AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 82~509-515(1990) Comparison of Muscle Weight and Force Ratios in New and Old World Monkeys MARIANNE BOUVIER AND STEPHEN M. TSANG Department of Cell Biology and Anatomy, University of Miami School of Medicine, Miami, Florida 33101 KEY WORDS Biomechanics, Craniofacial Skeleton, Masticatory Muscles ABSTRACT Thin mandibles and small incisors found in New World monkeys as compared with Old World monkeys suggest that there may be differences in craniofacial loading patterns between these two groups, particularly in levels of mandibular corpus twisting (Hylander, 1975,1979a; Eaglen, 1984; Bouvier, 1986a,b). This study examined the hypothesis that changes in the relative force contributions of the masticatory muscles were responsible for lowering torsion on the mandibular corpus in New World monkeys, Muscle weight and physiological cross-sections were compared using data from the literature (Schumacher, 1960; Turnbull, 1970; Cachel, 1979) as well as new data on adult male Cebus apella and Macaca mulatta. Both age and sex had an effect on muscle ratios. Mixed samples such as those used by Schumacher and Turnbull probably are not appropriate for drawing conclusions concerning species or group differences in muscle ratios. In addition, biomechanical conclusions based on muscle weight ratios alone to estimate muscle force may be misleading because fiber length inversely affects the amount of force a muscle can exert. A comparison of ratios based on physiological cross-section as an estimator of muscle force in New and Old World monkeys does not support the hypothesis that alterations in force contribution by individual masticatory muscles are responsible for minimizing mandibular corpus twisting in New World monkeys. Therefore, if twisting has been minimized in New World monkeys as suggested by their thin corpora, other changes in the craniofacial musculoskeletal complex, such as different muscle recruitment or pinnation patterns, may be responsible. Considerable information on the evolution of dietary adaptations in primates has been obtained through studies of the masticatory apparatus in monkeys. Such studies centering on two particular groups, the New and Old World monkeys, have shown that distinctive atterns of craniofacial morphology are like y related to the chewing stresses associated with different diets (Hylander, P 1986a,b).For short, dee , and wide jaws of the Old World colobines ave been related t o their characteristic diet of leaves. R 1990 WILEY-LISS, INC. In vivo bone strain studies have confirmed that diet affects mandibular loading during mastication (Hylander, 1979b, 1984). These strain gage studies demonstrate that the Old World monkey mandibular corpus is both bent and twisted about its long axis during mastication. In addition, these studies show that differences in food consistency, such as between hard fruits and leaves, significantly affect levels and atterns of mandibular bone strain. Thus, one strain studies have strengthened the relationship between dietary adaptation and jaw morphology. Consequently, the inferring of dietary adapta- E Received October 10,1988; accepted October 30,1989 510 M. BOUVIER AND S.M. TSANG tion from craniofacial skeletal morphology continues to be a productive approach to problems of rimate functional and evolutionary morp ology. Unfortunately, no bone strain data are available for New World monkeys; however, comparisons of their mandibular morphology with that of Old World monkeys suggest that there may be significant differences in mandibular stresses during mastication between the two groups. Compared with Old World monkeys, New World monkeys have small incisors and markedly thinner mandibular corpora (Eaglen, 1984; Bouvier, 1986b). The distinctive jaw morphology of New World monkeys, articularly the thinness of the mandibu ar corpus, indicates that their cor us may be subjected to considerably lower oads during mastication, with especially low levels of twisting. In the absence of bone strain data for New World monkeys, the size and arrangements of the chewing muscles can elucidate loading patterns on the mandible. Among the primary chewing muscles, temporalis, masseter, and medial pterygoid are chiefly responsible for twisting of the jaws (Fig. 1). In Old World monkeys, the origin of the masseter muscle, on the zygomatic bone, is located more laterally than its insertion on the angle of the mandible. Therefore, during mastication, the masseter will tend to evert the lower border of the Old World monkey mandible. Conversely, the medial pterygoid muscle produces inversion of the lower mandibular border because its origin, on the pterygoid plates, is medial to its insertion on the mandibular angle. Thus, because the masseter and medial pterygoid muscles twist in opposite directions, they can theoretically neutralize one another if their respective moments are e ual. The tem oralis muscle contributes slig tly to man ibular twisting. Depending on its precise orientation, the direction of twisting could be either with masseter or with medial pterygoid. In Old World monkeys, the masseter muscle is approximately twice as large as medial terygoid muscle (Hylander, 1979a). Thereore, the masseter muscle in Old World monkeys, by virtue of its relatively large size, overcomes the opposing pull of the smaller medial pterygoid muscle. The result is a torque on the mandible tending to evert its lower border. H lander’s (1979b, 1984) in vivo bone strain ata confirm that Old World monkey mandibles are twisted in this fash- g P P a F i l B Fig. 1. Lines of action for temporalis (TI, masseter (Ma), and medial pterygoid iMp) muscles. ion during mastication. The temporalis muscle in Old World monkeys probably contributes only slightly to twisting, most likely in concert with masseter. The degree of mandibular twisting, therefore, is determined largely by the positioning of the origins and insertions of temporalis, masseter, and medial pterygoid muscles and by their respective contributions to the total masticatory force. Mandibular twisting may be maximized when there is a lateral positioning of the chewing muscle resultant (Hylander, 1979b),which occurs when there is a large masseter: medial pterygoid andlor a large temporalis: medial pterygoid muscle force ratio. This study compares these masticatory muscle ratios in New and Old World monkeys, first using data available from the literature (Schumacher, 1961; Turnbull, 1970; and Cachel, 1979). Second, these results are compared with new data presented here for one New World monkey (Cebus upella) and one Old World monkey (Mucaca mulattu)in order to determine whether masticatory muscle ratios differ in a manner consistent with the hypothesis of lower mandibular corpus twistin in New World monkeys compared with 0 d World monkeys. In addition, this study examines the relationship between muscle weight versus muscle force ratios (i.e., physiological cross-section) in the chewing muscles of New and Old World monkeys. f 511 MUSCLE RATIOS IN MONKEYS MATERIALS AND METHODS Schumacher (1961) study Schumacher’s primate sample consisted of 3 New World monkeys (Cebus uariegatus, C. apella, Saimiri) and 7 Old World monkeys (2 Macaca mulatta, 2 M. sinica, Papio, Mandrillus, Colobus) (Table 1).This mixed sample includes both males and females, adults and ‘uveniles. Schumacher included dry musc e weight as well as physiological crosssection (PCS) after Weber (Carlsoo, 1952): i 2 Dry weight ( )/fiber length (cm) muscle specikc gravity ~ 1 . g/cm 0 1 Turnbull (1970) study Turnbull examined relative wei hts (i.e., percentages) of masticatory musc es using rimate data from two previous studies: chumacher (1961) and Fabian (Table 2). In addition to Schumacher’s primate specimens, Turnbull included the following specimens from Fabian’s study: 1 New World monkey (Callithrixpennicillata) and 11 Old World monkeys (Macaca mulatta, Papio sp., Theropithecus gelada; Cercopithecus diana, Erythrocebuspatas, and 2 Colobus s 1. This is a mixed sample consisting of bot males and females, adults and juveniles. F 8 R‘ Cachel (1979) study Cachel separated her sample by age and sex (Table 3). She included, among the adults, 10 male New World monkeys (5 Saimiri sciureus, 4 Saguinis fuscicollis, Alouatta palliata);9 male Old World monkeys (3 Macaca mulatta, Erythrocebus patas, 2 Cercopithecus ascanius, 2 Papio cynocephalus, Mandrillus sphinx); 13 female New World monkeys (5 Saimiri sciureus, Saguinus fuscicollis 4 Ateles geoffroyi, 2 Alouatta palliata, Cacajao rubicundus); and 15 female Old World monkeys ( 3 Macaca mulatta, Erythrocebus patas, 3 Cercopithecus ascanius, 2 C. aethiops, 2 C. neglectus, C. diana, 3 Colobus polykomos). Among the juveniles (grade II), she included no male New World monkeys; 8 male Old World monkeys (3 Macaca mulatta, Cercopithecus neglectus, C . albogularis, Presbytis cristatus, Papio cynocephalus, P. hamadryas); 3 female New World monkeys (Ateles geoffroyi) and 5 female Old World monkeys (Macaca mulatta Erythrocebus patas, Colobuspolykomos, Papio cynocephalus, Theropithecus gelada). In addition, Cachel included 3 infant (grade I) specimens, all males (Cercopithecus aethiops, Colobus polykomos, Papio cynocephalus). Cachel analyzed dry weight T A B L E 1. Analysis of Masticatory Muscle Weight and PCS Ratios i n New and Old World Mor~keys‘ GrouD N New World monkeys (SD) Old World monkeys (SD) P 3 7 Temporalis : medial pterygoid Weight PCS 4.20 (0.29) 4.73 (1.04) NS 3.17 (0.61) 2.66 (0.80) NS Masseter : medial pterygoid Weight PCS 2.58 (0.28) 2.18 (0.32) 0.04 1.89 (0.19) 1.47 (0.29) 0.05 Temporalis : masseter Weight PCS 1.64 (0.12) 2.18 (0.43) 0.04 1.68 (0.22) 1.80 (0.38) NS ‘Data frum Schumacher (1961). T A B L E 2. Analysis of Masticatory Muscle Weight-Percent Ratios in New and Old World Monkeys1 Group N New World monkeys (SD) Old World monkeys (SD) P 4 ‘Data from Turnbull (1970) 18 Temporalis : medial Pterygoid Masseter : medial Pterygoid Temporalis : masseter 4.28 (0.61) 4.42 ( 1.95) NS 2.51 (0.28) 2.17 (0.35) NS 1.72 (0.30) 2.00 (0.66) NS 512 M. BOUVIER AND S.M. TSANG T A B L E 3. Analysis OWM (SD) NWM of Temporalis : Masseter Weight Ratios i n New and Old World Monkeys' Infant Males' Juvenile 2.29'"' (0.97) 2.75 (0.51) - - (SD) Adult Infant 3,76!"-!;) (0.67) 2.55"' (0.92) - Females* Juvenile Adult 2.44(B) (0.96) 2.11"" (0.12) 2.85 (0.67) 2.26'"' (0.67) *Means with the same letter are significantly different (P< 0.05). Data from Cache1 (1979). ' T A B L E 4. Mean Fiber Length Imml of Masticatory Muscles: New Data Group N Temporalis Masseter Medial pterygoid Lateral pterygoid C. apella (SD) M. mulatta 3 17.60 (4.36) 32.60 (4.20) 0.02 15.63 (3.50) 19.97 (6.46) NS 9.03 (2.46) 12.93 (0.55) 0.02 8.70 (2.56) 11.17 (3.99) NS (SD) P 3 of only 2 masticatory muscles, temporalis and masseter. For this study, the anterior and posterior fibers of temporalis were considered together. New data A total of six adult male specimens were included in this study: 3 New World monkeys (Cebus apella) and 3 Old World monkeys (Macaca mulatta). A cercopithecine, Macaca mulatta, was chosen for this comparison because it represents an Old World monkey species with a comparatively wide mandible relative to length (Bouvier, 1986a), which was also readily available for dissection. Because mandibular width scaling patterns are similar in colobines and cercopithecines, M. mulatta can be considered to represent both of these subfamilies. Of the two New World monkeys species available to us for dissection, Cebus apella and Saimiri sciureus, C. apella was chosen because its mean species body weight falls within the Old World monkey range while that of Saimiri does not. Mandibular corpus dimensions in C. apella are not particularly narrow, but they do fall well below the Old World regression line (Bouvier, 1986b). Hence, Cebus apella was considered an acceptable, albeit perhaps not ideal, candidate for this comparison. Temporalis, masseter, medial, and lateral pterygoid muscles were dissected out completely. Ten muscles fibers were teased from the surface of each muscle and measured with dial calipers accurate to 0.1 mm (Table 4). Muscles were cleaned of all connective tissue and dried in an oven at 60°C until all moisture was removed. Dry weight was obtained for each muscle on a balance accurate to 0.001 g. Right and left values were averaged (Table 5 ) . Physiological cross-section (PCS) was calculated after Weber (Carlsoo, 1952): PCS = Dry weight (g)/mean fiber length (cm) x specific gravity (g/cm3) A value of 1.0 /cm3 was used for muscle s ecific gravity ( arlsoo, 1952). When musc e architecture is not complex (e.g., pinnated), PCS is proportional to the force that a muscle is capable of exerting (Table 6 ) . The following ratios were calculated using both dry weight and PCS (Table 7): (1)temporalis: medial pterygoid; (2) masseter: medial pterygoid; (3) masseter: medial and lateral pterygoid; and (4)temporalis: masseter. Weight and PCS percentages of total were also calculated for each muscle (Tables 5,6). Because of the small sample sizes in all studies examined here, data were ranked. Schumacher, Turnbull, and new data were then analyzed using Student's t-test to determine whether New and Old World monkey means differed significantly ( R 0 . 0 5 ) . Because Cachel's data were separated into a number of different agelsex groups, analysis P 8 513 MUSCLE RATIOS IN MONKEYS of variance with Duncan multiple range ralis : masseter and temDoralis : medial post-tests was used to determine iignificant pterygoid PCS ratios were ;lot different. differences among means ( R 0 . 0 5 ) . Turnbull data None of the weight-percent ratios was RESULTS different (P>0.05) (see Table 2). Schumacher data Cachel data The mean muscle weight ratio for masseter : medial pterygoid was larger in New The mean muscle weight ratio for tempoWorld monkeys, while the temporalis : mas- ralis : masseter was lar est in Old World seter ratio was smaller compared with Old monkey adult males (see able 3). This mean World monkeys (see Table 1).Mean differ- differed significantly from infant male and ences were significant for both ratios juvenile female Old World monkeys (P<0.05). The weight ratio for temporalis : (P<0.05). Old World monke adult males medial pterygoid was not significantly dif- also differed significantly rom all New ferent in the 2 groups. World monkey agehex groups (P<0.05). The mean physiological cross-section New data (PCS)ratio for masseter : medical pter goid Mucaca mulatta had a greater mean fiber was higher in New World monkeys an this difference was significant (P<0.05). Tempo- length compared with C. apella (Table 41, 8 P B T A B L E 5. Mean Dry Weight (g) and Percentage of Total Dry Weight (%) Group N C. apella 3 (SD) M. mulatta (SD) 3 P Temporalis Weight % Masseter Weight 3.61 1 (0.950) 9.154 (3.915) 0.02 1.436 (0.407) 2.245 (1.630) NS 64.2 76.5 0.02 1% 25.5 17.1 0.02 of Masticatory Muscles; New Data Medial pterygoid Weight 0.429 (0.050) 0.644 (0.236) NS %I 7.9 5.5 0.03 Lateral pterygoid Weight 0.130 (0.034) 0.125 (0.108) NS X!I 2.4 0.9 0.02 T A B L E 6. Mean Physiological Cross-section (PCS) (in cm') and Percentages of Total PCS (%) i n Masticatory Muscles: New Data Grow N C. apella (SD) M. mulatta (SD) P 3 3 Temporalis PCS w 1.942 (0.165) 2.601 (0.805) 57.0 NS NS 63.0 Masseter PCS % 0.859 (0.061) 0.981 (0.412) NS 25.3 23.4 NS Medial pterygoid PCS 0.462 (0.080) 0.470 (0.170) NS Lateral pterygoid PCS Yll 13.6 11.3 w 0.142 (0.010) 0.100 (0.069) 4.2 NS NS NS 2.3 T A B L E 7. Mean Dry Weight and PCS Ratios in Masticatory Muscles: N e w Data Group N C. apella (SD) M. mulatta (SD) P 3 3 Temporalis : medial pterygoid Wt. PCS 8.36 (1.50) 14.03 (0.87) 0.02 4.25 (0.88) 5.60 (0.51) NS Masseter : medial pterygoid Wt. PCS 3.35 (0.92) 3.20 (1.17) NS 1.91 (0.45) 2.07 (0.19) NS Masseter : medial and lateral pterygoid Wt. PCS 2.61 (0.84) 2.70 (0.78) NS 1.44 (0.25) 1.75 (0.33) NS Temporalis : masseter Wt. PCS 2.55 (0.38) 4.68 (1.25) 0.02 2.27 (0.29) 2.74 (0.52) NS M. BOUVIER AND S.M. TSANG 514 and this difference was significant for temporalis and medial pterygoid but not for masseter and lateral pterygoid ( R 0 . 0 5 ) . Mean dry weights (Table 5) were not significantly different, except for temporalis (P<0.05), which was greater in M. mulatta. Mean ercents were significantly different in all our masticatory muscles, with masseter and the pterygoids contributing a relatively large percentage in C. apella. None of the mean physiological cross-sections or percentages of PCS differs significantly in the two groups (Table 6, P>0.05). For weight ratios involving temporalis, C. apella had smaller values (Table 7). Mean weight ratios were significantly different in C. apella and M . mulatta for temporalis : medial pterygoid and temporalis : masseter but not for masseter : pterygoids. Mean PCS ratios were not significantly different in the 2 groups (l50.05). ! DISCUSSION Dry weights and weight ratios found here for adults were similar to those found by Cachel (1979) but are considerably larger than those found in Schumacher’s and Turnbull’s data. Weight ratios from Cachel’s ‘uvenile and infant animals were more simi ar to those from Schumacher’s and Turnbull’s studies. The dry weights that Schumacher reports (except for Sairnirz) are one tenth those found here and in Cachel’s study. This suggests that the majority of Schumacher’s specimens were infants or juveniles. Because Turnbull relied heavily on Schumacher’s data, most of his specimens also appear to be young. If all masticatory muscles grow at the same rate, weight ratios would not be affected by age; however, Cachel’s data indicate that, in males, there is a significant growth effect for temporalis : masseter ratios (her 1979 study did not include other muscles). Male infants had the smallest ratios, with juveniles intermediate, and adults greatest (see Table 3).A direct comparison of rhesus macaque temporalis : masseter ratios in the various studies shows a ratio for adult males measured here of 4.68; for adult males in Cachel’s study, 3.92; for ‘uvenile males in Cachel’s study, 2.98; and or Schumacher’s study, 2.17 (age and sex unknown). Comparisons for Cebus apella and for other weight ratios give similar results. Cachel’s(1984)study of growth and allometry in the masticatory muscles of monkeys 1 / from her previous study provides support for differential growth. She found that medial pterygoid underwent earlier relative growth than did either masseter or temporalis. A small and heterogenous sample did not permit further conclusions concerning other masticatory muscles; however, Cachel concluded that growth of these muscles does not proceed at a steady rate. Skeletal studies confirm that craniofacial bone growth in primates is not rate-constant (Oyen et al., 1979; Oyen and Rice, 1980; Sirianni et al., 1982; Bouvier, 1988). Sexual dimorphism in growth allometry may also be a compounding problem in comparing muscle ratios from mixed samples, particularly in Old World monkeys. Old World male monkeys had greater temporalis: masseter weight ratios compared to females (see Table 3); however, this difference was not significant. Thus, caution should be exercised when making biomechanical inferences from muscle data based on mixed samles for either age or sex. As a corollary, [ecause there may be significant agetsex differences in muscle growth and biomechanics, this should be investigated more closely. Furthermore, regardless of how carefully the sample is constructed with regard to age and sex, considering muscle weight ratios alone may give misleading results. Weight ratios do not take into account muscle length, which has a significant (inverse) effect on the force that a muscle can exert. If one is concerned with biomechanical loading, muscle force, or a reasonable estimate, rather than weight is the relevant arameter. Physiological cross-section may e used to provide an estimate of force, taking into account both muscle weight and fiber length (Carlsoo, 1952).Table 7 shows a direct comparison of ratios based on either weight or physiological cross-section. Weight ratios involving temporalis were significantly different in the New and Old World monkey species examined here leading t o the impression that there may have been adaptation in the New World monkey temporalis muscle to account for lower twisting. A small temporalis : medial pterygoid ratio would theoretically be associated with lower levels of mandibular corpus twisting because of more medial-positioning of the resultant force which could account at least partially for thin corpora in New World monkeys. However, when physiologic cross-section (taking into account both muscle weight and E MUSCLE RATIOS IN MONKEYS 515 fiber length) is compared, significant differ- heads for dissection. In addition, we wish to ences in ratios involvingthe temporalis mus- thank anonymous reviewers for their many cle disappear. This indicates that greater helpful comments. temporalis weight in M. mulatta was partially negated by increased fiber length. LITERATURE CITED Thus, adaptations in muscle force ratios to M (1986a) A biomechanical analysis of mandibminimize twisting are not apparent in C. Bouvier ular scaling in Old World monkeys. Am. J . Phys. upellu and may not explain thinner corpora Anthropol69:473-482. in New World monkeys as a group. Conclu- Bouvier M (198613)Biomechanical scaling of mandibular dimensions in New World monkeys. Int. J. Primatol. sions to the contrary on muscle weight ratios 7:551-567. alone would be misleading. However, beM (1988) Age estimation in rhesus macaques cause only one New and one Old World mon- Bouvier (Macaca mulatta) based on mandibular dimensions. key s ecies were examined in detail here, Am. J. Primatol. 15t129-142. musc e ratio adaptations to minimize twist- Cachel SM (1979) A functional analysis of the primate masticatory system and origin of the anthropoid posting may exist in some New World monkeys, orbital septum. Am. J. Phys. Anthropol. 47:l-17. particularly those with especially transSM (1984) Growth and allometry in primate versely narrow mandibular corpora such as Cachel masticatory muscles. Arch. Oral Biol. 29287-293. Alouattu (Bouvier, 1986b). Carlsoo S (1952) Nervous coordination and mechanical Other possibilities could account for less function of the mandibular elevators. An electromyographic study of the activity, and a n anatomic analysis twisting in New World monkeys, including of the mechanics of the muscles. Acta Odontologica changes in the orientations for masseter, Scand. 10(suppl.II):1-132. medial pterygoid and/or temporalis: 1)mas- Eaglen RH (1984) Incisor size and diet revisited: The seter to a more vertical position (less twistview from a platyrrhine perspective. Am. J. Phys. Anthropol. 64:263-275. ing);2) medial pterygoid to a more horizontal osition (more twisting); and/or 3) tempora- Hylander WL (1975)Incisor size and diet in anthropoids with special reference to cerocopithecidae. Science IS to a less vertical position (more twisting 189t1095-1098. along with medial ptery oid). In addition, Hylander WL (1979a) The functional significance of other explanations for t in jaws in New primate mandibular form. J. Morphol. 106:223-240. World monkeys include, for example, differ- Hylander WL (1979b) Mandibular function in Galago crassicaudatus and Macaca fascicularis: An in vivo ences in muscle recruitment patterns beapproach to stress analysis of the mandible. J . Mortween masseter and medial pterygoid, alphol. 159:253-296. tered muscle architectural adaptations Hylander WL (1984)Stress and strain in the mandibular affecting forces generated, or heavy reliance symphysis of primates. A test of competing hypothesis. Am. J. Phys. Anthropol. 64:1-46. on foods with mechanical consistencies associated with low torsional deformation of the Oyen OJ, Walker AC, and Rice RW (1979) Craniofacial growth in olive baboons (Pa io cynocephalus anubis): mandible durin ingestion and mastication. Browridge formation. growtk. 43t174-187. Electromyograp ic and bone strain experi- Oyen OJ and Rice RW (1980) Supraorbital development ments investigating there hypothesis would in chimpanzees, macaques and baboons. J. Med. Primatol. 9:161-168. contribute significantly toward resolving Schumacher GH (1961) Funktionelle Morphologie der this question. P F a 1 ACKNOWLEDGMENTS We are grateful to Dr. Richard Thorington at the Mammalogy Division, Smithsonian Institution, for providing the Cebus apella Kaumuskulatur. Jena: VEB Gustav Fischer Verlag. Siranni J E , Van Ness AL, and Swindler DR (1980) Growth of the mandible in adolescent pig-tailed macaques (Macaca nemestrina). Hum. Biol. 54:31-44. Turnbull WD (1970) Mammalian masticatory apparatus. Fieldiana Geology 18t147-356.