the quantitativetreatment of relative growth (Huxley, 1932; Thomp-son, 1942), and departures from isometry have beenlinked to important functional shifts during ontog-eny and interspecifically across adults by numerousinvestigators (Cock, 1963; Dodson, 1975; Cochard,1985; Shea, 1985b, 1986; Jungers and Cole, 1992;Taylor, 1995; Velhagen and Roth, 1997). The biolog-ical import of preservation of geometric similarityhas also been discussed (Gould, 1971; Dodson, 1975;Shea, 1982). Observed allometric relationships dur-ing ontogeny may provide important insights intodevelopment, historical constraint, and functionalshifts during growth, and these are currently beingexplored more fully elsewhere (Taylor, in prepara-tion).

Comparative sample

The African ape sample is comprised of a mixed-sex, cross-sectional ontogenetic series of G. g.beringei (n � 32), G. g. gorilla (n � 99), P. t. troglo-dytes (n � 126), and P. paniscus (n � 85) (Table 1and Fig. 2). Developmental ages were assigned us-ing a combination of dental eruption pattern, dentalwear, and status of basilar suture fusion that re-sulted in five discrete age classes (Shea, 1983a; Tay-lor, 1998) (Table 1). All specimens are wild-caughtand of known locality. Each taxon is represented byroughly equivalent numbers of males and females(Table 1). Unsexed specimens are few and primarilyrepresent young individuals.

Measurements

Measurements were selected that have been ex-plicitly linked to increasing load resistance and im-proving masticatory efficiency (Herring and Her-ring, 1974; Hylander, 1979a–c, 1984; Bouvier,1986a,b; Ravosa, 1990, 1991, 1996a; Cole, 1992; An-ton, 1996a; Wall, 1999; Taylor, in press) (Table 2 andFigs. 3A–D). Measures of corpus and symphysis ro-busticity include mandibular corpus depth andwidth (orthogonal to depth) taken at the midpoint ofM1, and symphysis depth and width (Hylander,1988) (Fig. 3A,B). Corpus measurements are re-ported for M1 in order to maximize the number ofnonadults in these analyses (Cole, 1992), and be-cause peak muscle force (though not necessarilymasticatory stress; Daegling, 1993), has been asso-

138 A.B. TAYLOR

ciated with M1, at least in humans (Spencer, 1998).Condylar dimensions include anteroposterior lengthas measured in the sagittal plane, and mediolateralwidth measured in the coronal plane (Bouvier,1986a) (Fig. 3B). Mandibular ramus height is mea-sured from gonion to the uppermost condyle (Anton,1996a) (Fig. 3C). Gonial angle was used as a mea-sure of the orientation of the mandibular ramus(Anton, 1996a) (Fig. 3C) and temporomandibularjoint height measured from the level of the molarocclusal plane to the uppermost condyle (Ravosa,1990) (Fig. 3C). Measures of masticatory muscle size(as a reflection of the ability to generate more muscleforce and, by implication, more bite force; Turnbull,1970; Hylander, 1979a,b; Ravosa, 1990; Anton,1996a,b) and muscle lever arm lengths were alsoused. A scalar was used as a measure of massetermuscle size, derived from the square root of the

product of ramus height and distance between thecondylion laterale and maxillary root of the zygoma(Ravosa, 1990); posterior condyle–anterior zygomadistance is also used as an estimate of massetermuscle lever arm length (Ravosa, 1990; Anton,1996a) (Fig. 3C). Relative position of the masseter inthe coronal plane was measured as the differencebetween bizygomatic and bicondylar breadths (Fig.3D) (Ravosa et al., 2000). The distance between thesuperior condylion and coronoid process was used asan estimate of temporalis lever arm length (Ravosa,1990) (Fig. 3C).

The effect of size increase on jaw curvature wasassessed using multiple approaches. Mandibularlength and bicondylar breadth, as well as palatelength and palate breadth, were compared across alltaxa. Bicondylar breadth is presumed to reasonablytrack mandibular breadth, though this measure is

TABLE 1. Skeletal material composition

Dentalstage5

G. g. beringei1 G. g. gorilla2 P. t. troglodytes3 P. paniscus4

M F ?6 M F ? M F ? M F ?

1 0 1 2 10 12 2 12 16 2 10 11 22 0 2 0 5 10 0 14 13 2 4 7 23 0 1 0 5 5 0 6 5 1 6 4 14 2 0 0 11 7 0 12 19 0 7 7 05 13 11 0 16 16 0 10 14 0 7 14 3

Total 15 15 2 47 50 2 54 67 5 34 43 8

1 National Museum of Natural History, Washington, DC (Virunga Volcano Region); Central African Museum, Tervuren, Belgium(Zaire).2,3 Powell-Cotton Museum, Kent, England; Field Museum of Natural History, Chicago; Cleveland Museum of Natural History(Cameroon).4 Central African Museum, Tervuren, Belgium (Zaire).5 Dental stage definitions: stage 1, incomplete deciduous dentition up through and including M1 partially or fully erupted; stage 2, M2partially or fully erupted; stage 3, C, M3 erupting; stage 4, C, M3 fully erupted, basilar suture open, teeth showing little wear; stage5, full permanent dentition, basilar suture fused, teeth showing moderate to heavy wear.6 Sex indeterminate.

Fig. 2. Ontogenetic series of a G. g. gorilla mandible.


not directly comparable to those used by previousinvestigators (Hylander, 1985a; Vinyard and Ra-vosa, 1998). Palate length and breadth were alsoused (Ravosa, 1991) because palate and mandibularlength are highly correlated and scale isometricallyacross primates (Ravosa, 1996c). These measureswere more readily available across all taxa due tofrequent unilateral damage to the alveolar region ofthe molar corpus; in addition, palate length andbreadth may be used in studies of fossil hominoidsfor which mandibular remains are fragmentary.However, mandibular breadth at M1 and mandibu-lar length were used to assess curvature in G. g.gorilla and P. t. troglodytes. All metric data wererecorded using Mitutoyo digital calipers accurate to0.01 mm, except for gonial angle, which was mea-sured with a mandibulometer to the nearest 1.0°. Asit was not possible to obtain all measurements on allspecimens, sample sizes vary across measurements.

Choice of independent size variable

Patterns of relative growth may vary according tothe choice of size variable, and investigators haveapproached this problem in a variety of ways (cf.Shea, 1983a; Darroch and Mossiman, 1985; Hy-lander, 1985a; Ravosa, 1990; Smith, 1993). In this

study, basicranial length is used as a measure ofskull size and is known to scale isometrically withbody weight in interspecific series of the Africanapes (Shea, 1983a). As body size may be arguablyless directly influential on skull and mandibularform (Hylander, 1985a; cf. Smith, 1993), previousinvestigators used basicranial length as a measureof overall skull size (Shea, 1983a,b; Ravosa, 1990,1991; Anton, 1996a). However, in scaling analyses ofmandibular form, in which explicit biomechanicalhypotheses are addressed, the effects of scale areappropriately assessed using a variable that reflectsthe ability of the face and mandible to resist forcesassociated with mastication (Hylander, 1985a; Bou-vier 1986a; Smith, 1993). Mandibular length is as-sumed to scale isometrically to the bending momentarm in the case of lateral transverse bending at thesymphysis (Hylander, 1985a; Daegling, 1990; Cole,1992; Ravosa, 1996a), and is frequently chosen as anindependent variable in studies assessing differ-ences in jaw robusticity and biomechanics (Hy-lander, 1979a, 1985a, 1988; Demes et al., 1984; Bou-vier, 1986a; Cole, 1992; Daegling, 1992; Anton,1996a; Vinyard and Ravosa, 1998). Therefore, man-dibular length is also used in analyses of corpus andsymphysis proportions.

TABLE 2. Measurements1

Variable Definition (abbreviation) Prediction2

Basicranial length Distance from nasion to basion.Bizygomatic breadth Distance from right to left zygion (Bizygom).Bicondylar breadth Distance between right and left condylion laterale (BiconBr).Palate breadth Distance between right and left ectomolare at M1.Palate length Distance between orale and alveolon.Mandibular length Distance from posterior condyle to incision (MandL). Ggb � Ggg � Pp � PttCorpus depth at M1 Maximum depth of mandibular corpus taken perpendicular to

the occlusal plane from the buccal alveolus to the inferiorborder of the mandible at the midpoint of dm2 (CDp).

Ggb � Ggg � Pp � Ptt

Corpus width at M1 Maximum buccolingual width of the mandibular corpus takenperpendicular to corpus depth through a transverse plane atthe midpoint of M1 (CWd).


Symphysis depth Maximum depth of the mandibular symphysis from gnathion toinfradentale perpendicular to the occlusal plane (SDp).


Symphysis width Maximum labiolingual width of the mandibular symphysistaken perpendicular to symphysis depth (SWd).


Condyle length Maximum anteroposterior length of articular surface in sagittalplane (CL).


Condyle width Maximum mediolateral dimension of articular surface incoronal plane (CW).


Temporomandibular jointheight

Measured from occlusal plane from M1 to uppermost condyle(JawJtHt).


Temporalis lever arm length Distance from posterior condyle to tip of coronoid process (TLA). Ggb � Ggg � Pp � PttMasseter muscle size Square root of product of mandibular ramus height (masseter

muscle origin length) and condylion laterale � anterior rootof zygoma distance (masseter muscle insertion length)(MMSize).


Masseter lever arm length Distance from posterior condyle to maxillary root of zygoma(MLA).


Masseter muscle position Difference between bizygomatic and bicondylar breadths(MMPos).

Ramus height Distance from gonion to uppermost condyle (RHt). Ggb � Ggg � Pp � PttGonial angle Angle formed between posterior border of horizontal ramus and

inferior border of mandibular ramus (GonAng).Ggb � Ggg � Pp � Ptt

1 See text for sources.2 Predictions are based on the assumption that dietary resistance increases from P. t. troglodytes (Ptt) to G. g. gorilla (Ggg) to G. g.beringei (Ggb). Predictions for P. paniscus (Pp) assume a more resistant diet than for P. t. troglodytes.

140 A.B. TAYLOR

Statistical analysesWithin each ontogenetic series, regression analy-

sis was performed on log10-transformed data to de-scribe scaling trajectories. There were no apprecia-ble differences in ontogenetic trajectories betweenthe sexes for G. g. gorilla, P. t. troglodytes, and P.

paniscus, as evaluated by regression coefficients and95% confidence intervals; sample sizes for G. g.beringei were too small to evaluate. Therefore, re-gression analysis was applied to combined samplesof males and females of each taxon. As the primarygoal of this investigation is to assess differences in

Fig. 3. Craniomandibular measurements. A: SDp, symphysis depth; SWd, symphysis width; CDp, corpus depth; JawJtHt,temporomandibular joint height. B: CWd, corpus width; MandL, mandibular length; CW, condyle width; CL, condyle length; BiconBr,bicondylar breadth. C: TLA, temporalis lever arm length; MLA, masseter lever arm length; RHt, ramus height; GonAng, gonial angle.D: MMPos, defined by the distance between Bizygom (bizygomatic breath) and BiconBr (bicondylar breath), which reflects theorigin/insertion angle of the masseter muscle (adapted from Anton, 1996a). Dotted line represents hypothetical position of the condyle.


ontogenetic trajectories among groups, ordinaryleast-squares (OLS) regression is the preferredmethod of analysis, because analysis of covariance(ANCOVA) provides a powerful statistical test ofdifferences in allometric trajectories (i.e., slopes andy-intercepts; Sokal and Rohlf, 1995). However, nat-ural variation and measurement error in both theindependent and dependent variables in this studyviolate the assumption that x is measured withouterror (i.e., that x is fixed; Rayner, 1985; Sokal andRohlf, 1995). Therefore, OLS and reduced major axis(RMA) regression analyses were performed, andboth sets of regression statistics are presented.ANCOVA was used to test for slope and y-interceptdifferences between ontogenetic trajectories derivedfrom OLS regressions. Clarke’s T-statistic (1980)was used to test for significant differences in slopesderived from RMA regressions, and Tsutakawa andHewett’s quick test (1977) was used to test for sig-nificant differences in modified y-intercepts. Isome-try in comparisons between linear dimensions istested against a slope of 1.0. To protect against typeI errors associated with multiple pairwise statisticalcomparisons, I applied the sequential Bonferronitechnique (Holm, 1979; Rice, 1989) to an a priorisignificance level of � � 0.05 (� � 0.05/20 statisticaltests), which resulted in a minimum significancelevel of � � 0.0025. All statistics were generatedusing Systat 8.0� (Wilkinson, 1998).

RESULTS

Virtually all linear dimensions are positively andsignificantly correlated with an increase in skull andjaw size (Table 3). Corpus width is an exception; it isweakly (but significantly) correlated with basicra-nial and mandibular lengths in gorillas and P. t.troglodytes, but uncorrelated with either in P. panis-cus. Gonial angle is negatively correlated with anincrease in skull size in all taxa, and consistent withangular variables, shows a relatively lower correla-tion with basicranial length as well (Table 3). Sometrajectories are curvilinear to varying degrees (e.g.,Figs. 5C,D), comparable to what has been observedin similar studies of jaw ontogeny (e.g., Cole, 1992;Ravosa and Ross, 1994). In such instances, slopedifferences should be interpreted with caution. Inaddition, wide confidence intervals for some bivari-ate regressions result in a considerable overlap oftrajectories among taxa (e.g., condyle length). Fi-nally, as in all studies of mountain gorilla morphol-ogy, samples of G. g. beringei are relatively smalland represent disproportionate numbers of adults,which may influence the regression statistics.

There are some consistent scaling patterns. Forexample, all taxa show a strong pattern of positiveallometry of jaw and cranial dimensions relative tobasicranial length (Table 3). Only corpus width andgonial angle scale with negative allometry againstbasicranial length. Relative to mandibular length,corpus depth is positively allometric in all taxa,whereas width of the mandibular corpus and sym-

physis scale with negative allometry. Symphysisdepth scales isometrically in G. g. gorilla and chim-panzees, but is negatively allometric in G. g.beringei and bonobos. The African apes are ontoge-netically scaled for mandibular length and gonialangle vs. basicranial length, and for palate lengthvs. palate breadth (Tables 3 and 4). Corpus depth(relative to both basicranial length and mandibularlength) differs only between G. g. gorilla and P. t.troglodytes. Slope differences are relatively few ingeneral, despite varying degrees of curvilinearity,and the lowest frequency of slope and y-interceptdifferences occurs in comparisons between gorillasubspecies and between species of Pan (Table 4); inother words, in the most phylogenetically restrictedcomparisons. Similarities in timing of dental erup-tion as well as greater comparability in size andgrowth at various dental stages may account for thispattern.

Neither assessment of symphyseal allometryyields a systematic change in symphyseal curvaturewith increase in size (Tables 3 and 4). Palate lengthscales with strong positive allometry relative to pal-ate breadth in all taxa, but while degree of positiveallometry increases with interspecific increase insize, slopes do not differ between taxa. Mandibularlength scales with strong positive allometry relativeto bicondylar breadth in all taxa as well, but with notrend towards increasing positive allometry withsize change. Alternatively, the slope for mandibularlength vs. mandibular breadth is strongly positivelyallometric in G. g. gorilla (k � 1.58) but isometric inP. t. troglodytes (k � 1.00), and this difference issignificant (df � 1,75; F � 9.28; P � 0.003). Figure 4shows an interesting pattern of differentiation of G.g. gorilla males above the common slope for Africanapes, suggesting that the positive allometry of jawlength relative to jaw breadth may result in an in-crease in symphyseal curvature at the extreme endof the size range for African apes. However, addi-tional data are needed to verify this pattern.

There are several other trends worth noting. Forexample, in some comparisons, G. g. gorilla com-mences early ontogeny transposed above Pan butconverges on the ontogenetic trajectory during laterstages of growth, such as for relative growth of themasseter muscle, depth of the symphysis, and widthof the condyle (Figs. 5E, 6A,B). Other differences, asalready noted, are statistically significant, but thedegree of separation is negligible, e.g., relative depthof the corpus between G. g. gorilla and P. t. troglo-dytes (Fig. 6C), or relative length of the condylebetween P. t. troglodytes and P. paniscus (Fig. 6D).Lastly, some of the most marked separations be-tween taxa run contrary to expectations, e.g., asseen in the bivariate plot of temporalis lever armlength vs. basicranial length in Pan vs. Gorilla(Fig. 6E).

Systematic differences among taxa that fit themorphological predictions based on diet are rela-tively few. G. g. beringei, the most specialized to-

142 A.B. TAYLOR

wards a diet of herbivory, differs from all other taxain having a wider mandibular corpus and symphysis(relative to both basicranial and mandibularlengths), temporomandibular joint elevated higher

above the occlusal surface, vertically higher ramus,and larger masseter muscle (Tables 3 and 4; Fig.5A–E). Among these comparisons, differentiation isgreatest for relative width of the symphysis (Fig.

TABLE 3. Regression statistics1

Measurement(mm)

G. g. beringei G. g. gorilla P. t. troglodytes P. paniscus

k y-Int r95%CI k y-Int r

95%CI k y-Int r

95%CI k y-Int r

95%CI

Versus basicranial lengthMandibular

length 1.25 �0.42 0.95 �0.19 1.31 �0.56 0.96 �0.08 1.29 �0.52 0.94 �0.09 1.36 �0.66 0.94 �0.121.31 �0.55 �0.19 1.37 �0.68 �0.08 1.38 �0.69 �0.09 1.45 �0.82 �0.12

Corpusdepth2 1.64 �1.84 0.96 �0.22 1.67 �1.91 0.91 �0.16 1.64 �1.83 0.90 �0.15 1.57 �1.70 0.91 �0.17

1.72 �2.00 �0.22 1.84 �2.27 �0.17 1.82 �2.20 �0.15 1.72 �1.98 �0.17Corpus

width2 0.39 0.50 0.54 �0.28 0.28 0.84 0.36 �0.10 0.34 0.41 0.46 �0.13 �0.61 1.15 0.08 �0.180.71 �0.16 �0.31 0.56 0.11 �0.13 0.79 �0.42 �0.15 �0.63 2.21 �0.19

Symphysisdepth 1.17 �0.66 0.93 �0.19 1.30 �0.95 0.92 �0.12 1.34 �1.05 0.90 �0.12 1.30 �0.99 0.95 �0.10

1.25 �0.83 �0.19 1.41 �1.18 �0.12 1.57 �1.50 �0.05 1.36 �1.12 �0.10Symphysis

width 1.02 �0.68 0.88 �0.23 1.00 �0.70 0.86 �0.12 0.68 �0.15 0.70 �0.13 0.72 �0.28 0.69 �0.181.15 �0.96 �0.24 1.16 �1.02 �0.13 0.97 �0.72 �0.14 1.05 �0.88 �0.20

AP condyle 1.31 �1.60 0.80 �0.42 1.67 �2.39 0.76 �0.30 1.38 �1.76 0.81 �0.19 2.06 �3.03 0.88 �0.271.65 �2.31 �0.45 2.21 �3.49 �0.32 1.71 �2.41 �0.20 2.35 �3.58 �0.28

ML condyle 1.11 �0.77 0.87 �0.26 1.11 �0.74 0.93 �0.10 1.40 �1.45 0.88 �0.14 1.63 �1.88 0.91 �0.181.27 �1.12 �0.28 1.20 �0.99 �0.10 1.60 �1.84 �0.15 1.79 �2.18 �0.18

TMJ height2 0.98 �0.13 0.81 �0.30 1.08 �0.38 0.90 �0.11 1.30 �0.93 0.83 �0.16 1.29 �0.92 0.85 �0.201.21 �0.60 �0.31 1.21 �0.64 �0.12 1.52 �1.36 �0.16 1.47 �1.27 �0.19

Temporalislever arm 1.20 �0.89 0.80 �0.38 1.63 �1.78 0.90 �0.16 1.58 �1.57 0.89 �0.15 1.76 �1.93 0.92 �0.18

1.49 �1.51 �0.40 1.81 �2.16 �0.17 1.77 �1.95 �0.15 1.92 �2.22 �0.19Masseter

muscle size 1.26 �0.61 0.96 �0.15 1.32 �0.77 0.96 �0.08 1.49 �1.13 0.93 �0.11 1.49 �1.13 0.96 �0.101.28 �0.64 �0.19 1.37 �0.87 �0.08 1.60 �1.34 �0.11 1.54 �1.24 �0.10

Masseterlever arm 1.27 �0.70 0.97 �0.14 1.37 �0.94 0.96 �0.08 1.54 �1.25 0.93 �0.11 1.56 �1.28 0.96 �0.11

1.28 �0.73 �0.17 1.43 �1.06 �0.09 1.66 �1.47 �0.11 1.63 �1.41 �0.11Masseter

position2 1.48 �1.70 0.79 �0.61 2.35 �3.48 0.90 �0.35 1.60 �1.90 0.69 �0.33 1.99 �2.60 0.74 �0.451.88 �2.53 �0.65 2.74 �4.27 �0.36 2.34 �2.34 �0.36 2.68 �3.91 �0.48

Ramusheight2 1.16 �0.34 0.89 �0.25 1.27 �0.59 0.94 �0.09 1.44 �1.00 0.91 �0.12 1.41 �0.96 0.94 �0.12

1.31 �0.64 �0.26 1.34 �0.75 �0.10 1.58 �1.28 �0.12 1.50 �1.13 �0.12Gonial angle �0.22 2.45 0.49 �0.16 �0.16 2.34 0.43 �0.07 �0.21 2.48 0.49 �0.07 �0.19 2.43 0.47 �0.07

�0.44 2.91 �0.18 �0.37 2.76 �0.09 �0.44 2.92 �0.08 �0.40 2.82 �0.09Versus mandibular lengthCorpus depth 1.18 �1.00 0.95 �0.17 1.23 �1.12 0.93 �0.10 1.22 �1.07 0.93 �0.09 1.11 �0.86 0.92 �0.12

1.24 �1.13 �0.17 1.32 �1.31 �0.10 1.31 �1.26 �0.09 1.21 �1.04 �0.12Corpus

width2 0.14 1.02 0.38 �0.15 0.22 0.80 0.49 �0.08 0.28 0.56 0.51 �0.09 �0.11 1.23 0.25 �0.110.36 0.53 �0.18 0.44 0.32 �0.09 0.55 0.03 �0.10 �0.43 1.84 �0.14

Symphysisdepth 0.89 �0.17 0.94 �0.14 0.99 �0.39 0.95 �0.07 1.01 �0.46 0.94 �0.07 0.89 �0.25 0.95 �0.07

0.95 �0.28 �0.14 1.05 �0.51 �0.07 1.08 �0.59 �0.07 0.94 �0.33 �0.07Symphysis

width2 0.70 �0.08 0.82 �0.21 0.75 �0.23 0.88 �0.08 0.50 0.18 0.72 �0.09 0.45 0.23 0.65 �0.130.85 �0.41 �0.22 0.86 �0.46 �0.09 0.70 �0.22 �0.10 0.69 �0.23 �0.15

Palate lengthvs. palatebreadth 1.94 �1.56 0.85 �0.55 1.76 �1.27 0.85 �0.23 1.60 �1.00 0.88 �0.16 1.68 �1.17 0.91 �0.20

2.29 �2.19 �0.57 2.06 �1.82 �0.24 1.81 �1.38 �0.16 1.86 �1.46 �0.20Mandibular

length vs.bicondylarbreadth 1.29 �0.57 0.94 �0.22 1.40 �0.80 0.94 �0.11 1.29 �0.55 0.94 �0.09 1.36 �0.70 0.91 �0.16

1.38 �0.76 �0.22 1.50 �1.00 �0.11 1.38 �0.72 �0.09 1.49 �0.95 �0.16

1 OLS regression statistics are presented on first line, and RMA regression statistics on second line. k, OLS and RMA slopes; Int, OLSy-intercept and RMA modified intercept; r, correlation coefficient; 95% CI, 95% confidence intervals for slopes.2 Indicates curvilinearity in ontogenetic trajectories.


5B), but all plots show separation of G. g. beringeiabove the other African apes. Compared to Pan, G.g. gorilla follows trends similar to those observed forG. g. beringei, with the exception of masseter musclesize (Tables 3 and 4; Fig. 5A–E). However, in alladditional comparative analyses, at least one groupdeviates from the predicted morphology based on

hypothesized loading regimes and dietary variation.Finally, despite various morphological differencesbetween P. paniscus and P. t. troglodytes, there is noclear or systematic pattern of differentiation in Panthat would suggest a mechanically different diet forbonobos. In most cases where gorillas and chimpan-zees differ, bonobos similarly deviate from gorillas inthe same direction and to a similar degree.

DISCUSSION

Several patterns emerge from this study. First,most jaw and cranial dimensions are moderately tostrongly positively allometric, depending onwhether they are scaled against mandibular or basi-cranial length (Table 3). Some of the strongest allo-metric increases occur in variables that reflect mus-cle size (also noted for cebids by Cole, 1992), such astemporalis lever arm length and masseter musclesize, suggesting the relative importance of rates ofmuscular as compared to skeletal growth. All taxashow ontogenetic allometric increases in cranioman-dibular dimensions that suggest improved mechan-ical efficiency (e.g., temporalis lever arm length) andthe potential to increase both muscle and bite forceduring growth. The decrease in gonial angle duringontogeny, and the concomitant increase in verticalorientation of the mandibular ramus, likewise sug-gest an improved ability to counter greater occlusalloads. The strong interspecific allometry indicatesthat similar advantages accrue with size increaseacross taxa. The positive and negative allometry ofmandibular proportions suggests that stress levelsdo not remain constant throughout growth. Devia-tions from isometry demonstrate that the jaws of

TABLE 4. Significance tests for differences in skull and jaw dimensions among african apes1

Measurement

Pp/Pt Ggg/Pp Ggg/Ptt Ggb/Ptt Ggb/Pp Ggb/Ggg

k Int k Int k Int k Int k Int k Int

Versus basicranial lengthMandibular length NS NS NS NS NS NS NS NS NS NS NS NSCorpus depth NS NS NS NS NS � NS NS NS NS NS NSCorpus width � — � — NS � NS � � — � —Symphysis depth NS � NS � NS NS NS � NS � NS NSSymphysis width NS � NS � NS � � — NS � NS �Condyle length (AP) � — NS � NS � NS NS � — NS NSCondyle width (ML) NS NS � — � — NS NS � — NS �TMJ height NS NS NS � NS � NS � NS � NS �Temporalis lever arm length NS NS NS � NS � NS � � — NS NSMasseter muscle size NS NS NS NS NS NS NS � � — NS �Masseter lever arm length NS NS NS � NS � NS NS � — NS NSMasseter position NS NS NS � NS � NS NS NS � NS NSRamus height NS NS NS � NS � NS � NS � NS �Gonial angle NS NS NS NS NS NS NS NS NS NS NS NSVersus mandibular lengthBicondylar breadth NS NS NS NS NS � NS NS NS NS NS NSCorpus depth NS NS NS NS NS � NS NS NS NS NS NSCorpus width � — � — NS � NS � � — NS �Symphysis depth NS � NS NS NS � NS NS NS NS NS NSSymphysis width NS � � — � — NS � NS � NS �Palate length/breadth NS NS NS NS NS NS NS NS NS NS NS NS

1 OLS y-intercept comparisons based on ANCOVA; of Tsutakawa and Hewett’s quick test (1977) for differences in RMA modifiedy-intercept.* OLS and RMA significant at the sequential Bonferroni-adjusted alpha level. NS, both OLS and RMA significant at P � 0.05, but oneor both did not achieve significance at the sequential Bonferroni-adjusted alpha level; NS, nonsignificant.—, y-intercept tests were not performed if slopes were significantly different.

Fig. 4. Bivariate plot of mandibular length regressed againstmandibular breadth for G. g. gorilla and P. t. troglodytes. Noteelevation of male gorillas above common slope for African apes.

144 A.B. TAYLOR

larger adults cannot be viewed as “scaled up” ver-sions of younger, smaller individuals.

Apart from alterations associated with allometricincreases in size, results indicate that when control-

ling for allometry, only a select few proportions dif-fer consistently across taxa in ways predicted bydietary variation. Certain trends are supported sta-tistically and are graphically evident, whereas for

Fig. 5. Bivariate plots of least-squares regres-sions of log10-transformed dimensions (mm) inwhich the trajectory for G. g. beringei departsconsistently from the other African apes. Com-pared to Pan, G. g. beringei and G. g. gorilla haverelatively: (A) wider mandibular corpora; (B)wider mandibular symphyses; (C) higher tem-poromandibular joints elevated above the occlu-sal surface; and (D) higher mandibular rami. E:G. g. beringei has a significantly larger massetermuscle than the other African apes. All symbolsas in A.


other comparisons differences are statistically sig-nificant but unaccompanied by any appreciablegroup separation. This may be due to sampling is-sues, or possibly because comparisons between Panand Gorilla involve analyses of individuals of com-

parable size but differing developmental stages.Convergence of ontogenetic allometries for corpusand symphysis dimensions during later stages ofgrowth is not uncommon, and is consistent withexpansion of the corpus during tooth eruption and

Fig. 6. Bivariate plots of least-squares regres-sions of log10-transformed dimensions (mm) depict-ing various trends across taxa. A–C: Bivariate plotsshow little or no differentiation, despite statisticaldifferences in various pairwise comparisons betweentaxa. D: Condyle length was predicted to be rela-tively longer in frugivorous taxa, but this dimensionis highly variable within African apes and results incontradictory results (e.g., no difference between go-rilla subspecies); note downward transposition ofpositive allometries with interspecific size increase.E: Temporalis lever arm length was predicted to berelatively longer in folivorous taxa, but instead pro-duces marked separation between gorillas and chim-panzees, with the latter exhibiting a relativelylonger temporalis lever arm. All symbols as in A.

146 A.B. TAYLOR

subsequent remodeling of the alveolar bone (Cole,1992). Nevertheless, it is biologically constructive tocombine statistical analyses with empirical observa-tion of plots to gain insight beyond the statistics, interms of both the pattern and degree of differentia-tion among taxa.

The inclusion of more resistant foods in the dietappears to be associated with an increase in thick-ness of the mandibular corpus (Tables 3 and 4; Fig.5A). Similar findings of a relatively more robustmandibular corpus were demonstrated in phyloge-netically restricted comparisons between taxawhose diets differ in toughness, including fossil pa-pionins (Benefit and McCrossin, 1990; Jablonski,1993), cebids (Cole, 1992), macaques (Anton, 1996a),and various colobines (Ravosa, 1996a). These datasuggest improved resistance to torsional loads asdietary toughness increases. However, whereas arelatively thicker corpus was predicted for P. panis-cus, assuming a more herbivorous diet, there is nobasis for predicting a relatively thicker corpus in P.t. troglodytes (Tables 3 and 4). Moreover, the overallallometric pattern for this dimension is one of up-ward transpositioning with interspecific increase insize (Fig. 5A). Therefore, the maintenance of geo-metric equivalence with size increase cannot beruled out; nor can this difference be adequately ex-plained by diet, as there is no evidence to suggestthat chimpanzees consume a tougher diet than dobonobos.

G. g. beringei may incur relatively greater tor-sional loads along the corpus as a function of moreworking-side masticatory muscle force generated bya relatively enlarged masseter muscle (Tables 3 and4; Fig. 5D) (Hylander, 1979a). However, torsion in G.g. beringei is not likely to be augmented by a morehorizontal component of postcanine bite force (Hy-lander, 1979a, 1988; Anton, 1996a), as gorillas havethe relatively narrowest cranium (Shea, 1983a), andtheir masseter muscle is positioned relatively closerto the skull (i.e., the cranial origin of their massetermuscle is most closely aligned with its insertion intothe mandible in a vertical plane) (Tables 3 and 4;Figs. 3D, 7). On the contrary, the more lateral posi-tion of the masseter may contribute to relativelygreater torsional loads in bonobos, whose relativelythin corpus offers the least resistance. Furthermore,while Gorilla has a relatively wider corpus thanPan, these taxa do not differ in relative masticatorymuscle size (Table 4).

It is important to emphasize that this study doesnot directly estimate the resultant muscle-force po-sition or take into account the point of application orposition of the bite force (Hylander, 1979a,b; Demeset al., 1984), all of which influence torsion. What iscontradictory, however, is that elevated torsionalloads along the postcanine corpus have been exper-imentally shown to produce symphyseal bending,which would be most efficiently countered by a ver-tically deeper symphyseal (Hylander, 1979a,b,1988). Perusal of the statistics indicates significant

differences in symphyseal depth for several pairwisecomparisons, but deeper symphyses are not system-atically associated with species hypothesized to ex-perience relatively higher torsional loads based ondiet, such as G. g. beringei vs. G. g. gorilla or G. g.gorilla vs. P. t. troglodytes (Tables 3 and 4). In ad-dition to an inconsistent pattern, G. g. beringei con-verges on the ontogenetic trajectories of other Afri-can apes during growth, resulting in considerableoverlap among taxa (Tables 3 and 4; Fig. 6A), all ofwhich lead one to question whether this differencecan be reasonably interpreted as being biologicallymeaningful (i.e., suggestive of real differences inresistance capabilities to symphyseal bending). Re-gardless of how one interprets the data, diet alone isclearly not adequate to explain differences in corpusthickness or symphyseal depth.

The thicker mandibular corpus relative to bothbasicranial and mandibular lengths suggests thatgorillas have a larger cross-sectional area when com-pared to chimpanzees and bonobos. If the gorillamandible behaves like a hollow elliptical beam (Hy-lander, 1979a; Daegling, 1990), then the gorilla cor-pus should have relatively more compact bone. How-ever, estimates of compact bone derived frommodeling the corpus in this manner may be unreli-able in extant hominoids; in other words, the modeldoes not accurately predict the actual geometricproperties of the mandibles (Daegling, 1989). Mod-eling the corpus as a closed section seems morecongruent with experimental data, but still poses

Fig. 7. Bivariate plot of masseter muscle position regressedagainst basicranial length. Downward transposition of positiveallometries results in a masseter muscle positioned relativelymore laterally in Pan (i.e., a greater angle of insertion) and closerto the skull in Gorilla (i.e., a smaller angle of insertion (see Fig.3D).


reliability issues in hominoids (Daegling, 1989; Dae-gling and Hylander, 1998). Theoretical modelsaside, as judged from the shape of the mandibularcorpus, P. troglodytes and G. g. gorilla show no ap-parent differences in the biomechanical properties ofthe mandible (Daegling, 1989, 1990).

There are several potential explanations for thecontrasting results of these two studies, and any orall may account for the variance in findings. First,shape variables in this study are derived from linearmeasurements, which are only first approximationsof the actual biomechanical properties of the corpus.Therefore, the approach taken here will not tracksecond moments of area as faithfully as analysis ofcross-sectional geometry (Daegling, personal com-munication). Second, the two studies rely on differ-ent moment arm estimates, which may produce dif-ferent results for the same morphological com-parisons. Finally, differences in the shape of thecorpus as observed in this study may also have gonepreviously undetected as a function of smaller sam-ples and relatively low power to detect a significantdifference (Daegling, 1989). The trend in gorillastoward a relatively larger mean cross-sectional areaat M1 (Daegling, 1989) offers tentative support forthis hypothesis. Unfortunately, neither bonobos normountain gorillas can be placed in comparative per-spective, as the internal geometry of their mandiblesremains to be evaluated. While modeling issues areproblematic, it seems clear that resolution of theseconflicting results will require more comparativedata on the shape and biomechanical properties ofAfrican ape mandibles.

In addition, as underscored earlier, corpus widthis not significantly correlated with either basicranialor mandibular lengths in bonobos, and is onlyweakly (though significantly) correlated with both inall other taxa, indicating that this dimension is in-herently problematic, though no less biologically im-portant. Corpus width, in particular, is often poorlycorrelated with both ontogenetic and interspecificsize increase in primates (e.g., Cole, 1992; Ravosa,1990; Anton, 1996a). Some insight into the underly-ing basis for this pattern in the African apes may begained by evaluation of corpus growth prior to erup-tion of the permanent dentition.

Width of the deciduous corpus is significantly cor-related with increase in skull size across taxa (Fig.8A). Deciduous corpus width scales with isometry inPan but is positively allometric in gorillas, and go-rillas are notably transposed above Pan (Fig. 8A).Conversely, ontogenetic allometries for the depth ofthe deciduous corpus are highly and significantlycorrelated with size increase and strongly positivelyallometric in all taxa (Fig. 8B). Ontogenetic trajec-tories are shifted downwards with interspecific sizeincrease at initial growth, but gorillas transposeabove Pan during ontogeny (Fig. 8B). These resultshighlight several important trends. Firstly, rates ofgrowth for corpus width are relatively highest dur-ing early ontogeny, prior to eruption of the perma-

nent first molar; thereafter, relative growth ratesdecrease across all taxa. This pattern is evidencedby comparison of the values of the slopes and corre-lation coefficients for dm2 and M1 corpus width vs.basicranial length (Table 3). Growth is completedearliest in P. paniscus. The lack of a linear relation-

Fig. 8. Bivariate plots of log10-transformed deciduous corpusdimensions against basicranial length. A: Gorilla has a relativelywider deciduous corpus as compared to Pan. Slope differences arenonsignificant (P � 0.05); Gorilla has a higher (P � 0.001) y-intercept. B: Pan has a relatively deeper mandibular corpus ascompared to Gorilla during early ontogeny, but Gorilla trans-poses above Pan. Pan has a higher (P � 0.05) slope. Note that inthese bivariate plots, gorillas with incompletely erupted decidu-ous dentition are comparable in skull size to chimpanzees andbonobos with M1 completely erupted.

148 A.B. TAYLOR

ship between M1 corpus width and basicraniallength in bonobos (Table 3) confirms that there isessentially no additional growth in corpus widthfollowing the eruption of M1, a pattern consistentwith heterochronic shifts in the timing of dentaleruption (Smith et al., 1994) and/or growth of thecranium (Laitman and Heimbuch, 1984; Leigh andShea, 1995, 1996) and mandible (Taylor, unpub-lished findings). Second, relative to basicraniallength, rate of growth for corpus depth is stronglypositively allometric and exceeds that of corpuswidth in all taxa. Thus, it is clear that early inontogeny, gorillas have a relatively wider corpus ascompared to dentally older chimpanzees or bonobos,but depth of the corpus does not “catch up” untilgorillas are dentally more mature.

Compared to Pan, gorillas also have absolutelylarger deciduous molars (dm2) buccolingually (df �3, 38; F � 46.23; P � 0.000) and mesiodistally (df �3, 38; F � 111.06; P � 0.000), and relatively largerdeciduous molars (Fig. 9). Keeping in mind that atcomparable skull sizes, taxa of very disparate dentalstages are being compared (e.g., gorillas character-ized only by an incompletely erupted deciduous den-tition are comparable in skull size to chimpanzeesand bonobos who already display a fully eruptedM1), these findings suggest that dental develop-ment, including crown formation, root formation,and dental eruption patterns, plays a role in thedevelopment and differentiation of the corpus inAfrican apes (Dean and Beynon, 1991), despite poorcorrelations between tooth and corpus dimensions(Taylor, 2000). The relatively early “drop-off” ingrowth of corpus width exhibited by the African apesmay be tied to dental eruption patterns, and couldaccount for the negative allometry and low correla-tions observed for this dimension in other taxa (e.g.,see Cole, 1992).

As predicted, labiolingual thickness of the sym-physis increases with intensification of herbivory,and represents one of the clearest departures fromontogenetic scaling of allometries (Fig. 5B). Theseresults concur with the observation of Daegling(1990) that gorillas have redistributed the compactbone of the anterior corpus and symphysis to achieveoptimal resistance to wishboning loads (Hylander,1985a; Ravosa, 1996a,b; Vinyard and Ravosa, 1998).If larger-bodied apes are constrained allometricallyto generate relatively less maximal masticatorymuscle force (Cachel, 1984), then gorillas wouldneed to recruit maximal amounts of balancing-sideadductor muscle force with greater frequency in or-der to masticate their tougher, more fibrous diet,which could augment wishboning forces at the sym-physis (Hylander, 1984).

Independent of diet, however, a relatively thickersymphysis would counter elevated wishboningforces that could accrue along the symphysis simplyas a function of allometric increases in symphysealcurvature associated with interspecific size increase(Hylander, 1985a; Vinyard and Ravosa, 1998).Changes in degree of symphyseal curvature are notsubstantiated on the basis of either mandibularlength vs. bicondylar breadth, or palate length vs.palate breadth (Tables 3 and 4). However, the posi-tive allometry of jaw length vs. jaw breadth in G. g.gorilla indicates that gorillas (males in particular)have relatively longer, narrower jaws and, presum-ably, more curved symphyses (Fig. 4). While thistrend cannot be confirmed for the African apes as agroup, neither can the possibility be ruled out thatthickening of the symphysis serves to counter allo-metric increases in wishboning forces associatedwith greater symphyseal curvature (Hylander,1985a). Thus, while gorillas show improved resis-tance to wishboning forces as compared to chimpan-zees, results do not offer strong support linking sym-physeal differences with diet over allometricconstraints.

Finally, ramus height and temporomandibularjoint height appear to increase with shifts in degreeof folivory (Tables 3 and 4; Fig. 5C,D). The advan-tage of a relatively taller mandibular ramus is theprovision of a larger attachment area for the mas-seter and medial pterygoid muscles, which implies alarger cross-sectional area for the adductor muscu-lature (Freeman, 1988). This is consistent with therelative increase in size of the masseter muscle forG. g. beringei (but not G. g. gorilla; Tables 3 and 4);size of the medial pterygoid muscle was not esti-mated in this study. I note, however, that whilecross-sectional area is proportional to muscle force,bony proxies of cross-sectional area are weakly cor-related with muscle force in macaques (Anton, 1999,2000). A relatively taller ramus may also increase themoment arm of the masseter and temporalis muscles(Maynard Smith and Savage, 1959; Greaves, 1974;DuBrul, 1977), and facilitate a more uniform distribu-tion of bite forces along the postcanine dentition (Ward

Fig. 9. Bivariate plot of buccolingual width of dm2 againstbasicranial length (all dimensions log10-transformed). Gorillashave relatively wider (buccolingually) deciduous molars as com-pared to Pan.


and Molnar, 1980). The relative increase in height ofthe jaw joint above the occlusal plane indicates thatgorillas are able to more evenly distribute occlusalloads along the postcanine dentition (Herring andHerring, 1974; Greaves, 1980). The combination of ataller and more vertically oriented mandibular ramushas been linked to reducing the forces associated withtougher diets in primates and other mammals (Jolly,1970; DuBrul, 1977; Daegling, 1992; Anton, 1996a;Satoh, 1997).

Apart from those features delineated above, thereis relatively little consistency in the patterning ofdifferences among the African apes. It was predictedthat gorillas would exhibit relatively wider mandib-ular condyles compared to chimpanzees, but thisexpectation is not consistently borne out statisticallyor graphically. For example, while G. g. gorilla hasrelatively wider mandibular condyles as comparedto P. t. troglodytes and P. paniscus, G. g. gorillaconverges on the trajectory for Pan later in ontog-eny. The clearest distinction is reflected in the dis-tribution of adult G. g. beringei (Fig. 6B), but giventhe small samples, this difference would be moreconvincing if the entire trajectory were elevated.Conversely, more frugivorous taxa were predicted toexhibit relatively longer condyles as compared tofolivores. Condyle length is variable among the Af-rican apes, as evidenced by wide confidence inter-vals and overlapping slopes (Tables 3 and 4; Fig.6D). Nevertheless, there is a downward transposi-tion of positive ontogenetic allometries such thatcondyle length decreases with interspecific increasein size, possibly suggesting the maintenance of func-tional equivalence as skull size increases. The rela-tively longer condyle in P. paniscus as compared toP. t. troglodytes further undermines the hypothesisthat bonobos are more folivorous than chimpanzees,while the link between condyle length and diet isweakened by the fact that G. g. gorilla does not haverelatively longer condyles than G. g. beringei (Tables3 and 4; Fig. 6C). Thus, while comparative studieshave shown relative increases in condyle length as-sociated with incisal behaviors, and relative in-creases in condyle width associated with postcaninemastication (Smith et al., 1983; Bouvier, 1986a; Ta-kahashi and Pan, 1994), the patterning shown forAfrican apes suggests these traits cannot be consis-tently linked to a particular dietary regime in pri-mates.

Differences in muscle lever arm lengths areplagued by similar inconsistencies. Relatively longerlever arms would improve masticatory efficiency intaxa with tougher diets, either by reducing theamount of muscular effort necessary to produce agiven bite force, or by providing for greater bite forcewith the same amount of muscle force. Again, how-ever, statistical differences are not consistent withpredictions based on diet, and there is no discerniblepattern of differentiation among taxa (Tables 3 and4). While temporalis lever arm length produces whatis clearly the most prominent separation between

gorillas and chimpanzees (Fig. 6D), here again wesee the downward transpositioning of positive al-lometries. Whether or not this pattern representsthe maintenance of functional equivalence with sizeincrease, the relatively longer lever arm in Pan runscounter to predictions based on diet. Experimentalstudies do not support the differential importance ofeither the temporalis or masseter muscles duringincisal behaviors (Hylander and Johnson, 1985;Ross and Hylander, 2000). However, it has beensuggested that primates processing large resistantfruits may generate bite forces at large gapes (Hy-lander, 1979a; Wall, 1999). Thus, one possible ben-efit of a relatively longer temporalis lever arm inPan is the minimization of muscle fiber stretch whilegenerating bite forces at relatively large gapes toprocess fruit. The relatively low temporomandibularjoint in Pan as compared to Gorilla is also consistentwith minimizing muscle stretch at a given gape(Herring and Herring, 1974), but this relationshipwould need to be explored in greater detail.

Interestingly, while gorillas are more prognathicthan chimpanzees and bonobos (Shea, 1983a), theAfrican apes are ontogenetically scaled for mandib-ular vs. basicranial lengths (Tables 3 and 4; Fig. 10).Gorillas, therefore, do not fit the predictions of arelatively shorter mandible, which would improvethe mechanical advantage of the jaw adductors, ashas been documented in other primates (e.g., Ra-vosa, 1990; Anton, 1996a). Assuming that muscleforce scales with negative allometry relative to bodymass (Hylander, 1985a; cf. Cachel, 1984; Anton,1999), adult gorillas would likely recruit relativelyless maximal muscle force compared to adult chim-panzees or bonobos. Anton (1999) observed that thepositive allometry of masseter cross-sectional areawith facial size in macaques provides a means ofoffsetting the biomechanically less efficient positionof the masseter lever arm in prognathic primates,which may have implications for gorillas, thoughthis cannot be directly tested here. Finally, I notethat ontogenetic scaling of mandibular vs. basicra-nial lengths in Pan clarifies that adult differences inmandibular length between bonobos and chimpan-zees (Cramer, 1977) reflect the shared, correlatedeffects of interspecific increase in skull size. Thus,the absolutely shorter mandible in adult bonoboscan be viewed as conferring a functional advantageover chimpanzees in the same way that juvenile andsubadult chimpanzees would have a mechanical ad-vantage over adult chimpanzees, but no special re-structuring of ontogenetic covariances is needed toproduce this effect.

Perhaps the most striking result shown here is theabsence of consistent and notable differences in rel-ative depth of the mandibular corpus across taxa(Tables 3 and 4; Fig. 6C), indicating that Africanapes have similar resistance capabilities to parasag-ittal bending loads, despite considerable differencesin the frequency with which leaves are comminuted.This result also contradicts the relatively larger

150 A.B. TAYLOR

masticatory forces in G. g. beringei presumably gen-erated by the relatively larger and more powerfulmasseter muscle. Daegling (1990) likewise notesthat, based on the biomechanical properties of themandibular corpus, chimpanzees, gorillas, and oran-gutans all appear to be equally effective at counter-ing parasagittal bending. This finding is particularlytroublesome in light of proposed arguments linkinga relatively deep corpus to the repetitive cycling ofthe jaws associated with pronounced folivory in nu-merous taxa, including folivorous colobines, platyr-rhines, and some leaf-eating prosimians (Hylander,1979a; Bouvier, 1986b; Ravosa, 1991). Thus, whilegorillas, and G. g. beringei in particular, exhibitsome features that may be linked to their relativelymore resistant diet, this particular result runscounter to one of the core morphological predictionshypothesized to distinguish folivores from frugi-vores.

Setting aside patterns of morphological variationshown to consistently differentiate between hard-and soft-object feeders, e.g., a transversely thickmandibular corpus, vertically oriented mandibularramus and face, facial shortening, or zygomatic but-tressing, (DuBrul, 1977; Cole, 1992; Daegling, 1992;Anton, 1996a), one would have to conclude eitherthat the mechanical properties of the African apediet are surprisingly similar, or that the Africanapes comprise an exception to the hypothesis thatfolivores are at risk for fatigue failure from repeti-tive chewing and may require larger average bite

force as compared to more frugivorous primates.Given their absolutely large size as adults, and thefact that much of their diet is arguably comprised offibrous but not “hard” foods (e.g., seeds, nuts; Lucaset al., 2000), size alone may be sufficient to counterthe risk of mandibular bone failure from repeatedbouts of chewing. Younger, smaller individuals maynot be faced with the same risk of fatigue failure,because their nutritional demands should be metwith relatively fewer calories. This translates intoabsolutely fewer chewing cycles per day, thoughtheir rate of bone turnover is undoubtedly higher ascompared to adults.

Interestingly, Gould (1966) argued, based on ob-servations across a variety of taxa, that in cases ofstrong positive allometry, upward transpositions orelevations tend to be disadvantageous. Downwardtranspositions of positive allometries in winglengths in birds, and tooth proportions in hyenasand cats (Kurten, 1954; as cited in Gould, 1966), areexamples of downward shifts that have been arguedas necessary to preclude maladaptive proportionsassociated with size increase. Downward transposi-tions of strong positive allometries, as seen here intemporalis lever arm length and condyle length (seealso Shea, 1983a), might well provide evidence ofshifts that are mechanically or functionally requiredto maintain geometric equivalence with size change(Gould, 1971). In light of these observations, thestrong positive allometry of other mandibular pro-portions, such as temporomandibular joint heightand ramus height, and the resulting upward trans-positions of ontogenetic allometries in gorillas, can-not be easily interpreted as the requisite correlatesof size increase for the maintenance of functionalequivalence, since these shifts could arguably beviewed as disadvantageous.

What of the proposed dietary differences betweenchimpanzees and bonobos? While data from thisstudy cannot be used to decipher the composition ormechanical properties of diet, there is no morpho-logical support for a mechanically different diet be-tween P. t. troglodytes and P. paniscus. Bonobos donot exhibit a clear pattern of differentiation fromchimpanzees; nor are there systematic differencesthat could be linked specifically to repetitive loadingof the jaws or resistance to larger internal forces. Atthe outset, I stated that functional models of masti-catory form would allow us to predict the morphol-ogy of bonobos, given the assumption of a structur-ally different diet. Rather than interpret the resultsas empirical evidence for rejecting a link betweendiet and morphology altogether, I would argue thatthe ecological data do not support a bonobo diet thatrequires unique mechanical solutions, particularlysince the evidence for a diet specialized towardsherbivory in bonobos is contradictory at best(Malenky and Stiles, 1991; Malenky and Wrang-ham, 1994; Malenky et al., 1994). Data on the me-chanical properties of foods consumed by these taxaare currently being analyzed (Lucas, personal com-

Fig. 10. African apes are ontogenetically scaled for mandib-ular length vs. basicranial length, indicating that taxa character-ized by mechanically resistant diets do not have relatively shortermandibles.


munication) and are key to substantiating or refut-ing this claim. It is noteworthy that even some of themore generally accepted differences in dentition,purported to differentiate between bonobos andchimpanzees on the basis of diet, such as sharperand higher cusped molars in bonobos (Kinzey, 1984),have been recently debated (Uchida, 1996).

Qualitative differences in the properties of foodsconsumed by bonobos and gorillas may have impli-cations for the absence of a shared masticatory pat-tern observed in this study. First, unlike gorillas,the evidence suggests that bonobos are quite selec-tive in their choice of herbaceous foodstuffs, choos-ing young pith, new shoots, and new, unopenedleaves (Malenky and Stiles, 1991; Wrangham et al.,1996). Furthermore, bonobos express a clear prefer-ence for pith and shoots over all leafy foods(Malenky and Stiles, 1991). Second, although someTHV consumed by bonobos is ubiquitously distrib-uted, it is not ubiquitously exploited (Malenky andStiles, 1991). Rather, bonobos express a preferencefor high-quality species of shoots and pith, even overfigs (Kano and Mulavwa, 1984; Malenky and Wrang-ham, 1994; Wrangham et al., 1996), and for specificfeeding sites and plants within those sites (Malenkyand Wrangham, 1994). Thus, although bonobos con-sume more vegetation than chimpanzees, they donot appear to be characterized by a greater degree ofleaf-eating, and what leaves they consume may beyoung and of higher quality than the folivorous ma-terial consumed by gorillas (Wrangham et al., 1996).Except where seasonally available fruit is concerned(Remis, 1997), evidence indicates gorillas are lessselective in their foraging efforts and consume low-quality, continuous resources that include relativelygreater amounts of leaves, vines, and bark (Rogerset al., 1988; White et al., 1995; Yamagiwa et al.,1996; Tutin et al., 1997). Thus, there may be littleappreciable difference in the mechanical demands ofchimpanzee and bonobo diets, despite variation indietary composition. Regardless of what the dataultimately reveal about the structural properties offoods consumed by bonobos, diet does not provide asatisfactory explanation for variation in jaw mor-phology in Pan.

Results also reveal the limitations of drawingfunctional inferences from masticatory morphology,which are hampered to some extent by the fact thatdifferent loading regimes are not necessarily tied tounique stress patterns in the mandible. Despite con-siderable experimental data elucidating mandibularstress and strain patterns, and theoretical and com-parative data on how masticatory loads are gener-ated, distributed, and resisted, anthropoid loadingregimes associated with postcanine mastication andincisal behaviors are not mutually exclusive. Para-sagittal bending moments, for example, are incurredduring unilateral mastication and incision, and ineither case the theoretically predicted biomechani-cal solution is an increase in corpus depth (Hy-lander, 1979a,b, 1988). Similarly, mastication and

incision produce torsional bending along the postca-nine corpus, and resistance to torsion is best resistedby a thicker corpus, regardless of the source of theload (Hylander, 1979a,b). Data from this study high-light the potential difficulties of resolving such con-tradictions, as both gorillas and chimpanzees ex-hibit relatively thicker mandibular corpora whencompared to bonobos, yet gorillas are folivorous, andchimpanzees are dedicated frugivores. Taxa maythus be characterized by different diets and loadingregimes and still manifest similar morphological re-sponses, rendering the formulation of mutually ex-clusive hypotheses problematic. As was alreadypointed out (Hylander, 1988), drawing inferencesabout masticatory loading regimes solely on the ba-sis of comparative morphology of the jaws is ill-advised. However, as demonstrated in this study,even a priori knowledge of diet is still insufficient forunambiguous interpretation of the functional conse-quences of patterns of jaw variation, reinforcing thedesirability of as much corroborative data as possi-ble. Further exploration of the developmental corre-lates of craniomandibular form will ultimately pro-vide a more complete picture of the evolution of thismorphological complex in the African apes.

CONCLUSIONS

Comparisons of ontogenetic allometries demon-strate that after controlling for differences in skulland jaw size, only a few morphological differencesconsistently fit the predictions of improved load re-sistance and/or increased masticatory efficiency as-sociated with shifts towards a more resistant diet. Insum, G. g. beringei exhibits a relatively wider man-dibular corpus and symphysis, higher mandibularramus, temporomandibular joints elevated higherabove the occlusal plane, and a relatively largermasseter muscle. Some of the same features thatdrive the separation of G. g. beringei from the otherAfrican apes also separate G. g. gorilla from Pan,consistent with the more mechanically resistant dietof gorillas. Apart from those features delineatedabove, all other analyses fail to result in the pre-dicted morphological differences in at least one pair-wise comparison, or they discriminate among taxain ways that run counter to dietary arguments. Mostsurprisingly, gorillas do not exhibit the predicteddeeper mandibular corpus that is the hallmark offolivorous primates, suggesting that in primates,there is not a consistent link between deep corporaand folivory. Finally, there is no consistent patternof morphological variation that supports the re-quirements of unique mechanical solutions to amore resistant diet in bonobos as compared to chim-panzees.

Thus, while some departures from shared pat-terns of ontogenetic allometric growth covariancemay reflect adaptations to diet, the dietary link isnot particularly strong. Patterns of divergenceamong the African apes as a group are clearly morecomplex than can be accounted for by diet alone.

152 A.B. TAYLOR

Allometric constraints and dental development mayalso be important factors in explaining mandibulardifferentiation among African apes. In addition,there are both ontogenetic and interspecific allomet-ric increases in size that may have a considerableimpact on masticatory morphology. As allometrictrends have been theoretically argued to be adaptiveonly in restricted size ranges, size alone could beresponsible for some of the allometric transpositionsin order to maintain functional equivalence.

ACKNOWLEDGMENTS

I am extremely grateful to Drs. Gene Albrecht,Susan Anton, Dave Daegling, F. Clark Howell, PeterLucas, Matt Ravosa, Brian Shea, Chris Vinyard,Christine Wall, and Richard Wrangham for theirwillingness to read and comment on various ver-sions of the manuscript. I am particularly indebtedto Susan Anton, Matt Ravosa, and Brian Shea fortheir continuous discussions and critical insightsduring all stages of this work. Valuable commentsfrom three anonymous reviewers considerably im-proved the quality of the manuscript. Dr. JamesPatton (Museum of Vertebrate Zoology, Berkeley,CA) kindly provided access to African ape materialduring initial stages of this work. I gratefully ac-knowledge the following individuals who providedaccess to the African ape materials used in thisstudy and assistance during data collection: Dr.Wim Van Neer, Central African Museum, Tervuren;Dr. Bruce Latimer and Lyman Jellema, ClevelandMuseum of Natural History; John Harrison andMalcolm Harman, the Powell-Cotton Museum andQuex House and Gardens Birchington, Kent, En-gland; Dr. Richard Thorington and Linda Gordon,Department of Mammalogy, US National Museumof Natural History, Smithsonian Institution; Drs.Bruce Patterson and Matt Ravosa, Field Museum ofNatural History.

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