bs_bs_banner Biological Journal of the Linnean Society, 2012, 106, 70–80. With 3 figures Mandibular shape correlates of tooth fracture in extant Carnivora: implications to inferring feeding behaviour of Pleistocene predators CARLO MELORO* Hull York Medical School, The University of Hull, Loxley Building, Cottingham Road, Hull HU6 7RX, UK Received 22 September 2011; revised 11 November 2011; accepted for publication 11 November 2011 bij_1843 70..80 Percentages of tooth fracture and mandible shape are robust predictors of feeding habits in Carnivora. If these parameters co-vary above the species level, more robust palaeobiological inferences could be made on fossil species. A test of association is presented between mandible shape and tooth fracture in a subset of extant carnivorans together with large Pleistocene fossil predators from Rancho La Brea (Canis dirus, Panthera atrox, and Smilodon fatalis). Partial least square (PLS) and comparative methods are employed to validate co-variation of these two parameters in extant carnivorans. Association between mandible shape and percentage of tooth fracture is strongly supported, even if both blocks of data exhibit a phylogenetic signal to a different degree. Dietary adaptations drive shape/fracture co-variation in extant species, although no significant differences occur in the PLS scores between carnivores and bone/hard food consumers. The fossil species project into PLS morphospace as outliers. Their position suggests a unique feeding behaviour. The increase in the size of prey, together with consumption of skin and hair from carcasses in a cold environment, might have generated unusual tooth breakage patterns in large predators from Rancho La Brea. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80. ADDITIONAL KEYWORDS: comparative methods – diet – geometric morphometrics – partial least square – Rancho La Brea. INTRODUCTION Different bones of the vertebrate skeletons are built to sustain different degrees of biomechanical stress (Frost, 1964; Oxnard, 1993). The skulls of mammalian Carnivora have received particular attention in this respect. Theoretical models suggest that skull shape differences among carnivoran species depend on adaptations to different mechanical requirements, as related to distinct feeding behaviours (Wroe, McHenry & Thomason, 2005; Slater, Dumont & Van Valkenburgh, 2009; Slater et al., 2010; Wroe, 2010; Figueirido et al., 2011; Tseng & Wang, 2011). Feeding adaptations are even more evident in the mandible, whose primary function is mastication (Herring, 1993). On the one hand, mandibles are optimally designed for chewing, catching food, and for with*E-mail: [email protected] 70 standing the movement of prey during killing. On the other hand, mandibles of closely-related species tend to resemble each other in shape regardless of their particular diet (Meloro et al., 2008; Piras et al., 2010; Raia et al., 2010). The role of dentition in explaining this process is crucial in Carnivora whose feeding adaptations imply either reduction or development of specific dental areas in the lower jaw. Families of Carnivora are clearly distinct in their mandible shape because of early morphological differentiation during their evolutionary history (Ewer, 1973; Holliday & Steppan, 2004; Van Valkenburgh, 2007; Meloro et al., 2008; Meloro & O’Higgins, 2011). For example, Felidae and large Hyaenidae have a reduced dentition in their lower jaw; their mandible is designed for meat consumption; and little variation occurs during their evolutionary history (with exceptions being the aardwolf Proteles cristata among hyaenids, or sabertooth cats among felids). On the © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80 MANDIBLES-FRACTURE other hand, similarities in mandible shape occur when the complete dental formula is retained thus allowing them (with modifications) to cope with a variety of food (e.g. Canidae and Viverridae; Meloro, 2011a, b; Meloro & O’Higgins, 2011). Consequently, feeding adaptations become difficult to interpret in extinct taxa even if external mandibular morphology is an informative starting point to make palaeobiological inferences (Meloro, 2011a). The quantification of tooth breakages is another robust predictor of feeding habits in both extant and fossil carnivorans (Van Valkenburgh, 1988a, 2009). Numerical models applied to the carnivorans of Rancho La Brea show a strong competition among large predators whose percentage of tooth fracture was higher than in extant species (Van Valkenburgh & Hertel, 1993). Percentages of tooth fracture are calculated for both upper and lower jaw dentition across different individuals of the same species. Tooth fracture varies also among populations, although feeding adaptation clearly causes interspecific differences (Van Valkenburgh, 2009). Consumers of hard food such as bones or shells (hyenas, sea otter) tend to break their teeth more often than meat eaters and omnivores. Other biological correlates of tooth fracture incidence in Carnivora are ageing (specimens of older age tend to exhibit high frequency of tooth fractures) and nonfatal injuries. Pasitschniack-arts, Taylor & Mech (1988) reported an individual arctic wolf with a fractured upper carnassial caused by the impact of a hoof of a large ungulate and suggested that this kind of trauma is quite common in populations of grey wolf. However, Van Valkenburgh (2009: 76) clearly demonstrated that ‘diet appears to be the fundamental factor determining rates of tooth fracture in carnivorans, and probably mammals, in general’. Because tooth fracture frequency and mandible shape reflect the type of food consumed, we might expect these two features to co-vary. This would lend support to palaeobiological inferences made on either one of these two factors. In the present study, the hypothesis is tested that mandibular shape and percentage of tooth fracture correlates in extant Carnivora. Species with low percentage of tooth fracture are expected to exhibit a mandible with a long premolar row, an elongated molar crushing area, and a short coronoid area (i.e. indicative of a relatively small area for the attachment of the temporalis) because they are all generalist feeders. On the other hand, species with high percentage of tooth fracture (specialized predators and hard object feeders) are expected to show a relatively thicker mandibular corpus, a shorter premolar row, a more developed molar slicing area, and a longer coronoid to provide a large area for the attach- 71 ment of the temporalis (Ewer, 1973; Van Valkenburgh, 2009; Meloro & O’Higgins, 2011; Meloro et al., 2011). If this hypothesis is supported, it is expected that the combination of these two features provide indication of feeding habits in both extant and fossil species. Consequently, the present study tests for the effect of diet on the shape/fracture association and includes in the analyses Pleistocene fossil species from Rancho la Brea for which data are available. Geometric morphometrics and comparative methods are employed to validate mandibular shape/ fracture relationship at the interspecific scale. Geometric morphometrics furnish an optimal solution in quantifying and visualizing shape variation in complex structures such as the mandible. Meloro et al. (2008) validated patterns of association of mandible shape with tooth sharpness and diet in Carnivora (Meloro & Raia, 2010; Figueirido et al., 2011; Meloro & O’Higgins, 2011). Meloro (2011a) also presented a survey of mandible shape in large Carnivora to predict feeding adaptations in PlioPleistocene taxa, supported by a high degree of statistical accuracy. Comparative methods become necessary when hypotheses at an interspecific scale need to be validated (Garland, Bennett & Rezende, 2005). The lower carnassial morphology of Carnivora exhibits a strong phylogenetic signal (Meloro & Raia, 2010) as does the mandible (Meloro et al., 2008, 2011; Figueirido et al., 2010, 2011; Meloro, 2011a, b; Meloro & O’Higgins, 2011). Yet, there is no evidence of a phylogenetic signal in tooth fracture. Van Valkenburgh (1988a) showed that hyaenids differ from felids and canids in tooth fracture frequency, even if larger dataset supports extensive overlap between carnivoran families (Van Valkenburgh, 2009). The present study reports multiple approaches that provide new insights into the underlying processes moulding mandible shape and percentage of tooth fracture in Carnivora. MATERIAL AND METHODS SAMPLE One hundred ninety-six digital images of mandibles were collected for 38 species of Carnivora (Table 1; see also Supporting information, Table S1) for which tooth fracture data were available from the literature (Van Valkenburgh, 2009). The mandible sample was assumed to be representative of interspecific variability. The number of specimens per species varied from one (Panthera atrox, Canis dirus, and Urocyon littoralis) to 14 (Otocyon megalotis) (mean of 5.16) (Table 1). Only mandibles of noncaptive individuals of both sexes with no evident pathologies were selected. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80 72 C. MELORO Table 1. Statistics for the mandibular sample of extant and fossil Carnivora Family Number of species Number of Specimens Minimum (N) Maximum (N) Mean number of specimens/ species Canidae Felidae Hyaenidae Mephitidae Mustelidae Procyonidae 12 10 3 3 8 2 67 50 16 11 42 10 1 1 4 2 4 4 14 8 7 5 10 6 5.58 5.00 5.33 3.67 5.25 5.00 categories in Carnivora (Crusafont-Pairó & TruyolsSantonja, 1957; Van Valkenburgh, 1988b; Meloro, 2011a, b; Meloro & O’Higgins, 2011). Landmarks 7 to 11 cover the ascending ramus region. A measurement error survey showed that these landmarks are repeatable with a good degree of accuracy (Meloro, 2011a). GEOMETRIC Figure 1. The position of landmarks on a mandible outline of Canis lupus BMNH 34.6.28.47. 1–2, anteroposterior diameter of c1; 2–3, diastema length; 3–4, length of the premolar row; 4–6, length of the molar row; 5, projection of the protocone cusp on the m1 baseline; thickness of the mandibular corpus under the canine (2–14) and molar row (4–13, 6–12) identified by the landmark projections perpendicular to the line 1–6; 7, tip of the coronoid process; 8–9, the maximum depth of the condylar process (Processus condylaris); 10, most posterior extreme point of angular process; 11, the ventral extreme of angular process. Scale bar = 1.0 cm. Fossil specimens were represented by casts housed at the Natural History Museum of London and Royal Museum of Scotland (see Supporting information, Table S1). Those casts were already employed in a previous study on mandible shape and did not present any kind of shape or growth anomaly (Meloro, 2011a). Digital photographs were collected with a Nikon camera at a distance of 2 m in accordance with the protocol described by Meloro et al. (2008), Meloro (2011a, b), and Meloro & O’Higgins (2011). Fourteen anatomical landmarks were digitized with TPSDIG, version 2.09 (Rohlf, 2006a) as in Figure 1. Landmarks from 1 to 6 were recorded at teeth alveoli, covering the corpus mandibulae, together with landmarks 12 to 14. Landmark 5 was placed to distinguish the slicing from the crushing molar region in the lower dentition, which is relevant to discriminate feeding MORPHOMETRICS Shape variables were extracted from raw landmark coordinates (on the x- and y-axes) by applying Generalized Procrustes Analysis (GPA; Rohlf & Slice, 1990). This algorithm aligns landmark configurations to a common reference (the consensus) after removing the effect of rotation, translation, and differences in size among specimens. The new landmark coordinates were projected into the Kendall tangent space (with respect to the consensus) and thin plate spline decomposition method was applied to extract affine (uniform; Uni) and non-affine (partial warps; PWs) components of shape. PWs and Uni represent regional variation of landmarks that can be visualized through deformation grids. GPA was repeated for each species separately to extract consensus coordinates, then the species consensus coordinates were analyzed into a common shape space re-performing the GPA. Partial least square (PLS; Rohlf & Corti, 2000) analysis was applied to detect possible correlation between shape variables (both PWs and Uni) and the tooth fracture data sensu Van Valkenburgh (2009). To quantify tooth fracture data, only the percentage of fracture quantified for Canines (C), premolars (P), and carnassials (CR) was considered (Van Valkenburgh, 2009: 74). This way, only teeth covered by the landmark configuration were included in the analyses. The PLS extracts pairs of orthogonal latent variables from the correlation matrices of each block, using singular value decomposition. Each pair of latent variables (singular warps; SW) maximize the possible co-variation between the two blocks. Because fossil taxa exhibit an unusual pattern of tooth fracture (Van Valkenburgh, 1988a, 2009; Van © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80 MANDIBLES-FRACTURE Valkenburgh & Hertel, 1993), PLS was applied only to test for the association between mandible shape and tooth fracture in a subset of extant species (N = 35). A nested analysis is also presented after selecting specific ecological groups (diet categories, sensu Van Valkenburgh, 2009: C, carnivorous; B/S, bone or shell hard-object feeders; O/I, omnivorous and/or insectivorous) that emerged from PLS plots (Meloro, 2011a). Fossil taxa were projected in the SW spaces to identify similarities (or dissimilarities) with extant taxa in relation to mandible shape and percentage of tooth fracture. This procedure was employed by Manfreda et al. (2006) in a study on the association between locomotion and atlas shape in primates. In that case, the aim was to detect whether humans exhibit unusual atlas morphology compared to other primates (Manfreda et al., 2006). GPA and PLS analyses were performed using TPSPLS, version 1.18 (Rohlf, 2006b). IDENTIFIABLE FACTORS Covariation between mandible shape and tooth fracture could be influenced by common factors. Parametric and nonparametric multivariate analysis of variance (MANOVA) (using PAST, version 2.4; Hammer, Harper & Ryan, 2001) were employed to test for differences in PLS scores as a result of diet (categories in Van Valkenburgh, 2009). This study also tested for an association between SWs and mandibular size (as quantified by centroid size of landmark configuration) with nonparametric correlation. Because of statistical non-independence of inter-specific data, comparative methods (Garland, Bennett & Rezende, 2005) were applied to take the phylogenetic effects into account. A K-statistic was employed to detect a phylogenetic signal in SW scores and tooth fracture data (Blomberg, Garland & Ives, 2003). The K-statistic varies between 0 (no phylogenetic signal in the data, such as with a star phylogeny) to 1 or even more (1 = data fit a Brownian motion model of evolution). The phylogenetic tree for the 35 extant species of Carnivora was pruned using MESQUITE (Maddison & Maddison, 2009) from the Bininda-Emonds, Gittleman & Purvis (1999) phylogeny. It includes time of divergence in million of years calibrated from the fossil record (see Supporting information, Fig. S1). The software PDAP (Garland et al., 1993; Garland, Midford & Ives, 1999; Garland & Ives, 2000) and PHYSYG (Blomberg et al., 2003) were used to manipulate the tree and to test for significance of the phylogenetic signal. Then, phylogenetic generalized least square (PGLS) analysis (Rohlf, 2001, 2006c) was applied to validate the PLS analyses, and to verify the effect of diet and size on SW scores. PGLS was 73 employed to validate the association between SWs including phylogenetic co-variance matrix as an error term in the regression model with SW shape as x and SW fracture data as y (Meloro et al., 2011). PGLS analysis was repeated to test for an association between diet or size (as x) and specific SW (as y). This procedure provided the same results as performing correlation tests between independent contrasts of paired SWs. PGLS analyses were conducted with NTSYS, version 2.21c (Rohlf, 1986–2009). RESULTS OVERALL SAMPLE PLS analysis supports a strong correlation between the percentage of tooth fractures and mandible shape in extant Carnivora. The analysis for 35 extant species extracts three pairs of SW vectors of which the first explains 81.98% of covariance, the second explains 15.35%, and the third explains 2.65%. The correlation coefficient for the first pair of SW is high (r = 0.728) and significantly larger than expected by 9999 random permutations (P = 0.0001). On the second SW, the correlation is lower (r = 0.568) but still significant (P = 0.0001). With the third pair of axes, the correlation is nonsignificant. Along the first pair of SWs, a high degree of overlap occurs between Canidae and Felidae, whereas members of Mephitidae, Hyaenidae, and Mustelidae appear distinct (Fig. 2A). The omnivores/insectivores (O/I) show more negative SW scores on both axes (shape and tooth fracture) compared to carnivores and B/S (Fig. 2A). The hard food feeders (B/S) fall within the range of variability of carnivores, even if only hyaenids occupy a discrete portion of the morphospace. Diet categories are significantly different along the first two pairs of SWs (nonparametric MANOVA F = 8.979; P < 0.0001), even though the pairwise comparisons show no difference between carnivores and bone/shell feeders in SW scores (P = 0.7824). On the negative scores of SW1, species exhibit a low percentage of fractures, a mandible with elongated crushing molar area, and a curved and posteriorly thick corpus (Fig. 2B). Positive scores are occupied by species with higher percentage of tooth fractures (particularly the premolars), whose mandibular corpus is less curved, and exhibit a longer diastema and a shorter crushing molar area. The ascending ramus is elongated posteriorly because of the shift of the condylar process landmark (Fig. 2B). When fossil taxa are projected in the SW1 space, they all exhibit positive scores and cluster within the range of C and B/S groups, with the exception of the sabertooth cat Smilodon (Fig. 2A). Canis dirus is within Canidae and Felidae with SW1 scores very © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80 74 C. MELORO Figure 2. Plot of the first pair of Singular Warps (SW) representing mandibular shape block (x-axis) and tooth fracture data block (y-axis) for 38 species of Carnivora. A, species are labelled for families. In the smaller plot taxa are labelled for diet. O/I, omnivores/insectivores are grey diamonds; C, carnivores are white diamonds; B/S bone shell consumers are black diamonds. Fossil species are projected. B, profile plot for tooth fracture data and deformation grids of mandibular shape data associated with SW1. The left side represents the extreme negative scores, and the right side represents the positive scores. On the profile plot: C, % Canine; P, % Premolar; CR, % Carnassial. close to that of the tiger (Panthera tigris), whereas P. atrox clusters within Canidae because of very high SW1 fracture scores that resembles the grey wolf (Canis lupus) and the island fox (U. littoralis) (Fig. 2A). Smilodon fatalis exhibits a high positive score for mandible shape and clusters much greater than the range of extant hyaenids (Fig. 2A). The effect of centroid size on SW1 (only extant taxa) is significant for both shape and fracture data, although no association occurs with either one of the SW2 axes (Table 2). NESTED ANALYSIS Because of the clear separation between carnivores and bone/shell feeders from the omnivore/insectivores in the SW1 plot (Fig. 2A), PLS was repeated on the 28 extant species belonging to the former two categories. Figure 3. Plot of the first pair of Singular Warps (SW) representing mandibular shape block (x-axis) and tooth fracture data block (y-axis) for 28 species of carnivores and B/S (bone shell) that includes Hyaenidae, Canis lupus, and Enhydra lutris. A, families and fossil taxa are projected. B, profile plot for tooth fracture data and deformation grids of mandibular shape data associated with SW 1. The left side represents the extreme negative scores, and the right side represents the positive scores. On the profile plot: C, % Canine; P, % Premolar; CR, % Carnassial. Three pairs of SWs are extracted, although only the first shows a very high significant correlation (r = 0.904, P < 0.0001 after 9999 randomizations). The first pair of SW explains 76.15% of covariance, whereas the second (nonsignificant) explains 20.72%. The strong association between the first pair of axis shows that Mustelidae are clearly distinct in the SW scores from the other families (Fig. 3A). They occupy negative scores of SW1 (Fig. 3A) being characterized by a small percentage of fractured premolars but higher canine fracture and a curved mandible with long crushing area (Fig. 3B). On positive scores felids, hyaenids, and canids show higher premolar and carnassial tooth fracture in relation to a straighter mandible with a longer slicing area (Fig. 3A). The diet signal is mixed in this plot because the sea otter Enhydra lutris (a B/S) clusters with other mustelids, whereas the grey wolf is closer to bone cracking hyenas (Fig. 3A). A nonparametric permutation test showed nonsignificant separation between C and B/S © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80 MANDIBLES-FRACTURE 75 Table 2. Spearman nonparametric r-values (below diagonal) and probability values (above) for correlation between Ln centroid size (CS) and Singular Warps (SW) 1 and 2 Ln_CS SW1_Sh SW2_Sh SW1_Fr SW2_Fr Ln_CS SW1_Sh SW2_Sh SW1_Fr SW2_Fr 1.0 0.69613 -0.09328 0.54675 0.066676 3.43 ¥ 10–6 1.0 -0.02563 0.75602 0.16299 0.59404 0.88379 1.0 0.061502 0.54619 0.000678 1.51 ¥ 10–7 0.72561 1.0 0.60315 0.70353 0.34952 0.000688 0.000126 1.0 Significant values are shown in bold. Table 3. K-statistics and probability values for phylogenetic signal in different variables for both the overall (N = 35) and the nested sample (N = 28) N = 35 C PM CR Ln CS SW1 shape SW1 fracture SW2 shape SW2 fracture N = 28 K P K P 0.24553 0.43108 0.15348 0.90907 1.3862 0.2774 0.5563 0.2924 0.01902 < 0.0001 0.47648 < 0.0001 < 0.0001 0.0050 < 0.0001 0.0110 0.18475 0.37992 0.13406 0.81130 1.1767 0.5950 – – 0.12613 0.00100 0.48448 < 0.0001 < 0.0001 < 0.0001 – – C, % canine; PM, % premolar; CR, % carnassial; Ln CS, natural log-transformed centroid size (CS); SW, Singular Warp. based on SW1 scores (Mahalanobis distance = 0.054, P = 0.8529). The projection of fossil taxa shows that they are all outliers in the SW1 plot because of a high percentage of canine fractures associated with negative scores of SW1 (Fig. 3A, vertical axis). Canis dirus is the only fossil species with SW scores close to the lower limit of other extant canids (the side-striped jackal Canis adustus). Panthera atrox has a shape score similar to felids but resembles mustelids in the fracture SW1 score. Smilodon fatalis is similar in fracture score to some felids like the cheetah (Acinonyx jubatus) and the jaguar (Panthera onca) but its shape is very distinct (Fig. 3A). In this nested sample, mandibular size shows a significant positive association only with SW1 fracture scores (rspearman = 0.44, P = 0.019). PHYLOGENETIC SIGNAL AND COMPARATIVE TESTS In Table 3, the K-statistic and probability values are reported for SW scores including the raw data for percentage of tooth fracture. All exhibit a significant phylogenetic signal, with the exception of the percentage of carnassial tooth fracture in both overall and nested samples, and the percentage of canine fracture only for the nested sample (N = 28). Centroid size and SW scores of mandible shape exhibit a very high phylogenetic signal. On the other hand, SW scores of tooth fractures have a low but significant signal. The association between the first pair of SWs is supported also when phylogeny is taken into account (PGLS when N = 35, r = 0.408, FS = 6.60, P = 0.015; with N = 28, r = 0.502, FS = 8.74, P = 0.006). However, the correlation between the second pair of SW in the overall sample is not significant (P = 0.81). Nonsignificance also applies to the association between centroid size and SW1 axes (P > 0.2) in all cases. On the other hand, diet is still a significant factor on discriminating the overall sample for both pairs of SW scores (FS = 6.1975, P < 0.0001) but not when only carnivores and B/S are analyzed (FS = 1.435, P = 0.257). DISCUSSION EXTANT CARNIVORA The association between mandibular shape and percentage of tooth fracture is robust in Carnivora and it is not influenced by phylogeny or by size (whose effect disappears when phylogeny is taken into account). Carnivory and hard food consumption are the main adaptations that drive this association. This is apparent in the SW plot of all species (Fig. 2A) where omnivores and insectivores clearly occupy a separate region of the morphospace. They all belong to the suborder Caniformia (see Supporting information, Table S1) and are adapted to chewing by means of a large crushing molar area. This adaptation allows omnivores/insectivores to distribute masticatory stress to the posterior area of the mandible, so that the corpus shape thickens below this region. Even herbivorous carnivorans show similar mandibular morphology (Figueirido et al., 2010, 2011; Meloro, 2011a). © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80 76 C. MELORO At the opposite extreme, carnivores and hard object feeders show a high percentage of fractures for all the teeth and they are characterized by a mandible with a more developed molar slicing area. The enlargement or reduction of molar slicing/ crushing area is a fundamental correlate of carnivoran feeding ecology (Van Valkenburgh, 1988b; Meloro, 2011a, b; Meloro & O’Higgins, 2011) and relates well to the percentage of tooth fracture. However, PLS analyses show that carnivory and hard object feeding are not mutually exclusive. Indeed, no significant differences occur in all PLS analyses between these two feeding categories. They clearly challenge carnivoran ecomorphology so that, when only carnivores and hard object feeders are analyzed, the association between SW becomes stronger (Fig. 3A). Such a differentiation in SW morphospace is related to the loading of tooth fracture vector (Fig. 3B): predatory mustelids and the sea otter (negative SW1 scores) are characterized by a relatively higher canine fracture percentage compared to canids, hyaenids, and felids, and their mandible is more curved and thicker below the molar slicing/crushing area (Fig. 3B). Mustelids show a well developed molar crushing area, allowing them to occupy a disparate range of feeding niches (including omnivory or insectivory). They have also a thicker corpus below the canine area, possibly related to higher physical stress in this region. Such high stress indicates an adaptation to killing very large prey (Ewer, 1973; Christiansen & Wroe, 2007): species such as Mustela erminea exhibit 17% of canines being fractured, almost doubling the grey wolf or the leopard (Panthera pardus), with 9.8%. Canids, felids, and hyenas show a higher percentage of fractures in premolars and carnassials. Their mandibles are less curved in the corpus area, possess a diastema, and have a relatively longer blade in the carnassial. The coronoid is also projected posteriorly, providing a larger area of attachment for the temporalis relative to the masseter (Figs 2B, 3B). As expected, this mandibular design relates to a predaceous lifestyle (Meloro & O’Higgins, 2011; Meloro et al., 2011). It is also interesting to note that the highest positive fracture score is exhibited by the least carnivorous predatory canids: the red fox (Vulpes vulpes) and the island fox (U. littoralis). In these species, the rate of premolars fracture is unusually high compared to that of larger canids. Possibly, the specialization for hunting on small rodents supplemented with eggs and vegetable matter challenges foxes’ feeding behaviour, whose contact with unexpected kinds of food material is more likely to occur than in the large predators (Van Valkenburgh, 2009). Addition- ally, foxes eat the entire body of small rodents (including skeletons), increasing the risk of contacting small bones with their anterior teeth. Felids and hyaenids share similar scores in both fracture and mandibular shape vectors because of their long carnassial blade. However, they also cluster with the phylogenetically distant large canids because of the low phylogenetic signal in fracture data (Table 2). Killing large prey is an ecomorphological challenge that constrains all predatory carnivorans to cope with high stress in the mandible as a result of prey holding (Biknevicius & Van Valkenburgh, 1996; Meloro et al., 2011). The SW vectors show that predatory canids, felids, and hyaenids cope with higher stress on the anterior canine area differently from mustelids. The similarity in SW scores of the grey wolf, hyenas, and the tiger does not support a distinct ecomorphological adaptation for bone consumption. A study by Van Valkenburgh (1996) on free-ranging African carnivores might help to explain this pattern. Both the African wild dog (Lycaon pictus, which occupies the central plot area in Figs 2A, 3A) and hyenas consume more bone than felids. This is achieved differently because Lycaon relies more on carnassials and post carnassials to crack bones, whereas hyenas use their premolars (Van Valkenburgh, 1996). Dentition again appears to constrain mandibular morphology in adapting differently to bone consumption (Werdelin, 1996; Tseng & Binder, 2010). It is noteworthy that premolars are also involved in skin, muscle, and bone processing (Van Valkenburgh, 1996). Clearly, if adaptation to carnivory and hard object feeding favours a functional association between percentage of tooth fracture and mandibular shape, processes related to developing dentition constrain masticatory function so that a phylogenetic signal also occurs in PLS morphospace (Figs 2A, 3A, Table 3). Previous studies on carnivoran mandible and dentition showed that ecomorphological differentiation occurred very early in the history of Carnivora (Meloro et al., 2008; Meloro & Raia, 2010; Meloro & O’Higgins, 2011), so that members of the same families tend to resemble each other. This applies also to mandibular shape correlates of tooth fracture percentage. Interestingly, a significant phylogenetic signal occurs in some tooth fracture percentage variables (percent of canines, premolars; Table 3), suggesting that they need to be interpreted with caution and treated statistically using comparative methods. The PGLS models support an adaptive response of the mandible shape to feeding stress. Dentition constrains the methods of chewing, although it does not prevent adaptation to distinct feeding habits taking place in Carnivora. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80 MANDIBLES-FRACTURE PLEISTOCENE FOSSILS The projection of fossil species in PLS plots suggests that some of them might show similar variability to extant taxa (Fig. 2A). Mandibular shape of C. dirus resembles the living canids, and the North American lion P. atrox is similar to extant felids (Anyonge & Baker, 2006; Christiansen & Harris, 2009; Meloro, 2011a). However, the SW plot (Fig. 2A) shows a reversed pattern, clearly as a result of the unusual tooth fracture data exhibited by those species. Smilodon fatalis appears distinct in both traits, confirming its unique morphological adaptations (Andersson, Norman & Werdelin, 2011; Christiansen, 2008; Slater & Van Valkenburgh, 2008; Meloro, 2011a). When only carnivores and hard object feeders are analyzed, all the three Pleistocene taxa are outliers (Fig. 3A). Competition for carcasses might have been stronger in these highly carnivorous species, generating higher stress during feeding (Van Valkenburgh & Hertel, 1993; Binder, Thompson & Van Valkenburgh, 2002; Van Valkenburgh, 2009), although why their mandibles did not evolve to match this condition remains unknown. Canis dirus possibly follows ecomorphological variation of extant taxa, even if its canine tooth fracture frequency is very high compared to extant canids (generating a low score on SW1 fracture in Fig. 3A). The pattern for P. atrox is even more unusual because its canine fracture frequency is similar to that of mustelids. Canines could be involved in muscle and bone mastication but Van Valkenburgh (1996) showed that they are more often used to manage skin and to open the carcass of dead prey. The convergence in tooth fracture of these Pleistocene fossils with mustelids suggests that the stress in prey holding could also explain their feeding behaviour. Both C. dirus and P. atrox were capable of killing prey larger than themselves at Rancho La Brea (Coltrain et al., 2004; Carbone et al., 2009; Meloro, 2011a) and this factor alone might explain the unusually high percentage of canine fracture. A specialization of killing large Pleistocene herbivores might have increased the risk of canine fracture during predation considering the larger size of ruminants in the Ice Age (Raia, Meloro & Barbera, 2007; Pushkina & Raia, 2008). Additionally, a study by Anyonge & Baker (2006) supported the strong similarity in craniofacial morphology between C. dirus and C. lupus. Tooth fracture pattern should also be expected to be similar, although this is not the case. Canis dirus shows a higher percentage of canine fractures and lower of premolars (that are also comparatively bigger) versus hyenas and the grey wolf. For P. atrox, the present study shows a similarity in mandible shape/tooth fracture pattern only with canids, felids (Fig. 2A), and mustelids (Fig. 3A), and 77 not with hyaenids. There is little support for a possible adaptation in bone consumption, except for the fracture frequency similarity with the shell eater E. lutris, whose dentition and mandible are completely distinct from that of bone consumers. When considering S. fatalis, it is difficult to make ecomorphological inferences because of its low bite force and its unique morphology (Andersson et al., 2011; McHenry et al., 2007). In the SW plots, Smilodon always shows SW fracture scores less than that of hyenas and much closer to that of extant felids (Figs 2A, 3A). Bone consumption also occurs in extant lions (Domínguez-Rodrigo, 1999), although they chew only thin ribs and long bone articular epiphyses. Additionally, Anyonge (1996) provided strong evidence to support a low bone consumption rate in Smilodon based on microwear. The unusual trend in mandible shape and tooth fracture for Pleistocene species appears to be more indicative of a distinct hunting behaviour and carcass consumption. The high percentage of canine fractures supports the idea of higher stress in prey catching and holding, together with higher (and possibly more difficult) skin consumption. Within this context, the environmental condition should also be considered to provide an alternative explanation for the fracture/shape pattern in Pleistocene fossils. Several studies indicate that tooth fracture might be facilitated by thermal stress or by distinct environmental conditions (Brown, Jacobs & Thompson, 1972; Clough, Kendall MacKenzie & Broders, 2010 on moose, Alces alces). Similarly, Van Valkenburgh (2009) found a higher percentage of tooth fracture for Alaskan red foxes that rely extensively on carcasses (possibly frozen). The late Pleistocene was a particularly cold period, facilitating the freezing of herbivore carcasses and a thickening of the hair and skin in these species. Interestingly, Leonard et al. (2007) found a very high percentage of tooth fracture in eastern-Beringian wolves that could be explained by increase in bone consumption. However, Stiner (1999) provided similar evidence for cave bears (Ursus deningeri) from Yarimburgaz cave of Turkey in the Middle Pleistocene. The same study also reported an unusually high percentage of canine fractures that could not be explained by a peculiar diet. More research is needed to clarify whether the increase in tooth fractures in Pleistocene carnivorans is a generalized phenomenon possibly related to distinct ecomorphologies of Pleistocene species, as well as peculiar environmental conditions. CONCLUSIONS Mandibular shape and the percentage of tooth fracture can be interpreted together to obtain insights © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80 78 C. MELORO into the feeding behaviour of both extant and fossil Carnivora. There is a strong association between these two parameters, suggesting that carnivoran mandibles are designed to sustain different degrees of masticatory stress. In carnivorous and bone/shell consumers, this association is much stronger, although the high phylogenetic signal in mandible shape is not suggestive of convergence between bone consumers and the specialist shell eater E. lutris. The projection of Pleistocene species into the shape/fracture morphospace suggests that those taxa might have exhibited a unique feeding behaviour. Higher stress in carcass feeding possibly occurred as a result of the size of their favourite prey, the thicker skin and hair, and the colder environmental conditions. ACKNOWLEDGEMENTS I am grateful to museum curators and staff for supporting my numerous visits for data collection. In particular, I would like to thank P. Jenkins, L. Tomsett, R. Portela-Miguez, A. Salvador, D. Hills, J. J. Hooker, P. Brewer, and A. Currant (Natural History Museum, London); E. Gilissen and W. Wendelen (Royal Museum for Central Africa, Tervuren, Belgium); P. Agnelli (Museo Zoologico ‘La Specola’ Florence); M. Reilly and J. Liston (Huntherian Museum and Art Gallery, University of Glasgow, Glasgow); B. Sanchez, J. Morales, J. Cabarga, and J. B. Rodriguez (Museo Nacional de Ciencias Naturales, Madrid); A. Kitchener (Royal Museum of Scotland, Edinburgh); and D. Goujet, P. Tassy, and C.Signe (Museum National d’Histoire Naturelle, Paris). I thanks P. Piras and F. Lucci for sharing their database of felids. This research was supported by the European Community’s program ‘Structuring the European Research Area’ under Synthesys at the Museo Nacional de Ciencias Naturales (ES-TAF 858) and Museum National d’Histoire Naturelle (FR-TAF 1680) for the project ‘The evolution of feeding habits in extinct European carnivores’. The visit to the Royal Museum for Central Africa was supported by the project ‘Ecomorphology of extant African carnivores’ (BE-TAF 4901). I am indebted to P. Raia for providing comments on an early version of this manuscript. J. Allen and two anonymous reviewers considerably improved the quality of this manuscript. This paper is dedicated to M. Flinn who is facing the challenge of a growing dentition. REFERENCES Andersson K, Norman D, Werdelin L. 2011. Sabretoothed carnivores and the killing of large prey. PLoS ONE 10: e24971. Anyonge W. 1996. Microwear on canines and killing behaviour in large carnivores: saber function in Smilodon fatalis. 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Bite club: comparative bite force in big biting mammals and the prediction of predatory behaviour in fossil taxa. Proceedings of the Royal Society of London Series B, Biological Sciences 272: 619–625. SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article: Figure S1. Phylogenetic tree of 35 extant Carnivora sensu Bininda-Emonds et al. (1999) Carnivora supertree. Although six polytomies occur, this tree was favoured among other more updated topologies because it allows a consideration of all the taxa presented in the present study with robust branch lengths in millions of years. Table S1. List of specimens belonging to extant and fossil Carnivora included in the present study. Diet categorization is given in parenthesis. Institutional abbreviations: B.M.N.H., British Museum of Natural History. London, UK; H.M., Huntherian Museum and Art Gallery. University of Glasgow, Glasgow, Scotland, UK; M.C.Z.R., Museo Civico di Zoologia. Roma, Italy; M.N.C.N., Museo Nacional de Ciencias Naturales, Madrid, Spain; M.N.H.N., Muséum National d’Histoire Naturelle, Paris, France; M.Z.L.S., Museo Zoologico ‘La Specola’ Firenze, Italy; N.M.B., Naturhistorisches Museum Basel, Switzerland; RMCA, Royal Museum for Central Africa, Tervuren, Belgium; R.M.S., Royal Museum of Scotland. Edinburgh, Scotland, UK; V.N.A., Museo di Anatomia Veterinaria Università di Napoli; Z.S.M., Zoologische Staatssammlung München, Munich, Germany. Please note: Wiley-Blackwell are not responsible for the content or functionality of any supporting materials supplied by the authors. Any queries (other than missing material) should be directed to the corresponding author for the article. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 70–80
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