AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 120:153–170 (2003) Comparative Functional Analysis of Skull Morphology of Tree-Gouging Primates Christopher J. Vinyard,2* Christine E. Wall,1 Susan H. Williams,1 and William L. Hylander1,2 1 Department of Biological Anthropology and Anatomy, Duke University Medical Center, Durham, North Carolina 27710 2 Duke University Primate Center, Durham, North Carolina 27710 KEY WORDS tree gouging; skull functional morphology; gape; forces; load resistance ABSTRACT Many primates habitually feed on tree exudates such as gums and saps. Among these exudate feeders, Cebuella pygmaea, Callithrix spp., Phaner furcifer, and most likely Euoticus elegantulus elicit exudate flow by biting into trees with their anterior dentition. We define this behavior as gouging. Beyond the recent publication by Dumont ( Am J Phys Anthropol 102:187– 202), there have been few attempts to address whether any aspect of skull form in gouging primates relates to this specialized feeding behavior. However, many researchers have proposed that tree gouging results in larger bite force, larger internal skull loads, and larger jaw gapes in comparison to other chewing and biting behaviors. If true, then we might expect primate gougers to exhibit skull modifications that provide increased abilities to produce bite forces at the incisors, withstand loads in the skull, and/or generate large gapes for gouging. We develop 13 morphological predictions based on the expectation that gouging involves relatively large jaw forces and/or jaw gapes. We compare skull shapes for P. furcifer to five cheirogaleid taxa, E. elegantulus to six galagid species, and C. jacchus to two tamarin species, so as to assess whether gouging primates exhibit these predicted morphological shapes. Our results show little morphological evidence for increased force-production or load-resistance abilities in the skulls of these gouging primates. Conversely, these gougers tend to have skull shapes that are advantageous for creating large gapes. For example, all three gouging species have significantly lower condylar heights relative to the toothrow at a given mandibular length in comparison with closely related, nongouging taxa. Lowering the height of the condyle relative to the mandibular toothrow should reduce the stretching of the masseters and medial pterygoids during jaw opening, as well as position the mandibular incisors more anteriorly at wide jaw gapes. In other words, the lower incisors will follow a more vertical trajectory during both jaw opening and closing. We predict, based on these findings, that tree-gouging primates do not generate unusually large forces, but that they do use relatively large gapes during gouging. Of course, in vivo data on jaw forces and jaw gapes are required to reliably assess skull functions during gouging. Am J Phys Anthropol 120:153–170, 2003. Tree exudates provide an essential food source for many primates (Kinzey et al., 1975; Charles-Dominique, 1977; Charles-Dominique and Petter, 1980; Sussman and Kinzey, 1984; Nash, 1986; Garber, 1992). Field researchers have observed exudate feeding or gummivory in at least 37 primate species, including representative taxa for most primate superfamilies (see Coimbra-Filho and Mittermeier, 1977; Garber, 1984; Nash, 1986 and references therein).1 Many of these species possess suites of morphological features that have been hypothesized to be functionally linked to exudate feeding, such as small body size, robust lower incisors, caniniform upper premolars, claw-like tegulae, camouflaged pelage, and/or expanded stomachs or large intestines (Kinzey et al., 1975; Petter et al., 1977; Hershkovitz, 1977; Rosenberger, 1978; Charles-Dominique and Petter, 1980; Chivers and Hladik, 1980, 1984; Coimbra-Filho et al., 1980; Garber, 1980; Martin, 1990; Hamrick, 1998). A limited number of field observations suggest that some of these gummivorous primate species actively elicit tree exudate flow by mechanically damaging trees with their anterior teeth. We define this type of biting behavior as gouging (Stevenson and Rylands, © 2003 WILEY-LISS, INC. © 2003 Wiley-Liss, Inc. 1 Nash (1986) discusses the potential differences in the definitions of exudate feeding vs. gummivory. We use these terms synonymously to include the relevant literature that applies either term to describe this feeding behavior. Grant sponsor: Sigma-Xi; Grant sponsor: Boise Fund; Grant sponsor: AMNH; Grant sponsor: NSF; grant numbers SBR-9701425; Grant sponsor: L.S.B. Leakey Foundation. *Correspondence to: Christopher J. Vinyard, Department of Biological Anthropology and Anatomy, Box 3170, Duke University Medical Center, Durham, NC 27710. E-mail: email@example.com Received 13 February 2001; accepted 16 April 2002. DOI 10.1002/ajpa.10129 Published online in Wiley InterScience (www.interscience.wiley. com). 154 C.J. VINYARD ET AL. 1988). Several of these gouging primates have elongate, labio-lingually thick, or otherwise modified anterior tooth crowns thought to be related functionally to gouging (Martin, 1972, 1979, 1990; Charles-Dominique, 1977; Coimbra-Filho and Mittermeier, 1977; Szalay and Seligsohn, 1977; Rosenberger, 1978; Muskin, 1984; Eaglen, 1986; Natori and Shigehara, 1992). Compared to the information on dental functional morphology, primatologists know far less about how the mechanical demands of gouging affect skull form in these primates (Dumont, 1997). Dumont (1997) examined skull shapes in several tree-gouging primates and marsupials. Species of primates, bats, and marsupials were compared together in a discriminant function analysis to determine if morphological adaptations to tree gouging could be recognized in the skull. The phylogenetic breadth of species included in the analysis was offered as an attempt to “highlight anatomical features that are correlated with dietary habit and to minimize emphasis on features that characterize closely related species” (Dumont, 1997, p. 188). We take a different view of this approach to discerning form-function relationships in specific taxa. We argue that lumping such phylogenetically diverse species in a single analysis makes it difficult, if not unlikely, to determine what component of variation in skull form among these species is related to the mechanical demands of tree gouging vs. skull variation linked to other evolutionary events that occurred during the largely separate phylogenetic histories of these various species (Felsenstein, 1985; Huey and Bennett, 1986, 1990; Bennett and Huey, 1990; Brooks and McLennan, 1991; Garland and Adolph, 1994; Harvey and Pagel, 1991; Miles and Dunham, 1993). Here we utilize an alternative method. We carry out multiple, pairwise morphometric comparisons of primate tree gougers to closely related species that do not gouge trees in order to assess differences in skull form that may be functionally related to gouging (Harvey, 1991; Moller and Birkhead, 1992; Purvis and Bronham, 1997; Maddison, 2000). This more phylogenetically restricted approach does not eliminate all confounding factors (e.g., size-correlated changes in shape), but it does reduce the complications created by comparing diverse species with markedly different phylogenetic histories. PRIMATE TREE GOUGERS The behavioral evidence for habitual tree gouging associated with exudate feeding is limited for most primates, with the exception of several marmosets. Based on available field reports, we consider Callithrix spp., Cebuella pygmaea,2 Phaner furcifer, and 2 We did not include Cebuella pygmaea in this study because not enough individuals could be measured, and there is no adequate, nongouging sister species of approximately similar body size for comparison. Euoticus elegantulus to be habitual tree-gouging species. We base this decision on the combination of three criteria. First, these species have been observed using their anterior teeth to either elicit exudate flow or extract exudates from trees (Petter et al., 1971, 1977; Charles-Dominique, 1974, 1977; Kinzey et al., 1975; Coimbra-Filho and Mittermeier, 1976, 1977; Ramirez et al., 1977; Charles-Dominique and Petter, 1980; Lacher et al., 1981, 1984; Rylands, 1981, 1984; Maier et al., 1982; Soini, 1982; Sussman and Kinzey, 1984; Stevenson and Rylands, 1988). Second, field observations and/or data from stomach contents show that exudates form a large percentage of the diet for these species (Petter et al., 1971, 1977; Charles-Dominique, 1974, 1977; Pariente, 1975; Ramirez et al., 1977; Szalay and Seligsohn, 1977; Charles-Dominique and Bearder, 1979; Hladik, 1979; Charles-Dominique and Petter, 1980; Hladik et al., 1979; Lacher et al., 1981; Maier et al., 1982; Fonseca and Lacher, 1984; Sussman and Kinzey, 1984). Third, each of these species exhibits derived dental morphologies that are arguably functionally linked to tree gouging (Martin, 1972, 1979; Petter et al., 1971, 1977; Coimbra-Filho and Mittermeier, 1976, 1977; Charles-Dominique, 1977; Szalay and Seligsohn, 1977; Rosenberger, 1978, 1992; Charles-Dominique and Petter, 1980; Muskin, 1984; Sussman and Kinzey, 1984; Eaglen, 1986; Nash, 1986; Stevenson and Rylands, 1988; Garber, 1992; Natori and Shigehara, 1992; Ferrari, 1993). Future field observations may add to this list of habitual tree gougers. MORPHOLOGICAL PREDICTIONS LINKED TO TREE GOUGING Several researchers suggest that tree gouging among specific primates produces large forces at the jaw or results in large jaw gapes relative to other behaviors involving the oral apparatus (Szalay and Seligsohn, 1977; Szalay and Delson, 1979; Dumont, 1997; Williams and Wall, 1999; Spencer, 1999; Vinyard, 1999; Williams et al., 2000). We want to be clear, however, that presently we lack sufficient in vivo data demonstrating that jaw forces and/or gapes are relatively large during gouging (for preliminary in vivo data, see Vinyard et al., 2001). Our goal in this study was to determine if there are changes in skull form in gouging primates that can be functionally related to the hypothesized large jaw forces and/or jaw gapes during gouging. We make two assumptions in our morphological comparisons: 1) that we can reasonably infer certain aspects of jaw forces, skull loads, and jaw gapes during gouging from in vivo and comparative data on primate incising and biting along their anterior teeth, and 2) that existing skull forms in gouging primates represent functional and/or evolutionary adaptive responses to these supposed increased functional demands. If a tree-gouging species exhibits a predicted morphology in all pairwise comparisons with non- SKULL MORPHOMETRICS IN TREE-GOUGING PRIMATES gouging species in its family or subfamily, then correlational support is offered suggesting that a particular skull form is functionally linked to gouging in that species. Predictions related to large jaw forces during gouging Several researchers suggest that tree gouging produces large jaw forces relative to other activities involving the oral apparatus (Szalay and Seligsohn, 1977; Szalay and Delson, 1979; Dumont, 1997; Williams and Wall, 1999; Spencer, 1999; Vinyard, 1999). We apply in vivo observations of skull loadings and jaw muscle-activity patterns during anterior tooth use (Hylander, 1979a, 1984; Hylander and Johnson, 1985), comparative studies of primate skulls (Hylander, 1979b, 1988; Ravosa, 1991, 1996a; Daegling, 1992; Cole, 1992; Ravosa and Hylander, 1994), and theoretical biomechanical expectations (e.g., Gysi, 1921; Maynard Smith and Savage, 1959; Turnbull, 1970; Hylander, 1975; Smith, 1978) to infer four predicted morphologies (predictions 1– 4) that would provide increased resistance to the internal loads created by these large gouging forces. Predictions 5–7 are taken from the findings made by Dumont (1997). Prediction 5 suggests a morphological response that would offer increased load resistance. Prediction 6 relates to increasing mechanical advantage for gouging, while prediction 7 pertains to producing larger jaw-muscle forces. Prediction 8 also focuses on increasing mechanical advantage for gouging. All eight predictions state the expected morphology if gouging routinely involves relatively large external forces acting on the skull. All predictions are stated relative to the nongouging condition for the respective family or subfamily. Prediction 1: tree gougers have deeper mandibular corpora. In vivo data in macaques indicate that both mandibular corpora are bent in a parasagittal plane during incision and biting along the anterior teeth (Hylander, 1979a,b, 1988). Increasing the vertical depth of the corpus is a more effective way of providing greater resistance to parasagittal bending moments than increasing the thickness of the corpus (Hylander, 1979a,b, 1988; Ravosa, 1991, 1996a; Daegling, 1992; Ravosa and Hylander, 1994). Prediction 2: tree gougers have thicker (or wider) mandibular corpora. Both mandibular corpora are also twisted about their long axes during incision and anterior tooth biting in macaques (Hylander, 1979a,b, 1988). Generally, the most effective solution for resisting this torsion is to increase the mediolateral (ML) width of the corpus, rather than increasing the vertical depth of the corpus (Hylander, 1979a,b, 1988; Ravosa, 1991, 1996a; Daegling, 1992; Ravosa and Hylander, 1994). 155 Prediction 3: tree gougers have vertically elongated symphyses. In vivo data in macaques show that the symphysis is primarily bent in a frontal plane during incision and anterior tooth biting due to the twisting of the mandibular corpora about their long axes (Hylander, 1984, 1985, 1988). This vertical bending results in compression along the alveolar region and tension along the basal portion of the symphysis. Setting aside the possibility of fusing the symphysis, increasing the vertical or dorsoventral (DV) length of the symphysis is one of two effective solutions for resisting this bending (Hylander, 1984, 1985, 1988; Daegling, 1992; Ravosa and Hylander, 1994; Ravosa and Simons, 1994). The other solution is to create a simian shelf (Hylander 1984, 1985). Prediction 4: tree gougers have larger condyle articular surface areas. Macaque mandibular condyles are loaded in compression during incision and biting at the anterior teeth (Hylander, 1979c; Hylander and Bays, 1979). Presumably, increasing condylar articular area offers a larger surface for resisting the potentially higher condylar reaction forces during gouging (Hylander, 1979b; Smith et al., 1983; Herring, 1985; Bouvier, 1986a,b; Wall, 1999). Prediction 5: tree gougers have wider crania in the temporal fossa region. Dumont (1997) found that tree-gouging primates have relatively wider crania between the temporal fossae. Increasing the relative width of the cranium in this region is argued to buttress the junction between the neurocranium and viscerocranium, and hence provide greater resistance to loads during tree gouging (Dumont, 1997). Prediction 6: tree gougers have shorter mandibles. Dumont (1997) found that tree gougers have relatively short mandibles. She argued that all other factors being equal, relatively shorter mandibles increase the mechanical advantage of the jaw muscles during gouging at the anterior dentition. Prediction 7: tree gougers have condyles elevated higher above the mandibular occlusal plane. Dumont (1997) found that tree gougers have relatively higher condyles above the occlusal plane. She rightly argued that these higher condyles facilitate a relative increase in size of the masseter and medial pterygoid muscles, and relatively larger muscles provide greater jaw-adductor force for tree gouging (Dumont, 1997). Prediction 8: tree gougers have longer masseter moment arms. All other factors being equal, increasing the length of the masseter moment arm increases the mechanical advantage of the masseter during gouging at the anterior teeth. 156 C.J. VINYARD ET AL. TABLE 1. Primate sample used in comparing skull morphologies Predictions related to large jaw gapes during gouging Preliminary observations in a laboratory setting suggest that Callithrix jacchus uses relatively larger maximum gapes, i.e., more widely opened jaws, during gouging vs. maximum gapes during insect chewing (Williams et al., 2000; Vinyard et al., 2001, and unpublished data). These larger gapes may be beneficial both for aligning the incisal cutting edge for penetrating the tree substrate and increasing the potential jaw-closing trajectory for removing isolated tree pieces. We hypothesize that tree-gouging primates routinely use larger maximum gapes during gouging than during other biting, chewing, and display activities. Below, predictions 9 –13 state what morphology would be associated with large maximum gapes. All predictions are relative to the nongouging condition in the family or subfamily. Prediction 9: tree gougers have longer mandibles. Gapes are created primarily by rotating the mandible about the rest of the skull. Gape typically is measured as the distance between the maxillary and mandibular central incisors at any point during this rotation. For a given degree of mandibular rotation, longer mandibles produce larger gapes. The prediction that gougers have longer mandibles is the opposite of prediction 6 taken from Dumont (1997). Prediction 10: tree gougers have lower condyles relative to the mandibular occlusal plane. The extent that a jaw muscle can be stretched is an important factor affecting the maximum gape of an animal. Herring and Herring (1974) provided a geometric model showing that increasing the included angle from a jaw muscle’s origin and insertion to the temporomandibular joint (TMJ) reduces the stretching in this muscle for a given gape. Lowering condyle height relative to the mandibular occlusal plane effectively increases this angle for the masseter and medial pterygoid. Thus, relatively lower condyles reduce stretching, and facilitate larger gapes during gouging. The prediction of lower condyle height is the opposite of prediction 7 taken from Dumont (1997). Prediction 11: tree gougers have higher masseter origin-insertion ratios. The model by Herring and Herring (1974) also shows that altering the ratio of a jaw muscle’s origin to insertion length, both measured to the TMJ, changes the amount this muscle is stretched for a given gape. A muscle is stretched less, making larger gapes possible, as this origin-insertion ratio departs in either direction from a value of 1.0 (Herring and Herring, 1974; Herring, 1975). All primates in this study have a masseter origin-insertion ratio greater than 1.0. Therefore, we predict that gougers have higher origin-insertion ratios to facilitate larger gapes. Primate species1 Cheirogaleidae Phaner furcifer Cheirogaleus major Cheirogaleus medium Microcebus murinus Microcebus rufus Mirza coquereli Galagidae Euoticus elegantulus Galago gallarum Galago moholi Galago senegalensis Galagoides alleni Galagoides demidoff Galagoides zanzibaricus Callitrichinae Callithrix jacchus Leontopithecus rosalia Saguinus fuscicollis Sample size (n) Diet2 Body mass (g)3 12 13 13 11 12 9 Go/F F/I F/I I/F/G F/I F/I/G 460 400 283 61 48 315 25 9 14 33 12 21 10 Go/F/I F/I 1/F/G I/F F/I I/F/G I/F 274 200 180 213 273 62 143 26 10 26 Go/I F/I/G I/G 321 609 351 1 Extant taxonomy from Fleagle (1999). Dietary data are from Bearder and Martin (1980), Nash (1986), Harcourt (1990), Mittermeier et al. (1994), Kinzey (1997), Fleagle (1999), and references therein. F, frugivory; G, gummivory; Go, tree-gouging gummivory; I, insectivory; L, folivory. 3 Body mass estimates are in grams (g). Body mass data are the average of male and female body mass estimates from Smith and Jungers (1997) and Fleagle (1999). 2 Prediction 12: tree gougers have anteroposteriorly elongated mandibular condyles. The primate mandible rotates on the articular surface of the condyle about an approximate ML axis during jaw opening and closing (Hiiemae and Kay, 1973; Kay and Hiiemae, 1974a,b; Hylander et al., 1987; Wall, 1999). Increasing the relative AP length of the condyle (an estimate of the condyle’s radius of curvature) increases the range of rotational excursion of the mandible and hence facilitates larger gapes (cf. Currey, 1984; Ruff, 1988; Hamrick, 1996). Prediction 13: tree gougers have anteroposteriorly elongated temporal articular surfaces. The primate condyle translates anteriorly on the articular surface of the temporal bone (i.e., the glenoid fossa, articular eminence, and preglenoid plane) during jaw opening. The extents of condylar rotation and translation are correlated with the magnitude of a gape during jaw opening (Hiiemae and Kay, 1973; Kay and Hiiemae, 1974a,b; Hylander et al., 1987; Wall, 1999). It is predicted that increasing the AP length of the articular surface of the temporal bone facilitates greater condylar translation and hence allows larger gapes. MATERIALS AND METHODS Sample We measured a sample of 256 skulls from 3 gouging and 13 nongouging primates species (Table 1). We compared each of the three species thought to gouge trees with the nongouging species from the 157 SKULL MORPHOMETRICS IN TREE-GOUGING PRIMATES TABLE 2. Measurements and variables used to compare skull morphologies in gouging vs. nongouging primates1 Definition2 Skull measurements and variables Corpus depth (CorpDep) Corpus width (CorpWid) Symphysis length (SymLng) Condyle length (CondL) Condyle width (CondW) Bizygomatic breadth (ZYB) Temporal fossa width (TempWid) Mandible length (MandL) Condyle height (ConMandHt) AP mandible length (APMandL) Masseter origin length (MassOr) Masseter insertion length (MassIn)3 Temporal articular surface length (TempL) Cranial length (CranLng) Facial length (NPH) Posterior tooth row length (PTLen) Symphysis width (SymWid) Maxillary arch width (BiPalBrd) Biglenoid breadth (BiGlenBrd) M1 width (UmolWid) Condyle area (CondArea) Minimum cranial width (MCW) Masseter origin-insertion Ratio Skull geometric mean (GM) Superoinferior (SI) distance of mandibular corpus at M1 Mediolateral (ML) distance of mandibular corpus at M1 Distance from incisor alveolus to inferior aspect of symphysis Anteroposterior (AP) length of condylar articular surface ML width of condylar articular surface Transverse distance across zygomatic arches Maximum ML width of temporal fossa Infradentale to posterior extent of condyle Perpendicular distance from top of condyle to mandibular occlusal plane Distance from infradentale to posterior margin of ramus, parallel to occlusal plane Distance from masseter tubercle to postglenoid process Distance from condyle to anteroinferior extent of masseter attachment on mandible AP length of temporomandibular joint articular surface on temporal bone Distance from prosthion to episthocranion Distance from nasion to prosthion Mesiodistal length of maxillary premolars and molars Labiolingual length of symphysis perpendicular to SymLng Distance between buccal grooves of left and right M1 Transverse distance between lateral extent of glenoid fossae Maximum buccolingual width of upper first molar 1/2(CondL) * 1/2(CondW) * ZYB ⫺ (2 * TempWid) Massor/MassIn (MandL * CorpDep * CorpBrd * SymWid * SymLng * UmolWid * NPH * CranLng * BiPalBrd * BiGlenBrd * PTLen)1/11 Prediction number 1 2 3 4, 12 4 5 5 6 7, 10 9 11 8, 11 13 4 5 11 1 Each measurement and variable is briefly defined and referenced for its relevant prediction(s). See Vinyard (1999) for further information. Linear dimensions are in mm and area dimensions are in mm2. 3 We used this measurement as an estimate of masseter moment arm length for testing prediction 8 (Jablonski 1993). 2 same subfamily or family (Table 1). Whenever possible, we included near-equal numbers of males and females for each species. We combined males and females from each species for analysis, because we have no reason to believe there are sex-specific differences in gouging behavior. Skull measurements and biomechanical shape variables We took 20 measurements on each skull (Table 2). We measured these dimensions to the nearest 0.01 mm, using either digital calipers (Fowler UltraCal III) on actual skulls or video images of skulls imported into SigmaScan Pro 4.0 software (SPSS, Inc.). Collection of video images followed the procedures outlined by Spencer and Spencer (1995). We assessed the predicted morphological differences between tree-gouging and nongouging species using biomechanical shape variables. Shape variables provide a scale-free way of examining variation across a size range by considering differences in form as a ratio of the dimension of interest to a second-criterion variable (Mosimann, 1970; Darroch and Mosimann, 1985; Falsetti et al., 1993; Jungers et al., 1995). We calculated shape variables as the ratio of the variable of interest to mandible length (MandL) for most comparisons.3 We used mandible length as a biomechanical standard because we are interested in the functional consequences of skull form for gouging. Mandible length is both an estimate of the load arm during biting at the anterior teeth (e.g., Hylander, 1979a,b, 1985, 1988; Bouvier, 1986a; Daegling, 1989) and an important component of linear gape at the incisors (e.g., Lucas, 1981, 1982; Smith, 1984).4 By using mandible length as a biomechanical standard, we were able to compare gouger and nongouger skulls while holding constant relevant mechanical factors thought to be significant in influencing skull loading and jaw gape. However, by using this biomechanical standard, we are not 3 The square root of condyle area (CondArea) was used in calculating the shape variable for this dimension. A shape variable was not created for the masseter origin-insertion ratio because it is already dimensionless. 4 Other biomechanical standards have been used to study the mechanical abilities of the mandibular corpus for resisting chewing and incisal loads. For example, Hylander (1979b, 1988) analyzed the ability of the mandibular corpus at the molar region to counter parasagittal bending by scaling corpus depth relative to the moment arm acting along this portion of the corpus. We repeated our analyses using an estimate of this moment arm length. As both results gave the same interpretation, we only report those using mandible length as a biomechanical standard. 158 C.J. VINYARD ET AL. conducting an allometric analysis relative to a general skull size estimate. We may not be “controlling for size,” as is often attempted with allometric size corrections, nor are we necessarily able to examine size-correlated changes in shape (e.g., Smith, 1993; Jungers et al., 1995). We used a geometric mean of 11 skull measurements (GM) as a skull size estimate when comparing mandible length and AP mandible length in predictions 6 and 9, respectively (Table 2).5 Statistical analyses We conducted all possible pairwise comparisons per variable between a gouging vs. nongouging species for a family or subfamily. Given the variation in diet and body mass among the species in each group (Table 1), we argue that the multiple pairwise comparisons offer a more thorough assessment of the predicted morphologies in gouging primates by varying these other factors that also potentially affect skull form. Performing multiple comparisons per gouging species also lessens statistical problems encountered when only comparing two species (Garland and Adolph, 1994). We used one-tailed, Mann-Whitney U-tests to assess the predicted differences in skull shapes between individuals of gouging vs. nongouging species. The P-value for determining statistical significance was calculated using the large sample equations in Siegal and Castellan (1988). When a biomechanical shape variable for a gouging species was significantly different in the predicted direction for all pairwise comparisons with nongouging species in its family or subfamily, then correlational support was offered, suggesting that a particular skull shape is functionally linked to gouging in that species. If the one-tailed Mann-Whitney U-test did not show the predicted significant difference for a variable in a pairwise comparison, then we performed a twotailed Mann-Whitney U-test to look for an overall difference in that variable between the two species (Zar, 1999). A significant difference in the two-tailed test indicates that the variable is significantly different between the two species in the direction opposite from the prediction. We assessed 13 morphological predictions for each pairwise species comparison. Because of the multiple statistical comparisons for each pair of species, the sequential Bonferroni technique was applied to set a pairwise significance level of ␣ ⫽ 0.05 for all statistical comparisons involving a gouging and nongouging species (Rice, 1989). 5 Across a sample of 97 primate species means, mandible length is highly correlated (0.996) with the geometric mean used here. Mandible length scales nearly isometrically with this geometric mean (LS slope ⫽ 0.98 ⫾ 0.02). RESULTS Morphological predictions related to large gouging forces in the skull Tree gouging species infrequently exhibit the morphologies predicted to be linked to large jaw forces during gouging (Table 3). With only one exception (see below), no predicted morphology is always observed in a gouging species relative to all other nongouging species in the same family or subfamily (Table 3). Further, there are few pairwise species comparisons where gouging species showed a significant shape difference in the predicted direction. Phaner furcifer does not show the skull shapes predicted to be linked to relatively large jaw forces in most pairwise comparisons with nongouging cheirogaleids (Table 3a). Although P. furcifer possesses more robust mandibular corpora, symphyses, and condyles relative to Microcebus rufus, and to a lesser extent to M. murinus and Mirza coquereli (Table 3a), this is not the case for comparisons with Cheirogaleus major or C. medius. Euoticus elegantulus exhibits the largest number of predicted shape differences relative to nongouging galagids (Table 3b). E. elegantulus often has significantly deeper and thicker mandibular corpora, longer symphyses, and larger condyles for a given size in comparison to nongouging galagids (Table 3b). However, no predicted shape variable is significantly larger in E. elegantulus in all pairwise comparisons with nongouging galagids. Contrary to prediction 5, minimum cranial width shape is either not different or is actually significantly narrower in E. elegantulus relative to other galagids (Table 3b). Mandible length also is not significantly different in E. elegantulus vs. these other galagids (Table 3b). E. elegantulus has a significantly longer relative masseter moment arm length than G. alleni or G. demidoff, but is not statistically different from the remaining galagids. While E. elegantulus appears to have a relatively robust jaw compared to most galagids, these results do not meet our strict criteria for linking skull form and gouging forces. Most skull shapes in Callithrix jacchus are either similar to nongouging callitrichids or differed significantly from them in the direction opposite from the prediction (Table 3c). Only minimum cranial width shape is significantly wider in C. jacchus vs. all other callitrichids (Table 3c). This predicted shape difference is the only one in this study that meets our criteria for linking skull form and gouging forces. Morphological predictions related to large jaw gapes during gouging Tree gouging primates exhibit several of the shape differences predicted to facilitate larger gapes in comparisons with nongouging species from the same family or subfamily (Table 3). For example, each of the three gouging species always has significantly 159 SKULL MORPHOMETRICS IN TREE-GOUGING PRIMATES TABLE 3. Results of pairwise species comparisons of skull shapes for (a) Phaner furcifer vs. other cheirogaleids, (b) Euoticus elegantulus vs. other galagids, and (c) Callithrix jacchus vs. other callitrichids a. P. furcifer vs. cheirogaleids Shape variable1 Cheirogaleus major2 Cheirogaleus medius Microcebus murinus Microcebus rufus Mirza coquereli 1. M1 depth (Pf ⬎) 2. M1 width (Pf ⬎) 3. Symphysis length (Pf ⬎) 4. Condyle area (Pf ⬎) 5. Minimum cranial width (Pf ⬎) 6. Mandible length (Pf⬍) 7. Condyle height (Pf ⬎) 8. Masseter moment arm (Pf ⬎) 9. AP mandible length (Pf ⬎) 10. Condyle height (Pf⬍) 11. Masseter origin-insertion ratio (Pf ⬎) 12. Condyle length (Pf ⬎) 13. Temporal articular surface length (Pf ⬎) Ns/0.009 Ns/Ns 0.01/Ns Ns/Ns 0.01/Ns Ns/Ns Ns/⫺ Ns/Ns Ns/Ns 0.0006/⫺ 0.004/⫺ 0.002/⫺ 0.007/Ns Ns/0.001 Ns/Ns 0.02/Ns 0.01/Ns Ns/Ns Ns/Ns Ns/⫺ 0.002/⫺ Ns/Ns 0.003/⫺ Ns/0.0006 0.001/⫺ Ns/Ns Ns/Ns Ns/Ns 0.006/Ns 0.002/⫺ Ns/Ns Ns/Ns Ns/⫺ Ns/Ns Ns/Ns 0.0001/⫺ Ns/Ns 0.0004/⫺ 0.001/⫺ 0.005/⫺ 0.005/⫺ 0.0001/⫺ 0.0007/⫺ Ns/Ns 0.04/Ns Ns/⫺ 0.005/⫺ Ns/Ns 0.00008/⫺ Ns/Ns 0.00004/⫺ 0.007/⫺ Ns/Ns Ns/Ns 0.009/Ns 0.0007/⫺ Ns/Ns Ns/Ns Ns/⫺ Ns/Ns Ns/Ns 0.0005/⫺ Ns/Ns 0.0002/⫺ 0.002/⫺ b. E. elegantulus vs. galagids Shape variable Galagoides alleni Galago moholi Galago senegalensis Galagoides zanzibaricus Galagoides demidoff Galagoides gallarum 1. M1 depth (Ee⬎) 2. M1 width (Ee⬎) 3. Symphysis length (Ee⬎) 4. Condyle area (Ee⬎) 5. Minimum cranial width (Ee⬎) 6. Mandible length (Ee⬍) 7. Condyle height (Ee⬎) 8. Masseter moment arm (Ee⬎) 9. AP mandible length (Ee⬎) 10. Condyle height (Ee⬍) 11. Masseter origin-insertion ratio (Ee⬎) 12. Condyle length (Ee⬎) 13. Temporal articular surface length (Ee⬎) 0.00005/⫺ 0.02/Ns 0.000009/⫺ 0.0001/⫺ 0.02/Ns Ns/Ns Ns/⫺ 0.005/⫺ Ns/0.01 0.000003/⫺ 0.0007/⫺ 0.004/⫺ 0.00001/⫺ 0.001/⫺ 0.001/⫺ 0.00002/⫺ 0.0005/⫺ Ns/0.00005 Ns/0.02 Ns/⫺ Ns/Ns 0.02/Ns 0.000001/⫺ Ns/Ns 0.002/⫺ 0.00004/⫺ 0.00003/⫺ 0.02/Ns 0.000001/⫺ 0.02/Ns Ns/0.00008 Ns/0.01 Ns/⫺ Ns/Ns 0.03/Ns 0.000001/⫺ Ns/Ns Ns/Ns 0.00001/⫺ 0.000006/⫺ 0.01/Ns 0.00001/⫺ 0.00009/⫺ Ns/Ns Ns/Ns Ns/⫺ 0.03/Ns Ns/0.02 0.000003/⫺ Ns/Ns 0.00005/⫺ 0.00003/⫺ 0.000002/⫺ 0.00004/⫺ 0.008/Ns Ns/Ns Ns/0.003 Ns/Ns Ns/⫺ 0.001/⫺ Ns/Ns 0.000001/⫺ Ns/Ns 0.05/Ns 0.000001/⫺ 0.05/Ns Ns/Ns 0.006/Ns Ns/Ns Ns/0.02 Ns/0.006 Ns/⫺ Ns/Ns 0.01/Ns 0.0006/⫺ 0.02/Ns Ns/Ns 0.00002/⫺ c. C. jacchus vs. callitrichids Shape variable 1. M1 depth (Cj⬎) 2. M1 width (Cj⬎) 3. Symphysis length (Cj⬎) 4. Condyle area (Cj⬎) 5. Minimum cranial width (Cj⬎) 6. Mandible length (Cj⬍) 7. Condyle height (Cj⬎) 8. Masseter moment arm (Cj⬎) 9. AP mandible length (Cj⬎) 10. Condyle height (Cj⬍) 11. Masseter origin-insertion ratio (Cj⬎) 12. Condyle length (Cj⬎) 13. Temporal articular surface length (Cj⬎) Leontopithecus rosalia Saguinus fuscicollis Ns/0.02 Ns/0.0001 Ns/Ns Ns/Ns 0.0001/⫺ Ns/0.006 Ns/⫺ Ns/0.04 0.004/⫺ 0.000002/⫺ 0.00001/⫺ 0.01/Ns 0.000002/⫺ Ns/Ns Ns/0.003 Ns/0.008 Ns/Ns 0.0001/⫺ 0.04/Ns Ns/⫺ Ns/Ns 0.02/Ns 0.000008/⫺ 0.0005/⫺ 0.00003/⫺ 0.000001/⫺ 1 We list shape variables predicted to differ in gouging vs. nongouging species at left. We indicate directionality of predicted difference by specifying whether gouging species should have a relatively larger (e.g., Pf⬎) or relatively smaller (e.g., Pf⬍) shape. 2 We use Mann-Whitney U-tests for all pairwise shape comparisons, and report P-values from these comparisons as described below. First entry is the P-value from a one-tailed Mann-Whitney U-test of predicted difference in shape between gouging vs. nongouging species in that pairwise comparison. Second entry gives the result of a two-tailed Mann-Whitney Whitney U-test for a difference in shape between the two species. Two-tailed tests were only performed when the one-tailed test resulted in no statistical difference in shape between two species. A significant result in two-tailed test indicates a difference in shape between two species that is opposite to the predicted pattern. Bold P-values signify a significant difference in shape (␣ ⫽ 0.05) after accounting for multiple shape comparisons between those two species, using an adjusted Bonferroni method. P-values that are not bold indicate a P-value less than 0.05, but not significant after accounting for multiple shape comparisons between those two species. Ns indicates a P-value larger than 0.05 and represents no statistical difference in shape between those two taxa. lower condyle height shapes relative to nongouging species (Fig. 1). P. furcifer possesses significantly lower condyle heights and anteroposterior (AP) elongated condyles for a given size relative to all nongouging cheirogaleids in this study (Table 3a). Relative AP temporal articular length in P. furcifer is significantly longer than similar relative lengths in Microcebus species, but not significantly different from those in species of Cheirogaleus (Table 3a). E. elegantulus exhibits significantly lower condyle height shapes and relatively longer AP temporal articular lengths in all of the comparisons with nongouging galagids (Table 3b). In many compari- 160 C.J. VINYARD ET AL. similar between E. elegantulus and nongouging galagids (Table 3b). C. jacchus exhibits the most shape differences predicted to facilitate large gapes (Table 3c). Shape variables for condyle height, AP temporal articular surface length, and masseter origin-insertion ratio show the predicted morphological differences in all comparisons of C. jacchus to nongouging callitrichids (Table 3c). For relative AP mandible and condyle length, C. jacchus shows the predicted difference in one comparison, but only approaches significance in a second comparison to a nongouging callitrichid (Table 3c). Because C. jacchus has a significantly longer relative mandible length than Leontopithecus rosalia (Table 3c), using mandible length as the denominator in our biomechanical shape variables may generate different results than shape variables created using an overall size estimate such as a GM. Among the 13 shape variables, this influence of mandible length appears to be an issue for hypothesis-testing in the comparison of AP condyle length shape. In fact, C. jacchus has a significantly longer relative AP condyle length than L. rosalia when using our GM as a size estimate. DISCUSSION Skull morphology and gouging forces Fig. 1. Box plots of condyle height shape, relative to mandible length, for (A) Phaner furcifer and other nongouging cheirogaleids, (B) Euoticus elegantulus and nongouging galagids, and (C) Callithrix jacchus vs. nongouging callitrichids. For each family or subfamily, the gouging species has a significantly lower condyle height shape when compared to each of the nongouging taxa in that group. Line within box denotes median. Boundaries of box represent 25th and 75th percentiles. Whiskers indicate 10th and 90th percentiles. Solid circles denote 5th and 95th percentiles. Complete species designations are given in Table 1. sons, E.elegantulus has significantly longer relative AP condyle lengths. Both relative AP mandible length and the masseter origin-insertion ratio are Many researchers have suggested that gouging primates generate relatively large external forces on the jaw and large internal loads in the skull during gouging (Szalay and Seligsohn, 1977; Szalay and Delson, 1979; Rosenberger, 1992; Dumont, 1997; Williams and Wall, 1999; Spencer, 1999; Vinyard, 1999). Furthermore, skull shapes in gouging primates have been linked functionally to these hypothesized forces and loads (e.g., Dumont, 1997). Our results suggest that gouging primates exhibit few of the predicted skull morphologies that should be linked to large gouging forces and loads. These findings certainly do not exclude there being large forces at the jaw during gouging in these species. Indeed, we did not consider other relevant factors such as the distribution of compact bone in the mandibular corpus and symphysis, jaw muscle sizes, or internal muscle architecture. Finally, it is also possible that larger samples, and hence greater statistical power, might allow us to identify smaller, yet still statistically significant, differences in skull form linked to gouging forces. Among the three gouging species we examined, Euoticus elegantulus shows the largest number of mandibular shapes predicted to offer increased resistance to internal loads in the jaw during gouging (i.e., predictions 1– 4; Table 3b). However, there is no immediately apparent pattern to these predicted mandibular shapes either within or among galagid species. For example, each of these four mandibular shapes is significantly larger in E. elegantulus vs. SKULL MORPHOMETRICS IN TREE-GOUGING PRIMATES 161 Galago moholi, but none differ from analogous shapes in Galagoides gallarum. This inconsistency makes it hard to interpret the functional significance of mandibular shapes in E. elegantulus. This difficulty is compounded by some uncertainty concerning how E. elegantulus extracts gums and the frequency of gouging during gum feeding (e.g., Charles-Dominique and Petter, 1980). We also cannot rule out that other feeding behaviors, unrelated to exudate feeding, are responsible for the robust jaws of E. elegantulus relative to some galagids. Our comparative results are sufficiently interesting to merit further behavioral and morphological research to clarify the relationship between jaw form, gouging, and feeding ecology in E. elegantulus. Comparing functional interpretations of skull form in gouging primates Dumont (1997) conducted the first comparative study of skull shapes in tree-gouging primates. She examined E. elegantulus, C. jacchus, and Cebuella pygmaea in the context of a wider range of gouging and nongouging mammals than examined here. Dumont (1997) described these gouging species as having higher condyles above the occlusal plane, shorter mandibles, and wider crania in the temporal fossa and nuchal regions relative to a skull GM as compared to frugivorous and nectivorous bats, marsupials, and primates. Gougers are also reported to have shorter relative AP condyle lengths when compared to these frugivores (Dumont, 1997). Based on the assumption that gouging involves high forces, these shape differences were interpreted by Dumont (1997) to provide greater force production or offer increased resistance in the skull to the elevated internal loads linked to gouging. Our analysis of skull shape in gouging primates gives several results that contradict the morphological findings reported by Dumont (1997). One difference is that the three gouging species we consider, including two studied by Dumont (1997), have low condyle heights relative to mandible length in all comparisons with nongouging species (Fig. 2). Contrary to Dumont (1997), we find mandible lengths relative to a skull GM to be statistically similar in gougers as compared to closely related nongougers, with the exception of one case where the gouging species has a significantly longer mandible (Table 3c). We found that Callithrix jacchus has relatively wider crania in the temporal fossa region (MCW) vs. other callitrichids, as suggested by Dumont (1997). The two strepsirrhine gougers, however, have similar or significantly narrower relative minimum cranial widths when compared to nongougers of the same family. Finally, the AP length of the condyle relative to mandible length is either not different or is significantly longer in gouging species. We identify three potential, nonmutually exclusive, explanations for these two contrasting reports of skull shapes in gouging primates. First, the two Fig. 2. Lateral views of mandibles for (A) Phaner furcifer and Cheirogaleus major, (B) Euoticus elegantulus and Galagoides demidoff, and (C) Callithrix jacchus and Saguinus fuscicollis. In A–C, the gouging species shows a condyle that is positioned lower, closer to the toothrow, in comparison with the nongouging species. Scale bar, 1 cm. Adapted from Hershkovitz (1977). studies do not examine precisely the same gouging primates. We do not include C. pygmaea, while Dumont (1997) did not analyze P. furcifer. Both studies did, however, include E. elegantulus and C. jacchus. Nevertheless, all three gouging taxa in our study show a basically similar pattern of comparative results for these skull shapes. Second, the two studies use different comparative samples. Given that the conclusions regarding skull shape in gouging primates are relative to the comparative sample, the different samples are likely to be a major factor underlying the dissimilar morphologies reported by the two studies. We examine skull shapes in gouging primates relative to closely related, nongouging taxa in the same family or subfamily. Dumont (1997) compared skull shapes in tree gougers to other species of primates, bats, and marsupials. We argue that the broad taxonomic sampling used by Dumont (1997) makes it difficult to identify morphological features functionally related to tree gouging vs. morphological variability related to the separate phylogenetic history of these different taxa (Fleagle, 1977a,b, 1978; Szalay and 162 C.J. VINYARD ET AL. Delson, 1979; Felsenstein, 1985; Huey and Bennett, 1986, 1990; Bennett and Huey, 1990; Garland and Adolph, 1994; Harvey and Pagel, 1991; Miles and Dunham, 1993). If the goal is to identify morphological changes in the skull related to gouging in a specific tree-gouging species, then it is preferable to compare the gouging species to closely related nongouging taxa. In effect, we are arguing that a comparative morphometric study aimed at identifying form-function relationships in a particular species performing a derived behavior is best accomplished by comparing this species to closely related species that span the presumed behavioral shift (see Coddington, 1988). This approach maximizes the form-function “signal” to unrelated phylogenetic “noise” ratio. Furthermore, this method mimics the empirically powerful approach applied in studying the effects of artificial selection where the populations before and after selection are compared to quantify selection. We make three sets of these comparisons. By comparing multiple gouging species to their closely related nongouging relatives, we are able to assess morphological convergence, or the lack thereof, in tree-gouging primates. The convergent reduction of relative condyle height in all three gouging species bolsters our functional hypothesis linking this morphological change with large jaw gapes associated with tree gouging. Lack of convergence, however, should not be interpreted as evidence that a predicted morphological change observed in one gouging species, such as the increased masseter origin-insertion ratio in C. jacchus, is unimportant for that species simply because it is not observed in other gougers. Our use of this comparative approach gives rise to at least two concerns that need to be addressed. First, we are arguably violating the spirit of our method outlined in the previous paragraph by comparing each species of interest to multiple comparative taxa within a family or subfamily, when in fact comparison to the sister taxon is really most appropriate. Unfortunately, we cannot at present definitively identify the appropriate sister taxon for most of the gouging species. For example, P. furcifer is identified as the sister taxon to all other cheirogaleids by Yoder (1997). More importantly, we do not know whether the extant sister taxa exhibit the morphology found in the nongouging ancestor of our species of interest. Therefore, we maintain that our criteria requiring a predictable change in multiple comparisons with closely related species offer a rigorous, albeit conservative, test of form-function relationship. A second concern relates to the fact that each gouging species is compared to a different number of nongouging taxa. These varying numbers of comparisons raise the question of whether there are differences in the power of the tests among the three gouging species. We can neither confirm nor reject this issue, based on the observed results. We want to be extremely careful to point out that we are not rejecting all broad, interspecific approaches to studying form and function with morphometric data. The utility and importance of interspecific allometric studies, for example, have been demonstrated numerous times. We simply argue that questions about form-function relationships in a particular species, or a clade, exhibiting a specific behavior may be better addressed when using morphometric data by comparing that group to a closely related one that does not perform that particular behavior. Third, the two studies use different denominators in calculating shape variables. Dumont (1997) used a geometric mean of several skull measurements to estimate skull size. We used mandible length as a biomechanical standard in most cases. Given that a shape is calculated relative to some other measure, different relative criteria will result in divergent shape estimates for the same morphology (Mosimann and James, 1979). This difference in calculating shape variables likely contributes to the contrasting results of the two studies (see Appendix). We agree with Dumont (1997) that fossil gougers can be identified using skull shapes derived from a generalized skull size estimate such as a geometric mean of skull dimensions. We are not attempting this kind of allometric analysis of skull form in gouging primates, and therefore we are not trying to describe size-related changes in skull shapes among gouging and nongouging primates. However, we contend that it may be problematic to develop functional interpretations of skull shapes derived from these general skull size estimates, because they do not directly consider relevant mechanical factors affecting skull functions during gouging. We argue that the biomechanical significance of mandible length for force- and gape-related jaw functions makes it a more appropriate estimate for addressing skull form-function relationships in gouging primates. From a functional perspective, it is the relationship between the two mechanically relevant components of the shape variable that is important for understanding skull function during gouging, and it is less relevant to identify which component(s) of the shape variable is changing with size. By contrasting our approach with that of Dumont (1997), we are revisiting an old argument debating the appropriateness of size adjustment with overall size estimates vs. relevant biomechanical standards in studying jaw biomechanics (cf. Smith, 1983, 1993 to Hylander, 1985, 1988; Bouvier, 1986a; Daegling, 1989; Ravosa, 1991, 1996b). In general, if a biomechanical relationship can be identified, then we suggest shapes should also be examined relative to a biomechanical standard before making functional interpretations. Our morphological findings challenge two of the conclusions made by Dumont (1997) based on her analysis of skull shapes. First, her argument that SKULL MORPHOMETRICS IN TREE-GOUGING PRIMATES gouging primates have increased force production abilities through both improved leverage for gouging and larger jaw-muscle attachment areas, as well as increased load resistance in their skulls, must be viewed with caution. In vivo data on jaw forces during gouging are needed before we can reliably interpret skull form-function associations in gouging primates. Second, the classification functions Dumont (1997) recommended for identifying tree gouging in fossil primates may not be as useful as previously stated. This is because the combined results of these two analyses show that the interpretation of skull shapes in gouging primates is highly contingent on the comparative sample. Skull form and jaw gapes during gouging While several researchers have speculated about gouging forces in the skull, the potential importance of jaw movements during gouging, as estimated by jaw gapes, has been largely overlooked. We have observed common marmosets in a laboratory setting using larger gapes during gouging than during chewing (Vinyard et al., 2001, and unpublished data). We examined whether gouging primate species exhibit morphologies that facilitate large gapes based on these preliminary observations. When compared to closely related nongouging primates, each gouging species does possess skull shapes that likely increase jaw gapes. Thus, we hypothesize that these derived skull shapes in gouging primates are functionally related to the need for relatively large gapes during gouging. Many researchers have addressed the importance of gape in mammalian skull functional morphology (e.g., Wolff-Exalto, 1951; Moss, 1968; Herring, 1972, 1975; Greaves, 1974, 1995; Herring and Herring, 1974; Hylander, 1979b; Emerson and Radinsky, 1980; Lucas, 1981, 1982; Smith, 1984; Joeckel, 1990; Ravosa, 1990; Jablonski, 1993; Jablonski and Crompton, 1994). These efforts functionally link large gapes to display behaviors, prey capture, fighting, slashing, incising large-diameter foods, and crushing large-diameter foods at the posterior teeth. Our results imply that tree gouging in primates may be another behavior necessitating large gapes. All three gouging species consistently display relatively low condyle heights when compared to closely related nongouging species (Fig. 2). Condyle heights vary dramatically among primates. This variability appears to be correlated with differences in diet, feeding behavior, canine displays, and fighting (e.g., Zingeser, 1973; Hylander, 1979b; Ward and Molnar, 1980; Lucas, 1981, 1982; Ravosa, 1990; Jablonski, 1993; Ravosa et al., 2000). A cursory glance at the skulls of living primates suggests that relatively high condyles above the occlusal plane occur in folivorous species (e.g., Alouatta and Brachyteles in contrast to Ateles) and relatively low condyles are found in species that use wide gapes during canine displays (e.g., Papio and Mandrillus in comparison 163 to Theropithecus). Our findings suggest that treegouging primates may offer additional evidence relating low relative condyle heights and wide gapes in primates. Variation in condyle heights has functional relevance for activities involving the oral apparatus. Many researchers consider high condyles above the toothrow advantageous for powerful and repetitive mastication by increasing attachment areas and lengthening the moment arms for the masseters and medial pterygoids, as well as distributing occlusal forces more evenly across the postcanine teeth (Wolff-Exalto, 1951; Maynard Smith and Savage, 1959; Davis, 1964; Turnbull, 1970; Greaves, 1974; Ward and Molnar, 1980). Low condyles are thought to decrease stretching of the masseters and medial pterygoids during jaw opening, reduce posterior displacements of the mandible during opening, and increase the temporalis moment arm (assuming coronoid height remains constant) (Herring, 1972, 1975; Herring and Herring, 1974). We identify two potential functional benefits of a low condyle relative to the mandibular toothrow in the context of tree gouging at large gapes. First, low condyles may aid bite force production at the anterior teeth during gouging. The jaw muscles elongate as the mouth opens. Empirical data in primates indicate that bite-force production diminishes as jaw-muscle fibers stretch beyond their resting length during jaw opening (Dechow and Carlson, 1982, 1986, 1990). Bite force reduction due to muscular stretching is further compounded by the relatively inefficient jaw-lever relationships for producing forces at the anterior teeth. Therefore, gougers that need to generate bite forces at large gapes would be under pressure to minimize stretching of jaw-muscle fibers at these large gapes. A low condyle reduces jaw muscle stretching at a given gape and provides one structural solution to this problem (Herring and Herring, 1974). A second potential benefit of a low condyle with respect to the occlusal plane relates to reducing the posterior displacement of the mandible at large gapes. Relative to the upper teeth, the lower anterior teeth move inferiorly and posteriorly during jaw opening. Lowering the height of the condyle relative to the mandibular toothrow reduces the amount of posterior displacement of these teeth for a given degree of jaw rotation (Davis, 1964; Herring, 1972; Lucas, 1981, 1982). If the lower anterior teeth are displaced too far posteriorly at large gapes during gouging, then it may be difficult to position the cutting edge of these teeth at an appropriate angle relative to the gouging substrate. Thus, we speculate that a low condyle height may be important for the effective alignment of the anterior teeth during gouging at large gapes. The anteroposterior (AP) lengths of the condyle and temporal articular surfaces are significantly longer in specific gouging primates relative to closely related 164 C.J. VINYARD ET AL. nongougers at a given size. For example, relative condyle length in P. furcifer is significantly longer than all cheirogaleids sampled, whereas E. elegantulus and C. jacchus have significantly longer relative temporal articular surfaces than all other species in their respective family or subfamily. Cineradiographic studies indicate that during jaw opening in primates, the condyle rotates about an approximate mediolateral axis and translates anteriorly along the temporal articular surface (Hiiemae and Kay, 1973; Kay and Hiiemae, 1974a,b; Hylander, 1978; Hylander et al., 1987; Wall, 1999). Wall (1999) further demonstrated that condylar rotation and translation are correlated with gape during jaw opening. AP lengthening of the condyle increases potential gapes by increasing the range of possible rotational excursion in the mandible (cf. Currey, 1984; Ruff, 1988; Hamrick, 1996). A longer temporal articulation increases the translational surface for the condyle during jaw opening. Thus, relative lengthening of these TMJ articular surfaces will provide increased gape potentials in gouging primates. In addition, the relatively elongated condyles of gouging primates may reduce stresses (i.e., force/area) in the TMJ during gouging by increasing relative condyle area. We stress that these results provide only preliminary support linking skull form, relatively large gapes, and gouging. Our comparative study only examined jaw shape and craniometric correlates of masseter (and assumably medial pterygoid) stretching, condylar rotation, and translation as they relate to large gapes. We did not consider stretching of the temporalis (e.g., Herring and Herring, 1974; Emerson and Radinsky, 1980; Joeckel, 1990; Ravosa, 1990). Furthermore, we did not examine jaw-muscle fiber lengths, even though it is well-known that the tension produced by a muscle fiber decreases as that fiber is stretched beyond an optimum length (e.g., Ramsey and Street, 1940; Hill, 1953; Gans and Bock, 1965; Gordon et al., 1966; Herring and Herring, 1974; Anapol and Herring, 1989). We also did not look at other soft-tissue components that might limit jaw gapes. Finally, we have not provided a compelling explanation of the functional benefit(s) of relatively large gapes during tree gouging. Perhaps large gapes are advantageous for optimal alignment of the incisal cutting edges for penetrating the tree substrate. A large gape also signifies a greater amount of anterior tooth movement during closing for removing isolated tree pieces. Additionally, changes in skull form that reduce jaw muscle stretching for a given gape theoretically will increase jaw muscle force production at that gape. We intend to address the functional significance of large gapes for gouging through in vivo analyses of gouging mechanics in Callithrix jacchus. Inferring gouging functions from comparative studies of skull form We implicitly assumed at the outset of this study that gouging involves larger jaw forces and/or larger jaw gapes relative to other behaviors involving the oral apparatus. We did this to determine if there are predictable changes in skull morphology in gouging primates that may be functionally related to these purported large forces and/or gapes during gouging. This assumption was necessary because there currently are only preliminary in vivo data pointing to the magnitudes of jaw forces and jaw gapes during gouging (Vinyard et al., 2001). We would like to apply the comparative morphological results presented here to address those hypotheses stating that jaw forces and jaw gapes are relatively large during gouging. However, we cannot conclusively address force- and gape-related functions during gouging with our morphometric data because of the two additional assumptions we made in this analysis. First, we assumed that skull form responds to these hypothesized functional demands. This assumption is common in comparative morphological studies of the skull, and is bolstered by in vivo data during mastication, incision, and biting that suggest jaw form and function are linked (Hylander, 1979a,b, 1984, 1985, 1988; Daegling and Hylander, 1997; Hylander et al., 1998, 2000). However, it has been convincingly argued and empirically demonstrated that form and function are not always closely linked in organisms (Bock, 1977, 1989; Lauder, 1995, 1996). Because of the lack of a strict, law-like relationship between form and function, our comparative morphometric analysis cannot definitively address whether jaw forces and/or jaw gapes during gouging are relatively large. Second, we assumed that incision and anterior tooth biting provide reasonable functional models for inferring the external forces at the jaw and internal loads in the skull as well as jaw movements during gouging. For example, this assumption allowed us to apply in vivo data from primate incision and anterior tooth biting to infer morphological responses to the hypothesized large external forces during gouging (see predictions 1– 4). Similarly, we assumed that jaw-opening movements during gouging involved jaw rotations and translations that are comparable to those observed during jaw opening for incision. The demonstration of a steep strain gradient in the macaque zygomatic arch by Hylander and Johnson (1997) highlights why inferring functions in primate skulls can be problematic. They showed that during chewing, the anterior portion of the macaque zygomatic arch exhibits higher strains relative to the intermediate strains in the middle portion of the arch and even lower strains in the posterior region of the arch. If we accept that the anterior portion of the arch is near optimized for resisting masticatory stresses,6 then the more posterior sections of the 6 In other words, the anterior portion of the zygomatic arch exhibits near-maximum strength with a minimum amount of tissue. SKULL MORPHOMETRICS IN TREE-GOUGING PRIMATES arch could be significantly reduced in size without compromising their load-resisting ability during chewing (Hylander and Johnson, 1997). Similar strain gradients during mastication have been shown throughout other areas of the macaque skull (Hylander et al., 1991; Hylander and Johnson, 1992; Ross, 2001). These gradients, coupled with the observation that form cannot predict masticatory stresses across the macaque mandible (Daegling, 1993), indicate that we cannot routinely determine function in primate skulls simply from observing skull form. However, comparative morphological studies of primate skulls still may be able to assess variation in function correctly, so long as in vivo data for at least one primate species demonstrate that a form-function relationship exists. Given the scarcity of in vivo data on jaw forces and gapes during gouging, we cannot definitively link form to function in this comparative analysis. Having stated the limitations imposed by our assumptions, we consider this comparative morphological analysis to be a reasonable first step in addressing these two functional hypotheses. We argued at the outset of this study that if a gouging species exhibits the predicted morphology in all comparisons with the nongouging species in its family or subfamily, then correlational support suggests that a particular skull form is functionally linked to gouging in that species. We currently are measuring the jaw forces and jaw gapes during gouging in Callithrix jacchus. These in vivo data will provide an empirical description of jaw mechanics during gouging and test the respective hypotheses that gouging is associated with large jaw forces and/or large jaw gapes relative to other behaviors involving the oral apparatus. Based on the results from this comparative morphometric analysis, we predict that jaw forces during gouging will not be relatively large, and therefore will not result in relatively large internal skull loads in comparison to forces associated with other voluntary activities. We also predict that maximum jaw gapes will be relatively large during gouging, and that gouging primates are able to open their jaws relatively wider than closely related nongouging species. CONCLUSIONS Our analysis of the skull shapes of Phaner furcifer, Euoticus elegantulus, and Callithrix jacchus indicate little evidence to suggest that these species have a greater ability either to generate force at the anterior teeth or to resist loads in the skull when compared to closely related nongouging species. Based on these morphological comparisons, we pre- 165 dict that forces in the jaw during gouging will be similar to or less than forces during other activities involving the oral apparatus. This prediction is a significant departure from previous speculations that forces are relatively high in the skull during gouging. We also show that these three gouging species possess several skull shapes that facilitate larger gapes. We predict that tree gouging will involve maximum gapes that are relatively larger than maximum gapes during other behaviors involving the oral apparatus. The theoretical foundation guiding decisions about comparative samples and shape variables for comparative morphometric research has received considerable attention (e.g., Mosimann and James, 1979; Harvey and Pagel, 1991; Jungers et al., 1995). Contrasting the findings of our study with those of Dumont (1997) provides a clear example of how the choice of a comparative sample and/or denominator of a shape variable can impact the results of comparative morphometric research. These two studies generate dissimilar results and hence offer widely different functional interpretations of skull form for essentially the same species of gouging primates. Clearly both studies cannot be correct in their interpretations of skull form-function relationships. While we obviously favor our decisions regarding comparative samples and the choice of shape variables, we strongly recommend that an in vivo approach must provide the foundation for determining jaw functions. In this instance, in vivo data are necessary to empirically establish jaw force- and gape-related functions during gouging. ACKNOWLEDGMENTS We thank the following institutions and individuals for providing access to primate skulls: Field Museum of Natural History (L. Heaney, B. Patterson, and W. Stanley); National Museum of Natural History (L. Gordon and R. Thorington); American Museum of Natural History (R. MacPhee); Natural History Museum, London (P. Jenkins); Muséum National d’Histoire Naturelle (J. Cuisin); Naturhistorisches Museum Basel (M. Sutermeister and F. Weidenmayer). B. Shea and D. Schmitt kindly allowed access to video capture and videometric analysis software. We thank K. Johnson, C. Kirk, P. Lemelin, B. Payseur, D. Schmitt, and P. Vinyard for numerous helpful discussions and comments that greatly improved the manuscript. Funding for collection of morphometric data was provided by Sigma-Xi, the Boise Fund, the AMNH, the NSF (SBR-9701425), and the L.S.B. Leakey Foundation. 166 C.J. VINYARD ET AL. APPENDIX At the request of multiple reviewers and the editor, we have included the results of pairwise species comparisons of skull shapes created with a geometric mean of 11 skull measurements (defined in Table 2) as the denominator in each shape variable for (a) Phaner furcifer vs. other cheirogaleids, (b) Euoticus elegantulus vs. other galagids, and (c) Callithrix jacchus vs. other callitrichids. We maintain that our use of a biomechanical standard to hold constant specific aspects of the biomechanical system we are studying is an important, and in many ways preferred, method of looking at the functional consequences of skull form in tree-gouging primates. That having been said, we agree with the reviewers and editor that it is important to be able to compare results that use different denominators in shape variables. We strongly caution, however, about extrapolating any conclusions from this comparison to size adjustment techniques in general. This concern is warranted, because creating shape variables using different geometric means in the denominator results in different interpretations of skull form in gouging primates. See Table 3 for explanatory footnotes. We omitted mandible length, AP mandible length, and masseter origin-insertion ratio in the Appendix because the shape variables are the same as those in Table 3. The numbering of shape variable comparisons is consistent with Table 3. a. P. furcifer vs. cheirogaleids Shape variable Cheirogaleus major Cheirogaleus medius Microcebus murinus Microcebus rufus Mirza coquereli 1. M1 depth (Pf ⬎) 2. M1 width (Pf ⬎) 3. Symphysis length (Pf ) 4. Condyle area (Pf ⬎) 5. Minimum cranial width (Pf ⬎) 6. Mandible length (Pf⬍) 8. Masseter moment arm (Pf ⬎) 9. AP mandible length (Pf ⬎) 10. Condyle height (Pf ⬍) 12. Condyle length (Pf⬎) 13. Temporal articular surface length (Pf⬎) Ns/Ns 0.04/Ns 0.009/Ns Ns/Ns Ns/Ns Ns/Ns Ns/Ns Ns/Ns 0.03/Ns 0.04/Ns 0.003/⫺ Ns/Ns Ns/Ns 0.002/⫺ Ns/Ns Ns/Ns Ns/Ns 0.01/Ns Ns/Ns 0.003/⫺ 0.004/⫺ 0.03/Ns Ns/Ns Ns/Ns 0.004/⫺ 0.004/⫺ Ns/Ns Ns/Ns Ns/Ns Ns/Ns 0.0007/⫺ 0.001/⫺ 0.001/⫺ 0.02/Ns Ns/Ns 0.001/⫺ 0.009/Ns Ns/Ns 0.04/Ns Ns/Ns Ns/Ns 0.002/⫺ 0.001/⫺ 0.02/Ns Ns/Ns Ns/Ns 0.008/Ns 0.003/⫺ Ns/Ns Ns/Ns Ns/Ns Ns/Ns 0.002/⫺ 0.001/⫺ 0.004/⫺ b. E. elegantulus vs. galagids Shape variable Galagoides alleni Galago moholi Galago senegalensis Galagoides zanzibaricus Galagoides demidoff Galagoides gallarum 1. M1 depth (Ee⬎) 2. M1 width (Ee⬎) 3. Symphysis length (Ee⬎) 4. Condyle area (Ee⬎) 5. Minimum cranial width (Ee⬎) 6. Mandible length (Ee⬍) 8. Masseter moment arm (Ee⬎) 9. AP mandible length (Ee⬎) 10. Condyle height (Ee⬍) 12. Condyle length (Ee⬎) 13. Temporal articular surface length (Ee⬎) 0.0001/⫺ 0.009/⫺ 0.00004/⫺ 0.00009/⫺ Ns/Ns Ns/Ns 0.002/⫺ Ns/0.01 0.00002/⫺ 0.0002/⫺ 0.000007/⫺ 0.0007/⫺ 0.00001/⫺ 0.00001/⫺ 0.001/⫺ Ns/0.0002 Ns/0.02 0.003/⫺ 0.02/Ns 0.000008/⫺ 0.006/⫺ 0.00003/⫺ 0.00007/⫺ 0.007/⫺ 0.00001/⫺ 0.002/⫺ Ns/0.008 Ns/0.02 0.0008/⫺ Ns/Ns 0.000006/⫺ Ns/Ns 0.0004/⫺ 0.0001/⫺ 0.03/Ns 0.0002/⫺ 0.002/⫺ Ns/Ns Ns/Ns Ns/Ns Ns/0.02 0.00007/⫺ 0.003/⫺ 0.001/⫺ 0.00003/⫺ 0.000003/⫺ 0.01/Ns 0.007/⫺ Ns/0.02 Ns/Ns 0.00009/⫺ Ns/Ns 0.00009/⫺ 0.03/Ns 0.000004/⫺ 0.003/⫺ 0.007/⫺ 0.004/⫺ Ns/Ns Ns/Ns Ns/0.006 Ns/Ns 0.01/Ns 0.0004/⫺ Ns/Ns 0.0001/⫺ c. C. jacchus vs. callitrichids Shape variable 1. M1 depth (Cj⬎) 2. M1 width (Cj⬎) 3. Symphysis length (Cj⬎) 4. Condyle area (Cj⬎) 5. Minimum cranial width (Cj⬎) 6. Mandible length (Cj⬍) 8. Masseter moment arm (Cj⬎) 9. AP mandible length (Cj⬎) 10. Condyle height (Cj⬍) 12. Condyle length (Cj⬎) 13. 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