Cranial morphology and dietary habits of rodents

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Cranial morphology and dietary habits of rodents

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JOSHUA X. SAMUELS*

Department of Ecology and Evolutionary Biology, 621 Charles E. Young Drive South, University of California, Los Angeles, Los Angeles, CA 90095-1606, USA

Received 1 February 2008; accepted for publication 3 July 2008; first published online 8 June 2009

Rodents are important components of nearly every terrestrial ecosystem and display considerable ecological diversity. Nevertheless, a lack of data on the ecomorphology of rodents has led to them being largely overlooked in palaeoecological reconstructions. Here, geometric and linear morphometrics are used to examine how cranial and dental shapes reflect the diets of living rodent species. Although most rodents are omnivores or generalist herbivores, some species have evolved highly specialized carnivorous, insectivorous, and herbivorous diets. Results show that living rodents with similar diets display convergent morphology, despite their independent evolutionary histories. Carnivores have relatively elongate incisors, elongate and narrow incisor blades, orthodont incisor angles, reduced cheek tooth areas, and enlarged temporal fossae. Insectivores display relatively degenerate dentition, elongate rostra, narrow and thin zygomatic arches, and smaller temporal fossae. Herbivores are characterized by relatively broader incisor blades, longer molar tooth rows, larger cheek tooth areas, wider skull and rostrum, thicker and broader zygomatic arches, and larger temporal fossae. These results suggest that cranial and dental morphology can be used to accurately infer extinct rodent diets regardless of ancestry. Application to extinct beavers suggests that most had highly specialized herbivorous diets.

doi: 10.1111/j.1096-3642.2009.00502.x

ADDITIONAL KEYWORDS: beaver – convergent evolution – ecomorphology – geometric morphometrics – paleoecology – Rodentia.

INTRODUCTION

Rodents are the largest mammalian order (over 2000 species) and show incredible ecological diversity. The remarkable adaptability and opportunism that exem- plify rodent feeding behaviours are evident in their diverse and versatile feeding apparatus. All rodents are characterized by a single pair each of chisel-like upper and lower incisors, which are both self- sharpening and ever-growing. Rodents use their incisors for many tasks, including cropping vegetation, capturing prey, cutting meat and bone, and digging and cutting down trees. The molariform cheek-teeth of rodents show a great diversity in occlusal form (bunodont to lophodont) and crown height (brach- yodont to fully hypselodont) (Hershkovitz, 1962).

Although the occlusal morphology of the cheek-teeth often reflects diet, rodent species with similar occlusal

patterns may have very different diets. Rodents also display a wide range of masseter muscle structure and orientation, which often allows their jaws to function as Class II levers when biting with the molars. Class II levers are more efficient and have a higher mechanical advantage than the Class III levers that characterize most other mammalian jaws (Becht, 1953; Turnbull, 1970). An expanded glenoid fossa allows anterior and posterior shifting of the lower jaw, which combined with the masseter muscles, divides rodent jaws into two distinct functional regions, one used for gnawing and the other for grinding (Becht, 1953; Turnbull, 1970).

Most living rodents are herbivores or omnivores, but nearly all rodents will opportunistically consume meat (Landry, 1970). Specialist carnivores and insectivores have evolved independently within multiple rodent families, most notably in the Muridae and Cricetidae. Convergence in both ecology and morphology amongst rodents are well known, with numerous examples of ecologically equivalent species living in

*E-mail: jsamuels@ucla.edu

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similar habitats on different continents (Wood, 1947).

Specialized carnivorous and piscivorous rodents are known from Australia, Africa, South America, and North America. Insectivorous rodents with long snouts and simplified dentition have radiated widely in both South America and the Philippines. In contrast to these omnivorous and faunivorous rodents, herbivores include species that have adapted to consume nearly any plant material, including grass, tree bark, and fibrous tubers.

Despite the fact that rodents show some of the most extreme dental and muscular specializations amongst mammals (Wood, 1955, 1959, 1965; Turnbull, 1970), few studies have examined cranial and dental morphology across a diverse array of rodent species.

Rodent dental structure has been widely studied, but as they are commonly viewed as less specialized for any particular diet than other mammal groups, com- parative studies of rodent dietary specializations are rare. This study uses an ecomorphological approach to examine how rodent skull shape and tooth structure reflect dietary habits. Craniodental morphology has been shown to predict aspects of diet in a wide range of carnivorans and ungulates with diverse feeding habits (Van Valkenburgh, 1989; Janis, 1995;

Mendoza, Janis & Palmqvist, 2002; Sacco & Van Valkenburgh, 2004; Friscia, Van Valkenburgh &

Biknevicius, 2006). It is expected that: (1) distantly related rodents with similar dietary habits will display convergent skull and tooth shapes; (2) dietary specializations in rodents will be analogous to those observed in other groups of mammals; and (3) differences in skull and tooth shape will be related to how food is acquired and processed and to the physical properties of that food. Quantification of characteristics related to functional cranial and dental properties in extant rodents will allow us to infer the diets of extinct rodents. Dietary habits have been postulated or inferred for many extinct rodents before, but these hypotheses are typically based on qualitative assess- ment of morphological characteristics and phylogenetic affinities. Here I infer the dietary habits of 21 extinct rodents, including 19 beaver species.

Given that traditional linear measurements cannot always capture the spatial arrangement of morphological features, I used a combination of linear and geometric morphometrics to analyse shape (Bookstein, 1991; Zelditch et al., 2004). In geometric morphometric analyses, landmark locations are quantified as sets of two-dimensional (2D) or three- dimensional (3D) coordinates on specimens. This set of landmark coordinates records the shape of specimens better than linear measurements alone (Book- stein, 1991; Zelditch et al., 2004). The use of geometric morphometrics also allows the influence of body size to be minimized by directly quantifying

specimen shape. The inclusion of numerous landmarks throughout the specimen can reduce the impact of potential a priori bias on the importance of particular measures (Zelditchet al., 2004). This study uses the data gleaned from geometric morphometric analyses to develop morphospaces that facilitate ecological and evolutionary inferences.

MATERIAL AND METHODS

This study uses a sample of 318 individuals of 79 extant rodent species (71 genera) from 17 rodent families (Appendix 1); sample sizes for species range from one to ten individuals (averagen=4). An equal representation of males and females of each species was included, where possible, to assess differences in skull shape related to sexual dimorphism. A sample of 21 fossil species from the Castoridae, Cricetidae, and Sciuridae were also included in the analyses (Supporting Information Appendix S1). A full list of specimens is found in Supporting Information Appendix S2; all extant specimens were wild caught, adult individuals (diagnosed by basioccipital – basisphenoid epiphyseal fusion; as in Robertson &

Shadle, 1954). The classification of rodent species included in this study was derived from several sources (primarily Carleton & Musser, 2005; Musser

& Carleton, 2005).

Information on feeding habits and primary dietary items from the current literature was recorded for each extant species to establish a set of dietary groups (Tables 1 and 2; groups were based partially on Williams & Kay, 2001). Nowak (1999) was used as a source of general dietary information for all species and supplemented by monographic sources from the literature (including Banfield, 1974; Kingdon, 1974;

Menzies & Dennis, 1979; Eisenberg, 1989; Eisenberg

& Redford, 1989; Redford & Eisenberg, 1989;

Emmons, 1990). Many species studied are able to switch diet spontaneously or exploit food resources opportunistically; thus, species were assigned to the most appropriate dietary category based on their primary dietary items. These categories are obviously a simplification of a complex reality of diets and are not meant to suggest individual species are obligate feeders with regard to any particular diet, but this categorization is necessary in order to examine the relationships between craniodental morphology and dietary habits. Note that the two herbivorous categories used here do not use the typical meaning of the terms ‘generalist’ and ‘specialist’ (i.e. choosing to eat many or only a few kinds of plants, respectively), but rather refer to whether or not a species consumes abrasive or fibrous foods that require anatomical specializations for oral processing. The dietary groups of

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extant rodents were used in statistical analyses and in the interpretation of dietary habits in fossil taxa.

Photographs used in this study were taken using a Mercury CyberPix (E5205) 5 megapixel digital camera at a resolution of 2560¥1920 pixels and saved in JPEG format. Digital photos were taken of the dorsal, left lateral, and ventral views of the skull of all specimens. Each specimen was photographed with a scale bar in dorsal and ventral views (with the palate parallel to the photographic plane), and left lateral view (with the mid-sagittal plane of the skull parallel to the photographic plane). Most specimens measured between 500 and 2000 pixels wide. The effects of flattening a 3D structure to 2D images were assumed to be similar for all specimens and the linearity of images was checked at all magnification levels.

Geometric morphometric analyses were used to assess morphological variation in skull shape. This study uses a coordinate data set including 30 landmarks digitized on the three views of the skull, with the tpsDig (version 1.40) program (Fig. 1, Table 3;

Rohlf, 2004). As there are few a priori hypotheses regarding which morphological features might be similar in ecologically similar taxa, the landmarks used were chosen to provide an even coverage of the skull and reliably identifiable locations. Many of these landmarks record functionally relevant features, indicating the relative dimensions of the skull and teeth, lengths of lever arms for muscular actions, and size of muscles. Although the origins of the masseter and temporalis muscles are not directly digitized, the posi- Table 1. Dietary categories used in the analyses and their

definitions. A complete list of species included and their classifications can be found in Appendix 1. Species were assigned to the categories deemed most appropriate, but as there is some gradation between categories, individual species may be capable of placement within more than one group (e.g. the grasshopper mouse, Onychomys leuco- gaster, readily switches from a largely carnivorous to an insectivorous diet)

Dietary category Definition

Carnivore Diet composed primarily of animal matter, including some vertebrate or larger invertebrate material.

Insectivore Diet composed of animal matter, but primarily small arthropods (insects and chelicerates), grubs, or earthworms.

Omnivore Diet composed of both plant and animal matter.

Generalist herbivore

Diet composed primarily of plant matter, including mostly soft leafy vegetation or seeds. Diet includes little fibrous plant matter or dust and grit.

Specialist herbivore

Diet composed primarily of plant matter, including large amounts of particularly fibrous or difficult to process plants (e.g. grass, bark, or roots) or dust and grit.

Table 2. Numbers of species sampled for each dietary category and family

Family Carnivore Insectivore Omnivore

Generalist herbivore

Specialist herbivore

Anomaluridae – – – 1 –

Aplodontidae – – – – 1

Bathyergidae – – – – 5

Castoridae – – – – 2

Caviidae – – – – 2

Cricetidae 2 3 9 3 5

Ctenomyidae – – – – 1

Dipodidae – – – 1 –

Erethizontidae – – – – 3

Geomyidae – – – – 4

Muridae 2 2 4 3 2

Myocastoridae – – – – 1

Octodontidae – – – – 2

Pedetidae – – – 1 –

Petromuridae – – – 1 –

Sciuridae – 1 5 5 –

Spalacidae – – – – 8

Total 4 6 18 15 36

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tions of several landmarks in the dorsal view indicate the relative robustness of the zygomatic arch and size of the muscles passing through it (Fig. 1). The distance between landmarks 7 and 8 in the dorsal view indi- cates the relative breadth of the zygomatic arch, which is the primary origin of the masseter. The positions of landmarks 5–7 in the dorsal view record the approxi- mate size of the muscles passing between the cranium and the zygomatic arch, whereas landmarks 6 – 10 indicate the total surface area of the braincase.

Although the temporalis’ origin typically does not fill this area, this provides a rough measure of the size of this muscle’s origin.

Landmark coordinates were collected for only one side of the skull to avoid possible variation because of lateral asymmetry. Landmarks were digitized on the left side of the skull for extant taxa; however, in some fossil specimens it was necessary to use whichever side was best preserved and reverse right side Figure 1. Landmarks indicated on: A, dorsal, B, left

lateral, and C, ventral views of the skull of Castor canadensis. Definitions of landmarks are included in Table 3.

Table 3. Definitions of skull landmarks used in this study. Also see Figure 1

Dorsal cranium

1. Meeting point between nasal and frontal along the midsagittal plane

2. Anterior (midsagittal) tip of the nasal

3. Anterior tip of suture between nasal and premaxilla 4. Anterior tip of suture between premaxilla and

maxilla

5. Posterior tip of suture between frontal and jugal 6. Postorbital constriction

7. Most posterior point of the temporal fossa along the squamosal process of the zygomatic arch

8. Most posterior meeting point between jugal and squamosal process of the zygomatic arch

9. Y-shaped suture where the squamosal, parietal, and occipital meet

10. Most posterior point of the interparietal along the midsagittal plane (meeting of sagittal and nuchal crests)

Lateral cranium

1. Anterior tip of suture between nasal and premaxilla 2. Anterior tip of the nasal

3. Meeting point between nasal and frontal along the midsagittal plane

4. Most posterior point of the interparietal along the midsagittal plane (meeting of sagittal and nuchal crests)

5. Most posterior point of the occipital condyle 6. Posterior end of the cheek tooth row 7. Anterior end of the cheek tooth row

8. Most posterior point of the upper incisor alveolus 9. Posterior edge of the upper incisor blade

10. Anterior edge of the upper incisor blade

11. Most anterior point of the upper incisor alveolus Ventral cranium

1. Lateral edge of the upper incisor blade 2. Medial edge of the upper incisor blade 3. Anterior end of the cheek tooth row 4. Posterior end of the cheek tooth row 5. Posterior (midsagittal) tip of the palate

6. Most lateral point of the suture between tympanic and squamosal (anterior edge of the tympanic bulla) 7. Suture where the tympanic and occipital meet

(posterior edge of the tympanic bulla, between the paraoccipital and mastoid processes)

8. Most posterior point of the occipital condyle 9. Midsagittal border of the foramen magnum

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images. A few fossil specimens were incomplete, and thus several missing landmark positions for an individual were estimated using other specimens of the same species or closely related congeners.

Coordinate sets were scaled, rotated, and aligned using generalized least squares Procrustes superimposition; this method allows superimposition of landmarks without altering the shape they record. The superimposed set of landmarks was then used to compute a consensus configuration of landmarks across all specimens. The consensus configuration represents the average shape of all specimens included in the analysis. Partial warp scores, which represent localized shape differences, were generated from a comparison of the individual landmark configurations to the consensus. These partial warp scores can be used as shape variables in conventional statistical tests. Additionally, global variations in shape (i.e. shearing) in the comparison of individual landmark configurations to the consensus are recorded by uniform components. Thin-plate splines were used to model shape differences as the deforma- tion of a grid based on the consensus configuration of landmarks. The bending energy at each landmark is the energy needed to bend the consensus landmark positions to the target configuration.

Relative warp analysis (RWA) was used to analyse the resultant data set; this method is similar to principal component analysis (PCA), but differs from PCA because it uses partial warp scores based on landmark data as variables and the components extracted are weighted by the bending energy matrix (Zelditch et al., 2004). Morphospaces of the observed variation in shape were created by plotting specimens according to their relative warp scores, with the first relative warp explaining the most variation in shape and each additional warp orthogonal to the preceding warps, and explaining decreasing amounts of variation. Relative warp analyses were performed using the tpsRelw (version 1.39) program (Rohlf, 2004).

Separate relative warp analyses were carried out for each of the three views of the skull, with individual warps summarizing the observed shape variations. Some of the relative warps are informative with regard to diet, whereas others may reflect phylogenetic affinities or other ecological characteristics (i.e.

digging types; Samuels, 2007). Only those warps related to dietary habits will be discussed here; as a criterion to determine whether dietary categories were related to warp scores, univariate analysis of variance (ANOVA) tests were used to assess whether dietary groups showed significantly different relative warp scores.

The position of taxa within morphospace was used to assess whether species or groups with similar

diets displayed convergent or parallel evolutionary trajectories when compared to their sister groups.

Additionally, the influence of phylogeny on ecologically informative warps was examined by comparing the positions in morphospace for members of each family.

Although relative warp analysis eliminates the effects of size through scaling of specimens, the effects of allometry can remain. In addition to other warp scores and uniform components, RWA yields centroid size (CS) for each specimen as a measure of overall size. The influence of allometry was assessed using regression of the uniform components, relative warp scores, and canonical variate scores against log CS.

Canonical variates analysis (CVA) was performed using the partial warp scores and uniform components as variables; CVA uses differences between groups to compute linear combinations of variables (canonical variates) that best separate groups.

Dietary categories were assigned a priori and the classification phase of the analysis assessed the ability of the canonical variates to classify group membership. Fossil specimens were included as unknowns in the classification phase to determine the probabilities of their belonging to any of the a priori groupings. Resultant skull shapes were visualized by regressing partial warp scores and uniform components onto the canonical variates using the tpsRegrw program (version 1.28; Rohlf, 2004).

One assumption of most multivariate statistical techniques is that the samples studied are independent; however, because of their phylogenetic relationships the species studied here do not represent truly independent samples for statistical analysis (Felsen- stein, 1985; Harvey & Pagel, 1991). The non- independence of samples can lead to some potential problems, but the main goal of this study was to examine the relationship between morphology and dietary ecology. Some important ecomorphological information can be lost through the correction of data for phylogenetic effects using phylogenetic autocorre- lation or independent contrasts (Mendozaet al., 2002;

Mendoza & Palmqvist, 2006). Sampling of diverse rodent species from multiple families with similar specializations in this study allowed the examination of ecological patterns while still recognizing potential phylogenetic effects.

In addition to landmarks, a set of linear and angular measurements were taken to reinforce the relationship between dental features, ecology and skull shape (Fig. 2). Incisor shape was measured as a ratio of anteroposterior (AP) to transverse (T) diameter, as well as an index of procumbency. The angle of incisor procumbency is described as either opisthodont (less than 90°, i.e. recurved), orthodont (approximately equal to 90°), or proodont (greater

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than 90°, i.e. procumbent) (Thomas, 1919). The area of the molariform cheek teeth (TA) was calculated as the sum of the individual areas for the premolars and molars, which were calculated as the product of the maximum length and width of each of these teeth (P3L and P3W through M3L and M3W). Relative cheek tooth area was calculated as the square root of TA divided by skull length (SL). Analysis of variance (ANOVA) was used to test for differences amongst dietary groups with Scheffe’s F and Tamhane’s T2 procedures used for post hoc comparisons; linear regression was used to assess correlations with relative warp and canonical variate scores. The rodents examined in this study include a wide range of body sizes, thus it was necessary to assess the influence of body size on the structures being examined. Log- transformed linear measurements were regressed against log centroid size (as a proxy for body size) to analyse interspecific allometry.

Software used for the analyses include SPSS 13.0 and programs from the tps software series for geometric morphometric data (tpsDig, tpsRelw, and tpsRegrw, all available from F.J. Rohlf at http://

life.bio.sunysb.edu/morph). Linear measurements were taken from digital images using ImageJ (available from the National Institutes of Health at http://

rsb.info.nih.gov/ij/, Rasband, 2007).

RESULTS RELATIVE WARP ANALYSES Dorsal skull view

Relative warp analysis of the dorsal view of the skull yielded seven significant warps (eigenvalues>1.0) explaining 91.16% of observed variation in skull shape (Fig. 3A). Although most dorsal relative warps were primarily related to digging behaviour and phylogenetic affinities, one dorsal relative warp was associated with dietary categories. Dorsal relative warp 3 (DRW3) explained 16.99% of variation and showed poor, but significant, separation of insectivores from most other taxa. Positive scores for DRW3 were associated with rostral elongation and a smaller temporal fossa (Fig. 4).

Lateral skull view

Relative warp analysis of the lateral view of the skull yielded eight significant warps (eigenvalues>1.0) explaining 93.82% of observed variation in skull shape (Fig. 3B). The first and fourth lateral relative warps were associated with diet. Lateral relative warp 1 (LRW1) accounted for 47.27% of variation and showed separation of specialist herbivores (mostly negative scores) from the other groups (mostly positive scores). Positive LRW1 scores were associated with more shallow skulls and more opisthodont incisors, whereas negative scores indicated deeper skulls and more procumbent and elongate incisors (Fig. 4).

LRW4 accounted for 6.03% of variation and showed partial separation of carnivores and insectivores (negative scores) from the other groups. Negative LRW4 scores were associated with a shorter tooth row, longer rostrum, and more flattened (less domed) skull roof (Fig. 4).

Ventral skull view

Relative warp analysis of the ventral view of the skull yielded six significant warps (eigenvalues>1.0) explaining 94.20% of observed variation in skull shape (Fig. 3C). Two of the ventral relative warps were associated with dietary habits. Ventral relative warp 1 (VRW1) accounted for 55.31% of variation and showed some separation of specialist herbivores (negative scores) from other taxa (positive scores) (Fig. 3C). Positive VRW1 scores were associated with narrower incisor blades and a shorter rostrum, whereas negative scores indicated broader incisor blades and a longer rostrum (Fig. 4). This warp is also linked to digging habits, as rodents with specializations for tooth digging had negative VRW1 scores.

VRW2 accounted for 15.09% of variation and showed relatively poor separation of the dietary groups (Fig. 3). Herbivores displayed a wide range of VRW2 scores, both positive and negative, whereas carnivores Figure 2. A, linear, and B, angular measurements illus-

trated on the skull of Castor canadensis. Note: although measurements are only illustrated for P4, all premolars and molars were measured.

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and insectivores tended to only show negative scores.

Positive VRW2 scores were associated with a longer tooth row and larger tympanic bullae, whereas negative scores are associated with shorter tooth rows and smaller bullae (Fig. 4).

MORPHOSPACE CONVERGENCE

Three of the rodent families (Cricetidae, Muridae, and Sciuridae) sampled include more than one dietary

type (Table 2), providing multiple potential examples of morphological convergence (species names and numbers are listed in Appendix 1). There is a generally noticeable phylogenetic signal with closely related species similar to one another, but the morphospace distribution of species within clades shows similar deviations in taxa with similar dietary habits. The convergent evolutionary trajectories in multiple families are apparent in some of the relative warp plots.

A

C

B

Figure 3. Relative warp plots for the dorsal, lateral, and ventral views of the skull. A, first (DRW1) and third (DRW3) dorsal relative warps, B, first (LRW1) and fourth (LRW4) lateral relative warps, C, first (VRW1) and second (VRW2) ventral relative warps. Individual points represent the average shape for each species. Numbers associated with each point identify individual species in Appendix 1. Shape deformations associated with each axis are illustrated in Fig. 4.

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In both the lateral and ventral relative warp analyses, the more specialized herbivores are positioned to the left of their relatives with other diets (Fig. 3B, C).

In the Cricetidae, for example, the specialist herbivore arvicolines (nos 6, 34, 38, 43, and 49) have a deeper skull, longer cheek tooth-row, wider incisor blades, and longer, more procumbent incisors (lower LRW1 and VRW1 scores, higher LRW4 and VRW2 scores) than the generalist herbivore (nos 13, 44, and 45) and omnivore (nos 37, 42, 46, 50, 51, 52, 56, 66, and 67) members of the family. Within the Muridae, the specialist herbivores (nos 32 and 35) also have a deeper skull, longer cheek tooth-row, wider incisor blades, and longer, more procumbent incisors (lower LRW1 and VRW1 scores, higher LRW4 scores) than the generalist herbivores (nos 16, 59, and 79) and omnivores (nos 20, 26, 60, and 61). Sciurids had no specialist herbivores, but the more herbivorous mar- motines (nos 19, 36, 71, and 72) had lower LRW1 and VRW1, and higher LRW4 scores than most omnivorous squirrels (nos 2, 27, 57, 65, 76, and 77).

Carnivores, insectivores, and omnivores overlap extensively in some of the relative warp analyses, but a closer examination revealed that many carnivores and insectivores show parallel deviations from their omnivorous relatives. Carnivorous cricetids in the analysis (nos 33 and 47) had narrower incisor blades (higher VRW1 scores) than other members of the family, andIchthyomys(no. 33) also had more anteroposteriorly robust incisors and a shorter cheek tooth- row (lower LRW4 and VRW2 scores) than other cricetids (Fig. 3B and C). Carnivorous murids (nos 15 and 31) also had narrower incisor blades, more anteroposteriorly robust incisors, and a longer rostrum (higher VRW1 scores and lower LRW4 scores) than their relatives, and Hydromys (no. 31) had shorter

cheek tooth-rows (lower VRW2 scores) than other murids (similar to Ichthyomys) (Fig. 3B, C).

CANONICAL VARIATES ANALYSIS

Partial warp scores generated by the previous relative warp analyses were saved and used as variables in stepwise canonical variates analysis. Both affine (uniform) and non-affine (non-uniform) components of shape variation were included as variables. Whereas RWA reveals overall variation in skull shape, CVA selects only the variables that best separate groups.

Extant rodent species in this analysis were classified a priori as belonging to one of five dietary groups:

carnivore, insectivore, omnivore, generalist herbivore, and specialist herbivore. Extinct species were included as unknowns in the classification phase of the analysis.

The stepwise canonical model included 24 of 48 partial warps; this analysis showed much better separation of dietary groups than RWA and was significant (Wilks’ l =0.011,F(4,313)=24.035,P<0.001). The analysis yielded three canonical variates with significant discriminating power, which accounted for 97.1%

of total variance in the data set (Table 4).

The first canonical variate (CV1) accounted for 78.0% of variance and primarily separated both groups of herbivores from the other groups. Specialist herbivores had highly positive scores, generalist herbivores had slightly positive or negative scores, and omnivores, carnivores, and insectivores had progressively more negative scores (Figs 5, 6). Positive CV1 scores were associated with a wider and deeper skull and rostrum, wider zygomatic arches, longer tooth rows, longer and more procumbent incisors, broader incisor blades, and larger temporal fossae. Negative CV1 scores were associated with a narrower and shallower skull and rostrum, shorter tooth rows, shorter and more opisthodont incisors, narrower incisor blades, and smaller temporal fossae.

Figure 4. Thin-plate splines corresponding to maximum observed deformations along each relative warp axis for the dorsal, lateral, and ventral views of the skull.

Table 4. Summary statistics for canonical variates analysis of extant rodent dietary categories

Canonical variate

1 2 3

Eigenvalue 11.098 1.986 0.724

% Variance explained 78.0 14.0 5.1

Cumulative proportion of variance (%)

78.0 92.0 97.1

Wilks’ lambda 0.011 0.138 0.411

X² 1351.9 599.0 268.7

Canonical correlation 0.958 0.896 0.648

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The second canonical variate (CV2) accounted for 14.0% of variance and separated insectivores (strongly negative scores) and carnivores (slightly negative scores) from omnivores (positive scores) (Fig. 5). Negative scores for CV2 were linked to longer rostra, narrower zygoma, and less robust incisors.

Positive CV2 scores were associated with a shorter rostrum, wider zygoma, and more robust incisors.

The third canonical variate (CV3) accounted for 5.1% of variance and separated carnivores (positive scores) from the other groups (Fig. 6). Positive CV3 scores were associated with a shorter and wider rostrum, dorsoventrally flattened skull, flattened and elevated nasals, larger temporal fossae, smaller audi-

tory bullae, and more elongate and robust incisors with longer blades. Negative CV3 scores were associated with a longer and narrower rostrum and smaller temporal fossae.

The ability of the canonical model to separate taxa into dietary groups was assessed using the classification phase (Table 5). This classification showed 98.1%

correct classification of individuals, as well as 95.6%

correct classification when cases were cross-validated (where individual specimens are excluded from creat- ing the functions and are classified using results from remaining specimens). Of 318 individuals sampled, only six were misclassified: one Chelemys macronyx was misclassified as omnivorous, one Uromys caudi- Figure 5. Plot of first (CV1) and second (CV2) canonical variates; included are thin-plate splines for maximum observed deformations in each of the three views of the skull along each canonical axis. Individual points represent the average shape for each species. Numbers associated with each point identify individual species in Appendix 1.

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maculatuswas misclassified as omnivorous, onePhlo- eomys pallidus was misclassified as a specialist herbivore, one Cavia cabaya was misclassified as a generalist herbivore, and two (of three) individuals of Hyomys goliath were misclassified as generalist herbivores.

A sample of 19 extinct species from the family Castoridae, the extinct giant marmotPaenemarmota barbouri, and the ancestral muskrat Pliopotamys minorwas included as ungrouped cases in the classification phase of the analysis, (Table 6, Fig. 7). The earliest beaver,Agnotocastor coloradensis, was classified as a generalist herbivore, whereas all later beavers

were classified as specialist herbivores.Paenemarmota barbouriwas classified as a generalist herbivore and Pliopotamys minor was classified as a specialist herbivore. Classifications of some extinct taxa showed high posterior probabilities and low conditional probabilities (Table 6), a result of these taxa being closest to the centroid for a group, but on the periphery or outside of the observed morphospace for that group.

BODY SIZE

Centroid size for each individual was also saved as a measure of skull size. Both herbivore groups have Figure 6. Plot of first (CV1) and third (CV3) canonical variates; included are thin-plate splines for maximum observed deformations in each of the three views of the skull along each canonical axis. Individual points represent the average shape for each species. Numbers associated with each point identify individual species in Appendix 1.

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Table 5. Canonical variates analysis classification matrix for extant taxa

Observed group % Correct

Predicted group Carnivore (N=14)

Insectivore (N=21)

Omnivore (N=88)

Gen. herbivore (N=55)

Spec. herbivore (N=140)

Original Carnivore 100.0 14 0 0 0 0

Insectivore 95.2 0 20 1 0 0

Omnivore 100.0 0 0 88 0 0

Gen. herbivore 96.4 0 0 1 53 1

Spec. herbivore 97.9 0 0 0 3 137

Total 98.1 14 20 90 56 138

Cross-validated Carnivore 92.9 13 0 1 0 0

Insectivore 90.5 0 19 1 1 0

Omnivore 95.5 0 0 84 4 0

Gen. herbivore 92.7 0 0 1 51 3

Spec. herbivore 97.9 0 0 0 3 137

Total 95.6 14 19 87 59 140

Gen., generalist; Spec., specialist

Table 6. Canonical variates analysis classification of extinct taxa

Species Most likely group P(D|G) P(G|D) Second most likely

Castoridae

Agnotocastor coloradensis Generalist herbivore 0.011 0.514 Specialist herbivore Castor californicus Specialist herbivore 0.664 1.000 Generalist herbivore Castor fiber (Pleistocene) Specialist herbivore 0.362 0.900 Generalist herbivore Castoroides leiseyorum Specialist herbivore 0.000 1.000 Generalist herbivore Castoroides ohioensis Specialist herbivore 0.000 1.000 Generalist herbivore

Dipoidessp. Specialist herbivore 0.265 0.994 Generalist herbivore

Eucastor tortus Specialist herbivore 0.031 1.000 Generalist herbivore

Euhapsis breugerorum Specialist herbivore 0.177 1.000 Generalist herbivore Euhapsis ellicotae Specialist herbivore 0.000 1.000 Generalist herbivore Euhapsis platyceps Specialist herbivore 0.000 0.998 Generalist herbivore Fossorcastor greeni Specialist herbivore 0.000 1.000 Generalist herbivore Migmacastor procumbodens Specialist herbivore 0.393 1.000 Generalist herbivore Palaeocastor fossor Specialist herbivore 0.241 1.000 Generalist herbivore Palaeocastor magnus Specialist herbivore 0.339 1.000 Generalist herbivore Palaeocastorcf. nebrascensis Specialist herbivore 0.235 1.000 Generalist herbivore Palaeocastor penninsulatus Specialist herbivore 0.008 1.000 Generalist herbivore Palaeocastor simplicidens Specialist herbivore 0.000 0.999 Generalist herbivore Pseudopalaeocastor barbouri Specialist herbivore 0.133 1.000 Generalist herbivore Unidentified castorid (KUVP 125061) Specialist herbivore 0.000 1.000 Generalist herbivore Cricetidae

Pliopotamys minor Specialist herbivore 0.000 0.566 Generalist herbivore Sciuridae

Paenemarmota barbouri Generalist herbivore 0.413 0.998 Specialist herbivore P(D|G) represents the conditional probability of the observed canonical score, given membership in the most likely group.

P(G|D) represents the posterior probability that a case belongs to the predicted group, given the sample used to create the canonical model.

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larger mean skull sizes (indicated by CS) than the other dietary groups (ANOVA F=5.946, P<0.001), but the range of skull sizes for herbivores in the sample overlaps completely with the other groups.

The uniform components, RW scores, and CV scores were regressed against log CS to test for allometric effects. Skull size (measured by CS) was not significantly correlated with most aspects of skull shape. Only two variables were significantly correlated with log CS: lateral uniform component 1

(r²=0.333, P<0.01) and lateral relative warp 1 (r²=0.225, P<0.01). Lateral uniform component 1 is associated with dorsoventral shearing of the skull, resulting in a deeper skull with elongate incisors.

This uniform component also contributes to lateral relative warp 1 (LRW1), thus LRW1 is correlated with log CS to a lesser degree. LRW1 is related to skull depth, incisor length, and incisor procumbency, and is associated with both body size and herbivory.

Figure 7. Plot of first (CV1) and second (CV2) canonical variates; included are thin-plate splines for maximum observed deformations in each of the three views of the skull along each canonical axis. This figure is identical to Fig. 5 except that extinct rodent taxa with inferred diets are also included. Individual points represent the average shape for each species.

Numbers associated with each point identify individual species in Appendix 1.

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LINEAR AND ANGULAR MEASUREMENTS

Means and standard deviations for each dietary group and the results for ANOVA tests are summarized in Table 7. The incisor shapes of different dietary groups vary widely (Fig. 8). In general, both groups of herbivores have broad incisors, with nearly equal AP and T diameters (Fig. 8A). Carnivores and omnivores have greater AP than T incisor diameters, and are significantly different from specialist herbivores in incisor shape (ANOVAF=32.332,P<0.001). No dietary categories had significant differences in mean incisor procumbency angles, but Levene’s test of homogeneity of variances found significantly different variances (Levene Statistic=5.055, P<0.001). The two groups

of herbivores vary widely in incisor procumbency angles, and both include taxa with proodont and opisthodont incisors (Fig. 8B). Carnivores display incisor angles near 90° and possess remarkably low variation in incisor procumbency.

The scaling of cheek tooth area to centroid size (as a proxy for body size) is significantly different from isometry, indicating that larger rodents have proportionately larger cheek tooth areas (Fig. 9A). Although the mean skull size of the two herbivore groups in the sample is larger than the skull size of the other groups, the size ranges for each group do overlap extensively. Most herbivores in the analysis fall above the regression line, whereas most omnivores, carnivores, and insectivores fall below the line. There are Table 7. Mean values and standard deviations of linear and angular measurements for each dietary category

Variable

Carnivore N=4

Insectivore N=6

Omnivore N=19

Generalist herbivore N=14

Specialist herbivore N=36 Incisor shape (AP/T) 2.169 (0.369)

GH, SH

1.616 (0.293) O, SH

2.097 (0.357) I, GH, SH

1.510 (0.318) C, O, SH

1.176 (0.264) C, I, O, GH Incisor procumbency angle (°) 87.8 (1.1) 96.1 (12.2) 88.2 (4.4) 93.8 (10.8) 96.7 (12.1) Relative cheek tooth area [(√TA)/SL] 0.083 (0.011) 0.070 (0.021)

GH, SH

0.082 (0.011) GH, SH

0.103 (0.013) I, O

0.106 (0.014) I, O

AP, anteroposterior; T, transverse; TA, cheek tooth area; SL, skull length. Tests were made using species averages.

Numbers of species included are listed below each category. Significant differences amongst groups at thePⱕ0.05 level are indicated with: C, carnivore; I, insectivore; O, omnivore; GH, generalist herbivore; SH, specialist herbivore.

A B

Figure 8. Box plots of incisor shape for dietary categories. A, incisor anteroposterior (AP) diameter divided by transverse (T) diameter. B, incisor procumbency angle. Bars display the mean, boxes represent the standard deviation, and whiskers represent the extreme values for each dietary group. Numbers associated with outliers identify individual species in Appendix 1.

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exceptions, but, in general, both groups of herbivores have larger cheek tooth areas than similar sized species from the other dietary groups.

Relative cheek tooth area results were unsurpris- ing, with a general trend of increasing cheek tooth area associated with diets that require more oral processing (i.e., herbivory). The length of the upper tooth row was one of the features that best separated all dietary groups in the canonical analysis and relative cheek tooth area is significantly correlated with CV1 (r²=0.413, P<0.001; Fig. 9B). Insectivores had the lowest cheek tooth area and the two groups of herbivores had the highest; both herbivore groups had significantly higher relative cheek tooth area than insectivores and omnivores (ANOVAF=16.325, P<0.001). Particularly low relative cheek tooth area is seen in the shrew-like rat, Rhynchomys soricoides (no. 64), which is characterized by degenerate cheek teeth.

DISCUSSION

Rodents with similar diets show broad scale conver- gences in skull shape. Although phylogenetic signal is evident, there is an observable and strong ecological effect on cranial and dental morphology in rodents.

Despite the fixed nature of certain rodent adaptations (ever-growing incisors, loss of canines and anterior

premolars), rodents with comparable diets have independently modified these structures to suit their habits. The following discussion describes morphological differences in rodent cranial and dental structures associated with different diets, functional implications of these differences, and finally what an application of this technique to some extinct rodents reveals about their ecology and evolution. Members of the Muridae from multiple dietary categories are illustrated to help visualize the some cranial and dental differences associated with varying dietary habits (Fig. 10).

DIETARY CATEGORIES Omnivores

Rodents are known for adaptability, which is aided by the versatility of their basic masticatory apparatus structure: ever-growing incisors, multi-layered and reorientated jaw muscles, and division of the jaw into two functional regions. The fundamental adaptability of an ‘average’ rodent was well illustrated by Laurie’s (1946) study of the typically omnivorous house mouse, Mus musculus. House mice from different ‘environ- ments’ in London were found to eat highly varied diets; those living in flour depots survived on only white flour whereas those living in cold storage (-9.5 °C) exclusively ate meat. The generally

A B

Figure 9. A, log-log plot of the square root of cheek tooth area (√TA) vs. centroid size (dorsal), regression line:

y= -1.220+1.216x, standard error of the estimate=0.088, correlation coefficientr=0.945, dashed reference line represents isometric scaling: y= -1.220+x. B, plot of relative cheek tooth area [(√TA)/skull length] versus first canonical variate scores. Individual points represent species averages. Numbers associated with each point identify individual species in Appendix 1.

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moderate features of omnivorous rodents facilitate their dietary versatility; where specialists may have difficulty surviving tough times, these opportunistic omnivores can survive on nearly any food source.

Many of the omnivorous species studied show sea- sonal changes in diet, with generalist herbivore ten- dencies supplemented by insectivory at different times of year. Given the remarkable flexibility of their feeding apparatus, some have suggested that rodents are ancestrally omnivorous (Landry, 1970).

Not surprisingly, omnivorous rodents generally display an array of moderate characters when com-

pared to carnivores, insectivores, or herbivores. The presence of a relatively short rostrum, narrow incisor blades, and moderate tooth row lengths characterize omnivores. When compared with carnivores and insectivores, omnivores have a shorter rostrum and more robust zygomatic arches. Omnivores also have relatively anteroposteriorly robust incisors, which differ greatly from those of insectivores and herbivores (Fig. 8A). Compared with herbivores, omnivores display a narrower and shallower skull, shorter cheek tooth rows and incisors, narrower incisor blades, narrower zygomatic arches, and smaller temporal fossae.

Figure 10. Skulls of selected members of the Muridae, illustrating some differences in cranial and dental structure associated with different diets. Each skull is scaled to the same total length. Scale bars with each skull represent 10 mm.

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Omnivore incisors are typically orthodont or moderately procumbent or opisthodont (Fig. 8B).

Relative molar cheek tooth areas of omnivores are also moderate (Fig. 9). Crown heights of the cheek teeth in omnivores are generally relatively low, because the plant matter in their diet is predominantly easily digested seeds and nuts (Williams &

Kay, 2001). The structure of these molariform teeth varies from relatively simple cuspidate teeth (e.g., Peromyscus) to more complex plicident (folded) teeth (e.g. chevrons of Rattus, sigmoidal crests of Sigmo- don) (Hershkovitz, 1962). Whether these teeth are cuspidate or lophed, they are effective in processing both animal and plant matter when paired with ever- growing incisors and propalinal or alternating transverse jaw movements.

Carnivores

Highly carnivorous rodents are relatively unusual, but those that do exist have evolved independently to fill similar ecological roles. Carnivorous rodents in this study were most similar to their omnivorous relatives, but do show some consistent craniodental differences from all other dietary groups, primarily in incisor structure. Compared to herbivorous and omnivorous rodents, carnivores display a dorsally flattened skull, shorter tooth rows, elongate rostrum, and narrower incisor blade (only relative to herbivores). Relative to insectivores and omnivores, carnivores possess a wider rostrum, dorsoventrally flattened skull, flattened and elevated nasals, more elongate incisors, longer incisor blades, and larger temporal fossae.

The incisors of carnivorous rodents are distinct from those of all the other groups studied, in that both the incisors and incisor blades are relatively elongate, producing an effective tool for piercing and cutting apart their prey. The ever-growing and self- sharpening nature of the incisor blades may actually make them better suited for cutting meat throughout the life of an individual than the carnassials of the Carnivora, which eventually dull through wear.

Carnivorous rodent incisors also have a significantly different cross-sectional shape (anteroposterior/

transverse diameter) than those of insectivores and both groups of herbivores (Fig. 8A). Their greater anteroposterior (relative to transverse) diameter has several functionally significant impacts on the useful- ness of the incisors as cutting tools. Anteroposteriorly robust incisors can accommodate the stresses encountered when biting prey, whereas a consequently narrower blade focuses the bite force on a small area, improving their effectiveness in puncturing and dis- membering prey (Frazzetta, 1988).

Incisors of carnivorous rodents are consistently orthodont (approximately at a 90° angle to cheek

tooth row), and show significantly lower variation in procumbency angle than all other groups (Fig. 8B, Levene Statistic=5.510, P<0.001). This conserved orthodont shape is likely to be linked to their use in prey capture and killing. Procumbent incisors pro- trude further from the jaw muscles, which increases the length of the out lever and reduces their mechanical advantage, effectively reducing bite strength.

Opisthodont incisors have a shorter out lever, which increases the mechanical advantage and reduces the velocity ratio of these muscles. At the same degree of jaw opening, the tips of opisthodont incisors are closer to the jaw joint than more procumbent incisors. This reduces their effective gape, which may limit the size of prey they can fit in their mouth. As procumbent incisors would generally reduce bite strength and opisthodont incisors would both reduce the bite velocity and may limit the size of prey taken; an intermediate condition is likely to be closer to optimal.

The length of the upper tooth rows and the relative cheek tooth areas of carnivores are lower than those of most herbivores (Fig. 9). Despite having lower cheek tooth areas, some carnivorous rodents have molars characterized by tubercular hypsodonty (elongation of cusps), as is the case for Onychomys and Ichthyomys (Hershkovitz, 1962). These cusps form prong-like projections that help cut and crush prey, but tend to erode rapidly (Hershkovitz, 1962).

Although rapid erosion of the molars may compromise their functionality, carnivorous rodents can cope by using their ever-growing incisors for primary processing of food.

The wider rostrum and enlarged temporal fossae of carnivorous rodents relative to insectivores and omnivores are particularly noteworthy. In most carnivorous mammals, increased rostral width helps to dissipate torsional stresses encountered when subdu- ing prey. Rostral width in carnivorous rodents may also be linked to enlarged olfactory turbinates or the presence of an enlarged vomeronasal organ, but this requires further study. The wider zygomatic arches, correspondingly enlarged temporal fossae, and more prominent temporal muscle scars on carnivorous rodent skulls reflect the relative enlargement of the temporalis. This is supported by the fact carnivorous murids also have mandibles with a well-developed coronoid process, which acts as the origin of the temporalis muscles (Michaux, Chevret & Renaud, 2007). Other groups of carnivorous mammals show a similar pattern of enlarged temporal fossae and corresponding temporalis muscles (Radinsky, 1981;

Wroe, McHenry & Thomason, 2005). The large temporalis in other carnivorous mammals serves primarily to enhance bite force at the canines and to resist ventrally and anteriorly directed forces at the front of the jaw that would otherwise lead to dislocation,

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typically as a result of struggling prey (Maynard Smith & Savage, 1959).

Data on the size and structure of the jaw muscles are lacking for many rodents, but where available they support the division of carnivores from other rodents. The South American Ichthyomyinae have enlarged temporal and reduced masseter muscles masses, with the temporalis accounting for 47% and the masseter only 46% of jaw muscle mass inIchthyo- mys tweedi (Voss, 1988). This is in sharp contrast to muscle masses reported for other rodents (typically herbivores and omnivores), where, on average, the temporalis is 17% and the masseter is 66% of jaw muscle mass (Turnbull, 1970; Ball & Roth, 1995).

Satoh & Iwaku (2006) compared jaw muscles of the grasshopper mouse, Onychomys leucogaster, to omnivorous cricetids and found it had somewhat reduced masseter muscles, and a reorientation of the jaw muscles to increase gape, allowing it to open its mouth widely when biting larger prey. Enlargement and a dorsal shift of the temporalis insertion in carnivorous rodents increases the angle between the jaw joint and the origin and insertion of the muscle;

according to models of gape this should result in decreased stretch factors when the jaws are wide open (Herring & Herring, 1974; Herring, 1975; Satoh

& Iwaku, 2006).

Three of the four carnivorous taxa in this analysis are semi-aquatic and exhibit elevated nasals and a dorsoventrally flattened skull, features that characterize some semi-aquatic rodents (Osgood, 1928). The auditory bullae of the three aquatic carnivores studied (Colomysfrom Africa,Ichthyomysfrom South America, andHydromysfrom Australia) are also significantly reduced (visible in Hydromys, Fig. 10C).

These semi-aquatic, predatory species all use their enlarged vibrissae and sense of smell to find their prey, rather than depending on their hearing (Voss, 1988; Kerbis Peterhans & Patterson, 1995). These semi-aquatic carnivorous rodents possess a relative enlarged medulla oblongata (and a correspondingly large foramen magnum) as well as large trigeminal nerves (Voss, 1988; Kerbis Peterhans & Patterson, 1995). As most extant carnivorous rodents are semi- aquatic, these characters reflect differences in forag- ing behaviour, an important aspect of their dietary ecology.

Insectivores

Insects are ubiquitous in nearly all terrestrial ecosys- tems, making them an abundant and high quality food source. Insectivorous rodents studied here can be divided into two distinct groups based on hardness of their prey, with one group specializing on ‘hard’ and the other on ‘soft’ prey (similar to Freeman, 1979, 1981; Strait, 1993). As the ‘soft’ prey group is repre-

sented by a single species in the current sample, the insectivore groups were not separated a priori. Both insectivore groups were most prominently characterized by differences in overall skull shape and the presence of at least partially degenerate dentition.

When compared to other dietary groups, both types of insectivores have a longer rostrum, narrow, thin zygomatic arches, smaller temporal fossae, and reduced incisors. Rostral elongation in insectivores increases the velocity of closing the mouth, which facilitates the capture of prey. Narrow zygomatic arches reflect reduction of the area of origin for the masseter muscles, whereas smaller temporal fossae indicate reduction of the temporalis. The incisors of insectivores are generally degenerate, showing both narrow blades and less robust anteroposterior diameters (resulting in an intermediate cross-sectional shape, Fig. 8A). Insectivore incisors are typically orthodont or moderately procumbent (Fig. 8B), which reflects their primary use in seizing prey rather than processing food (Hershkovitz, 1962). Degeneration of the jaw musculature and incisors of insectivorous rodents reflect the fact that their food requires little processing.

The ‘hard’ prey feeders include the South American Oxymycterini, Philippine Island Archboldomys, Southeast Asian Rhinosciurus, and African Deomyi- nae (not included in this study), among others.

Members of this group incorporate hard shelled arthropods (e.g. beetles) as a significant component of their diet, and display features similar to other insectivorous mammals. Whereas the incisors of these rodents are relatively reduced (Musser, 1982; Hino- josa, Anderson & Patton, 1987), the length of the upper tooth rows and relative cheek tooth areas of the molars are similar to many omnivores and carnivores (Fig. 9). Like some carnivorous rodents, most insectivorous rodents that eat ‘hard’ prey have cuspidate molars characterized by tubercular hypsodonty, similar to those seen in insectivorous marsupials, insectivores, and insectivorous bats (Hershkovitz, 1962; Strait, 1993). The prong-like projections on the teeth of species likeOxymycterus and Archboldomys (Musser, 1982; Hinojosaet al., 1987) are effective for cracking the exoskeletons of small arthropods (Her- shkovitz, 1962; Evans & Sanson, 1998). In addition to being able to effectively process invertebrate prey, the characteristics of ‘hard’ prey insectivores allow them to be more opportunistic and generalized in their feeding habits (Strait, 1993). Accordingly, many members of the Oxymycterini feed predominantly on insects, but also include some vegetation, fungi, and rhizomes in their diet (Nowak, 1999).

The second group, which feeds mostly on ‘soft’

bodied grubs and earthworms, is exemplified by the poorly knownRhynchomysfrom Luzon Island and its

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relatives (not included here) (Rickart, Heaney &

Utzurrum, 1991). As a diet composed primarily of soft-bodied invertebrates requires minimal processing, many groups of insectivorous mammals show degenerate dentition (e.g. anteaters, aardwolf, and pangolins); Rhynchomys generally resembles these myrmecophagous mammals. Rhynchomys has an incredibly elongate rostrum (resulting in the most extreme CV1 and CV2 scores of all species studied), degenerate dentition (reduced incisors, reduced number and size of molars), and falls as an outlier for relative cheek tooth area of the molars (Figs 9, 10B).

The long snout and fine incisors may help Rhyn- chomysseize prey in narrow spaces, but are of little use in processing food. InRhynchomys, the M3 is lost and the M1 and M2 are effectively simple pegs. The cheek teeth are reduced to the point of being nearly functionless and may only be used to grip food (Her- shkovitz, 1962). Although their dentition lacks the extreme degeneration of Rhynchomys, other shrew- like rats from the Philippines (e.g.Melasmothrixand Tateomys) also specialize on abundant ‘soft’ prey, including earthworms that commonly live in abundant forest floor mosses (Musser, 1982; Rickartet al., 1991).

Herbivores

Both herbivore groups share many features that separate them from the other dietary groups, but specialist herbivores show a greater degree of specialization relative to generalist herbivores. When compared to the carnivores, insectivores, and omnivores, herbivores have a relatively wider skull and rostrum, larger temporal fossae, thicker and broader zygomatic arches, broader incisor blades, and longer molar tooth rows with larger molar cheek tooth areas. Both herbivore groups show a wide range of incisor procumbency angles, but the generalists include more opisthodont taxa and the specialists include more highly proodont taxa than the other groups (Fig. 8B).

In contrast to generalists, specialist herbivores also have a relatively deeper skull and rostrum, more elongate incisors, and more transversely orientated incisor blades. The nuchal region of specialist herbivores also tends to be wider and more transversely orientated than what is seen in the other groups, possibly reflecting the presence of numerous fossorial specialists in this group with enlarged neck musculature used in head stabilization.

The primary task of incisors in most herbivorous rodents is cropping vegetation, with the same motion used for both grasping and cutting food items. This simultaneous action and the perpetually sharp incisor blade makes procuring vegetation less demanding in terms of muscular effort than the grabbing and pulling carried out by ungulates, which involves effort

by the head and neck musculature (Landry, 1970).

A broad and transversely orientated incisor blade results in a wider cutting surface and consequently a better structure for acquiring vegetation; it accom- plishes the same result seen in the increased muzzle width of grazing ungulates (Janis & Ehrhardt, 1988;

Janis, 1995; MacFadden, 2000; Mendozaet al., 2002).

Incisor procumbency varied widely within herbivorous rodents (Fig. 8B), which reflects the inclusion of typically opisthodont gramnivorous species and relatively proodont tooth-digging species in these groups.

The generally more massive skull of herbivorous rodents serves two functions: (1) to accommodate stresses resulting from mastication; and (2) to support larger masticatory muscles. A deeper skull and rostrum in herbivorous rodents helps to accommodate stresses encountered when processing food, either through repeated chewing of fibrous plant matter or biting of harder foods. The mediolaterally thicker, broader zygomatic arches and deeper, wider rostrum of herbivores result in larger areas of origin for the masseter muscles, whereas the correspondingly larger temporal fossae result in larger areas of origin for the temporalis. As the jaw musculature and dentition of rodents is divided into two separate functional regions, expansion of both the masseter and temporalis facilitate feeding. The expansion, specialization, and dominance of the masseter (66% of muscle mass on average) allow the propalinal and alternate transverse jaw movements used to crush and grind food with the cheek teeth (Turnbull, 1970).

Enlarged masseter muscles in rodents increase both the bite force at the molars and bite force and control at the incisors (Maynard Smith & Savage, 1959;

Greaves, 1991).

Many herbivorous rodents have particularly broad zygomatic arches and large temporal fossae. These features are combined with a pronounced sagittal crest in both tooth-digging rodents (e.g., Spalacidae, some Bathyergidae and Geomyidae) and lignivorous rodents (e.g. Castor and Erethizon), and there are several benefits of a larger temporalis in these herbivores. Although not seen in all herbivorous rodents, an enlarged temporalis may increase the mechanical advantage of the incisor bite (by increasing the in-lever); this is particularly important if the incisors are used to cut harder material (Turnbull, 1970). As in carnivorous mammals, the large temporalis of herbivorous rodents may also help resist dislocating forces encountered when biting hard materials, like soil and trees (Ball & Roth, 1995). Also, the enlarged and dorsally shifted temporalis origin of these herbivores increases the angle and distance between the jaw joint and the origin and insertion of the muscle, resulting in increased resting length and decreased stretch factors when the jaws are wide open (Herring

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& Herring, 1974; Herring, 1975; Satoh & Iwaku, 2006). A greater resting length allows a greater range of motion and because much of the masseter musculature in rodents is over-stretched when the jaws are wide open, a decrease in stretch for the temporalis is important for effectively biting larger and harder structures (Satoh & Iwaku, 2006).

Enlargement of the jaw muscles is also consistent with allometric scaling; for a larger structure to be functionally equivalent certain aspects of the morphology must be proportionately larger relative to body size. The strength of muscles is determined by their cross-sectional area, but mass is proportional to volume. Thus the muscular force required to move a more massive jaw should increase with the size of the jaw (Satoh, 1997; Michauxet al., 2007). The observed trend toward larger skull size and larger muscles in herbivores is consistent with the functional demands of processing a herbivorous diet including relatively tough or abrasive food (Satoh, 1997). This type of diet demands greater occlusal force, which can be accom- plished by increasing the strength of the jaw muscles, either through having proportionately larger muscles or more advantageous lever arms.

In both groups of herbivores, the length of the upper tooth rows and relative cheek tooth areas are larger than in omnivores and faunivores (Fig. 9). The slope of the regression line in Figure 9A shows a significant positive allometry, indicating that larger rodents do have proportionately larger cheek tooth areas. In general, most herbivores in the analysis fall above the regression line, whereas most omnivores, carnivores, and insectivores fall below the line; this demonstrates that herbivores have larger cheek tooth areas than similar sized species from the other dietary groups. The size and shape of the cheek teeth in herbivores reflect the fact that fibrous plant matter requires extensive dental processing for efficient microbial digestion (Stevens & Hume, 1995). A recent study by Evans et al. (2007) found strong links between diet and occlusal complexity and tooth shape in rodents and carnivorans, in which increasing dietary demands were correlated with an increased number of shearing surfaces available to cut or grind food. These workers also found a similar tendency toward larger tooth areas in herbivorous rodents and carnivorans, but in their study dental complexity more completely differentiated dietary groups (Evans et al., 2007). In rodents, higher cheek tooth area corresponds with more plicident dentition (increased folding on the occlusal surface of cheek teeth) and increased hypsodonty (including fully hypselodont teeth in some herbivorous species). The highly complex occlusal surfaces of specialist herbivores like Hydrochoerus and Hystrix have many shearing surfaces, which facilitate processing of fibrous plant

matter. High-crowned teeth (hypsodont or hypselodont) seen in some herbivorous rodents and other highly herbivorous mammals tend to be adapted for diets that include grass, other fibrous plant matter, or higher levels of dust or grit (Janis, 1988; MacFadden, 2000; Williams & Kay, 2001). Increased hypsodonty in many herbivorous rodents also results in increased maxillary depth, producing an overall deeper profile of the skull similar to what is seen in ungulates (Janis, 1995; Mendoza et al., 2002). A diet composed primarily of plant matter requires extensive processing; and in addition to complex teeth, many herbivorous rodents have modifications of the digestive tract that facilitate hindgut fermentation and also practice coprophagy (Langer, 2002).

APPLICATION TO EXTINCT RODENTS

Extinct rodents included in the canonical analysis showed a wide range of skull shapes, but the morphology of included species suggests that they were all herbivorous. The earliest beavers were classified as generalist herbivores. This is not surprising, as most Oligocene rodents are not particularly specialized and Agnotocastor has relatively low crowned cheek teeth (Stirton, 1935; Korth, 1994). All later beavers were classified as specialist herbivores, which is consistent with the progressively increasing hypsodonty seen in castorids through time (Stirton, 1935, 1947).

The burrowing beavers (Palaeocastorinae and Mig- macastorinae) arose in the Late Oligocene and Early Miocene, when global cooling and drying led to the expansion of open habitats (Retallack, 2001, 2007;

Zachoset al., 2001; Strömberg, 2002, 2005). Paleosol evidence and phytolith assemblages from the Great Plains, where burrowing beavers are most commonly found, suggest open-habitat C3grasses diversified and become common in the Oligocene and Early Miocene (between 34 and 23 Mya) (Strömberg, 2005; Retal- lack, 2007). Burrowing beavers were all classified by the analysis as specialist herbivores; they show pro- gressive hypsodonty in their cheek teeth, and are likely to have fed on grasses that radiated at this time (Stirton, 1935; Thomasson, 1985; Korth, 1994; Nevo, 1999). The timing of increasing adaptations for herbivory in burrowing beavers and other fossorial rodents (~20–30 Mya), corresponds with increased hypsodonty in South American notoungulates (Korth, 1994; MacFadden, 2000), and contrasts with the increased dominance of C4grasslands and the radiation of hypsodont herbivores in North American ungulates later on during the mid Miocene (~15–20 Mya;

MacFadden, 2000). The radiation of small herbivorous mammals before the well-known radiation of grazing ungulates suggests that small mammals may