Sicuro and Oliveira - Skull Morphology and Functionality of Extant Felidae 2010

Zoological Journal of the Linnean Society, 2010.
With 26 gures
Skull morphology and functionality of extant felidae (mammalia: carnivora): a phylogenetic and evolutionary perspective
FERNANDO LENCASTRE SICURO1* and LUIZ FLAMARION B. OLIVEIRA2
1
Instituto de Biologia Roberto Alcntara Gomes, Universidade do Estado do Rio de Janeiro, RJ 20550-013, Brazil 2 Museu Nacional, Universidade Federal do Rio de Janeiro, RJ 20940-040, Brazil
Received 15 June 2009; accepted for publication 7 October 2009
Felids morphology and ecological role as hypercarnivores are quite constant, despite considerable body size variation among species. Skull morphological and functional features of 34 extant cat species were evaluated under a phylogenetic framework of the Felidae. Twenty skull measurements were analysed through Principal Component Analysis to assess the species morphofunctional spaces. Force indexes were obtained from static equilibrium equations to infer jaw mechanics. Correlations between morphological, functional, and ecological traits were tested by phylogenetically independent contrasts. In spite of the general cat-like pattern, specic features on the skulls allowed differentiation among groups. Acinonyx jubatus, for instance, showed a shorter and shallower temporal fossa than other big cats, and their bite functionality is marked by an increased contribution of the masseteric system. A morphofunctional dichotomy between Neotropical and Eurasian/African small cats was detected, and is associated with the major transversal axes of the skulls. According to the contrast analyses, the skull size is correlated with the bite force and prey size, but it is uncorrelated with the variations on jaw mechanics (from temporalis or masseter muscle optimizations). Also, there was no correlation between functional differences on jaw muscles and the ratio of prey weight to cat weight. The efficiency of the jaw apparatus among cats is quite consistent; therefore, the different evolutionary trends of jaw mechanics seem to be caused by the casuistic xation of phenotypical variations, rather than by specic adaptative selections. 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010. doi: 10.1111/j.1096-3642.2010.00636.x
ADDITIONAL KEYWORDS: functional morphology morphometrics phylogenetically independent

contrasts.
INTRODUCTION
Regardless of size and form variations, all cats look alike, and they are easily recognized as members of the Felidae. The cat-like ecomorph suggested by Martin (1989) is consistent throughout the felid species, and is one of the most conspicuous among the families of the order Carnivora. Many cat species are quite distinguishable by differences in their body mass and colour pattern. However, the variations in their skeletal design are less evident, as well as the
*Corresponding author. E-mail: fsicuro@gmail.com
ecomorphological implications associated with these. Although cats show several ecological particularities along their distribution in many biomes worldwide, they are consistently successful hypercarnivores (Guggisberg, 1975; Neff, 1982; Sunquist & Sunquist, 2002). Both big and small cats show similarities on their hunting strategy: it starts with prey stalking, followed by a variable range sprint, and then they capture their prey with the anterior limbs and claws, holding it for the fatal neck bite. Usually, this attack injures the spinal cord, but some large cats bite the throat in order to suffocate the prey (Guggisberg,
2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010
F. L. SICURO and L. F. B. OLIVEIRA (Prionailurus bengalensis). Nevertheless, an unusual change in this later taxonomical review was the reallocation of jaguarundi (Herpailurus yagouaroundi) to the genus Puma. Jaguarundis and pumas are very apomorphic in their general morphology, despite their phylogenetic closeness (Johnson & OBrien, 1997; Mattern & McLennan, 2000; Johnson et al., 2006). Furthermore, with strictly phylogenetic logic applied to taxonomy, all the species of this clade would be placed on the most senior genus: Acinonyx. On the other hand, the debate regarding the lower taxa of felids becomes more controversial after the recent record of natural hybridization and gene introgression among small Neotropical cats species Leopardus tigrinus, Leopardus geoffroyi, and Leopardus colocolo in overlapping areas of occurrence, detected by Trigo and colleagues (Trigo, Freitas, Kunzler, Cardoso, Silva, Johnson, OBrien, Bonatto & Eizirik, 2008).
1975; Neff, 1982; Sunquist & Sunquist, 2002). Minor variations are observed in some cat species, such as the powerful bite to the preys head made by Panthera onca and the suffocating muzzle clamp performed by lions (Schaller, 1976; Turner & Antn, 1997, 1998; Anton, Garcia-perea & Turner, 1998). Cooperative hunting is sometimes observed in a few species, but lions display this behaviour more often, and in a more organized way, than other cats (Schaller, 1972; Stander, 1992). Hunting strategies used by small cats for birds, reptiles and shes are very consistent among species, usually involving stalking and sitand-wait ambushes.
CAT
PHYLOGENY AND TAXONOMY
Felids form a monophyletic group and, according to fossil records and molecular data, the adaptative radiation of extant taxa started in the last 10 million years (Johnson et al., 2006; Johnson & OBrien, 1997). Salles (1992) was the rst one to use a cladistic approach to infer felid phylogenetic structure based on a qualitative analysis of skull morphology. The author pointed out ten skull synapomorphies among extant species: six tooth characters and four osteological features. Johnson & OBrien (1997), using mitochondrial DNA sequences and fossil information, proposed a comprehensive phylogeographical analysis. They proposed names to eight main lineages: Panthera lineage, Ocelot lineage, Puma group, Lynxes group, Bay cat group, Domestic cat lineage, Caracal group, and Asian Leopard cat group. The latest complete phylogenetic hypothesis was proposed by Johnson et al. (2006) using nuclear genes (nDNA), which conrmed the eight lineages proposed by Johnson & OBrien (1997). Nevertheless, the relationship among these lineages changed signicantly, and the major topological consensus between these two last phylogenies remains in the basal position of the Panthera lineage. The most recent taxonomic reviews of the family Felidae differ in the number of extant genera and species (Wozencraft, 1993, 2005). In the former review, the family was organized into 18 genera and 36 species, and many synonymies were claried (Wozencraft, 1993). The later review includes novelties on the taxonomic structure: 14 genera and 40 species, where four subspecies were elevated to the status of species (Wozencraft, 2005). This new approach raises important matters, and has had a positive repercussion on the conservation efforts of endangered species (sensu Beer, 2002), e.g. the recognition of the geographic morphotypes of pampas cat (Oncifelis colocolo) as different species (sensu GarciaPerea, 1994), and the the Iriomote cat (Prionailurus iriomotensis) as a distinct species from the leopard cat
CAT
JAW MECHANICS
The cat jaw mechanics follow the general carnivore pattern suggested by Maynard-Smith & Savage (1959), Turnbull (1970), and Greaves (1980a; 1980b; 1982; 1983; 1995), i.e. a high coronoid process, a hinge-like jaw condyle, and the tooth row at the same level of this condyle. A high coronoid process (i.e. a large in-force moment arm), is related to an improvement on the mechanical leverage of the temporalis muscle. In this arrangement, the resultant force vector of this muscle has a vertical component for jaw elevation, and a backward component that resists against the contrary forward forces of a struggling prey. The moment arm of masseteric complex and pterygoideus muscular systems are shorter than the moment arm of the temporalis muscle, but the masseter and pterygoideus muscles have a crucial role in the lateral stabilization of the jaw. In cats, the masseter supercialis is the next-largest jaw adductor, and it is related to the angular process and posterior mandible (Turnbull, 1970). Felids have a short rostrum and, consequently, a short jaw out-force moment arm. For a given muscular in-force moment, the out-force effect on a short jaw is stronger than on a long one. A short rostrum in a predator is less effective than a longer one for catching a running prey, but cats compensate for this with powerful and agile limbs with curved retractile claws at the paws (Neff, 1982). Sharp-edged carnassials provide a shear cut on prey meat. In both the Felidae and the Nimravidae there is an optimization of carnassial action by the presence of carnassial notches between the metastyle and paracone of the P4, and between the protoconid and paraconid of M1, that arrange the food items for more efficient shear-
FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION ing action by the carnassials (Bryant & Russell, 1995; Evans & Sanson, 2003; Evans & Fortelius, 2008; Evans & Sanson, 2006). Some morphometric studies of skulls have shown ecomorphological differences in the felid species according to their size ratios (Christiansen & Adolfssen, 2005; Christiansen & Wroe, 2007; Dayan et al., 1990; Radinsky, 1981a; Radinsky, 1981b; Kiltie, 1984; Larson, 1997; ORegan, 2002; Therrien, 2005). None of these studies dealt with the phylogenetic integration of morphofunctional patterns in a comprehensive examination of the species in the family. The present study evaluates the skull functional morphology of 34 extant cat species through a classical morphometric approach. Inferences about the evolution of cat skull design and function are proposed through contrasts analysis based on Johnson et al.s (2006) phylogeny of the Felidae (Fig. 1). The current study analyses the interspecic craniomandibular differences in a broad evolutionary context. Thus, it is not concerned with the differences at the subspecic level (e.g. sexual dimorphism, geographic distribution, and particular ecotypes). On that matter, we followed Wozencrafts (1993) former taxonomical review.
MATERIAL AND METHODS

Twenty skull measurements (Fig. 2) were used to describe skull morphology, and to evaluate the performance of the masticatory muscle groups and robustness of the neck (Radinsky, 1981a; 1981b, Kiltie, 1982, 1984, 1989; Sicuro & Oliveira, 2002). A list of descriptions and acronyms for these measurements are listed in Appendix 1. Skulls of adult felids were studied in the following zoological collections: American Museum of Natural History (AMNH), NY, USA; Field Museum of Natural History (FMNH), Chicago, USA; Museu Nacional (MN), Rio de Janeiro, Brazil; and Museu de Zoologia of University of So Paulo (MZUSP), So Paulo, Brazil. The species and the specimens used are presented in Appendix 2. The small sample size of some species denotes the scarcity of the specimens in the collections visited. We included individuals from different geographic regions to take into account the morphotype variations of each species. The lack of specimens of Felis bieti, Oreailurus jacobitus, and Neofelis diardi forced the exclusion of these taxa from the analysis.
Figure 1. Cladogram of the family Felidae, after Johnson et al. s (2006) phylogeny, adjusted to the number of species analysed. Values on the branches indicate the divergence time between nodes; node numbers are parenthetic.
F. L. SICURO and L. F. B. OLIVEIRA
Figure 2. Diagram showing the 20 skull measurements used in the analysis (see Appendix 1 for denitions).
The use of fresh muscle samples or reconstructions based on osteological analysis to estimate the contraction force of a muscle is a simplication of the muscular mechanic system (Hildebrand, 1988; Bryant & Seymour, 1990; Bryant & Russell, 1995). This is especially true considering the muscle architecture, e.g. the degree of pennation, angles of origin and insertion of the aponeuroses or tendons (Gans & Bock, 1965; Herring, 1972), and differences in the response of the bres during the muscle contraction (Gorniak & Gans, 1980; Weijs, 1980; Wieshampel, 1993). Nevertheless, it is very useful when employed in morphofunctional comparisons between morphologically or phylogenetically related individuals (Radinsky, 1981a; 1981b; Kiltie, 1982, 1984, 1989; Eisenberg, 1985; Hildebrand, 1988; Bryant & Seymour, 1990, Bryant & Russell, 1995; Sicuro & Oliveira, 2002). Muscle scars and dimensions of fossae measured on the skull were associated with original muscle cross-sectional areas (Gans & Bock, 1965). The distances between the jaw condyle and the point of insertion of the temporalis muscle (coronoid process of the jaw), supercial masseter muscle (angular process of the jaw), and deep masseter muscle (along the coronoid fossa and lower mandibular rim) were associated with the in-force moment arms (Wieshampel, 1993). The out-force moment arm
was dened as the distance from the jaw condyle to the canines. This assumption is acceptable for bidimensional models of jaws with orthal movement. The action of the pterygoideus muscle is similar to the action of the masseter (Turnbull, 1970; Herring, 1972). Nevertheless, the origin of this muscle on the ventral surface of the skull is not clearly seen. Moreover, in felids, the mass of masseter muscle, in particular its pars supercialis, is well above the pterygoideus, which is the smallest of the adductors (Turnbull, 1970). The pterygoideus muscle represents less than 10% of total masticatory muscle mass (Turnbull, 1970), and thus it was not included in our functional model. The equation of static equilibrium (sum of moments equal to zero) was used to predict the theoretical maximum force performed by jaw muscles. The force indexes (FIs) are derived variables, and their computation presumes the maximum resistance torque of a food item (prey) during the bite. The origin area substitutes muscle in force in the equations; therefore, the FIs are estimators of the potential bite strength, according to the craniomandibular morphology of the species. The FIs general equation is FI = (LS L1)/L2, where LS is the linearized (square root) muscle origin area (S), L1 is the muscle moment arm, and L2 is the resistance moment arm of the jaw.
FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION The FIs of the masticatory muscles are corrected by the second moment of area (SMA) of the dentary bone. The SMA is an estimator of resistance of the dentary to the bending forces that act on this bone during the bite. If one assumes that there is a correlation between variation in the robustness of a species jawbone and the loads involved in mastication, thus SMA could be used to adjust the FIs. Therefore, the corrected FIs (CFIs) are functional estimators that include more morphological information about the potential bite force (Sicuro & Oliveira, 2002). Our functional model does not compare the action of the temporal and the masseteric muscular systems with each other because of the anatomical differences between them (e.g. areas of origin and insertion, muscle architecture, degrees of pennation, and angles of action). Furthermore, Becht (1953), Maynard-Smith & Savage (1959), Davis (1955, 1964), and Turnbull (1970) clearly pointed out the main participation of the temporal complex in carnivoran masticatory mechanics. This method evaluates the potential performance of these muscular mechanical systems along the Felidae, regarding the skull design of each species. The derived variables, their acronyms, and FI equations, based on the skull measurements, are also described in Appendix 1. The samples had their normality and homoscedasticity tested (ShapiroWilk W and Levene tests, respectively), as well as the skewness and kurtosis of the frequency distributions. Morphometrical data were log-transformed in order to reduce the variance heterogeneity caused by size differences between the species. Minor normality problems were detected, but they were associated with the small sample sizes of some species, sexual dimorphism, and/or inuence of geographic variations. These problems were regarded as aspects of the morphological diversity, and as important to the morphometrical characterization of the species as a whole. Larson (1997), in his study on the taxonomical status of Panthera onca, discusses the lowermost inuence of a lack of normally distributed samples in multivariate analysis results. Principal component analysis (PCA) was performed using standardized measurements of the individuals all together. The principal component eigenvalue indicates the variance that it accounts for out of the total variance (Manly, 1994; Mcgarigal, Cushman & Stafford, 2000), so the components with lesser eigenvalues were discarded. The contributions of the original measurements and FIs to the principal components (PCs) are indicated by their coefficients. The PCs were interpreted according to the associated skull measurements and species PC scores. Species were also compared through univariate statistical analyses. The PC scores, the original measure-
ments, FIs, and ratios between skull measurements and the condylobasal length (CBL) were tested by analysis of variance (ANOVA) or Kruskal-Wallis nonparametric ANOVA by ranks. The post hoc tests to these analyses were Tukey HSD and Dunn, respectively (Sokal & Rohlf, 1995). Mann-Whitneys U test were also used to pairwise comparisons. Parametric or non-parametric methods were used regarding frequency distribution, homogeneity of variances among groups, and sample sizes. Parametric or nonparametric methods were also used for frequency distribution, homogeneity of variances among groups, and sample sizes. The maximum prey weight (MPW) was inferred from the body mass of the largest species captured (not scavenged). Prey species with no reference to body mass had their weights averaged from the general literature (Table 1) regarding special characteristics of the individuals killed (calves, yearlings, or females). In cases of very large prey species, the lowermost body weights were considered. Large prey killed from cooperative hunting was not included, and only species reported as having been captured by single individuals were accounted. The minimum weight was arbitrarily limited to 1 kg, even to those cat species with a diet described as rodents and birds. Therefore, MPW assumes that a given species of cat would be able to dispatch any sort of small prey, and, at least, the smaller individuals among the large prey. The ratio between MPW and the average weight of the respective cat species is a theoretical attempt to estimate their capture performance. Ratio values of around 1 indicate a similarity between MPW and cat mean weight. The MPW was used to discuss possible ecological and adaptive correlations with the morphofunctional patterns observed. Cat size categories followed Mattern & McLennan (2000): small (< 10 kg), medium (1140 kg), and large (> 40 kg). Principal component scores from morphofunctional analyses and predatorprey ratios (MPW/cat body mass) were used as continuous characters in phylogenetically independent contrasts analysis (Felsenstein, 1985). This was performed to eliminate the inuence of the evolutionary framework between the species, and to bring statistical independence to the study of the co-evolution of the skulljaw complex traits (Felsenstein, 1985, 2003). The main assumption of Felsensteins method is the stochastic evolution of a phenotypic trait, which can be described by the Brownian motion model. The variation of a given trait is normally distributed, and its variance is a function of the time of divergence and the expected variance of change (Felsenstein, 1985, 2003; Garland, Harvey & Ives, 1992). The expected variance of change was inferred from the divergence times between nodes based on Johnson
Table 1. Ratios between the maximum average prey weight (MPW) and body mass of the cat. The weights of cats were averaged from Guggisberg (1975), Heptner & Sludskii (1992), Nowak (1999), and Nowell & Jackson (1996). Prey weights were averaged from Nowak (1999), Hayssen et al. (1993), and Weigl (2005); exceptions are cited. References used to assess prey capture are listed for each cat species. Rodents and birds were arbitrarily dened as 1 kg. Eventually, more than one species was used to infer the prey sizes
Cat species Panthera onca Panthera leo Panthera Panthera pardus Panthera tigris Uncia uncia Neofelis nebulosa Oncifelis colocolo Oncifelis geoffroyi Ocelot Oncifelis guigna Leopardus pardalis Leopardus tigrinus Leopardus wiedii Puma concolor Puma Herpailurus yagouaroundi Acinonix jubatus Lynx canadensis Lynx Lynx pardinus Lynx lynx Lynx rufus Dom. cat Felis Felis Felis Felis chaus margarita nigripes silvestris Weight Prey species 105.7 185.0 59.0 185.5 50.0 19.5 2.4 4.0 2.3 13.6 2.3 3.3 67.5 4.8 53.5 11.2 11.5 23.0 11.2 7.3 2.4 2.2 5.5 17.0 13.4 MPW References Ratio 2.0 2.3 2.0 2.7 1.9 2.7 0.4 1.0 0.4 0.6 0.4 0.9 1.7 0.6 1.0 1.2 1.7 1.0 2.4 0.5 1.0 1.1 0.7 1.5 0.4
Tapirus terrestris, cattle 213.5 Schaller, 1983; Taber et al., 1997 Syncerus caffer, Giraffa 425.0 Ewer, 1973; Owen-Smith & Mills, 2008; camelopardalis Schaller, 1972 Rusa unicolor, Bos gaur (calves), 120.5 Karanth & Sunquist 1995, Mills 1984, Connochaetes sp. Owen-Smith & Mills 2008 Bos gaur 500.0 Karanth & Sunquist, 1995; Mazk, 1981 Capra ibex 92.5 Hemmer, 1972; Heptner & Sludskii, 1992 Sus barbatus, Rusa unicolor 52.0 Grassman et al., 2005; Rabinowitz et al., (calves ?), Axis porcinus 1987 Cavia sp. Myocastor coypus, Lepus capensis (exotic) Rodents and birds Agouti paca Cavia sp. Didelphis marsupialis Alces alces (calves and yearlings) Didelphis sp. Gazella thomsonii, Gazella granti, Aepycerus melampus Rangifer tarandus (calves and yearlings) Dama dama, Cervus elaphus (calves) Cap. capreolus, Rup. rupicapra, Cervus elaphus (calves) Odocoileus virginianus Lepus Lepus Lepus Lepus europaeus capensis tolai capensis europaeus 1.0 Bagno et al., 2004 4.0 Sousa & Bager, 2008 1.0 8.0 1.0 3.0 Sanderson et al., 2002 Emmons, 1987 Trigo, 2008 Oliveira, 1998a
115.6 Ross & Jalkotzy, 1996 3.0 Oliveira, 1998b 56.0 Hayward et al., 2006; Marker, 2002 13.3 Bergerud, 1983; Stephenson et al., 1991 19.0 Beltran et al., 1985 23.7 Jobin et al., 2000; Okarma et al., 1997 27.0 Labisky & Boulay, 1998 3.8 2.3 2.3 3.8 Heptner & Sludskii, 1992 Heptner & Sludskii, 1992 Sliwa, 1994 Bir et al., 2005; Tryjanowski et al., 2002
Caracal
Caracal caracal Leptailurus serval
Profelis aurata Otocolobus manul Leop. cat Prionailurus bengalensis Prionailurus planiceps Prionailurus viverrinus Prionailurus rubiginosus Bay cat Catopuma temminckii Catopuma badia Pardofelis marmorata
10.7 3.3 5.0 1.9 10.9 1.4 11.8 3.5 3.5
Redunca fulvorufula Lepus saxatilis, Thryonomys swinderianus, Cephalophus sp (fawn) Cephalophus callipygus Lepus capensis tolai Tragulus javanicus Fish, rodents, and small aquatic vertebrates Fish, molluscs, rodents, Axis axis (calves and yearlings) Rodents, birds, and domestic fowl Bubalus bubalis (calves) Rodents and birds (supposed) Rodents and birds
25.5 Mukherjee et al., 2004 4.8 Smithers, 1983; York, 1973
16.5 Ray & Sunquist, 2001 (prey weight: Noss, 1998) 2.3 Flux & Angermann, 1990; Heptner & Sludskii, 1992 1.5 Grassman et al., 2005 1.0 Muul & Lim, 1970 15.1 Nowell & Jackson, 1996; Pocock, 1939 1.0 Pocock, 1939 27.9 Sharma et al., 2004 1.0 Sunquist & Sunquist, 2002 1.0 Nowell & Jackson, 1996; Pocock, 1939
1.5 0.7 0.3 0.5 1.4 0.7 2.4 0.3 0.3
FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION et al.s (2006: supplement) phylogeny. Their cladogram was modied to accommodate the absence of Felis bieti, Oreailurus jacobitus, Neofelis diardi, and the unication of Felis silvestris lybica, Felis silvestris catus, and Felis silvestris silvestris, under the specic name Felis silvestris, as used in this study (Fig. 1). Correlation analyses were performed with PDAP v1.14 (Midford, Garland Jr. & Maddison, 2008) in MESQUITE v2.6 (Maddison & Maddison, 2009). The assumptions and statistical approach follow Felsenstein (1985, 2003) and Garland et al. (1992). The number of contrasts is the number of species minus one, and refers to the number of nodes on the phylogeny. Despite the gain on statistical analysis and evolutionary inference, the interpretation of the meaning of the contrast and its relation with the original trait value of each species is less intuitive. Contrasts show the variation between adjacent branches, and are weighed by the evolution rate (usually proportional to the divergence time between groups). Thus, according to the amount of difference on a given trait and evolution rate, contrast values could show expressive variation between sister groups. The standardized contrasts were regressed against the square root of the sum of corrected branch lengths (standard deviation of the contrast). Nonsignicant correlations indicate an adequate standardization, and suggest the phylogenetic independence of the obtained contrasts (Garland et al., 1992). Ordinary least-square (OLS) regression through the origin was performed using positivized contrasts versus contrast values to access the correlation between different traits (Garland et al., 1992).
the species scores were plotted over a Cartesian diagram, where the axes are the rst two PCs, according to its phylogenetic lineages (Fig. 3). The most negative scores are related to big panthers and the most positive ones belong to the tiny rusty-spotted cat (Prionailurus rubiginosus). The middle-sized species appear as a gradient along this axis. The size inuence is much lower in PC2, and distinctive morphological features could be identied among the species. The measurements mainly associated with PC2 were: anterior width across parietals, just behind the supraorbital process (POC) and the masseteric scar width (MSW), both with negative coefficients; and temporal fossa length (TFL), with a positive coefficient. PC2 is associated with the breadth of the anterior part of the braincase, masseter robustness, and the elongation of the posterior half of the skull (denoted by the length of the temporal fossa). The coefficient of POC was considerably higher than the others, indicating a leading role in the morphological aspect depicted by this PC. On the other hand, postorbital constriction is quite invariant between males and females in the 14 species tested in relation to the sexual dimorphism (Table 2). This fact could suggest a constrained pattern of this feature within each species, despite the importance of the postorbital constriction as a variant feature among species. PANTHERA LINEAGE: The PC1 scores (Fig. 4) reect the size superiority of the panthers among the felids (F7, 607 = 240.61, P < 0.0000001; Tukeys HSD test, P < 0.0001). Lions and tigers are the largest species, and the clouded leopard is the smallest one (F5, 118 = 138.30, P < 0.00001). There is no difference in the overall skull size between lions (Panthera leo) and tigers (Panthera tigris), and both are bigger than all of the other cat species (Tukeys HSD test, P < 0.001). The jaguar (Panthera onca) is the second biggest cat (P < 0.001), followed by leopards (Panthera pardus) and snow leopards (Uncia uncia), which are of the same size (P < 0.001). The PC2 scores denote a marked dichotomy between the elongated skull pattern of the clouded leopard (Neofelis nebulosa), with a narrow width of anterior portion of braincase, and the short and broad skull of U. uncia. The intermediate-sized panthers (P. onca and P. pardus) show a bias to the elongated/ narrow pattern, whereas the big panthers have more regular skulls. The PC2 scores indicate no signicant differences between lions and tigers (F5, 118 = 45.16, P < 0.00001; Tukeys HSD test, P > 0.18), regarding the skull measurements associated with the second principal component. This could be noted as an overall morphological similarity between the skulls of P. leo and P. tigris, despite the conspicuous features
RESULTS AND DISCUSSION MORPHOLOGICAL ANALYSES

Skull morphological variation according to sex was quite common among the cat species tested (Table 2), except for Herpailurus yagouaroundi and Prionailurus bengalensis, which showed no variation between sexes, and the bobcat (Lynx rufus), in which males and females differed only in occipital height (OCH). The sexual dimorphism on skull traits were interpreted as the main determinants of the bimodal distributions found in some species. The PCA coefficient matrix is presented in Table 3. The rst two PCs show the highest eigenvalues, and are associated with 99.5% of the total variation in the data. They were considered as the main descriptors of the Felidae morphology. All skull measurements are highly associated with PC1, and the species scores are consistent with size variations among cat species. Thus, the concept of size is strongly associated with PC1. The centroids of
Table 2. Sexual variation in the skull morphology among the best sampled cat species (n > 6)
Species 10 11 9 15 17 17 7 15 18 10 15 20 9 10 7 11 10 8 13 6 10 Puma Lynx Lynx Domestic cat Domestic cat Caracal Leopard cat 0.001 0.01 0.60 0.02 0.31 0.13 0.26 0.001 0.01 0.08 0.01 0.0001 0.03 0.45 0.001 0.01 0.13 0.01 0.0001 0.08 0.94 0.001 0.01 0.26 0.02 0.0001 0.10 0.36 0.001 0.01 0.41 0.01 0.001 0.19 0.07 0.001 0.01 0.13 0.01 0.0001 0.08 1.00 0.001 0.01 0.36 0.05 0.0001 0.03 0.33 0.001 0.001 0.23 0.03 0.0001 0.13 0.94 8 7 6 16 8 6 6 Panthera Panthera Ocelot Ocelot Ocelot Ocelot Puma 0.001 0.001 0.72 0.01 0.70 0.07 0.89 0.01 0.001 0.05 0.01 0.15 0.04 0.78 0.01 0.001 0.03 0.01 0.45 0.06 0.89 0.01 0.001 0.03 0.01 0.32 0.03 0.78 0.01 0.001 0.02 0.001 0.08 0.06 0.78 0.01 0.001 0.03 0.01 0.29 0.06 0.78 0.02 0.01 0.48 0.01 0.01 0.10 0.32 0.01 0.001 0.02 0.01 0.77 0.04 1.00
Total N Lineage BBC CBL CCL CM1L JHM1 JL JWM1 MB MFL 0.01 0.001 0.06 0.02 0.18 0.07 0.25 0.01 0.01 0.23 0.01 0.001 0.35 1.00
Males n
Females n
MMA 0.01 0.01 0.02 0.04 0.60 0.05 0.48 0.001 0.01 0.33 0.12 0.001 0.16 0.06
25 25 20 57 38 42 31
Panthera leo Panthera pardus Oncifelis geoffroyi Leopardus pardalis Leopardus tigrinus Leopardus wiedii Herpailurus yagouaroundi Puma concolor Lynx canadensis Lynx rufus Felis chaus Felis silvestris Leptailurus serval Prionailurus bengalensis
37 31 26 25 45 23 24
Species 10 11 9 15 17 17 7 15 18 10 15 20 9 10 7 11 10 8 13 6 10 Puma Lynx Lynx Domestic cat Domestic cat Caracal Leopard cat 0.001 0.01 0.26 0.01 0.001 0.29 0.50 0.01 0.06 0.94 0.04 0.05 0.56 0.26 0.001 0.0001 0.03 0.01 0.01 0.05 0.85 8 7 6 16 8 6 6 Panthera Panthera Ocelot Ocelot Ocelot Ocelot Puma 0.01 0.01 0.06 0.01 0.68 0.07 0.39 0.01 0.01 0.06 0.03 0.86 0.10 0.32 0.01 0.001 0.08 0.05 0.01 0.02 0.39
Total n Lineage MSL MSW OCH OPL 0.01 0.001 0.03 0.01 0.27 0.08 0.57
Males n
Females n
POC 0.07 0.62 0.16 0.64 0.64 0.31 0.15
RWP2 0.01 0.001 0.03 0.0001 0.02 0.08 0.48
TFL 0.01 0.001 0.03 0.01 0.02 0.01 0.67
TMA 0.001 0.001 0.03 0.01 0.03 0.03 0.67
TRL 0.01 0.001 0.02 0.001 0.12 0.03 0.48
ZIB 0.01 0.01 0.10 0.001 0.04 0.14 0.67
25 25 20 57 38 42 31
Panthera leo Panthera pardus Oncifelis geoffroyi Leopardus pardalis Leopardus tigrinus Leopardus wiedii Herpailurus yagouaroundi Puma concolor Lynx canadensis Lynx rufus Felis chaus Felis silvestris Leptailurus serval Prionailurus bengalensis
37 31 26 25 45 23 24
0.001 0.01 0.10 0.02 0.0001 0.01 0.29
0.19 0.79 0.82 0.87 0.12 0.13 0.15
0.001 0.01 0.55 0.02 0.001 0.03 0.60
0.001 0.01 0.33 0.05 0.001 0.02 0.60
0.001 0.01 0.10 0.01 0.0001 0.48 0.26
0.001 0.001 0.08 0.01 0.0001 0.01 0.55
0.001 0.01 0.50 0.02 0.0001 0.05 0.36
Bolded P-values are signicant according to Mann-Whitney U-test.
FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION

Table 3. Coefficients of the 20 skull measurements related to the rst two principal components Skull Measurements CBL TFL MSL MSW MB BBC POC ZIB OPL TRL OCH RWP2 JL TMA MMA CM1L CCL JHM1 JWM1 MFL Eigenvalue Cumulative Variation (%) *High-value coefficients. PC 1 -0.96* -0.98* -0.92* -0.92* -0.93* -0.99* -0.89* -0.95* -0.96* -0.94* -0.95* -0.95* -0.98* -0.95* -0.99* -0.97* -0.98* -0.92* -0.90* -0.92* 18.9 94.5% PC 2 0.07 0.12* -0.02 -0.20* 0.05 -0.03 -0.42* 0.01 0.01 0.05 0.03 -0.01 0.04 0.04 0.01 0.02 0.03 0.07 0.06 0.03 1.0 99.5%
exhibited by these species. However, this result takes into account the pooled within variance among the very diverse panther species. The direct comparison between the PC2 scores of P. leo and P. tigris indicates that they are clearly different (F1, 41 = 6.81, P < 0.01). The comparison of measurement ratios allowed for a better perception of the panthers skull design. For instance, U. uncia shows the largest postorbital constriction (POC/CBL, F5, 118 = 33.51, P < 0.00001; Tukeys HSD test, P < 0.001) among the panthers; N. nebulosa possesses the highest proportion of temporal fossa length (TFL/CBL, F5, 118 = 33.80, P < 0.00001; Tukeys HSD test, HSD test, P < 0.04). Panthera leo and P. onca equally show the largest ratios of height of jaw bone at M1 (JHM1/CBL, F5, 118 = 24.54, P < 0.00001; Tukeys HSD test, P < 0.04); whereas P. tigris exhibits the widest jaw bone at M1 (JWM1/CBL, F5, 118 = 13.14, P < 0.00001; Tukeys HSD test, P < 0.04). These two latter measurements are related to the robustness of the dental bone, and, together, they are indicative of the potential load that a jaw could resist during the bite. Comparisons between the Panthera lineage and other felids indicate that panthers have the smallest anterior temporal fossa length ratio (TFL/CBL, F7, 607 = 31.85, P < 0.000001; Tukeys HSD test,
P < 0.0001), and their mean value lies below the lower quartile value of the family Felidae. As a matter of fact, lions and snow leopards showed the smallest temporal fossa length ratios among almost all other felid species (TFL/CBL, H29, 606 = 292.93, P < 0.00001; Dunns test, P < 0.05, except for the cheetah, Acinonyx jubatus, P > 0.05). This denotes the allometry between the anterior and posterior halves of the skull among different sized cats. The panthers postorbital constriction was smaller (POC, F7, 607 = 90.87, P < 0.000001; Tukeys HSD test, P < 0.0001) than in all other felid groups. The high scores of panthers on PC2 are related to the synergy between these morphological features. Panthers also have the narrowest breadth of braincase (BBC/CBL, F7, 607 = 111.78, P < 0.00001; Tukeys HSD test, P < 0.0001), as well as the largest ratios of jaw height at M1 (F7, 607 = 66.59, P < 0.000001; Tukeys HSD test, P < 0.05) and jaw width at M1 (JWM1/CBL, F7, 607 = 52.89, P < 0.000001; Tukeys HSD test, P < 0.0001). They also present a higher coronoid process than all other lineages (TMA/CBL, F7, 607 = 63.94, P < 0.00001; Tukeys HSD test, P < 0.001), except for the bay cat group; however, it seems to be caused by the well-developed coronoid process of Pardofelis marmorata. The snout of panthers is generally longer than all other extant cats, and is denoted by the orbit to premaxillae length ratio (OPL/CBL, F7, 607 = 192.72, P < 0.00001; Tukeys HSD test, P < 0.0001), which means the values lie quite a bit above the familys upper quartile, as well as the tooth row length ratio (TRL/CBL). The panther skull could be summarized as a massive one, but with a relatively narrow postorbital constriction and a comparatively short temporal fossa length (related to the allometric effect of the elongated rostrum). Panthers also show a powerful jaw with robust dental bones, and thus with a high SMA to resist strong bending loads. Their longer rostrum provides a wide gape between the canines, and could be interpreted as an adaptation for hunting large prey. Clouded leopards (N. nebulosa) have one of the widest gapes during biting (Christiansen, 2006); nevertheless, they have a relatively short rostrum when compared with the other panthers (OPL/CBL, F5, 107 = 175.39, P < 0.000001; Tukeys HSD test, P < 0.0001). Christiansen (2006) pointed out the importance of the angle between the upper tooth row and the basicranial axis to the N. nebulosa wide bite gape. This anatomical arrangement could compensate their short rostrum. The elongated temporal fossa, associated with a narrow postorbital constriction, provides an extensive space for the origin of a powerful temporalis muscle in the clouded leopard skull. The small coronoid process of N. nebulosa is markedly
10
Figure 3. Distribution of the 34 cat species, according to their scores from the morphological principal component analysis (PCA). Plots represent species centroids based on bivariate means of the scores. Arrows indicate the enlargement of the skull measurements related to each axis. Acronyms are dened in the text.
allometric compared with P. onca, P. leo, and P. tigris (TMA/CBL, F5, 118 = 14.01, P < 0.000001; Tukeys HSD test, P < 0.001). Puma lineage: The PCA of morphometrical data showed a total divergence of skull patterns in this group (Fig. 5), but there is some skull size similarity between the puma (Puma concolor) and cheetah (A. jubatus). There are no signicant differences between these two species in 12 out of 20 skull measurements (CBL, MSW, BBC, ZIB, OCH, RWP2, JL, TMA, MMA, CCL, JHM1, and MFL) including the main axis of the skull (i.e. length, width, and height). Pumas show higher mean values on temporal fossa length (TFL, F1, 52 = 15.79, P < 0.001), mastoid breadth (MB, F1, 52 = 8.04, P < 0.01), tooth row length (TRL, F1, 52 = 14.7, P < 0.001), and jaw width at M1 (JWM1, F1, 52 = 9.44, P < 0.01) than cheetahs. On the other hand, cheetahs have higher mean values on masseteric scar length (MSL, F1, 52 = 4.06, P < 0.05), postor-
bital constriction breadth (POC, F1, 52 = 133.05, P < 0.000001), orbit to premaxillae length (OPL, F1, 52 = 10.14, P < 0.01), and condyle to M1 length of jaw (CM1L, F1, 52 = 11.29, P < 0.01) than pumas. Thus, the skulls of pumas and cheetahs are equivalent in size, and Herpailurus yagouaroundi is clearly the smallest species of this group. The PC2 scores indicate signicant shape differences among the three species (F2, 82 = 128.96, P < 0.00001). The conspicuous morphology of the skull of A. jubatus is marked by a broad postorbital constriction associated with a short temporal fossa. Cheetahs show the greatest postorbital constriction ratios among the big cats (> 40 kg) (POC/CBL, F7, 170 = 92.20, P < 0.00001; Tukeys HSD test, P < 0.02). Furthermore, the mean ratio of the zygomatic arches breadth (ZIB/CBL) of A. jubatus lies quite a bit above the upper quartile value of the felids as a whole. Cheetahs also exhibit a well-developed coronoid process (TMA/CBL, F26, 572 = 74.08, P < 0.00001; Tukeys HSD
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Figure 4. Morphological relationships between the members of the Panthera lineage. Species images are digitally adjusted and scaled according to the skull of Panthera leo, and are positioned over the centroids of their principal component analysis (PCA) scores. Arrows indicate the enlargement of the skull measurements related to each axis. Acronyms are dened in the text.
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Figure 5. Morphological relationships between the members of the Puma lineage. Species images are digitally adjusted and scaled according to the skull of Puma concolor, and are positioned over the centroids of their principal component analysis (PCA) scores. Arrows indicate the enlargement of the skull measurements related to each axis. Acronyms are dened in the text.
FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION test, P < 0.01), comparable with the ratios in lions, tigers, jaguars, and manul cats. However, cheetahs show the smallest ratios of temporal fossa length (F26, 572 = 29.57, P < 0.00001; Tukeys HSD test, P < 0.04, except in U. uncia). The hypertrophy of the transversal measurements of the skull (POC and ZIB) and the short temporal fossa contribute to give a broad and high-domed, but compact, look to the cheetahs head. The sinus frontalis in the skull of the big cats is usually located in the region described by the postorbital constriction. However, the sinus frontalis of A. jubatus is apomorphically placed forwards, across the supraorbital process (Salles, 1992), and without a direct topological homology with the measurement of postorbital constriction. Nevertheless, the skull anatomy of the cheetah suggests a widening of the entire frontal region, beginning from the anterior portion of the supraorbital processes up to the postorbital constriction. The open angle of the supraorbital processes also indicates the hypertrophy of this region of the skull. The wide postorbital constriction in the A. jubatus skull seems like a secondary effect of the general hypertrophy around the postorbital processes, and is associated with the development of the sinus frontalis. The small mandibular diastema in the tooth row of A. jubatus also contributes to compound the unique design of the cheetah skull. According to PC2, the development of the width of the masseteric scar (MSW) is also a marked feature of the cheetah skull. They have the highest ratios of MSW among the members of the Puma lineage (F2, 82 = 48.26, P < 0.00001; Tukeys HSD test, P < 0.02), and also among the big cats as a whole (F8, 200 = 48.60, P < 0.00001; Tukeys HSD test, P < 0.02). This denotes the particular importance of the masseter action on the cheetahs bite. Jaguarundis are the smallest species of the Puma lineage, with an elongated braincase (associated with the long TFL ratio), and an intermediate postorbital width, but with a relatively narrow masseteric scar at the zygomatic arch. Herpailurus yagouaroundi has a temporal fossa length ratio similar to P. concolor, and greater than in cheetahs (TFL/CBL, F2, 82 = 36.47, P < 0.000001; Tukeys HSD test, P < 0.001). Their postorbital constriction width is proportionally smaller than in A. jubatus (POC/CBL, F2, 82 = 94.72, P < 0.000001; Tukeys HSD test, P < 0.03), but is larger than in P. concolor (Tukeys HSD test, P < 0.001). They also have the smallest width of the masseteric scar of this lineage (MSW/CBL, F2, 82 = 48.26, P < 0.000001; Tukeys HSD test, P < 0.001). The species of the Puma lineage have the smallest ratios of mastoid breadth among the groups (MB/ CBL, F7, 607 = 21.35, P < 0.00001; Tukeys HSD test,
13
P < 0.03), except for the Caracal lineage. Puma, Caracal, and domestic cat lineage members exhibit the largest ratios of masseteric moment arm (MMA) among the groups (F7, 607 = 42.44, P < 0.00001). Likewise, the members of these three lineages show an elongated angular process, which is also associated with masseter muscle mechanics. Herpailurus yagouaroundi has one of the smallest ratios between jaw and skull lengths, besides Oncifelis colocolo, Oncifelis geoffroyi, Oncifelis guigna, Leopardus tigrinus, Leopardus wiedii, Prionailurus bengalensis, Prionailurus rubiginosus, and Prionailurus planiceps among the other felid species (JL/CBL, H29, 609 = 545.61, P < 0.00001; Dunns test P < 0.05). Low ratios between these measurements denote an elongated postorbital area of the skull. Thus, there is no generalized skull design among the members of the Puma lineage, and few features could be considered conspicuous to them. This fact reinforces the idea of three species with markedly derived skull patterns, despite of their phylogenetic closeness. Lynx lineage: The lynx morphotype is quite conspicuous, and the variation among the species is mainly related to size (Fig. 6). The Canada lynx (Lynx canadensis) and the bobcat (L. rufus) are signicantly different according to PC1 (F1, 55 = 9.86, P < 0.01). Despite the small sample, the average PC1 score of the Eurasian lynx (Lynx lynx) is, as expected, higher than the maximum values of both L. rufus and L. canadensis. Moreover, there is a similarity between the skull size of the Canadian and Iberian lynxes (L. canadensis and Lynx pardinus). There are no signicant differences between the PC2 scores of L. canadensis and L. rufus, and it is likely that the same should be valid for L. lynx. The Iberian lynx (L. pardinus) seems to have a broader skull than the others. The position of the lynxes according to PC2 (Fig. 3) is mostly a result of their developed postorbital constriction, the average ratio of which is near to the upper quartile of all felids. Lynx canadensis and L. rufus show similar or higher postorbital constriction ratios than 25 species (out of the 30 compared), being just smaller than the manul cat (Otocolobus manul), wild cat (Felis silvestris), and margay (Leopardus wiedii), F. silvestris, and L. wiedii (POC/CBL, F29, 579 = 121.81, P < 0.00001; Tukeys HSD test, P < 0.001). The analysis of other measurements brings additional information about the general lynx morphology. Lynxes have some of the widest zygomatic arches and mastoid process breadths among the felids (ZIB/CBL, F7, 607 = 29.00, P < 0.00001; Tukeys HSD test, P < 0.001; MB/CBL, F7, 607 = 21.34, P < 0.00001; Tukeys HSD test, P < 0.0001; exceptions are cited for
14
Figure 6. Morphological relationships between the members of the Lynx lineage. Species images are digitally adjusted and scaled according the skull of Lynx lynx, and are positioned over the centroids of their principal component analysis (PCA) scores. Arrows indicate the enlargement of the skull measurements related to each axis. Acronyms are dened in the text.
FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION the bay cat, domestic cat, and leopard cat lineages). However, the members of the Lynx lineage, besides the bay cat and leopard cat lineages, show some of the smallest lengths of the angular processes of the jaw (MMA), being just larger than the Ocelot lineage (MMA/CBL, F7, 607 = 42.44, P < 0.00001; Tukeys HSD test, P < 0.001). The lynx skull design could be summarized as being broad and robust, with a marked hypertrophy of the anterior portion of the braincase. Their jaw bones are not projected backwardly, and the angular processes are relatively short. Ocelot lineage: According with the PC1 scores (Fig. 7), Leopardus pardalis is the largest species (F5, 168 = 379.06, P < 0.000001; Tukeys HSD test, P < 0.0001), followed by similar intermediate-sized L. wiedii, O. colocolo, and O. geoffroyi (Tukeys HSD test, P < 0.01), and the smallest ones, L. tigrinus and O. guigna (Tukeys HSD test, P < 0.01). The PC2 depicts the marked difference in the skull morphology between two sister species: L. pardalis and L. wiedii. The conspicuous narrow postorbital constriction of L. pardalis contrasts with the broadheaded margay (L. wiedii). According to the postorbital constriction ratio, L. pardalis has the narrowest postorbital constriction among Ocelot lineage species (POC/CBL, F5, 168 = 141.55, P < 0.000001; Tukeys HSD test, P < 0.02). On the other hand, L. wiedii exhibits the higher ratio of this feature (Tukeys HSD test, P < 0.02). As a matter of fact, margays have the widest postorbital constriction in the absolute sense (POC, F5, 168 = 28.21, P < 0.000001; Tukeys HSD test, P < 0.001). On the other hand, the postorbital constriction of the medium-sized L. pardalis do not differ from the small O. colocolo. Leopardus wiedii also has the smallest ratio of temporal fossa length (TFL/CBL, F5, 168 = 18.50, P < 0.000001; Tukeys HSD test, P < 0.01), whereas the other species do not show differences from each other. Other distinctive skull features can be cited within the Neotropical small cats. Leopardus tigrinus has, proportionally, the narrowest skull across the zygomatic arcs (ZIB/CBL, F5, 168 = 15.74, P < 0.000001; Tukeys HSD test, P < 0.01). This species and L. wiedii exhibit equally the smallest ratios of the temporal moment arm (AMT/CBL, F5, 168 = 57.82, P < 0.000001; Tukeys HSD test, P < 0.0001). The genus Oncifelis shows a very consistent skull design, and no particular feature could be highlighted for any of its species. The comparison between Ocelot and domestic cat lineages (Fig. 3) which could be cited as equivalentsized counterparts of the Neotropical and Palearctic/ Ethiopian regions, respectively (PC1 scores, Mann Whitneys U = 6117.0, P = 0.08) denotes a marked
15
divergence of skull patterns between them, according to their PC2 scores (MannWhitneys U = 616.0, P = 0.00001). The small Neotropical cats showed higher ratios of temporal fossa length than the African and Eurasian small cats, indicating their elongate braincase behind the supraorbital process (TFL/CBL, F1, 247 = 9.30, P < 0.01). On the other hand, the postorbital width across the parietals of the members of the domestic cat lineage is wider than of the Ocelot lineage (POC/ CBL, F1, 247 = 82.87, P < 0.00001), which confers to them a broad constitution of the anterior region of the braincase. The same is true for the masseteric scar width, which is wider in the domestic cat lineage than in the small Neotropical cats (F1, 247 = 213.33, P < 0.00001). Both lineages showed a similarity between the measurements associated with jaw bone robustness (JHM1 and JWM1). This suggests an equivalent bending stress over the jaws of these cats during the bite. Ocelot lineage members also show smaller ratios on other skull measurements than the other cat lineages: jaw length (JL/CBL, F7, 607 = 26.97, P < 0.00001; Tukeys HSD test, P < 0.001), condyle to M1 length of jaw (CM1L/CBL, Tukeys HSD test, P < 0.01, except for the bay cat lineage P > 0.05), and canine length of jaw (CCL/CBL, Tukeys HSD test, P < 0.01). These measurements are three length descriptors on jaw bone, and, in this case, they indicate a short overall jaw length associated with an elongated skull (CBL). These Neotropical cats exhibited a short and narrow rostrum when compared with other lineages, according to their orbit to premaxillae length and rostral width at the second premolar (P2) ratios (OLP/CBL, F7, 607 = 162.71, P < 0.00001; Tukeys HSD test, P < 0.01, except for the bay cat and leopard cat lineages; RWP2, F7, 607 = 95.81, P < 0.00001; Tukeys HSD test, P < 0.0001, except for the bay cat lineage). Proportionally, their occipital height and coronoid process are some of the smallest among the felids (OCH/CBL, F7, 607 = 63.94, P < 0.00001; Tukeys HSD test, P < 0.0001, except for the Caracal lineage; AMT/CBL, F7, 607 = 63.94, P < 0.00001; Tukeys HSD test, P < 0.01). The features described above and the narrowness of the braincase contribute to the elongated, slender, and low-lined skull design of the members of the Ocelot lineage. Their rostrum is also markedly short, as indicated by the average ratio of orbit to premaxillae length (OPL/CBL), which is closer to the lower quartile of all felids. Domestic cat lineage: Felis chaus is clearly the larger species among the members of this lineage (PC1 scores, H2, 73 = 23.27, P < 0.00001; Dunns test P < 0.01). Accordingly, F. silvestris and Felis marga-
16
Figure 7. Morphological relationships between the members of the Ocelot lineage. Species images are digitally adjusted and scaled according the skull of Leopardus pardalis, and are positioned over the centroids of their principal component analysis (PCA) scores. Arrows indicate the enlargement of the skull measurements related to each axis. Acronyms are dened in the text.
FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION rita show no signicant size difference (Fig. 8). Felis nigripes (n = 2) was excluded from the univariate analysis, however, their average PC1 score falls outside of the 95% condence interval of F. silvestris and F. margarita, reecting their small size. Direct comparisons of measurements related to the three major skull axes (length, width, and height) represented by the condylobasal length (CBL), zygomatic arches internal breadth (ZIB), and occipital height (OCH) corroborate the multivariate analysis. Felis chaus has a longer (CBL) and higher (OCH) skull than the other two species (H2, 73 = 27.11, P < 0.0001; Dunns test P < 0.01 for F. silvestris and P < 0.05 for F. margarita; H2,73 = 30.43, P < 0.0001; Dunns test P < 0.01). There is no difference in the condylobasal length between F. silvestris and F. margarita. The zygomatic arches breadth (ZIB) of F. margarita is similar to F. chaus and to F. silvestris, but this feature was wider in F. chaus than in F. silvestris (H2, 73 = 9.12, P < 0.01; Dunns test P < 0.01). This suggests allometry of these skull traits in sand cats when compared with the larger-sized F. chaus. The ratio between the PC1 scores and average body mass of F. margarita is more than three times greater than the upper quartile limit of this ratio in the domestic cat lineage (H2, 73 = 50.25, P < 0.00001, Dunns test P < 0.01). Thus, there is marked allometry between the overall skull size and the body mass in sand cats, regarding the mean body weights of the other cats of this lineage (F. chaus ~7.3 kg, F. silvestris ~5.5 kg, and F. margarita ~2.4 kg, after Guggisberg, 1975; Heptner & Sludskii, 1992; Nowak, 1999; Sunquist & Sunquist, 2002). The skull-size/body-mass ratio of F. nigripes indicates they are more similar to the general headbody pattern of F. margarita, than to the other species of the domestic cat lineage. Nonparametric analysis of the PC2 scores indicated no signicant differences between F. chaus, F. margarita, and F. silvestris. However, these three species and F. nigripes are strongly associated with the negative part of the PC2 axis (Figs 3, 8), denoting a broad postorbital constriction width and shortened temporal fossa. Comparisons between domestic cat and leopard cat lineages (Fig. 9) indicate different morphological patterns in PC2 (F1, 130 = 145.28, P < 0.00001), despite the phylogenetic proximity between them. The members of the domestic cat lineage exhibited one of the highest ratios in both masseteric scar length and width among the felids (MSL/CBL, F7, 607 = 18.56, P < 0.00001; Tukeys HSD test, P < 0.03; MSW/CBL, F7, 607 = 60.93, P < 0.00001; Tukeys HSD test, P < 0.0001), being comparable only with the leopard cat lineage. These features are somewhat related to the development of the zygomatic arches. As a matter of fact, members of the domestic cat
17
lineage show a broad face, and the ratio of their zygomatic arches breadth (ZIB) to skull length is signicantly larger than in most species of other lineages (ZIB/CBL, F7, 607 = 29.0, P < 0.00001; Tukeys HSD test, P < 0.03, except for the bay cat and Lynx lineages). The domestic cat lineage members could be described as possessing a broad skull, with wide braincase and robust cheek bones, typically associated with the allocation of strong masseters. Actually, the ratios of the transversal distances across the skull of domestic cats, i.e. zygomatic arches internal breadth (ZIB), postorbital breadth (POC), breadth of braincase (BBC), and mastoid breadth (MB), are higher than the limits of upper quartiles for the whole felid family. The same is observed on the measurements of length and width of the masseteric scar at the zygomatic arch. Leopard cat lineage: The PC1 scores of the shing cat (Prionailurus viverrinus) are distinguishably higher than the values in the other species (H4, 48 = 41.24, P < 0.0001; Dunns test P < 0.01), except for O. manul (Fig. 9). The small rusty-spotted cat (Prionailurus rubiginosus) differed signicantly from the others species (Dunns test P < 0.05, except Prionailurus bengalensis), despite the limited number of specimens (n = 3). Otocolobus manul does not show signicant size dissimilarities from the at-headed cat (Prionailurus planiceps), despite the evident sagittal length difference between these two species. It suggests an unusual expression in PC1 of dissimilarities on the skull shape of O. manul, rather than simply size allometry between the species. Analysis of original measurements of the three main axes of the skull indicate signicant differences between these four species (CBL, H4, 48 = 34.78, P < 0.0001; ZIB, H4, 48 = 35.64, P < 0.0001; OCH, H4, 48 = 32.58, P < 0.0001). Prionailurus viverrinus showed the largest skull according to these three measurements (Dunns test P < 0.01), except for its internal breadth of the zygomatics, which is similar to that of the manul cat. The skull of O. manul is clearly shorter than P. viverrinus and P. planiceps (CBL, Dunns test P < 0.01); however, the three species present the same internal breadth of zygomatic arches (ZIB). The occipital height (OCH) of O. manul is similar to P. planiceps, but is smaller than P. viverrinus (Dunns test P < 0.05). Considering the breadths across the transversal plane of the braincase (POC and BBC), O. manuls postorbital constriction is broader than that of other leopard cat lineage species (H4, 48 = 37.28, P < 0.0001, Dunns test P < 0.01; except P. viverrinus, not signicant), as is its breadth of braincase (H4, 48 = 32.58, P < 0.0001, Dunns test P < 0.01; except P. viverrinus, not signicant). Thus,
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Figure 8. Morphological relationships between the members of the domestic cat lineage. Species images are digitally adjusted and scaled according the skull of Felis chaus, and are positioned over the centroids of their principal component analysis (PCA) scores. Arrows indicate the enlargement of the skull measurements related to each axis. Acronyms are dened in the text.
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Figure 9. Morphological relationships between the members of the leopard cat lineage. Species images are digitally adjusted and scaled according to the skull of Prionailurus viverrinus, and are positioned over the centroids of their principal component analysis (PCA) scores. Arrows indicate the enlargement of the skull measurements related to each axis. Acronyms are dened in the text.
20
F. L. SICURO and L. F. B. OLIVEIRA striction (both related to a more extensive origin area of the temporalis muscle). On the other hand, they show a distinctive low ratio of the MMA, being smaller than almost all felid species (MMA/CBL, H29, 609 = 335.89, P < 0.00001, Dunns test P < 0.05, except for L. wiedii and P. marmorata, not signicant.). These features suggest an increased importance of temporal mechanics (or reduced participation of masseter) in the bite of the at-headed cats. The members of the leopard cats group show a great diversity of skull designs, and therefore the connected (or partially connected) supra- and infrapostorbital processes remain the major similarity among them. Caracal lineage: The members of the Caracal lineage (Fig. 10) share a similar overall skull size according to the PC1 scores (H2, 40 = 5.68, P = 0.06). The PC2 scores indicate a slight difference between the three species (H2, 40 = 9.53, P < 0.01). Profelis aurata and Leptailurus serval show signicant differences (Dunns test P < 0.05), but neither differ from Caracal caracal. Nevertheless, the ratios of skull measurements associated with PC2 indicate differences between species in temporal fossa length (TFL/CBL, F2, 34 = 8.71, P < 0.0001) and postorbital constriction (POC/CBL, F2, 34 = 16.59, P < 0.000001). Profelis aurata shows the smallest postorbital constriction of the three species (Tukeys HSD test, P < 0.02 for C. caracal, and P < 0.001 for L. serval), and the temporal fossa of C. caracal is shorter than that of L. serval (Tukeys HSD test, P < 0.01). Compared with the other lineages, the Caracal members show a particularly narrow masseter muscle scar width for their skull size (MSW/CBL, F7, 607 = 60.93, P < 0.000001; Tukeys HSD test, P < 0.02; except for Panthera and bay cat lineages, P > 0.88). This characteristic is evinced by their positive scores on PC2. Aside of this, the skull design of Caracal lineage members is quite ordinary among other medium-sized cats. The species skulls are moderately elongated, but not markedly narrow across the zygomatic arches, and almost all skull measurement ratios of this lineage lie between the lower and upper quartiles of the other felids. Bay cat lineage: The small sample size of Catopuma badia hindered a more detailed morphological analysis (Fig. 11); even so, the Asiatic golden cat (Catopuma temminckii) is the largest species of this lineage when compared with the marbled cat (Pardofelis marmorata) (PC1 scores, MannWhitneys U = 0, P < 0.01). Both species, however, do not show differences in PC2 scores (MannWhitneys U = 17, P = 0.66). The
despite the short condylobasal length, the manul cat skull is markedly broad. This strong allometric pattern therefore demands a less straightforward reading of the rst PC than being merely indicative of size between the species. The PC2 denotes the presence of three subgroups, ranging from species with a wider postorbital constriction to those with a more elongated posterior half of the skull (H4, 48 = 30.99, P < 0.00001). Prionailurus planiceps differed from the other four species (Dunns P < 0.05), with a markedly elongated temporal fossa and narrow postorbital constriction. There is no signicant difference between the scores of P. viverrinus, P. bengalensis, and P. rubiginosus, and the most distinctive feature of these species is the elongated posterior half of the skull. The negative scores from O. manul were higher than all other species of this lineage (Dunns test P < 0.05) because of its broadshaped skull. The analysis of the leopard cat lineage pointed out two extreme allometric patterns among phylogenetically close species: O. manul and P. planiceps. The singular look of the skull of O. manul within the leopard cat lineage suggests a convergent pattern to the wide skulls of the members of the genus Felis. Thus, in some comparisons between Leopard cat and the other lineages, the manul cat (O. manul) was removed from the analyses. The other members of the leopard cat lineage have the shortest jaws among other cat lineages. This is denoted by their small ratios of jaw length and condyle to canine length (JL/CBL, F7, 601 = 99.98, P < 0.00001; Tukeys HSD test, P < 0.01; and CCL/ CBL, F7, 601 = 83.54, P < 0.00001; Tukeys HSD test, P < 0.001), except for the bay cat and Puma lineages. Low ratios between jaw and skull length are an indication of an elongated posterior portion of the skull behind the postorbital processes. Short jaws could limit the bite gape, but it also means a short out-force moment arm and an improvement on the mechanical efficiency of the jaw. The temporal fossa length ratio to skull length of Prionailurus species is higher than the limit of the upper quartile of the family Felidae. This confers to them an elongated prole on the posterior portion of the skull. Nevertheless, manul cats (O. manul) also have an elongated temporal fossa, but their broad skull confers to them a distinctive bulky head. The ratios of features related to the transversal plane of their skull, such as the postorbital constriction (POC), breadth of braincase (BBC), zygomatic arches internal breadth (ZIB), and mastoid breadth (MB), are quite a bit higher than the limits of the upper quartile of these measurements for the Felidae family. The skull of the at-headed cat (P. planiceps) has a developed temporal crest and narrow postorbital con-
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Figure 10. Morphological relationships between the members of the Caracal lineage. Species images are digitally adjusted and scaled according to the skull of Profelis aurata, and are positioned over the centroids of their principal component analysis (PCA) scores. Arrows indicate the enlargement of the skull measurements related to each axis. Acronyms are dened in the text.
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Figure 11. Morphological relationships between the members of the bay cat lineage. Species images are digitally adjusted and scaled according to the skull of Catopuma temminckii, and are positioned over the centroids of their principal component analysis (PCA) scores. Arrows indicate the enlargement of the skull measurements related to each axis. Acronyms are dened in the text.

Table 4. Coefficients of the force indexes related to the rst two principal components Force-indexes CFTC CFMC AHN Eigenvalue Cumulative Variation (%) *High-value coefficients. PC1 -0.96* -0.96* -0.96* 2.87 95.7% PC2 0.19* -0.17* -0.13* 0.10 98.9%
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PC2 score value of the single specimen of C. badia lies completely outside the quartile range of the other two species, and it indicates the hypertrophy of the postorbital width. It also denotes the morphological differences and the size allometry between the sister taxa (C. badia and C. temminckii). The temporal fossa length and postorbital constriction ratios of the Asiatic golden cat are smaller than those of the marbled cat (TFL/CBL, MannWhitneys U = 1, P < 0.02; POC/CBL, U = 1, P < 0.02), but they have similar masseteric scar width ratios (MSW/ CBL). The bay cat (C. badia) ratios of postorbital constriction, masseteric scar width, and temporal fossa lie above the upper quartile of the ratios of these measurements for C. temminckii and P. marmorata. Bay cat lineage members could be described as having an elongated skull with a well-developed occipital region. Indeed, the temporal fossa length and mastoid breadth ratios of this lineage lie above the values of the upper quartiles of these measurements of the family.
FUNCTIONAL
ANALYSES
The coefficient matrix of the PCA based on the FIs is presented in Table 4. The rst two PCs were associated with 98.9% of the total variation. The FIs of both the temporalis (CFTC) and the masseter muscles (CFMC), and the attachment area of headneck muscular system (AHN), are highly correlated with PC1, suggesting the association between skull size and bite force. The PC1 could be easily labelled as bite strength and neck muscle robustness. The second PC shows a meaningful difference between the two major indicators of jaw muscles mechanics. PC2 could be labelled as contribution of the temporalis and masseter mechanical systems to the nal bite force or as the inuence of the skull design to the jaw muscles performance. The centroids of the species scores were plotted over a Cartesian diagram, where the axes are the rst two PCs (PC1 and PC2). The species are presented according to their phylogenetic lineages (Fig. 12).
Panthera lineage: Panthers, as expected, have the most powerful bite and neck robustness among felids (Fig. 13). Lions (P. leo) and tigers (P. tigris) show a similar nal bite force, with both of them being more powerful than all other cats (H26, 599 = 563.97, P < 0.0001, Dunns test P < 0.01). A bite strength gradient is observed on other panthers, with an obvious correlation to their skull and body sizes. Leopards (P. pardus) and snow leopards (U. uncia) show a similar efficiency on jaw occlusion (Dunns test P > 0.05), despite their skull shape differences. Lions and tigers share an overall similarity in skull morphology and size, and have the same potential for strong bites at the canines. However, according to PC2, the jaw occlusion of P. leo is greatly inuenced by the action of the masseteric complex, which is quite different from that of P. tigris (F5, 118 = 57.97, P < 0.0001; Tukeys HSD test, P < 0.001). Tigers (P. tigris) show the same pattern in jaw occlusion that is observed in jaguars (P. onca), leopards (P. pardus), and snow leopards (U. uncia). All these species display a smaller contribution of the masseteric muscle system to the bite than that observed in lions (P. leo). On the other hand, the jaw occlusion of clouded leopards is deeply marked by the mechanical system of the temporalis muscle (PC2 scores, Tukeys HSD test, P < 0.001), and the participation of the masseteric complex is much less substantial than that observed in other panthers. The coronoid process of the toothy N. nebulosa is one of the smallest among panthers, and, in some sense, resembles the trend observed in the sabertoothed Machairodontinae, and is related to the demands of a wide bite gape (see Christiansen, 2006). Despite the importance of the size of the coronoid (in-force moment arm) to the temporalis mechanics, there are other skull features involved that are crucial to the performance of this muscle. Clouded leopards show the largest temporal fossa length ratio to skull length as well as the smallest postorbital constriction ratio among the panthers (TFL/CBL, F5, 118 = 33.80, P < 0.00001; Tukeys HSD test, P < 0.01; POC/CBL, F5, 118 = 33.51, P < 0.00001; Tukeys HSD test, P < 0.03). These two features dene the limits of the origin of the temporalis muscle in the skull. Thus, the large temporal fossa and the small postorbital constriction of the clouded leopards indicate the presence of a robust temporalis muscle. This provides a great temporal system in force, and compensates for the small coronoid process in the equation of static equilibrium. Furthermore, the short coronoid process of N. nebulosa forms an angle of 90 with the line of action of the temporalis muscle during the wide gape, which maximizes the leverage of this muscle. These observations bring additional support to Christians-
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Figure 12. Distribution of the 34 cat species, according to their scores from the functional principal component analysis (PCA). Plots represent species centroids based on bivariate means of the scores. The abscissa arrow indicates the bite performance and the area of neck muscles, and ordinate arrows describe the mechanical optimization of the jaw muscles. Acronyms are dened in the text.
ens (2006) proposal for an adaptative convergence between clouded leopards and saber-toothed cats in relation to wide bite gapes. Puma lineage: The bite force and neck robustness of P. concolor do not differ from those of A. jubatus (PC1 scores, H2, 85 = 59.43, P < 0.001, Dunns test P > 0.05), with both species being superior to H. yagouaroundi (Dunns test P < 0.01), Fig. 14. The PC2 scores indicate a similarity in jaw mechanics between the sister species P. concolor and H. yagouaroundi (H2, 85 = 23.60, P < 0.00001, Dunns test P > 0.05), and both show a slight optimization of the masseter muscle system during the bite. Pumas and cheetahs show similarities in overall skull size (Fig. 5), in spite of differences in body mass (average weight: P. concolor = 67.5 kg; A. jubatus = 53.5 kg; Guggisberg, 1975). However, the nal bite force of A. jubatus is deeply inuenced by
the action of the masseteric complex (PC2 scores, Dunns test P < 0.01). The analyses of the raw values of the FIs, however, indicate a similarity in the action of the masseter muscle between pumas and cheetahs (CFMC, F2, 82 = 489.90, Tukeys HSD test, P > 0.05), but the cheetahs temporalis muscle FI is signicantly lower than that of the puma (CFTC, F2, 82 = 327.80, Tukeys HSD test, P < 0.02). The short temporal fossa length and the broad postorbital constriction of A. jubatus reduce the available origin area of the temporalis muscle in the skull, and it may decrease its mechanical performance. The conspicuous A. jubatus skull design magnies the importance of the masseteric system on their jaw mechanics. The inuence of the masseter muscular complex is remarkable in the Puma lineage, despite the skull design differences among the three species. This is particularly dramatic in A. jubatus, in which the
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Figure 13. Morphofunctional relationships between the members of the Panthera lineage. Species images are digitally adjusted and scaled according to the skull of Panthera leo, and are positioned over the centroids of their principal component analysis (PCA) scores. Arrows indicate bite force and neck robustness (abscissa), and jaw muscle optimization (ordinate). Acronyms are dened in the text.
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Figure 14. Morphofunctional relationships between the members of the Puma lineage. Species images are digitally adjusted and scaled according to the skull of Puma concolor, and are positioned over the centroids of their principal component analysis (PCA) scores. Arrows indicate bite force and neck robustness (abscissa), and jaw muscle optimization (ordinate). Acronyms are dened in the text.
FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION temporal mechanics are compromised by the reduction of the origin area of this muscle in the skull. The distinguished elongated angular processes (masseteric in-force arm), present in the members of the lineage, could also contribute to the masseteric optimization of bite mechanics. Lynx lineage: The potential bite force and neck robustness of lynxes are consistent with cats of their size (Fig. 15). Despite the small samples of L. pardinus, its scores lie inside the 95% condence limits of L. rufus and L. canadensis. The Canada lynx shows higher potential related to the bite strength and neck robustness than the bobcat (F1, 55 = 5.38, P < 0.03), even though their Maximum Average Prey Weight (MPW) used to be smaller than that associated with L. rufus (Table 1). The mean PC1 scores of the two specimens of L. lynx lie outside the 95% condence limits of L. canadensis. This denotes a strong bite force for the Eurasian lynx, which would be congruent with their skull and body sizes. According to PC2, the skulls of all lynx species do not show any marked maximization concerning the action of the temporalis and masseter muscles. Nevertheless, the mean scores values of the two individuals of L. lynx are higher than the upper quartile of L. canadensis and L. rufus. This could indicate a difference on the masticatory pattern of the Eurasian lynx, and thus a lesser inuence of the masseteric system. The opposite is observed on the Iberian lynx (L. pardinus), the PC2 score of which lies bellow the lower quartile of the other lynx scores. This could be interpreted as a possible higher inuence of the masseteric system to nal bite force in L. pardinus than in other lynxes. Ocelot lineage: The morphofunctional analysis of medium-sized L. pardalis indicates a stronger bite and tougher neck than other cats of this lineage (F5, 168 = 321.76, P < 0.00001, Tukeys HSD test, P < 0.0001, except L. geoffroyi, not signicant), the opposite is valid for the small L. tigrinus and O. guigna (Fig. 16). The second PC, however, indicates the presence of different bite patterns along this lineage, and therefore variations on the contribution of temporal and masseteric mechanical systems. Kodkods (O. guigna) show an intermediate skull morphofunctional pattern, and their scores do not differ signicantly from the other species of this lineage. Comparison of ratios between temporalis and masseter muscle FIs indicates a similar higher optimization of masseteric mechanics on margays (L. wiedii) and oncillas (L. tigrinus) than on other cats of this lineage (CFTC/CFMC, F5, 168 = 52.58, Tukeys HSD test, P < 0.01, except on O. guigna, not signicant). On
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the other hand, comparatively, L. pardalis, O. colocolo, and O. geoffroyi show skull designs equally less favourable for the action of the masseteric system (CFTC/ CFMC, Tukeys HSD test, P > 0.07). Some skull features could be highlighted as the main factors in the difference on jaw functionality among Neotropical small cats. The coronoid process (temporalis muscle moment arm) of L. tigrinus and L. wiedii, for instance, are some of the smallest among all cat species analysed regarding the skull length (AMT/CBL, H29, 608 = 463.47, Dunns test P < 0.05; except for H. yagouaroundi and P. planiceps). Furthermore, the oncillas (L. tigrinus) have the narrowest internal breadth of zygomatic arches among the Ocelot lineage (ZIB/CBL, F5, 168 = 15.74, Tukeys HSD test, P < 0.01), which means a limited space for the temporalis muscle in the skull. Margays (L. wiedii) have a well-developed zygomatic arches breadth, but their short temporal fossa length and hypertrophied braincase also reduces the space for the temporalis muscle. These skull designs compromise the performance of the temporal system in both species. Nevertheless, the skull pattern of the Ocelot lineage as a whole suggests a bite action less inuenced by the masseteric mechanical system, in spite of a slight optimization of this muscle in some species. Domestic cat lineage: The bite strength and neck toughness of Eurasian and African small cats (Fig. 17) are greater than those of their Neotropical relatives of the Ocelot lineage, excluding the mediumsized L. pardalis (PC1 scores, MannWhitneys U = 2043.0, P < 0.00001). The PC2 scores of the Felis lineage, however, indicate an increased inuence of the masseter mechanics on the jaw occlusion process. This is corroborated by the comparison of ratios of the temporalis FIs and masseter FIs between the domestic cat and Ocelot lineages (CFTC/CFMC, F1, 190 = 9.88, P < 0.01). The two lineages do not show differences in temporalis FIs (CFTC, F1, 190 = 1.81, P > 0.05), but they do differ in the masseter FIs (CFMC, F1, 190 = 77.81, P < 0.000001). Thus, Felis skull design has a marked increment in masseter mechanics performance, when they are compared with the same-sized Neotropical small cats. Felis species show some improvements in skull features directly associated with masseteric optimization that are not present in the Ocelot lineage: masseteric moment arm (MMA, F1, 190 = 124.73, P < 0.000001), masseteric scar length (MSL, F1, 190 = 208.66, P < 0.000001), and masseter muscle scar width (MSW, F1, 190 = 164.23, P < 0.000001). Although there are similarities in overall size and ecology of Neotropical and Eurasian/African small cats, the evolution of jaw mechanics in both lineages
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Figure 15. Morphofunctional relationships between the members of the Lynx lineage. Species images are digitally adjusted and scaled according to the skull of Lynx lynx, and are positioned over the centroids of their principal component analysis (PCA) scores. Arrows indicate bite force and neck robustness (abscissa), and jaw muscle optimization (ordinate). Acronyms are dened in the text.
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Figure 16. Morphofunctional relationships between the members of the Ocelot lineage. Species images are digitally adjusted and scaled according to the skull of Leopardus pardalis, and are positioned over the centroids of their principal component analysis (PCA) scores. Arrows indicate bite force and neck robustness (abscissa), and jaw muscle optimization (ordinate). Acronyms are dened in the text.
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Figure 17. Morphofunctional relationships between the members of the domestic cat lineage. Species images are digitally adjusted and scaled according to the skull of Felis chaus, and are positioned over the centroids of their principal component analysis (PCA) scores. Arrows indicate bite force and neck robustness (abscissa), and jaw muscle optimization (ordinate). Acronyms are dened in the text.
FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION seems to have followed divergent trends. The masseteric mechanical advantage in the Felis skull guarantees a superior bite force for these species than that estimated for the Neotropical small cats. Leopard cat lineage: The variation in the estimated bite forces along PC1 (Fig. 18) reects the wide range of body sizes, from the small rusty-spotted cat (P. rubiginosus, average weight 1.4 kg) to the mediumsized shing cat (P. viverrinus, average weight 10.9 kg). The at-headed cat (P. planiceps) shows an unusually strong bite force and neck robustness for a felid of its small body size (~1.9 kg), suggesting morphofunctional allometry. Comparison of raw values of temporalis muscle FIs denotes the powerful bite of P. planiceps in relation to other larger cats of this lineage (CFTC, H4, 48 = 33.12, P < 0.0001). Prionailurus planiceps presents higher temporalis FIs than P. bengalensis (Dunns test P < 0.01), and similar FIs to those of O. manul and the medium-sized P. viverrinus. The at-headed cat (P. planiceps) exhibits a lower masseter muscle FI than O. manul (CFMC, H4, 48 = 31.75, P < 0.0001, Dunns test P < 0.01) and P. viverrinus (Dunns test P < 0.01), but comparable with P. bengalensis. As a matter of fact, the temporal FI of P. planiceps is higher than that of some same-sized small cat species such as O. guigna, L. tigrinus, and L. wiedii (H20, 434 = 441.41, P < 0.00001; Dunns test P < 0.01), but is comparable with medium-sized cats, such as C. caracal, Lep. serval, Ly. canadensis, and Ly. rufus. The PC2 scores indicate an overall optimization of the temporalis muscle mechanical system among the members of the leopard cat lineage. The PC2 scores of manul cats (O. manul) denote a slight maximization of the masseteric system. Nevertheless, in spite of the broad face with developed zygomatic arches, O. manul does not show any marked inuence of the masseteric mechanical system. The hypertrophy of the zygomatic arches seems to counterbalance the reduction of the space of the temporalis muscle, because of the wide postorbital constriction. Flat-headed cats show a marked maximization of the temporal action, and possess a unique skull design that is distinct from the other members of this lineage. Their masseteric mechanical system seems to have the lowermost inuence in bite strength. One of the most distinctive features of at-headed cats, for instance, is the small ratio to the skull length of masseter MMA, the value of which lies quite below the lower quartile limit of the Felidae. The functional effect of this is a small in-force momentum to the masseter muscle mechanics in this species. Muul & Lim (1970) associated the habit of these cats of seizing slippery prey (e.g. shes) to some anatomical
31
traits, such as parallel toothrows, developed rst and second upper premolars, and a pronounced rostrum. The authors also describe the at-headed cat as possessing short legs, permanent partially exposed claws, and an overall mustelid-like look. Sunquist & Sunquist (2002) pointed out that P. planiceps possesses great biting power, based on the well-developed sagittal crest and strong zygomatic arches. The morphofunctional analysis corroborates the statement that skull design contributes to the powerful bite of P. planiceps; however, it seems much more associated with the temporal mechanics than with the masseteric system or development of zygomatic arches. Caracal lineage: The skull design of P. aurata indicates a stronger bite force and neck robustness than in L. serval (PC1 scores, H2, 37 = 9.33, P < 0.01, Dunns test P < 0.05); however, both species do not differ from C. caracal (Fig. 19). There is no difference among the three species according to the PC2 scores (H2, 37 = 5.59, P > 0.06), mostly because of the considerable intraspecic variation found in the specimens of C. caracal, P. aurata, and L. serval. Thus, despite the size and shape variations, no signicant difference on jaw functionality was found among the Caracal lineage members. The skull design of the Caracal lineage does not show any remarkable improvement to the masseteric mechanics. In agreement with this result, one feature was highlighted in the morphological analysis as been conspicuous to them: their masseter muscle scar width is one of the smallest among other cats. This denotes less robustness in the masseteric complex and a bite action that is associated more with the temporalis muscle mechanics. Bay cat lineage: The medium-sized Asian golden cat (C. temminckii) presents superiority in bite strength and neck robustness over the marbled cat (P. marmorata), according to PC1 (MannWhitneys U = 0.0, P < 0.01; Fig. 20). The potential bite performance of the bay cat (C. badia) suggested by the analysis is consistent with its small-sized skull. The PC2 scores of P. marmorata indicate the marked optimization of its temporalis muscle mechanical system (MannWhitneys U = 2.0, P < 0.02). Accordingly, they show a high coronoid process, an elongated temporal fossa, and wide zygomatic arches, the ratios of which lie quite a bit above the upper quartile values of the family Felidae. The coronoid process is the in-force lever-arm of the temporalis muscle, and the following two traits are indicators of the anatomical limits of this muscle origin area. The PC2 score of the single specimen of the Bornean bay cat (C. badia) is three times smaller
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Figure 18. Morphofunctional relationships between the members of the leopard cat lineage. Species images are digitally adjusted and scaled according to the skull of Prionailurus viverrinus, and are positioned over the centroids of their principal component analysis (PCA) scores. Arrows indicate bite force and neck robustness (abscissa), and jaw muscle optimization (ordinate). Acronyms are dened in the text.
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Figure 19. Morphofunctional relationships between the members of the Caracal lineage. Species images are digitally adjusted and scaled according to the skull of Profelis aurata, and are positioned over the centroids of their principal component analysis (PCA) scores. Arrows indicate bite force and neck robustness (abscissa), and jaw muscle optimization (ordinate). Acronyms are dened in the text.
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Figure 20. Morphofunctional relationships between the members of the bay cat lineage. Species images are digitally adjusted and scaled according to the skull of Catopuma temminckii, and are positioned over the centroids of their principal component analysis (PCA) scores. Arrows indicate bite force and neck robustness (abscissa), and jaw muscle optimization (ordinate). Acronyms are dened in the text.
FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION than the lower quartile limit of this lineage. It indicates a high inuence of the masseteric mechanical system on the jaw occlusion of the bay cat, and denotes a diverging trend from its sister species, the Asian golden cat (C. temminckii). Comparisons between P. marmorata and C. temminckii indicate the superiority of the Asian golden cat in both the masseter FI (CFMC, MannWhitneys U = 0, P < 0.01) and the estimated area of neck musculature (AHN, MannWhitneys U = 0, P < 0.01). However, there are no signicant differences in the raw values of temporal FI between these two species (CFTC, MannWhitneys U = 7, P > 0.05). The body mass and skull volume differences are remarkable between the small marbled cat (P. marmorata) and the medium-sized Asian golden cat (C. temminckii) (Fig. 11; Table 1). The similarity in the temporal FI observed in these two cats indicates a morphofunctional allometry in the P. marmorata skull, and corroborates the mechanical maximization of their temporalis muscle.
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PHYLOGENETIC
INDEPENDENT CONTRASTS
Contrasts were obtained from the rst two PC scores of both morphological and functional analyses, as well as the MPW ratios (Table 1). Each contrast was regressed against its respective standard deviation (square root of the sum of corrected branch lengths) and no signicant correlations were found. Pearsons correlation coefficient (R) values were usually lower than 0.20 (F1, 31 = 1.62, P > 0.22). The absence of correlation between the contrasts and their standard deviations indicates an adequate independence and standardization of the traits (Diaz-Uriarte & Garland, 1996; Diaz-Uriarte & Garland, 1998; Garland et al., 1992). The positivized contrast of the trait Skull Overall Size (PC1 in the morphological analysis) was used as an independent variable in OLS regressions against skull morphology (morphological PC2), bite force (functional PC1), jaw muscle optimization (functional PC2), and prey/predator weight ratio (MPW/cat average weight). Bite force positivized contrast was regressed against jaw muscle optimization and prey/ predator weight ratio. Finally, the positivized contrast on the independent variable jaw muscle optimization was regressed against prey/predator weight ratio. Contrasts from the OLS regression corroborate the already high correlation expected between the skull size and bite force (R = 0.91, F1, 32 = 151.66, P < 0.000001; Fig. 21). Nevertheless, there is no signicant correlation between the contrasts in skull size and skull morphology (R = 0.17, F1, 32 = 0.96, P > 0.34), as well as with the mechanical congura-
tion of how the bite is produced (R = 0.05, F1, 32 = 0.08, P > 0.76; Fig. 22). These ndings indicate a nonassociative evolutionary process between the skull size variation and morphological differentiation, i.e. cat skull design evolution goes beyond mere size allometry. Accordingly, cat skull size evolution is not correlated with the jaw lever system optimization and mechanics. There is also no correlation between bite force and jaw muscle optimization (R = -0.25, F1, 32 = 2.14, P > 0.15; Fig. 23), suggesting that differences in the individual contributions of temporalis and masseter muscles do not affect the nal bite force. This means that bite strength among the cat species did not evolve as a function of how the resultant in force is generated by the jaw muscles. On the other hand, the muscular functionality during the bite is correlated with the evolution of the skull design (R = 0.77, F1, 32 = 45.53, P < 0.0001). A signicant correlation is observed on the regression between contrasts of prey/predator weight ratio and overall skull size (R = -0.41, F1, 32 = 6.37, P < 0.02). This result indicates an evolutionary dependence between the size variation of cat species and their selection of prey size and diet (Fig. 24). The same is observed in the correlation between contrasts in the bite force and the prey/predator weight ratio (R = -0.45, F1, 32 = 8.17, P < 0.01) (Fig. 25). Among sister groups, small contrast values in bite force and high values in the MPW ratio indicate a big variation in the maximum prey weight, despite the similar potential bite strength. This is the case in the Lynx and Caracal lineages. Sister groups with high contrast values in bite force but small contrasts in MPW ratio are usually those with greater size variation, but with some isometry between prey/cat weights among the species (i.e. similar MPW ratios between the sister taxa). This could be observed in some clades in the Ocelot, Puma, and Panthera lineages. In some clades, great contrasts in bite force and also in the MPW ratios denote an expressive variation in the cat size and/or bite force, and very different ratios between the cat body mass and the prey selected (e.g. some members of bay cat, leopard cat, and Ocelot lineages). The domestic cat lineage seems to be the most consistent group: small variation in bite force contrasts and in MPW ratios. The small Eurasian/African cats differ from the Ocelot lineage mostly because the contrast between the medium-sized L. pardalis and its sister species, the small L. wiedii. Nevertheless, among clades with medium- and large-sized species (e.g. Lynx, Caracal, Puma, bay cat, Panthera lineages), the variation seems to be greater than in those composed of small cats. The prey size is very constrained by bite force in small cats. In medium- to large-sized cat lineages, the
36
Figure 21. Ordinary least-square (OLS) regressions between standardized contrasts in bite force and the positivized standardized contrasts in skull size. Plots indicate the nodes and lineages of the phylogeny. Nodes connecting different cat lineages are indicated by the age of cladogenesis (Myr), according the cladogram of Johnson et al. (2006) presented in Figure 1.
body mass or bite force are not constraining factors for the capture of bigger prey, and so the dietary spectrum is much more diverse among the sister species. Modern big cats prey on both small and large prey, and food items could virtually range from insects to large mammals. Finally, prey/predator weight ratio is not correlated with how the bite is performed at the muscular level (Fig. 26). Regression between contrasts in prey/ predator ratio and in jaw muscle optimization shows no signicant correlation (R = -0.04, F1, 32 = 0.06, P > 0.81). It suggests the low adaptative importance of how the bite is executed by the jaw muscle groups among cat species, and raises the supposition that the variations in bite patterns may have originated from casuistic phenotypic uctuations xed along the speciation process. Accordingly, it would be reasonable to interpret both temporal and masseteric jaw muscular systems
as a single unity that evolved along the lineages, where selection acts over the maximization of bite strength, rather than the design variation itself; therefore, muscular group optimizations would be a consequence of the skull design phenotypic uctuations, and the maintenance of a powerful bite remains the leading evolutionary trend.
CONCLUSION
Dispersal and sympatric evolution are the main factors associated with modern cats speciation in the past 10 million years (Salles, 1992; Johnson & OBrien, 1997; Turner & Antn, 1997; Johnson et al., 2006). Despite the similarity in general physical and behavioral characteristics, felids show a notorious size variation among species. Size differences between phylogenetically closely related species are usually interpreted as an evolutionary attempt to reduce the
37
Figure 22. Ordinary least-square (OLS) regressions between standardized contrasts in jaw muscle optimization and the positivized standardized contrasts in skull size. Plots indicate the nodes and lineages of the phylogeny. Nodes connecting different cat lineages are indicated by the age of cladogenesis (Myr), according the cladogram of Johnson et al. (2006) presented in Figure 1.
niche overlap as a result of character displacement or size assortment (Dayan & Simberloff, 1994; Dayan & Simberloff, 1998; Dayan et al., 1990; Losos, 1990, 2000; Schluter, 2000; Dayan & Simberloff, 2005). The origins of this selective pressure are variable. Interspecic killing in carnivores, for instance, is related to body size and diet overlap, and is usually found among those species with similar behaviour and/or phylogenetic closeness (Donadio & Buskirk, 2006). On the other hand, if there is a size gap in the niche spectrum, selective pressure will act, favouring size diversication of small or large organisms in order to ll the gap (Bonner & Horn, 2000). Whatever the main pressure for size diversication among cats, it is an example of minor inuence of an allometric size change to the performance of a complex mechanical system, such as the jaw movement. Therefore, the diversity of extant felids suggests morphological variation along the size axis,
rather than a character displacement related to the classical ecomorphological binomial: skulljaw design versus dietary preferences. Unexpectedly, the variations in the performance of jaw muscles are not correlated with their predatory performance and/or prey choice. Furthermore, contrasts analysis does not indicate a clear adaptative correlation between different patterns of jaw mechanics and size evolution among the cat species. According to the data presented, only skull size and bite force show a correlation with prey/predator weight ratio. Regardless of some remarkable exceptions (e.g. the Lynx and bay cat lineages), the direct association big catsstronger bitesfewer constraints in prey selection is the leading pattern, but even so, the relation between size and shape changes is not necessarily a linear function (see Koehl, 2000). The casuistic nature of morphofunctional variation could be exemplied by the comparison between the
38
Figure 23. Ordinary least-square (OLS) regressions between standardized contrasts in jaw muscle optimization and the positivized standardized contrasts in bite force. Plots indicate the nodes and lineages of the phylogeny. Nodes connecting different cat lineages are indicated by the age of cladogenesis (Myr), according the cladogram after Johnson et al. (2006) presented on Figure 1.
domestic cat and Ocelot lineages. The diet of all small cats worldwide is composed of rodents and other small vertebrates, and the general predation strategy is the same. Despite this, small cats from the Neotropics (genera Leopardus and Oncifelis) show a slender skull with a narrower braincase and postorbital constriction than African and Eurasian small cats. In contrast to the Neotropical small cats, the bite mechanics in the African and Eurasian small cats shows a marked participation of the masseteric complex. Nevertheless, there is no reason to suppose that any advantage in prey capturing performance in either lineage results from these different functional trends. More likely these divergent patterns seem to be caused not by an adaptative process, but from the xation of phenotypic variations along the natural history of these two lineages, independently. The same logic could be used to explain the functional differences in P. leo and P. tigris, where despite
having a comparably powerful bite the optimized participation of the masseteric muscular complex in the lions bite is evident. The inuence of different hunting strategies (e.g. cooperative hunting), however, was not included in the analysis, and its possible inuences could not be assessed by the model. The radiation of the different skull designs and functional performances are more likely to have followed a Brownian model of evolution, than to have resulted from an ecomorphological t to ll a specic niche. Therefore, size and bite force are the main sources of variation and niche differentiation among cats. On the other hand, the variation in the breadth of the postorbital constriction is remarkable among felids (but quite constant among sexes of the same species), ranging from the broad state found in cheetahs (A. jubatus) to the narrow state found in
39
Figure 24. Ordinary least-square (OLS) regressions between standardized contrasts in the ratios of maximum prey weight (MPW)/cat average weight and the positivized standardized contrasts in skull size. Plots indicate the nodes and lineages of the phylogeny. Nodes connecting different cat lineages are indicated by the age of cladogenesis (Myr), according the cladogram of Johnson et al. (2006) presented in Figure 1.
clouded leopards (N. nebulosa), for instance. The importance of this feature is highlighted in both the morphological and the functional analyses. The postorbital constriction is directly related to the space available for the temporal muscle, and, consequently, is related to the functional differences among cat species. ORegan (2002), studying the skull morphology of big cats, also observed an association of the postorbital indicators with the detached position of A. jubatus. However, the selective pressures that lead to the allometry of this feature are controversial. Salles (1992) demonstrated the close relationship between the hypertrophied frontal, postorbital processes, and postorbital constriction, and the sinus frontalis space, among the cat species. The position of the frontal sinus of A. jubatus lies centralized in the region of the postorbital process, being the largest among cats.
The vascular surface of this well-developed sinus frontalis (as well as other paranasal cavities) would heat and moisten inhaled air before it ows to the lungs (Rae & Koppe, 2004). On the other hand, the ow of cold air would involve heat transfer from the bloodstream, and, together with the evaporation of moisture on the surface of the sinus, would act as a vascular mechanism for brain cooling (Rae & Koppe, 2004). Certainly, these functional aspects would be useful for a fast running cat in semi-arid regions. The body temperature of cheetahs at the end of a sprint is close to 41 C (Hildebrand, 1959; Taylor & Rowntree, 1973), and a large frontal sinus with a developed vascular surface could also perform an important role in preventing dangerous heating of the brain. This marked hypertrophied frontal sinus is conspicuous along the cheetah evolutionary lineage (Christiansen & Mazk, 2009). A phylogenetic contrast analyses between frontal sinus and limb adaptations for fast
40
Figure 25. Ordinary least-square (OLS) regressions between standardized contrasts in the ratios of maximum prey weight (MPW)/cat average weight and the positivized standardized contrasts in bite force. Plots indicate the nodes and lineages of the phylogeny. Nodes connecting different cat lineages are indicated by the age of cladogenesis (Myr), according the cladogram of Johnson et al. (2006) presented in Figure 1.
running, as well as their paleodistribution, should be addressed to enlighten a possible coevolution of these traits along the cheetah lineage. The overall bite performance of cheetahs, however, is not compromised by these skull modications, once the masseteric system compensates for the less favoured temporal mechanics. Therefore, variations in a given trait are compensated for by variation in others, and the overall adaptative efficiency of cat jaw mechanics is preserved. The basic hunting strategy of cats includes the functional performance of skulljaw and limbclaw systems, as well as complex behavioural displays. These different sets could be interpreted as a single predatory functional unit. Thus, some changes in the pattern of the bite mechanics are less relevant to a full-scale ecomorphological scenario. A quantitative approach to Felidae limb biomechanics, despite the scarcity of specimens, would result in a better
understanding of cat predatory behaviour, and could provide new insights into the interpretation of evolutionary ecomorphological trends.
ACKNOWLEDGEMENTS
This study has taken a long time to prepare, and many people contributed to its development. We would like to express our gratitude to Ronaldo Fernandes, Leandro R. Monteiro, Leslie Marcus (in memoriam), and P. David Polly for their suggestions regarding the analytical approach used to analyse the data. We thank the curators and museum staff who granted us access to the felid collections in their care: Joo A. de Oliveira and Leandro O. Salles (Museu Nacional, Federal University of Rio de Janeiro); Mario de Vivo (Museu de Zoologia of University of So Paulo); Ross MacPhee and Robert Voss (American Museum of Natural History), and Bruce Patterson
41
Figure 26. Ordinary least-square (OLS) regressions between standardized contrasts in the ratios of maximum prey weight (MPW)/cat average weight and the positivized standardized contrasts in jaw muscle optimization. Plots indicate the nodes and lineages of the phylogeny. Nodes connecting different cat lineages are indicated by the age of cladogenesis (Myr), according the cladogram of Johnson et al. (2006) presented in Figure 1.
and William Stanley (Field Museum of Natural History). Unfortunately, most of the original photographs of specimens were lost; this fumble, however, led us to contact people whose kindness and scientic collaborative sense allowed us to replace the images of all species we have worked on. Therefore, we would like to express our gratitude to the authors of photographs, institutions, and to all that courteously allowed us to reproduce images of specimens to illustrate this study. We credit them, as follows: Ashley Gosselin-Ildari, Pamela Owen and Timothy Rowe (Digimorph.org/University of Texas at Austin, USA) for images of Neofelis nebulosa, Panthera pardus (lateral view), and Felis silvestris lybica (lateral view); Elena I. Zholnerovskaya (Siberian Museum of Zoology, Russia) for images of Panthera pardus (dorsal view), Felis margarita (skull and jaw originally separated), and Felis silvestris lybica (dorsal
view); Igor Y. Pavlinov and Olga Nanova (Moscow Museum of Zoology, Russia) for images of Uncia uncia, Otocolobus manul, Felis chaus, and Lynx lynx; Mammalian Crania Photographic Archive of the Department of Anatomy Dokkyo Medical University, Japan (http://1kai.dokkyomed.ac.jp) for images of Oncifelis geoffroyi (dorsal view) and Leptailurus serval (dorsal view); Marcelo Weksler (American Museum of Natural History, USA) for images of Catopuma temminckii, Pardofelis marmorata, Profelis aurata (dorsal view), and Felis nigripes; Fabio O. do Nascimento (Museu de Zoologia of University of So Paulo, Brazil) for images of Oncifelis geoffroyi (lateral view); Jos Cabot (Estacin Biologica de Doana, Spain) for images of Lynx pardinus; Jos Luis Brito (Museo Municipal de Ciencias Naturales e Arqueologa de San Antonio, Chile) for images of Oncifelis guigna (lateral view); Bruce Patterson (Field Museum of Natural History, USA) for images of
42

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Oncifelis guigna (dorsal view), Catopuma badia, and Prionailurus rubiginosus (skull and jaw originally separated); Vu Ngoc Thanh (Zoology Museum of Vietnam National University) for images of Prionailurus bengalensis; Emmanuel Gilissen and Wim Wendelen (Africamuseum, Belgian) for images of Leptailurus serval (lateral view) and Profelis aurata (lateral view); Georges Lenglet (Royal Belgian Institute of Natural Sciences) for images of Prionailurus viverrinus and Prionailurus planiceps; and Nico Avenant (National Museum of Bloemfontein, South Africa) for images of Caracal caracal. Many of those cited above have sent us several images not included in the nal form of this work. We extend our gratitude to James P. Dines (Natural History Museum of Los Angeles County, USA), Louise Tomsett (Natural History Museum, UK), and Lucas Thibedi (Amathole Museum, South Africa) who sent us many images of skulls of rare cats not included in this paper, but that helped us to assemble a precious source of qualitative morphological information. Teresa R. Gaskill, Aki Ohnuki, and Ronaldo Fernandes provided helpful revisions of the manuscript. We also thank Eliete Bouskela and the staff of BioVasc, University of the State of Rio de Janeiro, for all their support. This research was supported by the Brazilian National Council to Scientic and Technological Development (CNPq) and the American Museum of Natural History Grant Program.
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APPENDIX 1
Skull measurement Breadth of braincase Condylobasal length Acronym BBC CBL Description The widest point across parietals From the anterior edge of the premaxillae to the posteriormost projection of the occipital condyle it is an estimator correlated with specimen size From the posterior margin of the alveolus of the canine to the posteriormost edge of the jaw condyle it measures the resistance moment arm when an animal is biting with canine teeth From the anterior margin of the alveolus of M1 to the posteriormost edge of the jaw condyle it measures the resistance moment arm when an animal is biting at the lower carnassial molar Measured about the midpoint of the dentary between M1 and P4 From the anterior limit of the dentary bone between I1 to the posterior end of the jaw condyle it is another estimator correlated with specimen size Measured near the point of JHM1 it estimates the cross section of dentary bone and the second moment of area of jaw (SMA) From the lateral limit of the jaw condyle to the anterior limit of the masseteric fossa in the dentary it is a complementary estimator of masseter muscle length From the dorsal surface of the condyle to the ventral border of the angular process it estimates the moment arm of this muscle
Condyle to canine length of jaw
CCL
Condyle to M1 length of jaw
CM1L
Jaw height at M1 Jaw length
JHM1 JL
Jaw width at M1
JWM1
Masseteric fossa length
MFL
Masseteric moment arm
MMA
46
APPENDIX 1 Continued
Skull measurement Masseteric scar length Acronym MSL Description Measured on the ventral face of the zygomatic arch, from the anterior limit of the muscle scar in the jugal to the anterior end of the glenoid fossa (temporomandibular fossa) The widest point of the masseteric scar in the jugal bone it is an estimator, with anterior measurement, of the area of cross section of the masseter muscle Greatest width of skull including the mastoids it is an estimator, with the anterior measurement, of the attachment area of the headneck muscular system (AHN) From the ventral border of foramen magnus to the lowest limit of the middle of the complex muscle scar From the anterior end of the premaxilla to the anterior orbit rim it indicates the length of the rostrum The shortest distance across the top of the skull posterior to the postorbital process Width between external limits of maxillary bones about P2, indicates robustness of rostrum From the posteriormost point of the temporal fossa to the supraorbital process it is an estimator of the temporalis muscle size From the posterior end of the condyle to the apex of the coronoid process it estimates the moment arm of the temporalis muscle From the anterior end of I1 to the posterior end of M1, both near the alveolus it estimates the functional bite space The largest distance between the inner margins of the zygomatic arches, with two anterior measurements it estimates the temporalis muscle width (TMW)
Masseteric scar width
MSW
Mastoid breadth
MB
Occipital height Orbit to premaxillae length Postorbital constriction Rostral width at the second premolar P2 Temporal fossa length
OCH OPL POC RWP2 TFL
Temporalis muscle moment arm Tooth row length Zygomatic arches internal breadth
TMA
TRL ZIB
SKULL
MEASUREMENTS VARIABLES
DERIVED
Variable Temporalis muscle width Force index of masseter muscle at canines Force index of temporalis muscle at canines Second moment of area of dentary bone at M1 Corrected force index of masseter muscle at canines Corrected force index of temporalis muscle at canines Attachment area of headneck muscular system
Acronym TMW FMC FTC SMA CFMC CFTC AHN
Equation {ZIB - [(BBC + POC)/2]}/2 {[(MSW + MFL)/2 MSL]1/2 MMA}/CCL [(TFL TMW)1/2 TMA]/CCL {[p (JWM1/2) (JWM1/2)3]/4}1/4 (SMA FMC)1/2 (SMA FTC)1/2 (OCH MB)1/2
APPENDIX 2
LIST
OF MEASURED SPECIMENS
Abbreviations: AMNH, American Museum of Natural History, USA; FMNH, Field Museum of Natural History, USA; MN, Museu Nacional, Brazil; MZUSP, Museu de Zoologia of University of So Paulo, Brazil; , male (m); , female (f); ?, no data record (nd). Acinonyx jubatus (n = 17: m = 7, f = 3, nd = 7): AMNH 119656, 161139, ; AMNH 35998, ?; AMNH 35997, ?; AMNH 27897, ; AMNH 119657, ; AMNH 114517, ?; AMNH ; AMNH 119655, ; AMNH 36426, ?; AMNH
FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION 100309, ; FMNH 29633, 39475, ?; FMNH 29634, . ; FMNH 29635, ; FMNH 89918, ?; FMNH 34589,
47
; FMNH 26900, ?; FMNH
Caracal caracal (n = 9: m = 2, f = 4, nd = 3): AMNH 89841, ?; AMNH 24220, ?; AMNH 116512, ; AMNH 187788, ; AMNH 113794, ; FMNH 32945, ; FMNH 105607, ; FMNH 135042, ?; FMNH 95922, . Catopuma badia (n = 1: nd = 1): FMNH 8378, ?. Catopuma temminckii (n = 7: m = 3, f = 3, nd = 1): AMNH 84396, ; AMNH 84394, 84395, ; AMNH 17103, ; FMNH 75826, ; FMNH 89919, ?. ; AMNH 84393, ; AMNH
Felis chaus (n = 25: m = 15, f = 8, nd = 2): AMNH 171166, ; AMNH 238649, ; AMNH 184683, ; AMNH 54553, ; AMNH 163169, ?; AMNH 54759, ?; FMNH 84811, ; FMNH 105559, ; FMNH 94103, ; FMNH 104412, ; FMNH 105558, ; FMNH 114385, ; FMNH 104413, ; FMNH 97866, ; FMNH 97864, ; FMNH 99027, ; FMNH 99026, ; FMNH 91256, ; FMNH 29754, ; FMNH 83100, ; FMNH 29789, ; FMNH 29755, ; FMNH 29753, ; FMNH 91252, ; FMNH 91257, . Felis margarita (n = 3: m = 2, f = 1): FMNH 107299, ; FMNH 60613, ; FMNH 127296, .
Felis nigripes (n = 2: nd = 2): AMNH 214380, ?; AMNH 214381, ?. Felis silvestris (n = 45: m = 20, f = 13, nd = 12): AMNH 80893, ?; AMNH 169458, ; FMNH 107294, ; FMNH 106749, ; FMNH 107295, ; FMNH 123384, ; FMNH 95877, ; FMNH 95878, ; FMNH 98740, ; FMNH 101877, ?; FMNH 140228, ?; FMNH 105529, ?; FMNH 107296, ?; FMNH 123383, ; FMNH 57696, ; FMNH 104579, ; FMNH 104712, ; FMNH 104719, ; FMNH 104720, ; FMNH 96260, ; FMNH 104005, ; FMNH 98755, ?; FMNH 38197, ?; FMNH 97872, ; FMNH 112453, ; AMNH 160967, ; AMNH 83634, ?; AMNH 51970, ; AMNH 185173, ; AMNH 89007, ?; AMNH 161125, ?; AMNH 116519, ?; AMNH 81233, ; AMNH 179132, ; AMNH 179131, ; AMNH 179134, ; AMNH 187787, ; AMNH 187785, ; AMNH 187786, ; AMNH 55851, ; AMNH 82404, ; AMNH 82410, ; AMNH 51971, ; AMNH 161769, ?; AMNH 185173, . Herpailurus yagouaroundi (n = 31: m = 7, f = 6, nd = 18): MN 24885, ; MN 24901, ; MN 33513, ?; MN 1039, ?; MN 3142, ?; MN 3153, ?; MN 49076, ?; MN 49316, ?; MN 384, ?; MZUSP 5176, ; MZUSP 5175, ; MZUSP 13481, ?; MZUSP 3692, ?; MZUSP 13606, ; MZUSP 13598, ; MZUSP 13607, ; MZUSP 2647, ; MZUSP 2441, ?; MZUSP 1272, ; MZUSP 7351, ; MZUSP 1648, ?; MZUSP 3800, ?; MZUSP 7203, ?; MZUSP 2916, ; MZUSP 2978, ; MZUSP 7388, ; MZUSP 2031, ?; MZUSP 1399, ?; MZUSP 37, ?; MZUSP 1003, ?; MZUSP 1647, ? Leopardus pardalis (n = 57: m = 15, f = 16, nd = 26): MN 4812, ; MN 4811, ; MN 7630, ?; MN 625, ?; MN 624, ?; MN 622, ?; MN 25691, ?; MN 24883, ?; MN 24882, ?; MN 24881, ?; MN 48873, ?; MN 48874, ?; MN 48875, ?; MN 48877, ?; MN 48880, ?; MN 48894, ; MZUSP 11472, ?; MZUSP 5553, ; MZUSP 13595, ?; MZUSP 13470, ?; MZUSP 20427, ; MZUSP 2733, ; MZUSP 3070, ; MZUSP 3069, ; MZUSP 4232, ; MZUSP 4239, ; MZUSP 7027, ; MZUSP 13673, ; MZUSP 8879, ?; MZUSP 3113, ; MZUSP 2964, ; MZUSP 2963, ; MZUSP 9422, ; MZUSP 9414, ?; MZUSP 1167, ?; MZUSP 2914, ; MZUSP 2913, ; MZUSP 2968, ; MZUSP 2966, ; MZUSP 2931, ?; MZUSP 10354, ?; MZUSP 1937, ?; MZUSP 2962, ; MZUSP 2967, ; MZUSP 9423, ; MZUSP 9684, ; MZUSP 9012, ; MZUSP 1936, ; MZUSP 1805, ; MZUSP 6277, ?; MZUSP 2839, ; MZUSP 9615, ; MZUSP 2465, ; MZUSP 2467, ; MZUSP 440, ?; MZUSP 11825, ?; MZUSP 13601, ?. Leopardus tigrinus (n = 38: m = 17, f = 8, nd = 13): MN 24894, ; MN 6693, ; MN 3133, ?; MN 24896, ?; MN 5885, ; MN 25651, ; MN 25650, ; MN 7261, ; MN 5145, ?; MN 610, ?; MN 49356, ; MN 49354, ?; MZUSP 2810, ; MZUSP 2646, ; MZUSP 1877, ; MZUSP 1393, ?; MZUSP 2362, ?; MZUSP 6262, ; MZUSP 2321, ; MZUSP 1395, ?; MZUSP 2320, ; MZUSP 3299, ; MZUSP 1878, ; MZUSP 1168, ?; MZUSP 6728, ; MZUSP 22416, ?; MZUSP 2971, ; MZUSP 3811, ?; MZUSP 401, ; MZUSP 13796, ; MZUSP 810, ; MZUSP 396, ; MZUSP 6549, ?; AMNH 80396, ; AMNH 34349, ; AMNH 181498, ; AMNH 33896, ?; AMNH 69166, .
48
Leopardus wiedii (n = 42: m = 17, f = 6, nd = 19): MN 6084, ; MN 5114, ?; MN 25725, ; MN 4816, ; MN 5621, ; MN 24910, ?; MN 24887, ?; MN 24890, ; MN 24886, ; MN 25726, ; MZUSP 34, ; MZUSP 10426, ; MZUSP 28311, ?; MZUSP 5561, ; MZUSP 2645, ; MZUSP 5562, ; MZUSP 5560, ; MZUSP 2644, ?; MZUSP 3503, ; MZUSP 1936, ?; MZUSP 2969, ; MZUSP 2915, ; MZUSP 2686, ?; MZUSP 1169, ?; MZUSP 19906, ; MZUSP 6649, ; MZUSP 467, ?; MZUSP 468, ; MZUSP 9998, ?; MZUSP 2840, ; MZUSP 2242, ; MZUSP 1765, ?; MZUSP 1677, ; MZUSP 1764, ?; MZUSP 2901, ; MZUSP 1398, ?; MZUSP 1397, ?; MZUSP 1400, ?; MZUSP 1649, ?; MZUSP 40, ?; MZUSP 22413, ?; MZUSP 22414, ?. Leptailurus serval (n = 23: m = 9, f = 6, nd = 8): AMNH 119872, ?; AMNH 81672, ?; AMNH 81674, 85166, ?; AMNH 27837, ; AMNH 34767, ; AMNH 36369, ; AMNH 51984, ; AMNH 88382, 18956, ; FMNH 29629, ; FMNH 29632, ?; FMNH 79415, ; FMNH 127844, ; FMNH 127843, 93309, ; FMNH 93310, ; FMNH 27165, ; FMNH 27164, ; FMNH 18862, ; FMNH 38191, 90022, ; FMNH 38192, ?. ?; AMNH ?; FMNH ; FMNH ?; FMNH
Lynx canadensis (n = 31: m = 18, f = 11, nd = 2): MN 49353, ?; MZUSP PL898, ; MZUSP PL899, ; MZUSP PL910, ; MZUSP PL918, ; MZUSP PL924, ?; AMNH 239791, ; AMNH 239784, ; AMNH 239788, ; AMNH 239786, ; AMNH 239783, ; AMNH 239797, ; AMNH 239793, ; AMNH 239792, ; AMNH 239795, ; AMNH 239798, ; AMNH 239799, ; AMNH 239800, ; AMNH 239801, ; AMNH 239802, ; AMNH 239804, ; AMNH 239805, ; AMNH 239806, ; AMNH 239807, ; AMNH 239808, ; AMNH 239809, ; AMNH 239764, ; AMNH 29048, ; AMNH 29037, ; AMNH 239769, ; AMNH 239757, . Lynx lynx (n = 2: m = 1, nd = 1): AMNH 41337, ?; FMNH 51820, Lynx pardinus (n = 1: m = 1): AMNH 169482, . .
Lynx rufus (n = 26: m = 10, f = 10, nd = 6): MN 49355, ; AMNH 1344, ; AMNH 1352, ; AMNH 2245, ; AMNH 5512, ?; AMNH 6420, ; AMNH 144930, ; AMNH 144932, ; AMNH 31765, ; AMNH 24664, ; AMNH 24666, ; AMNH 24066, ; AMNH 24067, ; AMNH 255666, ; AMNH 255671, ; AMNH 255663, ; AMNH 255670, ; AMNH 189301, ?; AMNH 214941, ?; AMNH 148937, ; AMNH 128527, ?; AMNH 11060, ; AMNH 237993, ?; AMNH 164480, ?; AMNH 164720, ; AMNH 2443, . Neofelis nebulosa (n = 9: m = 3, f = 2, nd = 4): AMNH 184931, ?; AMNH 22919, ?; AMNH 35808, ; AMNH 35273, ; AMNH 19383, ?; AMNH 22916, ; FMNH 75830, ; FMNH 42583, ; FMNH 75831, ?. Oncifelis colocolo (n = 11: m = 9, f = 2): MZUSP 13671, ; MZUSP 7786, ; AMNH 189394, ; AMNH 16695, ; AMNH 133977, ; AMNH 243110, ; FMNH 80994, ; FMNH 52488, ; FMNH 43291, . ; AMNH 76150, ; FMNH 68318,
Oncifelis geoffroyi (n = 20: m = 9, f = 6, nd = 5): MZUSP 1432, ?; MZUSP 1443, ?; MZUSP 111, ?; MZUSP 110, ?; AMNH 205904, ; AMNH 205903, ; AMNH 205905, ; AMNH 205907, ; AMNH 205908, ; AMNH 205909, ; AMNH 205910, ; AMNH 205911, ; AMNH 205913, ; AMNH 205914, ; AMNH 39010, ; AMNH 39004, ; AMNH 80298, ?; AMNH 16696, ; FMNH 28404, ; FMNH 24360, . Oncifelis guigna (n = 6: nd = 6): MZUSP 43, 24359, ; FMNH 24417, . ; AMNH 33283, ; AMNH 33285, ; AMNH 93323, ; FMNH
Otocolobus manul (n = 6: m = 1, f = 3, nd = 2): AMNH 180268, ?; AMNH 185371, ?; FMNH 60734, 125386, ; FMNH 135319, ; FMNH 135737, .
; FMNH
Panthera leo (n = 25: m = 10, f = 8, nd = 7): AMNH 80609, ; AMNH 83617, ; AMNH 83620, ; AMNH 83618, ; AMNH 161003, ; AMNH 161011, ; AMNH 81836, ?; AMNH 28151, ; AMNH 81837, ; AMNH 169463, ?; AMNH 17274, ?; AMNH 52073, ; AMNH 83410, ?; AMNH 52074, ; AMNH 52077, ; AMNH 52078, ; AMNH 52082, ; AMNH 30241, ; AMNH 30242, ; AMNH 30244, ?; AMNH 30245, ?; AMNH 30247, ?; AMNH 85141, ; AMNH 85144, ; AMNH 54996, . Panthera onca (n = 40: m = 9, f = 4, nd = 27): MN 1007, ?; MN 634, ?; MN 633, ?; MN 1013, ?; MN 1017, ?; MN 1021, ?; MN 3349, ?; MN 1023, ?; MN 13508, ?; MN 24861, ?; MN 36218, ?; MN 48868, ?; MN 48869, ?; MN
49
48870, ?; MN 48871, ?; MN 32707, ; MN 32705, ?; MN 24860, ; MN 6021, ; MN 628, ?; MZUSP 22452, ?; MZUSP 469, ; MZUSP 2332, ?; MZUSP NP 1, ?; MZUSP 13600, ?; MZUSP 3752, ; MZUSP 17550, ?; MZUSP 11844, ?; MZUSP 11843, ?; MZUSP 3685, ; MZUSP 3330, ?; MZUSP 19853, ?; MZUSP 11469, ?; MZUSP 6806, ; MZUSP 2330, ; MZUSP 7161, ; MZUSP 3420, ; MZUSP 2551, ; MZUSP 3331, ; MUZUSP 28869, . Panthera pardus (n = 25: m = 11, f = 7, nd = 7): AMNH 167357, ?; AMNH 170293, ?; AMNH 170296, ?; 170301, ?; AMNH 170297, ?; AMNH 170298, ?; AMNH 52010, ; AMNH 52012, ; AMNH 52006, ; 52009, ; AMNH 52013, ; AMNH 52023, ; AMNH 52024, ; AMNH 52039, ; AMNH 60774, ?; 47864, ; AMNH 90017, ; AMNH 57008, ; AMNH 54854, ; AMNH 81006, ; AMNH 52041, ; 34745, ; AMNH 34746, ; AMNH 89009, ; AMNH 165112, . AMNH AMNH AMNH AMNH
Panthera tigris (n = 18: m = 8, f = 4, nd = 6): AMNH 85396, ; AMNH 85405, ; AMNH 45519, ; AMNH 45520, ?; AMNH 85404, ; AMNH 60771, ?; AMNH 201798, ; AMNH 61, ?; AMNH 90016, ?; AMNH 119680, ?; AMNH 113743, ; AMNH 113744, ; AMNH 54459, ; AMNH 54458, ; AMNH 54460, ; FMNH 31153, ; FMNH 31798, ?; FMNH 31152, . Pardofelis marmorata (n = 4: m = 3, f = 1): AMNH 102844, 60358, . ; AMNH 106615, ; FMNH 68728, ; FMNH
Prionailurus bengalensis (n = 24: m = 10, f = 10, nd = 4): AMNH 35327, ; AMNH 163609, ; AMNH 87351, ; AMNH 87355, ; AMNH 55564, ?; AMNH 83999, ; AMNH 84398, ; AMNH 57062, ; AMNH 59959, ; AMNH 59957, ; AMNH 60054, ?; AMNH 57376, ; AMNH 58371, ; AMNH 185464, ?; AMNH 110458, ?; AMNH 101628, ; AMNH 102072, ; AMNH 102085, ; AMNH 102073, ; AMNH 102458, ; AMNH 102212, ; AMNH 104000, ; AMNH 103709, ; AMNH 106063, . Prionailurus planiceps (n = 5: m = 2, f = 2, nd = 1): AMNH 173515, ?; FMNH 58951, 127432, ; FMNH 127433, . Prionailurus rubiginosus (n = 3: m = 1, f = 2): FMNH 95137, ; FMNH 96334, ; FMNH 60476, ; FMNH
; FMNH 96335, ; AMNH 102181, ; FMNH 105561,
. ; AMNH ; FMNH
Prionailurus viverrinus (n = 10: m = 6, f = 4): AMNH 102691, ; AMNH 101627, 106323, ; AMNH 70128, ; FMNH 96332, ; FMNH 96331, ; FMNH 99533, 105562, . Profelis aurata (n = 5: m = 1, f = 3, nd = 1): AMNH 51998, ; AMNH 54332, ? ; AMNH 51993,
; AMNH 51994,
; AMNH 89441,
Puma concolor (n = 37: m = 15, f = 7, nd = 15): MN 1016, ?; MN 1014, ?; MN 381, ?; MN 1025, ?; MN 1029, ?; MN 24867, ; MN 49075, ?; MN 6023, ; MN 17506, ; MN 49073, ?; MZUSP 8878, ; MZUSP 3801, ; MZUSP 11470, ; MZUSP 9010, ; MZUSP 3334, ; MZUSP 9425, ; MZUSP 7343, ?; MZUSP 2687, ; MZUSP 9637, ; MZUSP 9811, ; MZUSP 10352, ; MZUSP 9418, ; MZUSP 1637, ?; MZUSP 28868, ?; MZUSP 20935, ?; MZUSP 10467, ?; MZUSP 19854, ?; AMNH 17459, ; AMNH 17458, ; AMNH 73221, ; AMNH 144512, ; AMNH 206992, ?; AMNH 92205, ; AMNH 130147, ?; AMNH 188349, ; AMNH 188351, ; AMNH 188349, . Uncia uncia (n = 7: m = 4, f = 1, nd = 2): AMNH 35360, AMNH 100110, ; AMNH 119662, ?; FMNH 122235, ; AMNH 24215, ?; AMNH 35529, . ; AMNH 35476, ;

Sicuro and Oliveira - Skull Morphology and Functionality of Extant Felidae 2010

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Sicuro and Oliveira - Skull Morphology and Functionality of Extant Felidae 2010

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Zoological Journal of the Linnean Society, 2010.

ADDITIONAL KEYWORDS: functional morphology morphometrics phylogenetically independent

PHYLOGENY AND TAXONOMY

MATERIAL AND METHODS

F. L. SICURO and L. F. B. OLIVEIRA

F. L. SICURO and L. F. B. OLIVEIRA

Caracal caracal Leptailurus serval

10.7 3.3 5.0 1.9 10.9 1.4 11.8 3.5 3.5

25.5 Mukherjee et al., 2004 4.8 Smithers, 1983; York, 1973

1.5 0.7 0.3 0.5 1.4 0.7 2.4 0.3 0.3

RESULTS AND DISCUSSION MORPHOLOGICAL ANALYSES

F. L. SICURO and L. F. B. OLIVEIRA

POC 0.07 0.62 0.16 0.64 0.64 0.31 0.15

RWP2 0.01 0.001 0.03 0.0001 0.02 0.08 0.48

TFL 0.01 0.001 0.03 0.01 0.02 0.01 0.67

TMA 0.001 0.001 0.03 0.01 0.03 0.03 0.67

TRL 0.01 0.001 0.02 0.001 0.12 0.03 0.48

ZIB 0.01 0.01 0.10 0.001 0.04 0.14 0.67

0.001 0.01 0.10 0.02 0.0001 0.01 0.29

0.19 0.79 0.82 0.87 0.12 0.13 0.15

0.001 0.01 0.55 0.02 0.001 0.03 0.60

0.001 0.01 0.33 0.05 0.001 0.02 0.60

0.001 0.01 0.10 0.01 0.0001 0.48 0.26

0.001 0.001 0.08 0.01 0.0001 0.01 0.55

0.001 0.01 0.50 0.02 0.0001 0.05 0.36

Bolded P-values are signicant according to Mann-Whitney U-test.

FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION

F. L. SICURO and L. F. B. OLIVEIRA

FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION

FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION

FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION

FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION

F. L. SICURO and L. F. B. OLIVEIRA

FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION

FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION

FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION

F. L. SICURO and L. F. B. OLIVEIRA

FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION

F. L. SICURO and L. F. B. OLIVEIRA

FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION

F. L. SICURO and L. F. B. OLIVEIRA

FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION

F. L. SICURO and L. F. B. OLIVEIRA

FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION

F. L. SICURO and L. F. B. OLIVEIRA

FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION

Condyle to canine length of jaw

Condyle to M1 length of jaw

Jaw height at M1 Jaw length

Masseteric fossa length

Masseteric moment arm

F. L. SICURO and L. F. B. OLIVEIRA

Masseteric scar width

OCH OPL POC RWP2 TFL

Acronym TMW FMC FTC SMA CFMC CFTC AHN

; FMNH 26900, ?; FMNH

F. L. SICURO and L. F. B. OLIVEIRA

FELID SKULL MORPHOLOGY, FUNCTIONALITY, AND EVOLUTION

; FMNH 96335, ; AMNH 102181, ; FMNH 105561,

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