The Function and Evolution of the Syncervical in Ceratopsian Dinosaurs with a Review of Cervical Fusion in Tetrapods

Home , Darren Tanke, Epoicotheriidae, Erethizontinae, Pappogeomys, Stegoceras, Yinlong

Collin S. VanBuren

A thesis submitted in conformity with the requirements for the degree of Master’s of Science Ecology & Evolutionary Biology University of Toronto

The Function and Evolution of the Syncervical in Ceratopsian Dinosaurs with a Review of Cervical Fusion in Tetrapods

Collin S. VanBuren

Master’s of Science

Ecology & Evolutionary Biology University of Toronto

2013 Abstract

Mobility of the vertebral column is important for many ecological aspects of vertebrates, especially in the cervical series, which connects the head to the main body. Thus, fusion within the cervical series is hypothesized to have ecological and behavioural implications. Fused, anterior cervical vertebrae have evolved independently over 20 times in ecologically disparate amniotes, most commonly in pelagic, ricochetal, and fossorial taxa, suggesting an adaptive function for the ‘syncervical.’ Fusion may help increase out-force during head-lift digging or prevent anteroposteriorly shortened vertebrae from mechanically failing during locomotion, but no hypothesis for syncervical function has been tested. The syncervical of neoceratopsian dinosaurs is hypothesized to support large heads or aid in intraspecific combat. Tests of correlated character evolution within a ceratopsian phylogeny falsify these hypotheses, as the syncervical evolves before large heads and cranial weaponry. Alternative functional hypotheses may involve ancestral burrowing behaviour or unique feeding ecology in early neoceratopsians.

Acknowledgments

I thank David C. Evans, Hernán López-Fernández, and Gerry De Iuliis for their supervision during the course of this work, and Mary Silcox and Deborah McLennan for serving on my examination committee (at 9am on a Friday, no less). This project was inspired initially by

Darren Tanke and then progressed by Nicolás Campione and David Evans, which set the stage for my M.Sc. research. For access to specimens housed at their respective institutions and assistance in osteology and palaeontology collections, I thank Judy Galkin, Carl Mehling, Mark

Norell, Eileen Westwig (American Museum of Natural History, New York, NY), Kieran Shepard

(Canadian Museum of Nature, Ottawa, ON), Jack Horner (Museum of the Rockies, Bozeman,

MT), Kevin Seymour (Royal Ontario Museum, Toronto, ON), Brandon Strilisky (Royal Tyrrell

Museum of Paleontology, Drumheller, AB), Michael Brett-Surman, Darrin Lundy, John Ososky, and Charley Potter (National Museum of Natural History, Washington, D. C.). My supervisor, whose guidance helped develop my project and my future research direction in so many ways, graciously provided funding and support. Thanks for investing in me, David. For help with making my figures more artistic, putting up with me when I bombarded him with questions while he was busy working on his side-projects and thesis, and being a constant enabler of “Chocolate

PM,” I thank my office-mate Caleb Brown. Because all work and no play creates an insane graduate student, I am grateful to Kirstin Brink, Sarah Steele, Sophia Lavergne, and Alix

Cameron for all the brunches, cooking adventures, and glasses of wine during my twenty months in Toronto. I would also like to thank all of my lab mates, Kirstin Brink, Caleb Brown, Nicolás

Campione, Thomas Cullen, and Derek Larson, as well as Kentaro Chiba, Lorna O’Brien, and the

López-Fernández lab for their help and support. A special thanks to Nicolás Campione for helping with analyses, the many distracting discussions of science, being my TA ‘partner in crime’ for multiple courses, and overall serving as an unrecognized co-supervisor in so many iii respects. Finally, a big “Thank you” to all of my friends and family back home for believing in me and being there for me, even from a different country.

Table of Contents

ACKNOWLEDGMENTS...... III

TABLE OF CONTENTS...... V

LIST OF TABLES ...... VII

LIST OF FIGURES...... VIII

LIST OF APPENDICES...... X

CHAPTER 1 CONVERGENCE AND FUNCTION OF THE TETRAPOD SYNCERVICAL...... 1

1.1 ABSTRACT...... 1

1.2 INTRODUCTION...... 2

1.3 MATERIALS AND METHODS ...... 3

1.4 SYSTEMATIC REVIEW ...... 5 1.4.1 Mammalia...... 5 1.4.2 Reptilia ...... 14

1.5 GENERAL CHARACTERISTICS OF FUSED CERVICAL VERTEBRAE...... 18

1.6 WHAT IS THE FUNCTION OF THE SYNCERVICAL?...... 19 1.6.1 Function of the syncervical in fossorial taxa ...... 20 1.6.2 Function of the syncervical in ricochetal taxa ...... 21 1.6.3 Function of the syncervical in cetaceans...... 22 1.6.4 Function of the syncervical in hornbills...... 24 1.6.5 The mysterious syncervical of porcupines and pacaranas...... 24 1.6.6 Interpreting the syncervical as an adaptation ...... 25

1.7 IMPLICATIONS FOR FOSSIL TAXA ...... 26

1.8 CONCLUSIONS ...... 28

REFERENCES ...... 30

CHAPTER 2 HEAD SIZE, WEAPONRY, AND CERVICAL ADAPTATION: TESTING CRANIOCERVICAL EVOLUTIONARY HYPOTHESES IN CERATOPSIA ...... 61

2.1 ABSTRACT...... 61

2.2 INTRODUCTION...... 61

2.3 MATERIALS AND METHODS ...... 64 2.3.1 Syncervical Specimens and Measurements ...... 64 v

2.3.2 Construction of Phylogeny...... 65 2.3.3 Quantifying Relative Skull Size...... 66 2.3.4 Phylogenetic Analyses...... 68

2.4 DESCRIPTION OF UNFUSED SYNCERVICALS ...... 70 2.4.1 Atlas...... 70 2.4.2 Unfused C3 ...... 71

2.5 RESULTS...... 72 2.5.1 Quantifying Relative Skull Size...... 72 2.5.2 Syncervical Measurements ...... 74 2.5.3 Coevolution of Craniocervical Characters ...... 74

2.6 DISCUSSION ...... 76 2.6.1 Determining Relative Skull Size in Amniotes...... 76 2.6.2 Head Size in Ceratopsia...... 78 2.6.3 Function and Evolution of the Ceratopsian Syncervical...... 80

REFERENCES ...... 85

List of Tables

Table 1.1: Previously proposed functional hypotheses for the syncervical in each clade ...... 48

Table 2.1: Scorings for Auroraceratops into Makovicky (2010) ...... 95

Table 2.2: Relative head size in extant tax shown as percentages ...... 96

Table 2.3: Goodness-of-fit statistics for one-dimensional models when compared to the volumetric metric ...... 97

Table 2.4 Taxa that fall outside of one and two standard deviations of the mean when skull length is compared to femur length...... 98

Table 2.5: Residuals of ceratopsian taxa with known vertebral chains compared to one standard deviation from the mean ...... 99

Table 2.6: Measurements of fused and unfused syncerical elements used in the analysis ...... 100

vii

List of Figures

Figure 1.1: The number of convergences within higher-level taxonomic groups shown in a phylogenetic context...... 49

Figure 1.2: Syncervicals of some mammals...... 51

Figure 1.3: Syncervicals of some reptiles...... 53

Figure 2.1: An example of a ceratopsid syncervical ...... 101

Figure 2.2: A diagrammatic view of the measurements taken of fused and unfused syncervicals...... 103

Figure 2.3: The isolated, unfused atlases ...... 105

Figure 2.4: The isolated atlas-axis ...... 107

Figure 2.5: The isolated third cervical vertebra ...... 109

Figure 2.6: Measurements of fused and unfused syncervical elements ...... 111

Figure 2.7: Character evolution in Ceratopsia without the frill, first phylogeny ...... 113

Figure 2.8: Character evolution in Ceratopsia without the frill, second phylogeny..... 115

Figure 2.9: Character evolution in Ceratopsia without the frill, third phylogeny ...... 117

Figure 2.10: Character evolution in Ceratopsia with the frill, first phylogeny...... 119

Figure 2.11: Character evolution in Ceratopsia with the frill, second phylogeny ...... 121

Figure 2.12: Character evolution in Ceratopsia with the frill, third phylogeny ...... 123

Figure 2.13: Relative head size in amniotes based on previously proposed metrics..... 125

Figure 2.14: Absolute head size reconstructed on a phylogeny of Ceratopsia ...... 127

viii

Figure 2.15: Absolute head size including the frill reconstructed on a phylogeny of Ceratopsia...... 126

List of Appendices

Appendix 1...... 55

Appendix 2...... 131

x 1

Chapter 1 Convergence and Function of the Tetrapod Syncervical 1.1 Abstract

Non-pathological fusion of the anterior cervical vertebrae occurs convergently in numerous extant and extinct reptiles and mammals, suggesting that the formation of a

‘syncervical’ is an adaption that arose to confer biomechanical advantage(s) in these lineages.

We review its anatomy and evolution in a broad phylogenetic context for the first time, and also provide a comprehensive summary of proposed adaptive functional hypotheses. While the syncervical generally consists of only two vertebrae (hornbills, porcupines, etc.), fusion of all seven cervical vertebrae occurs in some cetaceans. Based on a review of the ecologies of the groups that have a syncervical, fusion most often occurs in fossorial and pelagic taxa. In fossorial taxa, the syncervical likely serves to increase the out lever force during head-lift digging. The syncervical may serve to stabilize the head and neck during locomotion in ricochetal rodents and cetaceans, although considerable variation exists in its composition without apparent variability in locomotion or ecology. This indicates gaps in our knowledge of these taxa and suggests that the highly reduced cervical vertebral centra may require the syncervical to form to prevent failure of the vertebrae. Syncervicals in hornbills may have evolved in response to their unique casque-butting behaviour, or due to increased head mass. This increased understanding of the syncervical in extant taxa allows more accurate interpretation of the ecologies of extinct animals with this unique vertebral structure. Syncervicals occur convergently in several groups of marine reptiles; in plesiosaurs and post-Triassic ichthyosaurs, further stabilization of the neck at the atlas-axis joint may aid in locomotion or stabilize the cranio-cervical. The hypothesis that the syncervical supports the large heads in neoceratopsian dinosaurs is not supported by our comparative study, as cervical fusion in extant terrestrial animals occurs in predominatly small 1

2 forms, with average-sized heads. Overall, the origin and function of the syncervical is poorly understood in every group, emphasizing the need for comparative biomechanical studies to test the functional hypotheses summarized and proposed here.

1.2 Introduction

The degree of mobility between successive units of the vertebral column of vertebrates is related to many behaviours (e.g., Johnson & Shapiro, 1998; Long et al., 1997). Increasing mobility by adding vertebrae has occurred in numerous lineages, and has been related to numerous aspects of locomotion and feeding ecology (Müller et al., 2010). Fusion of the vertebrae significantly reduces mobility in areas of the vertebral column, which also has behavioural and ecological implications (e.g., Gambaryan, Zherebtsova & Platonov, 2005;

Gupta, 1966; James, 2009; Mulder, 2001). Non-pathological vertebral fusion in many lineages occurred as an adaptation for body support or locomotion. The best known examples include multiple convergences of fused sacra in tetrapods, for body support and rigidity (e.g., Abitbol,

1987; Hildebrand & Goslow, 2001), and in the caudal region of birds and oviraptorid dinosaurs, in which the formation of a pygostyle is hypthesized to anchor tail remiges for display (Persons

IV, Currie & Norell, In press) and aerodynamics (e.g., Gatesy & Dial, 1996; Hildebrand, 1985).

Fusion of anterior cervical vertebrae is another form of vertebral fusion that has occurred convergently in multiple tetrapod lineages with a wide range of ecologies, from cetaceans to hornbills, but has received comparatively little attention in the literature. Because the cervical series provides a direct connection between the skull, which houses all sensory and feeding anatomy, and the body, mobility in this region will influence many aspects of an animal’s ecology, such as feeding behaviour (e.g., Herrel, Van Damme & Aerts, 2008; Montuelle et al.,

2012).

Gupta’s (1966) review of cervical fusion in rodents is currently the most comprehensive study to focus solely on the occurrence of fused cervical vertebrae in any higher taxonomic group. He notes that fused cervical vertebrae can vary in position along the cervical column, and the number of fused vertebrae can vary within a genus or between subspecies. He also notes examples of infrequent fusion (Gupta, 1966), likely attributable to some pathology. Because pathologies occur in only a few members of a species and are easily recognizable because of the deformation they cause (e.g., Félix, Haase & Aguirre, 2007; Gill & Fisk, 1966; Kompanje, 1995;

Kompanje, 1999; Mulder, 2001; Rothschild, 1987; Rothschild & Berman, 1991), these species- or subspecies-specific occurrences of fusion that occur in most members of a population are likely morphological adaptations.

Here, we review occurrences of cervical vertebral fusion in tetrapods for the first time.

We will also provide ecological, behavioural, and morphological data that may have contributed selective pressures during the evolution of fused cervical vertebrae with the goal of inspiring future research on this highly convergent, homoplasious trait. Because a paucity of previous functional research exists on this trait, the number of functional hypotheses is limited (Table

1.1). However, we aim to identify correlations in the aforementioned aspects of the biology of these taxa to propose overarching hypotheses to best explain this phenomenon in the various forms in which it exists.

1.3 Materials and Methods

A survey of the taxa noted in the literature to have syncervicals was taken at the

American Museum of Natural History (AMNH), Field Museum of Natural Hisotry (FMNH),

Royal Ontario Museum (ROM), and Smithsonian Institute (USNM) to confirm the presence of syncervicals in these groups and document its composition in different species. For taxa

4 unavailable at these institutions, we relied on reports in the literature that consisted of both genus- and species-level data, which tend to lack discussion of how this trait varies throughout ontogeny. Because strictly fossorial mammal populations show a high amount of reproductive isolation (e.g., Nevo, 1979) and Gupta (1966) found variation between subspecies of ricochetal rodents, counts were also taken from subspecies when possible.

The use of genus-level descriptions is problematic. For example, the genus Amblysomus has been divided into Amblysomus and Neamblysomus after many of these studies were performed.

The only species we found within either genus to show vertebral fusion is N. juliane (see below), although we were unable to access specimens of every species. At this point, the pattern of fusion within members of these genera is unclear and requires future clarification. While this uncertainty is not critical for our review, it provides an example of the importance of species- level discussion in future studies. The species examined for this review were limited, and we therefore apply the generalizations in the literature to our analysis with the caveat that more precise studies of fossorial mammals are needed.

Vertebral fusion is noted to progress through ontogeny in some mammal groups (e.g.,

Buchholtz, 2001a; Hatt, 1932; Ray, 1958). The effects of ontogeny do not appear to have been recognized in earlier studies of syncervical formation, and therefore, variability of fusion within a genus (e.g., Dipodomys; Gupta, 1966) might be attributable to the age of the specimens examined. In the current study, we assessed maturity of the specimens based on the ossification of the epiphyses of limb bones of mammals and recorded the number of fused vertebrae in adult specimens.

Given the number of convergences, it is not surprising that no unifying term exists for fused cervical vertebrae in tetrapods. In neoceratopsian dinosaurs, the anterior, fused cervical 4

5 vertebrae are referred to as the syncervical or cervical bar (e.g., Campione & Holmes, 2006;

Tsuihiji & Makovicky, 2007). Sometimes this structure in cingulates is termed the mesocervical

(Galliari, Carlini & Sánchez-Villagra, 2010; Serres, 1865), whereas fusion of the posterior cervical vertebrae to the anterior-most thoracic vertebra(e) is the metacervical (Serres, 1865).

Cervical ankylosis is sometimes used in the cetacean literature (e.g., Rice, 1967), as is

‘synarcual’ (e.g., Muizon & Daryl, 2002) although neither is prevalent. However, formal terminology for fused cervical vertebrae in other taxa is lacking. The term ‘syncervical,’ first introduced by Ostrom and Wellnhofer (1986) for Triceratops is probably the most frequently used term for fused, anterior cervical vertebrae, and we feel the frequency of this term within a clade merits its use for other occurrences of similar, analogous structures. Here, we use

‘syncervical’ to describe nonpathological cervical vertebral fusion.

1.4 Systematic Review

The results of our literature and museum collection survey coupled with optimizations of syncervical presence on mammalian phylogenies (Bininda-Emonds et al., 2007) found that the syncervical has convergently evolved at least 20 times in amniotes (Figure 1). These independent evolutionary events have occurred in taxa spanning wide ranges of ecologies, including fossorial, ricochetal (saltatorial), marine, and aerial lifestyles, as well as fossil taxa for which a variable amount of data is available on aspects of their lifestyles. General aspects of the biology of these taxa are presented below, along with a brief discussion of the anatomy of their respective syncervicals.

1.4.1 Mammalia

Mammals undoubtedly have the most numerous and diverse occurrences of independent, derived cervical fusion among any clade within the Tetrapoda. The atlas almost never contributes

6 to mammalian syncervicals (except in cetaceans), which is different than the typical reptilian syncervical. Unfortunately, the fossil record of many small-bodied mammals is restricted to dental remains, so the evolution of the syncervical in some of the clades noted below can only be discussed in terms of extant taxa. However, given the variability of this character between some subspecies (Appendix 1), it is possible that the syncervical has converged multiple times within species and may have evolved very recently in some cases.

1.4.1.1 Notoryctes (Marsupialia: Notoryctidae)

The marsupial moles (Notoryctes spp.) are subterranean mammals native to Australia with a generalist diet (Pavey, Burwell & Benshemesh, 2012). Syncervicals in this genus appear to be composed of five cervical vertebrae with anterolaterally and dorsoventrally short centra

(C2-6; Appendix 1). The marsupial mole primarily uses head-lift digging to begin its tunnels

(Hildebrand, 1985). While this digging style can be used reinforce the walls of a tunnel system, the sand in which Notoryctes digs does not maintain a tunnel-like configuration (Reichman &

Smith, 1990). Like many subterranean mammals, little is known about its biology.

1.4.1.2 Cingulata (Eutheria: Xenarthra)

Cingulata is the Order that includes extant and extinct armadillos and their extinct relatives, glyptodonts and pampatheres (Figure 1.2A). The composition of the syncervical varies between two (e.g., Cabassous chacoensis; Appendix 1) to five vertebrae in some glyptodonts

(Huxley, 1865). All cervical vertebrae are dorsoventrally and anteroposteriorly short, but mediolaterally wide, with xenarthrous processes characteristic of all xenarthrans (Rose & Emry,

1993b). Most non-axial cervical vertebrae have reduced or absent neural spines, but the axial neural spine will extend along the entire length of the syncervical. Most extant armadillos are fossorial, utilizing both scratch-digging and head-lift digging strategies (Hildebrand, 1985;

Milne, Vizcaíno & Fernicola, 2009). However, Tolypeutes has more cursorial habits, similar to what is hypothesized for glyptodonts, but fossoriality is likely the ancestral condition for cingulates (Milne et al., 2009; Vizcaíno et al., 2011).

1.4.1.3 Chrysochloridae (Afrosoricida: Chrysochloroidea)

Cervical fusion has been reported previously in the genus Amblysomus (Rose & Emry,

1983; Rose & Emry, 1993a). The seven species are all strictly subterranean, although little is known about their biology or preferred digging strategy, they are considered head-lift diggers capable of producing powerful out-forces with their skulls (Bateman, 1959; Hildebrand, 1985).

The species A. julianae and A. gunningi have been separated into a distinct genus,

Neamblysomus, since the original reports of fusion within the genus (Bronner, 1995). In our survey of museum specimens, we did not find fusion in any species within the genus

Amblysomus (A. hottentotus, USNM 351327, USNM 351328, USNM 351326, USNM 344221,

USNM 344218; A. iris, USNM 342426, USNM 342425, USNM 342424), but did find that the axis and third cervical vertebra of Neamblysomus julianae were fused (USNM 398632). The cervical centra are anteroposteriorly shortened, and the axial neural arch is large. We therefore suggest that fusion is limited to the genus Neamblysomus until it can be confirmed in

Amblysomus.

1.4.1.4 Geomyidae (Rodentia: Geomyoidea)

Pocket gophers are small, subterranean mammals native to North and Central America

(Spradling et al., 2004). Fusion, when present, is between the axis and third cervical vertebra and is only found in the genera Cratogeomys, Orthogeomys, and Pappogeomys (Appendix 1), suggesting that fusion would have only evolved once in Geomyidae (Spradling et al., 2004). Like in other fossorial mammals, their cervical vertebrae, including those of the syncervical, are

8 anteroposteriorly and dorsoventrally short, and the vertebrae of the syncerical have high neural spines relative to those of the consecutive cervical vertebrae. Fusion varied between subspecies within species of these genera (Appendix 1), but the factors affecting this variation are unknown.

Some of these taxa are thought to be scratch diggers (e.g., Lessa & Stein, 1992), although the limb morphology of head-lift and scratch diggers is similar (Hildebrand, 1985).

1.4.1.5 Dipodomyinae (Rotendia: Heteromyidae)

Kangaroo rats (Dipodomys spp.) are small, ricochetal rodents native to North America.

Syncervicals are not described for Microdipodomys, the sister group to Dipodomys, or other heteromyids, suggesting an independent evolution of a syncervical in this Family (Alexander &

Riddle, 2005). Fusion in this genus varies between species and ontogenetically within an individual (Gupta, 1966; Appendix 1; Hatt, 1932; Howell, 1932). The cervical vertebrae of

Dipodomys have anteroposteriorly and dorsoventrally short centra, but the axial neural spine is tall and extends the length of all fused cervical vertebrae (Emerson, 1985). Hatt (1932) noted that fusion through ontogeny begins in the neural spines, continues to the transverse processes, and finishes with the centrum. Howell (1932) hypothesized that fusion may be correlated with the degree of ricochetal adaptations, but recognized that a lack of fusion in taxa such as the jerboa

Allactaga contradicted this hypothesis. Hatt (1932) notes that ricochetal rodents, like Dipodomys, have relatively large heads, but hypothesizes that fusion of the cervical vertebrae is a result of the neck shortening to less than 15% thoracolumbar length. He also notes that it is plausible the syncervical functions during fossorial behaviour, but he was not aware of any fossorial taxa with syncervicals (but see above). Dipodomys primarily uses scratch-digging to loosen soils, although can also use its teeth to break through extremely tough soils (Nikolai & Bramble, 1983).

1.4.1.6 Pedetidae (Rodentia: Anomaluromorpha)

Fusion of the cervicals in springhares (Pedetes) has been uncertain. Hatt (1932) found fusion in P. surdaster, but not P. cafer. Howell (1932) notes that fusion does not occur in

Pedetes, although he was not examining this genus at the species level. Fusion of the axis and third cervical vertebra occurs in P. surdaster (FMNH 18836) and P. capensis (ROM 85746, but none in FMNH 60073), but these elements were not fused in specimens of P. cafer (USNM

49647, USNM 295258, USNM 221381). The cervical vertebrae are not as condensed as in other ricochetal rodents, but still exhibit some anteroposterior shortening. The axial neural spine is the tallest neural spine of the cervical series and extends over the third cervical vertebra.

Springhares inhabit open areas of eastern and southern Africa and burrow in areas with sandy soils near short-grass (Butynski & Mattingly, 1979; Matthee & Robinson, 1997). Burrows are created using a behaviour thought to incorporate the forelimbs, hind limbs, and head. The forelimbs are used to break and remove soil, while the hind limbs and head are used to remove soil from the burrow through the entrance (Butynski & Mattingly, 1979). This digging style is comparable to scratch-digging (Hildebrand, 1985).

1.4.1.7 Spalacidae (Rodentia: Muroidea)

The spalacids Spalax (blind mole rats) and Myospalax (zokors) are documented to have fused cervical vertebrae. Cervicals two through four are fused in Myospalax and four through six are fused in Spalax (Gambaryan et al., 2005). All spalacids are fossorial, and these two genera use a head-lift digging style, while other members of the Family will utilize chisel-tooth digging

(Hildebrand, 1985).

1.4.1.8 Erethizontidae (Rodentia: Hystricomorpha)

New world porcupines (Family Erethizontidae) inhabit North and South America. Fusion is known in all members except Chaetomys, in which the presence or absence of fusion is currently unknown (Ray, 1958; Figure 1.2B). In the subfamily Erethizontinae, the axis and third cervical vertebra have fused centra and neural spines in which the axial neural spine extends both slightly anteriorly and posteriorly to the posterior extreme of the C4 centrum (Figure 1.2B; Ray,

1958). Extant species are adapted for arboreal locomotion, and studies of fossil taxa suggest this ecology was present in early members of this group (Candela & Picasso, 2008; Woods, 1973).

1.4.1.9 Cetacea (Laurasiatheria: Cetartiodactyla)

Cetaceans are the only mammals to typically incorporate the altas into the syncervical, but syncervical composition is variable in the clade (Buchholtz & Schur, 2004; Appendix 1;

Rice, 1967; Yoshida et al., 1994). Variability exists between species, but has also been noted within a species (Buchholtz & Schur, 2004). In our survey, we found that most delphinids only fuse their atlas and axis with little or no variation among or within species (e.g., Tursiops truncates and Deliphinus delphis; Appendix 1). Variation was uncommon within species of

Mesoplodon, although variation exists among species (Appendix 1). Globicephala melas exhibited highly variable syncervical composition (Figure 1.2C; Appendix 1) that may follow the pattern of fusion progression described by Hatt (1932) for ricochetal rodents (see above).

Without knowing the age of these individuals, it is difficult to assess if variation in G. melas could be explained by ontogeny. However, the syncervical of another species, G. macrorhynchus, fully develops prenatally (Ogden et al., 1981), and this early development might be common to all cetaceans, as very young delphinid specimens had fused cervicals.

The cervical vertebrae of all cetaceans are anteroposteriorly short, but the atlas remains relatively robust (e.g., Flower, 1885). In closely related taxa, a difference in centrum length between fused and unfused homologous vertebrae is not apparent. Fusion occurs between the centra and neural spines. Thin neural arches are still maintained in most taxa, but in Physeter and

Kogia, the neural arches are reduced to small prominences on the dorsal centrum and ventral neural spine, making identifying individual vertebrae sometimes difficult. The neural spine of the axis is the tallest neural spine, with other cervical vertebrae having reduced or absent neural spines. In taxa with a fused atlas-axis, the axis is the most robust cervical centrum, but in

Physeter, which fuses C2-C7, the atlas is nearly as robust as the entire syncervical.

While no hypothesis has been formulated for why the syncervical has evolved in cetaceans, Buchholtz (1998) hypothesized that it evolved multiple times in the clade. However, an optimization on a recently published phylogeny suggests syncervicals are plesiomorphic for extant cetaceans with some losses (Figure 1.2C). This optimization assumes homology between the syncervical of Physeter and other cetaceans, which may not be true given the differences in composition mentioned above.

Seven cervical vertebrae are retained in all cetaceans, but their centra are extremely reduced (e.g., Buchholtz & Schur, 2004; Flower, 1885). This reduction has been hypothesized to limit cranial mobility as the body is propelled using the caudal fin (Buchholtz, 1998; Gupta,

1966; Long et al., 1997). The degree of mobility throughout other aspects of the vertebral column are known to correlate with ecological feeding behaviours in at least some species (Fish,

2002). Taxa with no fused cervical vertebrae, such as monodontids (belugas and narwhals) and some river dolphins, have very flexible necks and are required to traverse around submerged glaciers or forests (Flower, 1867; Martin & Silva, 2004; Muizon & Daryl, 2002; Rice, 1967).

Furthermore, cetaceans experience a variety of stresses on their cranium, such as frictional and pressure components of drag (see Fish, 2000 and references therin) and strain during feeding

(Field et al., 2010).

1.4.1.10 Castoridae (Rodentia: Castorimorpha)

While extant beavers are restricted to aquatic habitats, extinct taxa of this Family had more diverse ecologies (e.g., Samuels & Van Valkenburgh, 2008; Samuels & Van Valkenburgh,

2009). One of the species was shown to have fossorial habits, Paleocastor fossor, was described with a fused axis and third cervical vertebra in an adult specimen, but not in a juvenile (Peterson,

1905). This ontogenetic pattern is seen in other terrestrial mammalian taxa (Hatt, 1932; Ray,

1958). Paleocastor has been reconstructed as a chisel-tooth digger by Samuels and

VanValkenburgh (2009). Other taxa included in this study have not had post-cranial elements described (Martin, 1987), so the prevalence of the syncervical in fossil castorids remains unknown. However, extant beavers do not possess syncervicals.

1.4.1.11 Dinomyidae (Rodentia: Chinchilloidea)

Only one species of the diverse Family Dinomyidae exists today. Dinomys branickii, the pacarana, is an arboreal rodent native to South America (White & Alberico, 1992). Like many other mammalian taxa, its syncervical consists of the axis and third cervical vertebra, and its syncervical is very similar to that of Erethizon in morphology without the anterior extension of the axial neural spine (Ray, 1958). The past diversity of this clade is inferred from a speciose fossil record that is primarily composed of incomplete remains (e.g., Rinderknecht, Bostelmann

T & Ubilla, 2011), thus making tracing the syncervical through the clade’s evolutionary history difficult. Dinomys branickii has a relatively large head (White & Alberico, 1992), which has

13 been proposed as a selective pressure for the syncervical in other taxa, but this hypothesis has never been proposed for this group.

1.4.1.12 Epoicotheriidae (?Pholidota: Palaeanodonta) †

Epoicotheriid palaeanodonts are an extinct clade of mammals with uncertain phylogenetic relationships. Two taxa, Epoicotherium and Xenocranium, from the Oligocene of the western United States possess syncervicals composed of the axis C3-C5 (Rose & Emry,

1983). These taxa have been hypothesized to be the most efficient scratch-diggers to have ever lived based on aspects of their postcranial skeletal morphology (Rose & Emry, 1983). Their syncervical is hypothesized to provide a more stabile fulcrum for employing a head-lift digging strategy (Rose & Emry, 1983).

1.4.1.13 Mesoscalops (Proscalopidae) †

Mesoscalops montanensis is a proscalopid mole from the Miocene of Montana with fused

C2-C5(Barnosky, 1981). Fused anterior cervical vertebrae are hypothesized for all proscalopids, but only those of M. montanensis are known (Barnosky, 1981). Based on the presence of a syncervical and inferred out force production of the skull generated from lever arms, M. montanensis is hypothesized to have been a head-lift digger, and fusion of the cervical vertebrae is hypothesized to act as to increase the attachment area of muscles and reinforce the neck

(Barnosky, 1981).

1.4.1.14 Dipodidae (Rodentia: Dipodoidea)

Fusion of the cervical vertebrae has been documented in the jerboa genera Dipus,

Jaculus, and Stylodipus (Hatt, 1932) and is reported in the subfamily Cardiocraniinae (Miljutin,

2008). Fusion tends to occur between most or all post-atlantal vertebrae. The cervical vertebra are all anteroposteriorly shortened and are covered by the long, tall axial neural spine (Emerson, 13

1985). As in the kangaroo rats and mice, fusion of the cervical vertebrae is thought to be associated with ricochetal locomotion (Hatt, 1932). They are native to the deserts of Asia and northern Africa and are ecologically very similar to North American dipodomyines (Feniuk &

Kazantzeva, 1937; Happold, 1967). Much less of their biology is known compared to the dipodomyines, but field studies do report digging using the forelimbs (Feniuk & Kazantzeva,

1937).

1.4.2 Reptilia

Syncervicals have evolved fewer times in reptiles and are more frequent in extinct taxa.

In fact, fusion has only occurred in one living reptile, the hornbill. Unlike a typical mammalian syncervical, the reptilian syncervical incorporates the atlas. Ecological data are more difficult to obtain for fossil taxa, especially in clades without any living members or obvious ecological analogues. Therefore, the information we are able to present here about some of these taxa is limited.

1.4.2.1 Bucerotidae (Aves: Coraciiformes)

All hornbills have a fused atlas and axis (Figure 1.3A). The atlas forms a concave, cup- shaped cotyle, which receives the single occipital condyle. The axial neural spine is high, and the syncervical is anteriorposteriorly short compared to the successive cervical vertebrae. The syncervical is thought to aid in supporting a relatively large head that is equipped with a casque in many species (Kemp, 2001). The skulls of hornbills and toucans weigh relatively the same amount, however, and both groups use a ballistic method of feeding (Baussart & Bels, 2011;

Baussart et al., 2009; Seki, Bodde & Meyers, 2010), yet toucans are not known to have specialized adaptations in their cervical vertebrae. In some of the casqued species, a behaviour involving head-to-head combat has been observed, called ‘casque-butting’ or ‘aerial jousting’

15 and locking of the bills, called ‘bill grappling’ (Cranbrook & Kemp, 1995; Kasambe, Charde &

Yosef, 2011; Kinnaird, Hadiprakarsa & Thiensongrusamee, 2003). These interactions, which have been documented between males or males and females, can occur while two birds are in flight during aerial bouts, or one bird may come down on an individual perched in a tree

(Kasambe et al., 2011). This behaviour is still not well-understood, but it may play a role in mate-choice or male-male competition and is expected to impart force on the craniocervical joint

(Kasambe et al., 2011).

1.4.2.2 Ichthyopterygia †

Ichthyosaurs are open-water (pelagic), piscivorous reptiles that evolved during the

Mesozoic. The syncervical of ichthyosaurs contains the atlas and axis (Figure 1.3B) The earliest taxa lack fusion, and the syncervical evolves after the Triassic-Jurassic boundary (Egerton, 1836;

Kirton, 1983; McGowan & Motani, 2003; Nace, 1939). All cervical vertebrae of these taxa are anteroposteriorly shortened. Fusion of these elements is hypothesized to have stabilized the neck and improved hydrodynamic shape (Buchholtz, 2001b), which, in turn, is correlated with the evolution of thunniform (fast swimming) locomotion in Jurassic ichthyosaurs (Motani, You &

McGowan, 1996). In Platypterygius, fusion of the atlas and axis may have occurred early in ontogeny (Maxwell & Kear, 2010), similar to the pattern of fusion in cetaceans (Ogden et al.,

1981), but other ichthyosaurs, such as Ichthyosaurus communis, may fuse their syncervical at different stages of ontogeny (Buchholtz, 2001a).

1.4.2.3 Plesiosauria (Reptilia: Sauropterygia) †

Plesiosaurs, like ichthyosaurs, are piscivorous pelagic marine reptiles from the Mesozoic.

Fusion of the atlas and axis (Figure 1.3C) is known in both the long-necked, small-headed plesiosauroids and short-necked, large-headed pliosauroids (Bakker, 1993; Owen, 1847; Welles,

1943). The atlas forms a cup-shaped cotyle, and the axis has a dorsoventrally short neural spine that extends posteriorly beyond the posterior extreme of the axial centrum. This structure appears to have evolved only once in this group or convergently early in the evolution of these two broad clades (e.g., Benson et al., In press; Stutchbury, 1846; Welles, 1943). Many plesiosaurs also fuse their cervical ribs to the cervical vertebrae (Welles, 1943; White, 1940), and a general trend toward stiffening the cervical series from a plesiomorphically flexible neck in long-necked elasmosaurids is hypothesized (Zammit, Daniels & Kear, 2008). Bakker (1993) hypothesized that the rigid attachment site for muscles that run from the neural arches to the skull and the cup- shaped atlas cotyle would allow for faster and more powerful skull movements, which might have aided during feeding. This hypothesis is the only one proposed for the syncervical in plesiosaurs.

1.4.2.4 Ceratopsia (Dinosauria: Ornithischia) †

Ceratopsians are terrestrial quadrupedal herbivores from the Late Jurassic to Late

Cretaceous Periods. The ceratopsian syncervical contains the first three cervical vertebrae

(Campione & Holmes, 2006; Tsuihiji & Makovicky, 2007; Figure 1.3D). The atlas forms a cup- shaped cotyle, and atlantal neural arches are variably fused to the centrum (Campione & Holmes,

2006). In taxa such as Protoceratops and Leptoceratops, the axial neural spine is high and hatchet shaped, and fusion only occurs between the vertebral centra (Brown & Schlaikjer, 1940;

Sternberg, 1951). In ceratopsids, such as Triceratops and Centrosaurus, the axial neural spine becomes posteriorly inclined, and fusion occurs between the neural spines of the axis and C3

(e.g., Campione & Holmes, 2006; Ostrom & Wellnhofer, 1986; Tsuihiji & Makovicky, 2007).

Because Late Cretaceous ceratopsian dinosaurs (Ceratopsidae) have large skulls and elaborate cranial ornamentation, hypotheses for the function of the syncervical have focused on

17 these two aspects of cranial morphology, namely that the syncervical helped to support the large skull (Dodson, Forster & Sampson, 2004; Sereno et al., 2007; Tanke & Rothschild, 2010), acted as a buttress during intraspecific combat (Sampson, 1997; Spassov, 1979), or increased cranial mobility with the ball-and-socket atlanto-occipital joint (Bakker, 1986; Farlow & Dodson, 1975;

Molnar, 1977; Ostrom & Wellnhofer, 1986). These hypotheses are all untested and may be difficult to test directly given the difficulties associated with reconstructing combative behaviour from the fossil record (see Dodson et al., 2004 and references therein).

1.4.2.5 Ankylosauria (Dinosauria: Ornithischia) †

Ankylosaurs are heavily armoured, terrestrial herbivorous quadrupeds of the late

Mesozoic. A syncervical containing the first two cervical vertebrae (Figure 1.3E) evolved independently in large-bodied taxa in Ankylosauridae (Saichania) and Nodosauridae

(Edmontonia and Panoplosaurus) (Maryanska, 1977; Sternberg, 1921; Sternberg, 1940;

VanBuren, Arbour & Evans, 2012; Vickaryous, Maryanska & Weishampel, 2004). Fusion occurs between the centra and between the atlantal neural arch and axial neural spine. The atlantal cotyle, as in other reptilian syncervicals, forms a cup-shaped cotyle. The axial neural spine is relatively short, both anteroposteriorly and dorsoventrally. When the syncervical evolved in these families in uncertain given the low resolution of recent systematic studies of ankylosaurs

(Thompson et al., 2012) and incomplete or missing remains of cervical vertebrae for many taxa.

No functional hypotheses exist for the syncervical in any of these taxa.

1.4.2.6 Pterosauria †

Pterosaurs are flying reptiles that were present throughout the Mesozoic. A syncervical containing the atlas and axis (Figure 1.3F) evolved in the pterosaurs Pteranodon, Nyctosaurus,

Ornithocheirus, and azhdarchids including Quetzalcoatlus, Azhdarcho, and Dsungaripterus

(Bennett, 2001; Howse, 1986; Witton & Naish, 2008). A cup-shaped atlantal cotyle is present, and the axial neural spine is relatively high. The syncervical is small relative to successive cervical vertebrae (Howse, 1986; Witton & Naish, 2008). Uncertain phylogenetic affinities (e.g.,

Kellner, 2003; Lü et al., 2008; Unwin, 2003) and poor preservation of many species hypothesized to be closely related to those with syncervicals hinders our ability to accurately track the evolution of the syncervical in pterosaurs. Pterosaurs like Pteranodon and Nyctosaurus possess elaborate crests, and these crests were likely for display purposes rather than for flight control (Elgin et al., 2008). Other forms, like Zhejiangopterus and Quetzalcoatlus have large heads, especially for taxa with long, slender necks (Wilkinson & Ruxton, 2012), but Witton and

Naish (2008) hypothesize the syncervical was too diminuitive to have been an attachment site for powerful head support. Instead, they hypothesize that the syncervical compliments the rigidity of the post-axial cervical vertebrae to further stabilize the neck (Langston, 1981; Nessov, 1984;

Witton & Naish, 2008).

1.5 General Characteristics of Fused Cervical Vertebrae

Generally, only two cervical vertebrae fuse (e.g., Howse, 1986; Kemp, 2001; Ray, 1958;

Vickaryous et al., 2004). In reptiles, fusion usually occurs between the atlas and axis (e.g.,

Bakker, 1993; Howse, 1986; McGowan & Motani, 2003; Vickaryous et al., 2004), while in mammals, fusion tends to occur between the axis and third cervical vertebra (e.g., Gupta, 1966;

Hatt, 1932; Ray, 1958). Mammals, which have two occipital condyles (reptiles have one), rely on their specialized atlas-axis joint to maintain the skull’s range of motion (e.g., Evans, 1939), and this requirement is likely the reason for the regional difference of this fusion. Many mammals with syncervicals also have anteroposteriorly shortened cervical centra, although this is not true of all taxa (e.g., New World porcupines, pacarana). In neoceratopsians, ankylosaurs,

19 hornbills, and plesiosaurs as well as some ichthyosaurs, the morphology of the occipital condyle is circular instead of reniform (the plesiomorphic morphology), and the cotyle of the atlas is cup- shaped, allowing for equal if not enhanced mobility at the cranio-cervical joint compared to reptiles without syncervicals (e.g., Bakker, 1993; Bakker, 1986; Farlow & Dodson, 1975;

Maxwell & Kear, 2010; Molnar, 1977). It does not appear that reptilian syncervicals are associated with shortening cervical centra, except in the case of ichthyosaurs.

However, this structure is quite variable. For example, neoceratopsians fuse the first three cervical vertebrae to form the syncervical. In mammals, the number of fused elements can include all seven cervical vertebrae in some cetaceans (e.g., Cummings, 1985; Fraser, 1945), and syncervical composition among mammals spans this range from two to seven vertebrae (e.g.,

Galliari et al., 2010; Gupta, 1966; Hatt, 1932). The zokor Spalax is unique as it has cervicals four and five fused (Gambaryan et al., 2005), demonstrating regional differences in cervical fusion.

1.6 What is the function of the syncervical?

Syncervicals likely serve different functions in different organisms, given the ecological diversity of the taxa reviewed here, despite being similar in composition or morphology.

However, all extant taxa with syncervicals fall into four broad ecological categories, allowing a comparative approach can be used to make predictions about the evolution of this structure. By far, fossoriality characterizes most of the extant taxa with syncervicals, including Notoryctes,

Neamblysomus, Myospalax, and the armadillos. Rodents that converged on ricochetal locomotion also converged on having a syncervical, so this locomotor style can be used as a second grouping for the dipodids, heteromyids, and pedetids. Cetaceans (pelagic) and hornbills

(volant) are each unique in lifestyles among taxa with syncervicals and cannot be grouped with other taxa for ecological comparison. Outside of these categories are New World porcupines and

20 pacaranas, which have similar lifestyles that do not present apparent selective pressures for the evolution of the syncervical.

1.6.1 Function of the syncervical in fossorial taxa

Many authors have hypothesized that fused cervical vertebrae are an adaptation for fossorial lifestyle (Asher et al., 2007; Barnosky, 1981; Gambaryan et al., 2005; Rose & Emry,

1983; Rose & Emry, 1993b; Shimer, 1903). How fusion of the cervical vertebrae might assist in fossorial behaviour, however, is unclear. Some hypothesize that the syncervical acts as a better fulcrum during digging (Rose & Emry, 1983; Rose & Emry, 1993b). This hypothesis supposedly centres around the idea that the cervical muscles, which divide into multiple slips and insert onto individual vertebrae (Nishi, 1916), might increase in out-force production because the muscle slips inserted onto the vertebrae of the syncervical would contract a single element simultaneously. The vertebrae of fossorial taxa are typically anteroposteriorly shortened, as well

(Flower, 1885; Gambaryan et al., 2005), so fusion may be required in some diggers with extremely short necks to avoid mechanical failing of the vertebrae.

Many of the fossorial taxa with syncervicals whose digging style has been studied use a head-lift digging to create their burrows (Bateman, 1959; Hildebrand, 1985). Head-lift digging not only produces high strain on the skull, but also requires the production of strong out-force by the skull (e.g., Barnosky, 1981; Hildebrand, 1985). Therefore, both functional hypotheses may be valid. Not all head-lift diggers have syncervicals, but not all taxa that share similar ecologies should be expected to have the exact same adaptations.

Our survey found that fossorial squamates and amphibians lack syncervicals, which is unexpected given the prevalence of this structure in fossorial mammals. Fossorial frogs differ from fossorial mammals by using their hind feet to dig (e.g., Emerson, 1976). Fossorial 20

21 squamates (e.g., Daniels et al., 2005; Navas et al., 2004) and caecillians (e.g., Summers &

O'Reilly, 1997) have independently evolved worm-like bodies with reduced or absent limbs, and the similar bauplan of snakes is hypothesized to be related to fossorial behaviour in Serpentes

(e.g., Vidal & Hedges, 2004). Taxa without limbs penetrate the soil with their heads without creating permanent burrow structures like fossorial mammals, and the substrate collapses behind them as they locomote (e.g., Pough et al., 2004; Summers & O'Reilly, 1997). Differences in digging style perhaps in combination with evolutionary constraints imposed by forelimb posture

(sprawling in amphibians an squamates, parasagittal in mammals) may explain morphological and behavioural differences between fossorial squamates and amphibians and fossorial mammals. However, this hypothesis requires further examination.

1.6.2 Function of the syncervical in ricochetal taxa

Like fossorial taxa, ricochetal rodents have shortened necks, and functional hypotheses for the syncervical have focused on the relationship between their unique locomotor style and cervical shortening (Hatt, 1932; Howell, 1932; Lull, 1904; Nikolai & Bramble, 1983). Fusion has been hypothesized to further shorten and stabilize the neck (Hatt, 1932; Nikolai & Bramble,

1983), supposedly to avoid mechanical failing of the vertebrae, as in fossorial mammals.

Alternatively, restricting movements of the head by fusing the cervical vertebrae has been hypothesized to have a locomotor advantage for ricochetal rodents (Hatt, 1932; Howell, 1932).

Hatt (1932) hypothesized that neck shortening and cervical fusion reduces head-bobbing, but

Nikolai and Bramble (1983) note that no functional model has been proposed for an advantage to this restriction. Howell (1932) hypothesized that mobility between the cervical vertebrae is actually disadvantageous because it inhibits the ability of the long tail to equilibrate and that cervical mobility is often needless.

It is also worth noting that these ricochetal rodents also have fossorial habits. While studies of their ecology describe digging behaviours most similar to scratch digging (Butynski &

Mattingly, 1979; Feniuk & Kazantzeva, 1937; Happold, 1967; Hildebrand, 1985), these behaviours are described from surface-level observations, and behaviours within burrows may differ. Without such data, we are left to hypothesize that ricochetal locomotion and enlarged relative head size capable of producing relatively large downward forces during such locomotion may act as selective pressures. Shortened necks and anteroposteriorly shortened cervical vertebrae, potentially for digging, may also contribute to selecting for syncervicals, but the addition of these characters would require an alternate explanation for the syncervical in Pedetes.

1.6.3 Function of the syncervical in cetaceans

Cetaceans are unique among mammals in fusing their atlas to their syncervical in all cases except Physeter (e.g., Buchholtz, 2001b; Buchholtz & Schur, 2004; Caldwell & Caldwell,

1989; Cummings, 1985). The variation among species of cetaceans suggests that the syncervical morphology may correlate with ecological differences. Taxa without syncervicals, such as beluga whales and narwhals (Family Monodontidae) and some of the river dolphins, must traverse through habitats filled with more obstacles, in the forms of glaciers and trees, than their open-water relatives. However, even in species that appear ecologically similar, such as the large baleen whales, fusion varies from no fusion in the blue whale, Balaenoptera musculus

(Appendix 1), to seven in the right and bowhead whales, Eubalaena and Balaena (Cummings,

1985; Reeves & Leatherwood, 1985; Appendix 1). A possible explanation for this variation could be that the ecological differences separating these taxa are underappreciated, and these potential ecological differences impose varying forces on the skull and cervical column.

Because skeletons of these more massive animals are rare compared to those of delphinids, for example, differences in syncervical presence and composition could be due to intraspecific variation captured in our sample. Intraspecific variation in syncervicals was seen in some pocket gophers, but seemed to be consistent within subspecies (Appendix 1). Some cetacean species may have phylogenetically distinct parapatric populations (Hoelzel, Potter &

Best, 1998), and new, sometimes large-bodied, species are still being discovered (Beasley,

Robertson & Arnold, 2005; Wada, Oishi & Yamada, 2003). It may be that these reported cases of intraspecific variation in cetaceans could reflect distinct, but unrecognized, species or subspecies. This hypothesis needs to be tested, however. The variation we observed in many species was restricted to fusion of the neural arches, neural spines, and/or transverse processes.

Pathological vertebral fusion in cetaceans is not uncommon (Félix et al., 2007; Kompanje, 1995;

Kompanje, 1999), so determining the nature of these accessory fusions may require more knowledge about potential pathologies affecting the cervical vertebrae.

The function of the syncervical in cetaceans is difficult to assess, given the amount of reported variability in this structure and potentially unknown ecological differences between species. However, we suggest that the number of vertebrae fused correlates with an ecological requirement of the cetacean neck. Increased (or plesiomorphically maintained) neck flexibility may be beneficial for some taxa (monodontids and river dolphins), while others may benefit from limited cranial movements for high-speed travel through water. Finally, as cetacean cervical vertebrae are anteroposteriorly short, some taxa may require fusion to further shorten the neck, like the hypothesis for ricochetal rodents (see above), to prevent the vertebrae from failing mechanically, or to stabilize the neck for to withstand extrinsic forces place on their craniocervical joint, as in head-lift digging taxa (see above).

1.6.4 Function of the syncervical in hornbills

The syncervical of hornbills has been hypothesized to help support their relatively large head (Kemp, 2001). Given the similar size of hornbill and toucan heads, as well as similar feeding behaviours (Baussart & Bels, 2011; Seki et al., 2010), a similar adaptation would be predicted in toucans, yet none has been reported. We suggest a lack of cervical vertebral adaptations in toucans related to either head size or ballistic food transport would weaken this hypothesis for the hornbill syncervical.

Alternatively, an interesting behaviour in hornbills may suggest another hypothesis for syncervical function. Intraspecific combative behaviours are reported in some species that have prominent casques on their skulls (Cranbrook & Kemp, 1995; Kasambe et al., 2011; Kinnaird et al., 2003; Raman, 1998), and these confrontations could produce enough force on the cranium to require a cervical adaptation. However, prominent casques are not present in the ground hornbills (Bucorvus), which suggests that large casques evolved after the syncervical given the phylogenetic placement of ground hornbills (Gonzalez et al., In press). More data on behaviours involving the skull in all hornbills are required to make definitive predictions about the evolution of the syncervical in this clade. However, we are left to conclude that the ability to withstand forceful impacts on the skull may require a syncervical in hornbills.

1.6.5 The mysterious syncervical of porcupines and pacaranas

Two groups of arboreal rodents, the New World porcupines (Erethizontidae) and the pacarana (Dinomys) do not fit into any of these major categories yet possess syncervicals. Based on our review, the syncervical in extant taxa may 1) stabilize anteroposteriorly shortened necks,

2) reduce mobility in the neck for locomotor purposes or 3) provide a more rigid attachment site and, thus, greater out-lever force by the head during a certain behaviours. None of these

25 functions, however, seem to be required by these arboreal taxa(White & Alberico, 1992; Woods,

1973). The head of the pacarana is relatively large (White & Alberico, 1992). A head-support hypothesis has also been applied to ceratopsians, but without a mechanical explanation of how fusion of the cervical vertebrae would help support a heavy head, this functional hypothesis seems unlikely. Instead, a stronger nuchal ligament likely supports large skulls, which is present in mammals and reptiles (e.g., Nishi, 1916; Tsuihiji, 2004). It is alternatively possible that syncervicals evolved in response to different lifestyles, such as fossoriality, present in the ancestors of these clades or may have arisen by chance. These two rodents may provide a model with which over-arching generalisations about syncervical function can be tested.

1.6.6 Interpreting the syncervical as an adaptation

Adaptations, by definition, must be shown improve the performance of an individual within a population for a particular task by lowering the amount of energy required for a task or increasing the effect of a behaviour (e.g., out-force) while maintaining equal levels of energy consumption (e.g., Bock, 1980). To date, no evolutionary or experimental work on the origin of the syncervical in any taxon exists, so we are unable to define this structure as an adaptation.

However, situations where sister-species or subspecies variation exist in syncervical presence/absence allow for future evolutionary and experimental tests for adaptation. An exemplary group for such tests may be pocket gophers. Our survey found syncervicals presence varied not only between species, but also between subspecies. Therefore, future research can elucidate if these differences reflect behavioural differences in digging style and if the syncervical improves digging performance in individuals that possess them. Similar situations exist in cetaceans (e.g., Globicephala) and ricochetal rodents (e.g. Dipodomys), which may act as future models for testing the hypotheses presented here for syncervical function.

1.7 Implications for fossil taxa

Reconstructing behaviour in the fossil record is a difficult, but necessary step in understanding how taxa respond to changes in their environment (Benton, 2010). Given our comparative analysis of extant taxa, we propose and evaluate functional hypotheses for the syncervicals of long-extinct animals. For example, our review supports the hypothesis that

Mesoscalops, a Miocene proscalopid mole from Montana, U.S.A., was likely a head-lift digger

(Barnosky, 1981), and we suggest this behaviour for the phylogentically ambiguous taxon

Necrolestes (Asher et al., 2007), as well. Reconstructing head-lift digging behaviour for

Palaeocastor contradicts other studies of craniodental anatomy, in which it was classified as a chisel-tooth, or possibly scratch digger (Samuels & Van Valkenburgh, 2009). Armadillos are not strictly head-lift diggers, although they do employ this behaviour (Hildebrand, 1985), so it is possible that Palaeocastor may have utilized a more complicated suite of digging styles to construct its burrows. Epoicotheriid palaeanodonts have been hypothesized as the most advanced scratch diggers to have evolved (Rose & Emry, 1983) instead of head-lift diggers, as well.

However, their syncervical suggests, as in Palaeocastor, that at least a portion of their digging style was composed of head-lift digging.

Inferring behaviours of other extinct terrestrial taxa is more difficult. Ceratopsids and ankylosaurs were too large to be considered fossorial, and their limb anatomy and body size are not consistent with ricochetal locomotion. The syncervical of ceratopsians has been hypothesized to support large skulls or play a role in intraspecific combat (e.g., Dodson et al., 2004; Farlow &

Dodson, 1975; Spassov, 1979). The head-support hypothesis has been presented for hornbills, as well, but a comparison with toucans does not support this hypothesis. Hornbill syncervicals may

27 also play a role in intraspecific combat, but this hypothesis (presented here) is not well-supported by the sequence of evolution of the syncervical and casques.

The syncervical of ceratopsians evolved outside of Ceratopsidae (Brown & Schlaikjer,

1940; Brown & Schlaikjer, 1942), so formulating hypotheses about its origins by only examining traits of ceratopsids may be inappropriate if these traits are not present in the common ancestor in which the syncervical evolved. However, this assumption needs to be tested in a phylogenetic framework. Determining the function of the ankylosaur syncervical is much more difficult, given its rarity throughout their evolutionary history. Some features of their limb anatomy suggest that ankylosaurs may have had basic digging abilities, possibly equivalent to rooting (Coombs Jr,

1978), and the fulcrum hypothesis for the syncervical of fossorial mammals may not be out of the question for ankylosaurs if subterranean roots comprised a significant portion of their diet.

This hypothesis remains difficult to test until higher phylogenetic resolution and more data about their cervical vertebrae are obtained.

Given the uncertainties about the function of fused cervical vertebrae in cetaceans, it is difficult to extrapolate possible functions of this structure in marine reptiles. The syncervical of plesiosaurs likely evolved early in the group before the evolution of elongated necks

(plesiosauroids) or enlarged heads (pliosauroids). Given that no reconstruction of the anterior cervical muscles has been performed to help infer how vertebral fusion affects muscle activation patterns, it is difficult to assess Bakker’s (1993) hypothesis of a feeding ecology function. The evolution of a syncervical in open-water, fast-swimming cetaceans, such as delphinids, might be supporting evidence that the syncervical of plesiosaurs and ichthyosaurs evolved in response to increased locomotor speeds and associated forces at the craniocervical joint produced by the fluid medium (Fish, 2000; McGowan & Motani, 2003). However, swimming styles in marine

28 reptiles are debated (e.g., Massare, 1988; Motani, 2002), making hypotheses about syncervical function and locomotor performance difficult to assess, as well.

Uncertainties in hornbill syncervical function also impede interpretations for the function of fused cervicals in pterosaurs. Pteranodon and Nyctosaurus, are known for their unique and elaborate crests, which may be analogous to the casques of hornbills. If a combative function is found to contribute to the selective pressure for the hornbill syncervical, then it may provide some evidence that pterosaur crests, which are considered visual display structures (e.g., Elgin et al., 2008), may have a more direct role in intraspecific interactions. Better descriptions of pterosaur syncervicals and more phylogenetically-based tests and in-vivo experiments of behaviour in hornbills are required to establish the persistence of these two factors through the evolution of these aerial clades.

We are unfortunately limited in the inferences we can make about behaviour in the fossil record because syncervical function is poorly understood in extant taxa. In fact, no hypothesis for why syncervicals evolved has ever been formally tested. Therefore, there exists research potential for elucidating ecological and mechanical mechanisms that select for fusion of the cervical vertebrae in an ecologically and taxonomically wide range of extant and extinct animals.

It is only by filling in these gaps in our knowledge of this structure that we can begin making predictions about the evolution of this relatively common form of vertebral fusion.

1.8 Conclusions 1. The syncervical is a structure of fused anterior cervical vertebrae that has evolved

independently over 20 times in the history of Tetrapoda. The prevalence of this structure

in ecologically similar taxa suggests that it is serves an adaptive function.

2. The syncervical in extant fossorial mammals is correlated with head-lifting behaviour,

possibly because it increases the out lever force produced by the cranium.

3. Syncervicals of ricochetal taxa may further stabilize an already stiffened neck or prevent

the anteroposteriorly shortened cervical vertebrae from failing during locomotion.

Alternatively, fossorial behaviours in these taxa suggests other potential advantages for

this structure.

4. While cetaceans are reportedly variable in this character, the ecology of some taxa with

characteristically unfused cervical vertebrae suggest an ecological association with

fusion, in which the degree of fusion may correlate with a need for increased or decreased

cervical mobility.

5. Of the previous hypotheses suggested in the literature, the hypothesis that the syncervical

helps support an extremely large head in hornbills is not supported by the comparative

anatomy of other taxa presented here. Instead, the hornbill syncervical may be an

adaptation for their unique casque-butting behaviour.

6. The prevalence of syncervical in fossorial, ricochetal, and pelagic taxa makes the

syncervical a useful tool when interpreting the biology of fossil taxa that possess this

structure by providing extant comparisons.

7. Rigorous biomechanical or functional test has never been performed on the syncervical in

any clade. Therefore, these hypotheses remain speculative until such experimental work

is performed.

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Table 1.1 Previously proposed functional hypotheses for the syncervical in each clade

Taxon Previously Proposed Hypotheses References

Dasypodidae Better fulcrum for digging Rose & Emry (1983, 1993)

Fossorial Rodents Head-lift digging strategy Hildebrand (1985)

Notoryctes Head-lift digging strategy Rose & Emry (1983, 1993); Hildebrand (1985)

Amblysomus Head-lift digging strategy Rose & Emry (1983, 1993); Hildebrand (1985)

Ricochetal rodents Further shorten the neck Howell (1932)

Stabilize the neck to improve locomotion Hatt (1932)

Erethizontinae None

Dinomyidae None

Cetaceans Stabilize the head during posterior propulsion Buchholtz (1989)

Bucerotidae Support for a large head e.g., Kemp (2001)

Necrolestes None

Epoicotheriidae Scratch digging strategy Rose & Emry (1983)

Extinct cingulates None

Neoceratopsians Support for a large head Sereno et al. (2007); Dodson et al. (2004); Tanke & Rothschild (1997)

Buttress during intraspecific combat Molnar (1977)

Ankylosauria None

Pterosauria None

Plesiosauria Accelerate cranial movements Bakker (1993)

Ichythosauria None

Figure 1.1 The number of convergences within higher-level taxonomic groups shown in a phylogenetic context. Broad, general phylogeny (A) where a ‘+’ demonstrates a clade where the number of convergences is currently unknown, but a minimum number of convergences is given, primarily based on the number of different Families that possess syncervicals. Expansion of the rodent (B) and cetacean (C) phylogenies is also presented. Bolded taxa possess syncervicals; greyed taxa are unknown; * presence of a syncervical in one extinct member; § no fusion plesiomorphic for the group (see text).

Laurasiatheria 3+ Echimys A B Capromys Glires 8+ Octodon Xenarthra 1 Abrocoma Chinchilla Afrotheria 1 Dinomys Marsupialia 1 Erethizon Agouti Ankylosauria 2 Cavia Hydrochaeris Ceratopsia 1 Thryonomys Aves 1 Petromus Bathyergus Pterosauria 1 Heterocephalus Ichthyopterygia 1 Trichys Hystrix Sauropterygia 1 Massoutiera Ctenodactylus C Tursiops aduncus Thomomys Delphinus capensis Geomys Stenella coeruleoalba Dipodomys* Tursiops truncatus Castor§ Sousa chinensis Anomalurus Stenella attenuata Pedetes Grampus griseus Dipus Lagenorhynchus albirostris Jaculus Phocoena phocoena Tachyoryctes Monodon monoceros Rhizomys Inia geo!rensis Spalax Pontoporia blainvillei Rodentia Lipotes vexillifer Mesocricetus Hyperoodon ampullatus Microtus Berardius bairdii Mus Platanista minor Rattus Kogia breviceps Acomys Physeter catodon Gerbillus Balaenoptera brydei Eliomys Cetacea Balaenoptera edeni Dryomys Balaenoptera borealis Glis Balaenoptera amurai Aplodontia Balaenoptera musculus Marmota Balaenoptera physalus Sciurus Megaptera novaeangliae Eschrichtius robustus Balaenoptera bonaerensis Balaenoptera acutorostrata Caperea marginata Eubalaena japonica Eubalaena australis Balaena mysticetus Hippopotamus amphibius

Figure 1.2 Syncervicals of some mammals. Syncervicals of the armadillo Priodontes maximus

(USNM 270373) (A), the porcupine Erethizon dorsatum (USNM 90475) (B), the cetacean

Globicephala sp. (ROM R3701) (C), the pacarana Dinomys branickii (FMNH 152061) (D), the kangaroo rat Dipodomys microps (ROM 112516) (E), and the pocket gopher Orthogeomys hispidus (ROM 95936) (F). Abbreviations for figures: at, atlas; ata, atlantal neural arch; atr, atlantal cervical rib; ax, axis; axa, axial neural arch; axr, axial cervical rib; axs, axial neural spine; c3, third cervical vertebra; c3a, neural arch of the third cervical vertebra; c3s, neural spine of the third cervical vertebra; c4, fourth cervical vertebra; c3-c7, third through seventh cervical vertebrae; c4a, neural arch of the fourth cervical vertebra; c4s, neural spine of the fourth cervical vertebra; c5, fifth cervical vertebra; tp, transverse process. Scale bar = 2cm (A-D); scale bar =

1cm (E and F).

/ ! #$' %&' %(' #$'

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#$ #$ *+ *+ %& %( *+ %& *+

" 0 #$' #$' %&' %&'

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#$' , 1 #$#

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*+ #$ *+ *+ #$ %&-%. %&

Figure 1.3 Syncervicals of some reptiles. Syncervicals of the hornbill Bucorvus leadbeateri

(ROM 35556) (A), the ichthyosaur Platypterygius americanus (UW 5547, modified from

Maxwell, 2010) (B), the plesiosaur Dolichorynchops sp. (ROM 29010) (C), the ceratopsian

Achelousaurus horneri (MOR 485) (D), the ankylosaur cf. Panoplosaurus mirus (ROM 1215)

(E), and the pterosaur Pteranodon sp. (USNM 407644) (F). For abbreviations, see Figure 1.2.

#%) . ! " #$ #% &' #%) #$# $,

#$# #$ #$ #%

/0&1 /0&1 #% /0&1 #%( #%) + * #$# - &') #%) #$ #%# #%)

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$, $, #$( #% #% #$ &' 20&1 20&1 /0&1 #%(

Appendix 1

Results from the survey of museum specimens

Taxon Number Fused Vertebrae Fused References Referred Specmens Cetacea 0-7 BALAENIDAE Balaena mysticetus 7 C1-C7 Reeves & Leatherwood 1985 Eubalaena australia 7 C1-C7 Cummings 1985b E. glacialis 7 C1-C7 Cummings 1985b E. japonica 6 C1-C6 + NS C7 USNM 339990 BALAENOPTERIDAE Balaenoptera borealis 3 C1-C3 USNM 236680 B. edeni 0 Cummings 1985a B. musculus 0 USNM 124326 B. physalus 0 USNM 16045 Megaptera novaeangliae 0 Winn & Reichley 1985 DELPHINIDAE 2 C1-C2 Ogden et al. 1981 Delphinus delphis 2 C1-C2 USNM 572911 USNM 572980 USNM 593396 USNM 572592 USNM 572859 USNM 572871 USNM 572893 USNM 572900 USNM 572776 USNM 572630 Lagenorhynchus acutus 2 C1-C2 FMNH 15556 Orcinus orca 2 C1-C2 + NS C3, C4 USNM 23004 USNM 37166 Orcaella brevirostris 2 C1-C2 FMNH 99613 Stenella attenuata 2 C1-C2 USNM 36051 USNM 123290 USNM 258641 USNM 49633 USNM 261428 USNM 259311 FMNH 127187 S. clymene 2 C1-C2 USNM 550511 (3) USNM 550528 USNM 550525 USNM 550534 USNM 550536 USNM 550531 USNM 550532 S. coeruleoalba 2 C1-C2 USNM 571260 USNM 571267 USNM 571359 USNM 571363 USNM 572891 USNM 572853 S. fluviatilis 2 C1-C2 FMNH 99612 S. longirostris 2 C1-C2 USNM 395412 USNM 395414 USNM 395533 USNM 395593 Tursiops truncatus 2 C1-C2 USNM 21536 USNM 21538 USNM 22111 USNM 22112 USNM 22113 USNM 22114 USNM 49557 USNM 252100 USNM 252101 USNM 252102 USNM 252103 USNM 252104 USNM 22116 USNM 22117 USNM 22118 USNM 22119 USNM 22120 USNM 22121 USNM 22122 USNM 22123 USNM 22124 USNM 22898 USNM 252118 USNM 252114 USNM 252107 USNM 252108 USNM 252109 USNM 252110 USNM 252117 USNM 252112 55 56

USNM 22115 FMNH 92934 FMNH 57410 USNM 49577 USNM 252119 USNM 252115 USNM 252106 USNM 252123 USNM 252124 USNM 252122 ESCHRICHTILLIDAE Eschrichtius robustus 0 Wolman 1985 GLOBICEPHALIDAE 7 C1-C7 Ogden et al. 1981 USNM 395369 Globicephala melas variable variable USNM 20980 USNM 20981 USNM 21118 (1-6) USNM 395367 USNM 395368 (1-5) (1-5; 6-7 NS only) (1-2; 3-7 NS only) (1-2; 3-7 NS only) (1-3 + NS 4, 5) G. macrorhynchus 6 or 7 C1-C6 or C7 USNM 292259 (6) USNM 37261 (6) USNM 292260 (7) USNM 500200 (7) INIIDAE Inia geoffrensis 2 (0) C1-C2 Best & de Silva 1989 USNM 395602 KOGIIDAE Kogia 7 C1-C7 Caldwell & Caldwell 1989 USNM 550396 USNM 550494 USNM 550492 LIPOTIDAE Lipotes vexillifer 0 Peixum 1989 MONODONTIDAE Delphinapterus leucas 0 USNM 504339 USNM 504767 PHOCOENIDAE Phocoena dioptrica 6 C1-C6 USNM 571485 P. phocaena 2 C1-C2 FMNH 194123 P. spinipinnis 2 or 3 C1-C2 or C3 USNM 395730 USNM 395729 USNM 395749 USNM 395754 PHYSETERIDAE Physeter catodon 6 C2-C7 De Smet 1972 USNM 301634 PLATANISTIDAE 0 Brownell, Jr. 1989 Platanista gangetica 0 USNM 23456 ZIPHIDAE Birardius bairdii 3 C1-C3 USNM 49726 USNM 49725 Hyperoodon 7 C1-C7 Fraser 1945 FMNH 15553 Indopacetus sp. 4 C1-C4 USNM 593534 Mesoplodon bidens 3 or 4 C1-C3 or C4 USNM 572378 (3) USNM 572008 (3) USNM 572009 (4) USNM 500414 (3) USNM 572007 (4) M. carlhubbsi 3 C1-C3 USNM 504128 M. densirostris 4 C1-C4 USNM 593422 USNM 593423 USNM 572986 USNM 550951 USNM 550952 USNM 572751 USNM 550228 USNM 550746 USNM 550754 USNM 486173 USNM 504217 FMNH 58840 M. europaeus 4 C1-C4 USNM 23346 USNM 306302 USNM 504256 USNM 504349 (5) USNM 504473 USNM 504738 USNM 550824 USNM 571568 USNM 572438 (5) USNM 550404 USNM 550451 USNM 593429 M. mirus 4 C1-C4 USNM 504724 USNM 593425 56 57

M. stejnegeri 4 C1-C4 USNM 504330 USNM 504331 USNM 550113 Tasmacetus shepherdi 5 C1-C5 USNM 484878

Proscalopidae Mesoscalops 4 C2-C5 Barnosky 1981

?Pholidota Xenocranium 4 C2-C5 Rose & Emry 1983 Epoicotherium 4 C2-5 Rose & Emry 1983

Erethizontidae Erethizontinae 2 C2-C3 Ray 1958 Erethizon dorsatum 2 C2-C3 USNM 564251 USNM 88619 USNM 90478 USNM 564252 Coendou prehansilis 2 C2-C3 USNM 281898 USNM 297843 USNM 362242 USNM 240312 C. bicolor 2 C2-C3 AMNH 214610 C. melanurus 2 C2-C3 AMNH 70120 AMNH 94174 AMNH 266565 C. nycthemera 2 C2-C3 AMNH 96320 C. sanctamartae 2 C2-C3 AMNH 23473 C. spinosus 2 C2-C3 FMNH 43289 Sphiggurus mexicanus 2 C2-C3 USNM 257008 USNM 240269

Dinomyidae Dinomys branckii 2 C2-C3 Ray 1958 USNM 395453 USNM 395160 USNM 522974

Geomyidae Cratogeomys 2 C2-C3 Gupta 1966 Orthogeomys hispidus 2-3 C2-C3 or C4 USNM 63651 USNM 63652 hispidus O. h. yucatensis 0 USNM 244963 USNM 244965 USNM 244962 O. cavator cavator 0 USNM 323661 Pappogeomys bulleri 2 C2-C3 USNM 523473 nayaritensis P. merriami merriami 2 C2-C3 USNM 57970 USNM 57971 P. m. fulvescens 0 USNM 58167 USNM 58166 P. m. saccharalis 0 USNM 540918 USNM 540921 USNM 540924

57 58

P. tylorhinus tylorhinus 0 FMNH 141794 FMNH 141793 Thomomys bottae 0 USNM 568107 USNM 568108 USNM 1280 USNM 234643 USNM 262902 T. umbrinus 0 USNM 450987 USNM 540988 USNM 540983 Zygogeomys trichopus 2 C2-C3 FMNH 51970 FMNH 51971

Heteromyidae Dipodomys deserti deserti 2-5 (4) C2-C3, C4 or C5 Gupta 1966 USNM 34370 USNM 505968 D. d. aquilus 4 C2-C5 FMNH 191209 D. agilis cabazonae 4 C2-C5 Gupta 1966 D. californicus californicus 5-6 C2-C7 USNM 564149 USNM 512851 D. elator 4 or 6 C2-C5 or C7 USNM 506332 USNM 506331 D. hermanni morroensis 2 C2-C3 USNM 271152 D. merriami merriami 2-5 (3) C2-C3, C4 or C5 Gupta 1966 USNM 526475 FMNH 186601 D. me. melanurus 2 C2-C3 USNM 555169 D. me. simiolus 2-4 C2-C3, C4 or C5 Gupta 1966 D. microps bonnevillei 2 C2-C3 USNM 43412 D. mi. aquilonius 2 C2-C3 USNM 94429 D. mi. microps 0 Gupta 1966 D. mi. occidentalis 3 C2-C4 FMNH 123330 FMNH 123334 FMNH 123329 D. ordii ordii 3-4 (2) C2-C3, C4, or C5 Gupta 1966 USNM 23525 D. o. luteolus 2 or 3 (3) C2-C3 or C4 Gupta 1966 FMNH 123445 FMNH 135226 D. o. richardsoni 3-6 (2) C2-C4, C5, C6 or C7 Gupta 1966 FMNH 51333 D. o. attenuatus 2 or 5 C2-3 or C6 Gupta 1966 D. o. palmeri 3 C2-C4 USNM 53271 D. simulans simulans 3 C2-C4 USNM 349407 D. spectabilis perblandus 2 C2-C3 USNM 235509 D. sp. spectabilis 2 C2-C3 Gupta 1966 D. sp. baileyi 2 or 3 C2-C3 or C4 Gupta 1966 FMNH 125242

Spalacidae Myospalax 3 C2-C4 Gambaryan 2005 M. fontanieri 0 USNM 240750 Spalax 3 C4-C6 Gambaryan 2005

Dipodidae

58 59

Jaculus 5 C2-C6 Gupta 1966 J. jaculus 5 C2-C6 USNM 308387 USNM 308398 J. orientalis 5 C2-C6 USNM 14606 USNM 256516 Dipus 6 C2-C7 Hatt 1932 Stylodipus 5 or 6 C2-C6 or C7 Hatt 1932

Paleocastorinae Paleocastor fossor 2 C2-C3 Peterson 1905

Pedetidae Pedetes cafer 0 Hatt 1932 USNM 49647 USNM 295258 USNM 221381 P. surdaster 2 C2-C3 Hatt 1932 P. capensis 0-2 C2-C3 ROM 85746 (2) FMNH 60073 (0) P. c. surdaster 2 C2-C3 FMNH 18836

Amblysominae Amblysomus ? Rose & Emry 1983, 1993 Neamblysomus julianae 2 C2-C3 USNM 398632 Amblysomus hottentotus 0 USNM 351327 USNM 351328 longiceps A. h. hottentotus 0 USNM 351326 USNM 344221 USNM 344218 A. iris 0 USNM 342426 USNM 342425 USNM 342424

Cingulata Rose & Emry 1983, 1993 Cabassous tatouay 0 Galliari et al. 2010 Ca. centralis 3 C2-C4 FMNH 121224 Ca. chacoensis 2 C2-C3 Galliari et al. 2010 Ca. unicinctus 3 C2-C4 USNM 23441 Chaetophractus villosus 0-2 (3) C2-C3 Galliari et al. 2010 USNM 543430 Ch.vellerosus 0-2 (2) C2-C3 Galliari et al. 2010 AMNH 261305 Dasypus novemcinctus 2 (3) C2-C3 or C4 Galliari et al. 2010 USNM 49398 D hybridus 2-3 (3) C2-C3 or C4 Galliari et al. 2010 USNM 205707 D. kappleri 3 C2-C4 USNM 256761 Euphractus sexcinctus 0 (2) C2-C3 Galliari et al. 2010 USNM 259462 Glyptodon ornatus 4 C2-C5 Serres 1865

59 60

Priodontes maximus 0 (3) C2-C4 Galliari et al. 2010 USNM 270373 Tolypeutes matacus 0-2 (3) C2-C3 or C4 Galliari et al. 2010 USNM 248394 Zaedypus pichiy 0-2 (2) C2-C3 Galliari et al. 2010 FMNH 153782

Notoryctidae Notoryctes 5 C2-C6 AMNH 2000241 AMNH 16717

Nodosauridae Edmontonia 2 C1-C2 Vickaryous et al. 2004 Panoplosaurus 2 C1-C2 Vickaryous et al. 2004 ROM 1215

Ankylosauridae Saichania 2 C1-C2 Vickaryous et al. 2004

Neoceratopsia 3 C1-C3 You et al. 2004

Bucerotidae 2 C1-C2 Kemp 2001

Pterosauria 2 C1-C2 Pteranodon 2 C1-C2 Howse 1986 Nyctosaurus 2 C1-C2 Howse 1986 Ornithocheirus 2 C1-C2 Howse 1986 Quetzalcoatlus 2 C1-C2 Bennet 2001 Dsungaripterus 2 C1-C2 Bennet 2001 Azhdarcho 2 C1-C2 Bennet 2001 Dsungaripteroidea 2 C1-C2 Kellner 2003

Euichthyosauria 2 C1-C2 McGowan & Motani 2003

Plesiosauria 2 C1-C2 Bakker 1993 Bolded numbers indicate deviations from reports in the literature or number fused in a specimen to show variation

60 61

Chapter 2 Head Size, Weaponry, and Cervical Adaptation: Testing Craniocervical Evolutionary Hypotheses in Ceratopsia 2.1 Abstract

The neoceratopsian syncervical is a coalesced element composed of the three anterior- most cervical vertebrae. In ceratopsids, the syncervical is hypothesized to function as either a support structure for the large skull or a buttress for the cranium during intraspecific combat.

Here we present evidence of the occurrence of unfused syncervical elements in

Pachyrhinosaurus and Centrosaurus that challenge these functional hypotheses, and test hypotheses of syncervical function with a phylogenetic framework for the first time. Given a combat and/or support function, the cranial weapons (brow and nasal horns) and/or enlarged head size are predicted to evolve in concert with, or before, cervical fusion. However, results indicate that neither of these features correlate with the evolutionary first appearance of syncervical fusion. Therefore, we reject both hypotheses as the selective pressure(s) associated with syncervical origin. Although we cannot reject the alternative hypothesis that the syncervical was exapted in ceratopsids for either combat or head support, strong functional hypotheses for the syncervical should reflect its origin in small-bodied neoceratopsians. Anterior cervical fusion has evolved independently in a number of extant taxa with a terrestrial mode of life, including armadillos, rodents, and hornbills, which provide a model with which to predict ecologies or behaviours associated with cervical fusion early in neoceratopsian evolution.

2.2 Introduction

Dinosaurs were the largest and some of the most decorated terrestrial animals to have ever lived (Sereno 1999). As dinosaurs increased in body mass, allometric differences in their

62 skeletal anatomy related to hypothesized ecological selective pressures evolved. Relative skull size is a factor thought to have affected postural, locomotor, and behavioral aspects of dinosaur biology (Sereno et al. 2007). Ceratopsians comprise a large portion of dinosaur diversity during the Cretaceous of Laurasia and are recognized by their elaborate horns and frills (e.g., Dodson et al. 2004, You and Dodson 2004). They are also known for having evolved the largest skulls of any terrestrial animal (Marsh 1891, Sereno et al. 2007). Large heads may require postcranial adaptations to support increased weight on the anterior extremity of the body. The syncervical is a coalesced element containing the first three cervical vertebrae in neoceratopsians (Campione and Holmes 2006, Hatcher et al. 1907, Lull 1933, Tsuihiji and Makovicky 2007; Figure 2.1).

Syncervicals are known in smaller taxa outside of Ceratopsidae (Brown and Schlaikjer 1940,

Brown and Schlaikjer 1942, Makovicky 2010, Sternberg 1951), but functional hypotheses for the syncervical center around the large heads and cranial weapons of ceratopsids (Bakker 1986,

Dodson et al. 2004, Farlow and Dodson 1975, Marsh 1891, Molnar 1977, Sereno et al. 2007,

Spassov 1979, Tanke and Rothschild 1997). Spassov (1979) and Sampson (1997) hypothesized that the syncervical would act as a buttress during intraspecific combat, while others have hypothesized that the syncervical increased cranial mobility at the craniocervical joint for such combat (Bakker 1986, Farlow and Dodson 1975, Molnar 1977, Ostrom and Wellnhofer 1986,

Tait and Brown 1928). The most prevalent hypothesis, however, is that the syncervical evolved as an adaptation to supported the large ceratopsid head (Dodson 1996, Dodson et al. 2004,

Hatcher et al. 1907, Marsh 1891, Sereno et al. 2007, Tanke and Rothschild 1997).

Three thresholds for determination of relatively large head have been proposed. Xu et al.

(2006) used head size as a discrete character in their phylogeny and coded any taxon with a skull length that was 13% total body length or greater as one with a large head. Sereno et al. (2007) used a threshold of 40% trunk length (measured from pelvic to pectoral girdle) to distinguish

63 relatively large heads among dinosaurs, and they suggest that a relative head size at or above this threshold is selective pressure for quadrupedality. However, both of these quantified thresholds lack support from non-dinosaurian taxa. Ostrom (1966) defines a large head as one that is one- third back length (measured from the occipital condyle to the middle of the acetabulum), but he notes that this limit is approached by taxa like Tyrannosaurus rex, some crocodilians, gomphodont cynodonts, and some anomodonts. These three thresholds use different portions of the body and cannot be easily compared. Furthermore, they require relatively complete specimens, which are not always preserved in the fossil record.

Because the proposed hypotheses of head support or stabilization in combat for syncervical function in ceratopsians have not been tested, it is difficult to discern if they are, or need be, mutually exclusive. Furthermore, without a consensus of what defines a ‘relatively large head,’ falsifying a head support hypothesis is difficult. The characteristic spherical occipital condyle and ball-and-socket atlanto-occipital joint of ceratopsids suggests that cranial mobility was at least maintained, if not enhanced, by the evolution of the syncervical based on our understanding of these joints (e.g., Hildebrand and Goslow 2001). However, how increased mobility may have aided in combative or display behavior is unknown, but plausible (Dodson et al. 2004, Farlow and Dodson 1975, Ostrom and Wellnhofer 1986).

The recent discovery of large, unfused syncervical elements from ceratopsid bonebeds also provides insight into these functional hypotheses. The size of these elements is similar to that of fused syncervicals, suggesting a large, ‘adult’-sized head (Anderson 1999). The possibility of ceratopsids reaching adult sizes without fusion of the syncervical suggests fusion may not be as critical for its function as previously implied. Here, we critically evaluate hypotheses of syncervical function within a phylogenetic framework. Although only ever suggested to apply to ceratopsids, the functional hypotheses for the syncervical make predictions

64 about its evolutionary history, namely that fusion evolved in concert with, or after, the evolution of large head size and/or cranial weapons. The goals of the present study are to document the unfused syncervical elements for the first time and to phylogenetically test for the congruence in the evolution of these traits as predicted by the functional hypotheses. To accomplish this, we also use a large phylogenetically inclusive data set of extant and extinct amniote taxa to assess variability in relative skull size for amniotes.

2.3 Materials and Methods

2.3.1 Syncervical Specimens and Measurements

The unfused syncervical elements are TMP 91.36.263 (isolated atlas), TMP 87.55.315

(isolated atlas), TMP 86.55.217 (isolated atlas and axis), and TMP 86.55.53 (isolated third cervical vertebra). TMP 91.36.263 is from Bonebed 31, a monodominant Centrosaurus apertus bonebed in Dinosaur Provincial Park, Alberta (Dinosaur Park Formation), and is thus assigned to this species. TMP 87.55.315, TMP 86.55.217, and TMP 86.55.53 are all from the Pipestone

Creek Bonebed, a monodominant Pachyrhinosaurus lakustai bonebed near Grand Prairie,

Alberta (Wapiti Formation), and are thus assigned to this species.

Measurements shown in Figure 2.2 for 20 fused and four unfused syncervical elements were taken from specimens at the Royal Ontario Museum (ROM), Royal Tyrrell Museum of

Palaeontology (TMP), and Museum of the Rockies (MOR) to determine the range of size variation present in fused, presumably adult syncervicals. For fused specimens, the anterior and posterior centrum height and width were considered equal for successive elements. Due to the taphonomic distortion of certain specimens, simple bivariate regressions of log-transformed data were used instead of traditional multivariate methods, such as Principal Components Analysis

(PCA), to more carefully control for taphonomic effects in our analyses. Lateral taphonomic

65 compression common to the Pipestone Creek bonebed material hindered the use of centrum width measurements. However, centrum length and height were not as obviously affected by taphonomy and were thus deemed more useful.

2.3.2 Construction of Phylogeny

We compiled a phylogeny for Ceratopsia on which to map discrete and continuous craniofacial characters and test for correlated character evolution. To incorporate the most phylogenetically expansive data set possible of taxa with known postcranial remains, we used the

Makovicky (2010) character matrix and coded Auroraceratops based primarily on the original species description by You et al. (2005) (Table 2.1). Ambiguities were resolved using the description of Auroraceratops sp. (You et al. 2012), and syncervical character states were supplemented from Morschhauser (2012).

Cerasinops was reported to lack a syncervical (Chinnery and Horner 2007), which would constitute a reversal to the plesiomorphic, unfused condition. The axis centrum of the holotype specimen (MOR 300) is weathered anteriorly, but the texture of the posterior surface is similar to that of the unfused atlas and axis described here (see below) which differs from that of the smooth texture of the centra of posterior cervical vertebrae. While the condition of the atlas-axis fusion is here described as unknown (contra Chinnery and Horner 2007), the deeply rugose posterior surface of the axial centrum indicates that fusion likely occurred in the syncervical of

Cerasinops; the syncervical character states for Cerasinops were modified in the Makovicky

(2010) matrix to reflect this new interpretation. The phylogenetic analysis was conducted using

PAUP 4.10b (Swofford 2002) after Makovicky (2010) using the branch-and-bound search algorithm, all characters unordered, and with Stegoceras and Hypsilophodon designated as the outgroups. Characters associated with the syncervical and facial horns (characters 1, 18, 31, 108-

112; Makovicky 2010) were removed to determine their effect on the topology because they 65

66 were similar to our discrete functional characters. The phylogeny of Makovicky (2010) is restricted to primarily non-ceratopsid neoceratopsians. Therefore, we expanded the Families

Psittacosauridae, Centrosauridae, and Chasmosauridae with the topology of these clades recovered by Sereno (2010), Ryan et al. (2012), and Sampson et al. (2010), respectively, to more accurately reflect the evolution of our continuous characters (see below) in the phylogeny, resulting in our composite phylogeny (Figures 2.7–2.12) Having this phylogeny permits mapping of characters associated with the hypotheses for syncervical function.

2.3.3 Quantifying Relative Skull Size

To determine measures of relative head size that are both effective predictors of the true volumetric relationship of relative head size (i.e., head mass to body mass) and practical for paleontological studies, we collected a data set of 45 quadrupedal extant taxa consisting of 26 mammals and 19 reptiles. For each specimen, we collected body mass, skull mass (as a proxy for head mass, measured on a scale), basal skull length (measured from the tip of the premaxilla to the occipital condyle(s); BSL), length of the cervical vertebral series, length of the dorsal series, sacrum length, length of the caudal series, femur length and circumference, tibia length, metatarsal III length, and humerus circumference. If body mass was not collected before osteological preparation of the specimen, it was estimated using combined log-transformed humerus and femur circumference (Campione and Evans 2012). These data were also collected for 18 dinosaur taxa at the Royal Ontario Museum, and measurements for Stegosaurus (Gilmore

1914), Leptoceratops (Sternberg 1951), and Triceratops (Hatcher et al. 1907) were supplemented from the literature.

Our measurement of skull mass does not include the mass of non-ossified portions of the head. The brain is arguably the second heaviest portion of in-life head weight after skull mass (at least in mammals), but brain masses are rarely taken during the skeletonization of specimens. 66

Including estimates of brain masses based on published brain to body mass relationships is a potential solution for this issue. However, using such estimations from specimens other than those measured here introduces an unknown amount of error, which is why we opted not to include this measurement in the dataset.

The fossilization process permineralizes bones so that their fossilized weight is no longer reflective of their weight during life. We therefore first tested if there was a strong relationship between BSL, a frequently used metric for head size in extinct taxa, and skull mass in extant taxa. Because simple ratios can be highly influenced by body size and allometry (e.g., Atchley et al. 1976), we used the residuals from a linear regression to eliminate the influence body size might have on our results and to standardize our data. We obtained residuals from regressions of skull mass to body mass (skull mass on the y-axis) as our proxy for ‘real’ relative head size

(RRHS). All data used in regressions in this study were first log-transformed.

For one-dimensional proxies (combinations of linear measurements used as proxies for volumetric relative head size), we obtained residuals from regressions of BSL against total body length (TBL; Xu et al. 2006), length of the combined cervical, dorsal, and sacral series for ‘Back

Length’ (BL; Ostrom 1966), length of the combined dorsal and sacral series for Precaudal

Length (PL; Sereno et al. 2007), Femur Length (FL), and total Hind Limb Length (HLL; combined lengths of the femur, tibia, and metatarsal III). The residuals of each of the one- dimensional proxies were regressed against RRHS. We used Akaike information criteria to then determine the goodness of fit for each of our models using the R-package ‘stats’ (R-

Development-Core-Team 2010), and Akaike weights were calculated using the R-package

‘paleoTS’ (Hunt 2006).

2.3.4 Phylogenetic Analyses

Functional hypotheses for the syncervical predict that the syncervical evolved concurrently with, or after the acquisition of, large head size and/or cranial weaponry. Relative skull size is used as a discrete character in phylogenetic analyses by Makovicky (2010) and Xu et al. (2006), while Sereno et al. (2007) and Ostrom (1966) considered it a continuous character.

The syncervical and cranial weaponry (nasal and orbital horns) were considered discrete characters due to their categorical presence/absence nature (see below), but the evolution of large relative skull size in Ceratopsia was likely a gradual process. Making this character discrete would limit our ability to make conclusions about its evolution in relation to the syncervical, so we considered relative skull size to be a continuous character. To include the highest sample size of our phylogeny (see Discussion below), we quantified relative skull size by using residuals produced by a regression of BSL (with and without the frill) to FL. For taxa with a known humerus but no known femur, femur length was estimated using the slope of a regression of humerus length to femur length based on taxa in our data set with measurements of both elements.

Branch lengths for the phylogeny were estimated using the function ‘timePaleoPhy’ in the package ‘paleotree’ using default input (Bapst 2012) in which the earliest known occurrence of a taxon is considered the speciation event.. Formation data used to estimate branch lengths was taken from the literature (Dodson et al. 2004, Farke et al. 2011, Gilmore 1946, Kirkland and

DeBlieux 2010, Loewen et al. 2010, Makovicky and Norell 2006, Ryan 2007, Ryan et al. 2012,

Sampson et al. 2010, Sereno et al. 2007, Wu et al. 2007, Xu et al. 2010, You and Dodson 2004).

The three equally parsimonious trees from our phylogenetic analysis were used as sensitivity analyses. Ancestral character state reconstruction for relative skull size was performed in the open access statistical platform R v. 2.15 (R-Development-Core-Team 2010) using the function

‘ace’ in the package ‘ape’ (Paradis et al. 2004), which utilized a Brownian-motion maximum likelihood estimator. Ancestral character state reconstruction cannot use missing data, so rather than estimate the data for taxa with unknown skull or limb measurements, these taxa were excluded from our analyses to limit the amount of uninformed estimation. However, eliminating taxa from the analysis also neglects their influence on the hypothetical ancestral value. We recognize that limiting taxon sampling could produce non-real signals in the analyses. However, it is impossible to independently estimate the missing values needed without making assumptions about the way in which these variables evolve in relation to one another (i.e., without using regressions of other ceratopsian taxa). Therefore, the residuals of the skull vs. femur regressions and the log-transformed absolute skull lengths only for taxa in which these values are known were plotted on the phylogeny to determine the pattern of absolute and relative skull size evolution. For absolute skull size, reconstructions at each node of the tree (outside of

Psittacosauridae Leptoceratopsidae, and Protoceratopsidae) with 95% confidence intervals were plotted against node number to test for significant increases in absolute head size along the main

‘stem’ of the tree.

The threshold with which to falsify the hypothesis that neoceratopsians evolved a syncervical to support a relatively large head was determined from standard deviations (one and two SD) from the mean value of residuals produced from a regression of BSL to femur length using 46 extant taxa, 40 dinosaur taxa (38 when the length of the frill was included in basal skull length), and two fossil non-dinosaurian archosaurs.

The syncervical and cranial weaponry characters were considered discrete characters.

Binary presence/absence was used for the cranial weaponry, but the syncervical was coded as a multistate character to capture the morphological changes throughout its evolution. Character state ‘0’ was no fusion, ‘1’ indicates fusion of the centra only, and ‘2’ indicates the ceratopsid

70 morphology with complete fusion and a posterior-inclined axial neural spine. The syncervical character states were ordered given the compound nature of our defined character states. These discrete characters were mapped onto our phylogenies using parsimony-based accelerated

(ACTRAN) and delayed (DELTRAN) optimizations. The same method was used on both characters simultaneously as optimizing the characters differently could artificially increase our chances of supporting (by delaying the dependent weaponry character change) or falsifying (by delaying the independent syncervical character change) the functional hypotheses. These characters were then mapped onto the phylogeny and were compared to our results from the relative skull size analysis to test for correlated character evolution.

2.4 Description of Unfused Syncervicals

The ceratopsid syncervical has been described in detail by Campione and Holmes (2006) and Tsuihiji and Makovicky (2007). Here, we focus on key diagnostic features that allow us to identify these elements, features that can be used to distinguish them as unfused, and putative ontogenetic characters.

2.4.1 Atlas

The neoceratopsian atlas is distinguished by its circular, concave cotyle that receives the spherical occipital condyle (Figure 2.3). In anterior view, the cotyle of TMP 91.36.263 bears a small, thin indentation slightly dorsal to the center of the cotyle that is dorsoventrally long.

Fusion of the atlantal neural arches seems to be rare without an obvious ontogenetic pattern.

TMP 91.36.263 is weathered on the left lateral surface, but the pedicle for the right atlantal neural arch is preserved and slightly developed. The left neural arch of TMP 87.55.315 is fused to the centrum but only extends about two centimeters dorsally where it is broken. The right neural arch appears to have been completely broken off or weathered away in this specimen. An

71 atlantal cervical rib has never been described for a ceratopsid but is present in non-ceratopsid neoceratopsians (Brown and Schlaikjer 1940, Sternberg 1951). Despite being the smallest atlas element described here, TMP 91.36.263 bears a slightly raised, rugose area on its right lateral surface in the area where the atlantal cervical rib articulates in other neoceratopsians (Brown and

Schlaikjer 1940, Sternberg 1951) that is not present on TMP 87.55.315. The left surface of TMP

91.36.263 is very weathered away in this area, but a small portion of the attachment site for the atlantal rib is preserved.

The posterior surface of the atlantal centrum has a rugose texture instead of the smooth texture of other ceratopsid cervical centra. The dorsal and ventral portions are separated by a V- shaped groove that is deeper and more prominent in TMP 91.36.263 than it is in the larger specimen, TMP 87.55.315. The dorsal protion is likely the atlantal pleurocentrum and the ventral portion is likely the atlantal intercentrum (Tsuihiji and Makovicky 2007). The contribution of each to the atlas is probably similar to the condition seen in Protoceratops (Tsuihiji and

Makovicky 2007).

2.4.2 Unfused C3

No isolated axis has been recovered from a ceratopsid bonebed, but TMP 86.55.217, a fused atlas and axis (Figure 2.4), allows us to determine some features of unfused ceratopsid axes. The suture between the atlas and axis is not completely obliterated. The specimen is taphonomically crushed laterally, but the overall morphology of the ceratopsid axis is preserved

(Campione and Holmes 2006, Tsuihiji and Makovicky 2007). The axis centrum is normally fused to that of the atlas and third cervical vertebra (C3) in all neoceratopsians for which cervical vertebrae are known. The postzygapophyses and neural spine of the axis are also fused to the prezygapophyses and neural spine of C3 in ceratopsids. The unfused axial postzygapophyses of

TMP 86.55.217 are not rugose, and are comparable to the postzygapophyses of C4-9. The 71

72 posterior surface of the axial centrum, however, is rugose, but there is a radiating pattern to the rugosity that is not present on the atlases. This texture is also present on the posterior surface of the axis of the holotype specimen of Cerasinops (MOR 300) and a ceratopsid fused atlas and axis (TMP 81.16.400).

The ceratopsid C3 is identified by its short neural spine, acoelus posterior centrum, and small transverse processes (Campione and Holmes 2006, Tsuihiji and Makovicky 2007). TMP

86.55.53 is an isolated C3 (Figure 2.5), but the anterior surface is too weathered to determine the texture of the general unfused C3. However, we predict that the anterior surface should mimic the posterior surface of the axis. The preserved, unfused prezygapopyses allow us to determine that this specimen was at least partially unfused despite the missing dorsal-most portion of the neural spine. The prezygapophyses are smooth without signs of the unfused rugosity seen on the centra of the atlas and axis. There is a foramen ventral to each transverse process on TMP

86.55.53 that is connected with the neural canal, a feature never before described on a ceratopsid cervical vertebrae and not present on any other syncervical specimen examined.

2.5 Results

2.5.1 Quantifying Relative Skull Size

The average skull size of extant taxa was over 13.00% body length for all taxa (Table 2.2). Basal skull length was an average of 38.52% trunk length for all extant taxa (Table 2.2). Using

Ostrom’s (1966) measurement, the average relative head size for extant taxa is 30.07% precaudal length (Table 3). Basal skull length was, on average, 51.41% total hind limb length, and

120.15% femur length (Table 2.2).

BSL and skull mass were highly correlated (r2 = 0.97, df = 43, p < 2.2E-16). BSL was highly correlated with all one-dimensional body mass proxies (p < 0.0001; Table 2.3). On

73 average, extant taxa had a skull that weighed 1.62% body mass. Residuals of a regression of skull mass and body mass were then regressed against residuals of one-dimensional relationships

(Table 2.3). Mass vs. TBL was the best model for predicting relative head size (r2 = 0.28, p <

0.001, AIC = -3.09, Akaike weight = 0.64) followed by mass vs. PL (r2 = 0.26, p < 0.05, AIC = -

1.69, Akaike weight = 0.317) and mass vs. TL (r2 = 0.18, p < 0.001, AIC = 2.45, Akaike weight

= 0.04). The poorest model was mass vs. FL (r2 = 0.06, p > 0.05, AIC = 9.05, Akaike weight <

0.01) followed by mass vs. HLL (r2 = 0.08, p < 0.05, AIC = 7.80, Akaike weight < 0.01).

When we compared basal skull length to femur length in a phylogenetically broad sample of taxa (µ = 6.123e-18, σ = 0.1218), we found that only Alligator mississipiensis had a relatively large skull compared to femur length (Table 2.4). Pachyrhinosaurus, Pentaceratops,

Udanoceratops, and Utahceratops, however, did have residuals greater than one standard deviation from the mean, along with taxa such as Hippopotamus amphibious and Prestosuchus.

Cerasinops fell more than one standard deviation below the mean, along with taxa such as

Hypsilophodon, Basiliscus vittatus, and Carnotaurus. Rapetosaurus, Malawisaurus, and

Stegosaurus were all more than two standard deviations below the mean. When frills were included with basal skull length (µ = -1.148744e-17, σ = 0.1825299), the only extant taxa with large skulls are Alligator mississipiensis and Caiman crocodilius (one standard deviation; Table

2.4). The only dinosaurs that have relatively large skulls are ceratopsians, and Pentaceratops,

Utahceratops, and Styracosaurus have residuals greater than two standard deviations from the mean. Including the frill causes Lambeosaurus, Corythosaurus, and Ouranosaurus to be classified as having relatively small skulls (one standard deviation) and no extant taxa to have relatively small skulls (Table 2.4).

Ceratopsians with preserved partial vertebral columns (Psittacosaurus meileyingensis,

Leptoceratops, Centrosaurus, Chasmosaurus, and Triceratops) were compared to the dataset of

74 extant taxa and other dinosaurs to test the thresholds proposed by Ostrom (1966), Xu et al.

(2006), and Sereno et al. (2007) (Table 2.5). All ceratopsians fell within two standard deviations of the mean. Neoceratopsians were above one standard deviation of the mean for precaudal length and total body length (Table 2.5). Only Centrosaurus was above one standard deviation from the mean for trunk length (Table 2.5), although only three of the ceratopsian taxa have trunk lengths reported.

2.5.2 Syncervical Measurements

Linear measurements taken of 20 fused syncervicals and the four unfused syncervical elements described above were plotted against one another to determine if the unfused elements fall within the range of fused syncervicals. When plotted with measurements taken from fused elements, all unfused specimens fell within the size range for Ceratopsidae (Figure 2.6). At the genus level, unfused elements belonging to Pachyrhinosaurus all fell within the size range for fused elements belonging to that genus (Figure 2.6). TMP 91.36.263 is smaller than any other specimen in our data set belonging to Centrosaurus. However, it is still larger than the atlases of

TMP 83.18.56 (Ceratopsidae indet.) and MOR 591 (Achelousaurus horneri), both of which are fused.

2.5.3 Coevolution of Craniocervical Characters

Ancestral character state reconstruction recovered a general increase in relative head size with maximum relative head size reached in Bagaceratops and Avaceratops (Figure 2.7–2.9).

When the length of the frill is included, Protoceratops is recovered as having the largest relative head (Figure 2.10–2.12). Some ceratopsian taxa with vertebral measurements published fell outside one standard deviation from the average, but no taxon fell outside two standard deviations, which we consider a significantly large skull (Table 2.5, Figure 2.13). Furthermore,

75 the acquisition large absolute head size in ceratopsians is a gradual process (Figures 2.14, 2.15) and does not appear to change dramatically with syncervical evolution. However, a significant increase in head size was found at the node representing the transition from character states 1

(fusion of only the centra) to 2 (fusion of the neural arches, transverse processes, and posterior inclination of the axial nueral spine) in syncervical evolution for skull lengths including and excluding the frill (Figures 2.14, 2.15).

Character optimization indicated that the syncervical evolved in the ancestor of

Auroraceratops and Ceratopsidae for both ACTRAN and DELTRAN (Figures 2.7-2.12). Due to the limitations imposed by the available fossils, this analyses excludes Liaoceratops,

Yamaceratops, Archaeoceratops, and Asiaceratops, for which anterior cervical vertebrae are undescribed. It is therefore possible that the syncervical evolved much earlier in ceratopsian evolution, but our knowledge of their postcranial anatomy is too minimal to confidently determine and earlier origin of this character.

The nasal horn character was optimized by both ACTRAN and DELTRAN to have evolved in the ancestor of Ceratopsidae. Orbital horns are optimized by both ACTRAN and

DELTRAN to have evolved in the common ancestor of Ceratopsidae and Zuniceratops (Figures

2.7-2.12). The non-ceratopid taxa Turanoceratops and Zuniceratops have large brow horns, and this character likely optimizes to the ancestor of these two taxa and Ceratopsidae

(Turanoceratops not included in the phylogeny, Sues and Averianov 2009). These taxa have poorly represented postcrania and could not be included in the analysis; however it does not change the interpretations regarding syncervical evolution (see below).

2.6 Discussion

2.6.1 Determining Relative Skull Size in Amniotes

Determination of anatomical extremes in living animals allows more accurate interpretation of anatomy, and its evolutionary significance, in extinct taxa. Large heads in ceratopsians have been hypothesized to limit cranial mobility, require obligate quadrupedality, and therefore cause ecological constraints (Sereno et al. 2007). Definitions of what constitutes a relatively large skull size, however, have been variable in the literature, making tests of these hypotheses difficult. Previously proposed metrics for determination of skull size include comparison of basal skull length to 1) total body length, 2) precaudal vertebral series length, and

3) trunk length. Results of analyses on living animals indicate that the published thresholds for determining a relatively large head in ceratopsians (13%, 33%, and 40%, respectively) are all near (trunk length and precaudal vertebrae length) or below (total body length) the average for the extant taxa (Table 2.2; Appendix 1). These definitions, with respect to basal skull length, merely indicate that ceratopsians have a skull that is greater than average for terrestrial amniotes, rather than an extreme case of positive allometry. In order to test for extreme features, such as large skull size, a broad sample is required to distinguish taxa with ‘relatively small’ or

‘relatively large’ features from the average state for terrestrial amniotes, and establishing a baseline is critical for studies interested in potential anatomical extremes in the fossil record.

Within this context, only some ceratopsians (e.g., Udanoceratops, Pentaceratops) have potentially large skulls (outside one standard deviation; Table 2.4) compared to living mammals and reptiles, after allometry is taken into account.

This study is the first to include volumetric measures (mass) for comparisons of relative head size, which were compared to the previously proposed one-dimensional proxies. There are strong correlations between basal skull length and total body length (r2 = 0.86), precaudal length

(r2 = 0.93), trunk length (r2 = 0.92), hind limb length (r2 = 0.91) and femur length (r2 = 0.93), indicating that all three linear metrics for body size are good predictors of BSL. A strong relationship between skull mass and BSL (r2 = 0.97) confirms that skull length is an acceptable proxy for skull size. Comparisons of the three proposed methods for quantifying relative skull size, as well as comparisons of basal skull length to hind-limb length and femur length, to the relationship between skull mass and body mass indicates that the residuals from the relationship between total body length and basal skull length are best correlated with the residuals of body mass to skull mass. There is a strong relationship between inclusiveness of skeletal elements and the goodness-of-fit for the one-dimensional models. Total body length, the model with the best fit, includes the most amount of skeletal information (cervical, dorsal, sacral, and caudal vertebral series lengths), and femur length, the model with the worst fit, includes only one bone.

Although variance on the x-axis can affect correlations, this result is unlikely to be explained statistically, as the variables (with the exception of skull mass and femur length) were normally- distributed after being log-transformed, and pair-wise comparisons found no significant differences in the level of variance of our variables with the exception of basal skull length and trunk length (data not shown).

Given the often fragmentary fossil record of extinct taxa, assessment of relative head size based on indices that include the entire vertebral column is not ideal for paleontological data sets

(Hone 2012). In our investigation of ceratopsians, less than 10 taxa included in our sample of 57 ceratopsians preserve complete or relatively complete vertebral columns, allowing for total body length measurement. Therefore, metrics using the complete vertebral column severely limit sample size and compromises the power of quantitative analyses in paleontological studies of head size evolution. Precaudal vertebral length and trunk length have slightly better representation in the fossil record (n = 11 in our sample) and have strong correlations with basal

78 skull length (r2 = 0.93 and 0.92, respectively). Thus, they serve as better standards of comparison than total body length.

Femur length is commonly used to assess body size in paleontological studies (e.g.,

Carrano 2006, Sookias et al. 2012) and can therefore also be used to assess relative head size.

Twenty-four of the 57 taxa in the sample preserve femora and relatively complete skulls, allowing for a sample size increase of about 30% compared to metrics using vertebral column lengths. Although femur length is not as strong of a predictor of volumetric relative skulls size compared to metrics such as total body length, studies wishing to preserve statistical power may be limited to using this metric to increase sample size. This approach using femur length was used here to better capture patterns in relative head size evolution in Ceratopsia.

2.6.2 Head Size in Ceratopsia

Ceratopsids have the absolutely largest skulls of any terrestrial vertebrate (Dodson et al.

2004, Marsh 1891, Ostrom 1966, Sereno et al. 2007). In addition, a number of ceratopsian taxa have been shown to have relatively larger skulls than other terrestrial vertebrates (e.g., Ostrom

1966, Sereno 1986). Ostorm (1966) was the first to quantify relative skull size in ceratopsians and determined that a skull one-third the length of the precaudal vertebral series constitutes a large head. Forty years later, Xu et al. (2006) considered that a large skull is one that is 13% total body length. Most recently, Sereno et al. (2007) suggested that a skull that is 40% trunk length is not only large, but may incur ecological restrictions, such as limiting cranial mobility and requiring obligate quadrupedality.

The use of ratios in previous metrics attempted to accommodate for differences in head size as a strict consequence of body size increase. However, ratios have long been considered to inadequately remove effects of a standard variable (e.g., Atchley et al. 1976) and are therefore inappropriate here. As a result, we used residuals derived from Model I regression analyses of 78

79 basal skull length to the three previously proposed standard variables and used thresholds for large head size based on standard deviations from the mean of the current sample. Comparing relative head size of ceratopsians that preserve these standard variables (i.e., total body length, precaudal length, and trunk length) to other taxa found that no ceratopsian has an extremely large skull (two standard deviations from the average; Table 2.5; Figure 2.13). Neoceratopsians do have skull sizes outside one standard deviation from the mean when basal skull length is compared to total body length and precaudal length. Using trunk length only suggests that

Chasmosaurus has a relatively large skull (outside one standard deviation; Table 2.5). These results indicate that some extant taxa surpass ceratopsians in relative skull size based on these metrics (Figure 2.13). The use of a larger sample size that uses femur length as a proxy for size support the notion that ceratopsians are not unique in skull size, and it was only when skull length included the frill that some ceratopsian taxa (e.g., Pentaceratops, Styracosaurus) had large skulls relative to all other taxa in the data set (Table 2.4; see Discussion below).

Given the results, only certain ceratopsians have unusually long skulls, a trend that is related to the evolution of the prietosquamosal frill. The ceratopsian frill is a thin projection of bone that can extend far beyond the occipital condyle posteriorly. Because basal skull length is a one-dimensional measurement of skull size, it assumes homogeneity along the axis it measures.

This assumption is never met perfectly, given the complexity of the vertebrate skull, but the results show a strong correlation between basal skull length and skull mass (r2 = 0.97), thereby giving support to the use of this measure as a proxy for skull size. The portion of skull length to which the frill would contribute likely violates the assumption of homogeneity to a greater degree, given the relatively low volume of the frill compared to the rest of the skull. For example, in Triceratops, the frill adds significant length to the skull (approximately 71%), resulting in a long skull relative to body length (an estimate measured from the tip of the snout to 79

80 the tip of the tail; approximately 12.6%; Hatcher et al. 1907). In comparison, the mass of the frill accounts for only 1.5% total body mass (Henderson 1999). Therefore, although inclusion of the frill as a measure of skull size suggests relatively large skulls in ceratopsians, mass estimates indicate that the size of the frill is negligible, and should therefore not be included in studies of relative head size.

2.6.3 Function and Evolution of the Ceratopsian Syncervical

The large and ornamented heads of ceratopsians have been important in the interpretation of many aspect of their biology, such as intraspecific head-to-head combat (Farke 2004, Farlow and Dodson 1975, Molnar 1977), sexual selection (Sampson 1999, Spassov 1979) or species recognition (Padian and Horner 2011), and potential thermoregulation (Barrick et al. 1998).

Cranial features have also influenced functional interpretations of cervical adaptations in the form of fusion of the anterior neck vertebrae. The current functional hypotheses for the ceratopsid syncervical are that it helped mitigate stresses related to 1) skull weight (Dodson et al.

2004, Hatcher et al. 1907, Marsh 1891, Ostrom and Wellnhofer 1986, Sereno et al. 2007) and 2) intraspecific head-to-head combat (Bakker 1986, Farlow and Dodson 1975, Molnar 1977,

Spassov 1979).

Marsh (1891) first proposed that the syncervical functions to support a large ceratopsid head, which was later emphasized by Hatcher et al. (1907). This hypothesis assumes the downward forces of gravity related to skull mass are transferred through the craniocervical joint to the neck. The head support hypothesis has become the default in the literature (Campione and

Holmes 2006, Dodson 1996, Dodson et al. 2004, Sereno et al. 2007, Tanke and Rothschild 1997) but lacks a specific biomechanical explanation. However, this is not the only proposed adaptive hypothesis. Farlow and Dodson (1975) were first to note that this structure could reflect a possible increase in mobility at the cranio-cervical joint and hypothesized that it played a role 80

81 during intraspecific combat, which Ostrom and Wellenhoffer (1986) later described in more detail by hypothesizing head posture and less mobile areas of the anterior vertebral column potentially related to combat behavior. The combat hypothesis suggests that the syncervical evolved in response to torsional and compressive forces on the neck generated during intraspecific head-to-head combative behavior, potentially resulting from horn-locking (Farke

2004). However, combative behavior is difficult to reconstruct in the fossil record (see Dodson et al. 2004 and references within), but this hypothesis has been proposed multiple times without a detailed biomechanical explanation of the effects of fusion on skull buttressing or increased mobility on combat (Bakker 1986, Farlow and Dodson 1975, Molnar 1977, Ostrom and

Wellnhofer 1986, Sampson 1997, Spassov 1979).

In both cases, these hypotheses imply that fusion of the anterior cervical vertebrae is an adaption and predict that fusion should occur in adult ceratopsids. However, the occurrence of unfused syncervical elements in large-headed (based on inferred occipital condyle size;

Anderson 1999), presumably adult ceratopsids suggests that fusion was not critical to its function. Ontogenetic processes cannot explain the unfused elements because they all fall within the size range of fused syncervical elements (Figure 2.6). Furthermore, the anterior cervicals of a juvenile specimen of Avaceratops are completely fused (Penkalski and Dodson 1999), which suggests that fusion of the syncervical occurs early in ceratopsid ontogeny. The occurrence of unfused syncervicals could represent individual variation or pathology. Although evidence of pathological bone texture is lacking (e.g., Kompanje 1999, Mulder 2001), the low frequency of unfused elements within large samples of Centrosarus and Pachyrhinosaurus is suggestive of a developmental abnormality rather than individual variation. Regardless of the mechanism by which these elements remained unfused, they also challenge the previously proposed functional hypotheses related to cervical fusion in ceratopsids.

Tests within a broad ceratopsian phylogenetic framework support neither adaptive hypothesis. The earliest ceratopisans, including Yinlong and psittacosaurids, do not possess a syncervical, and the morphology of the syncervical varies throughout the evolutionary history of neoceratopsians. In Auroraceratops, Protoceratops and Leptoceratops, only the centra of the first three cervicals are fused (Morschhauser 2012, Sternberg 1951). In Montanoceratops

(Makovicky 2010), the neural spines are also partially fused, whereas ceratopsids have fully fused centra, neural arches, and neural spines with an anteroposterior expansion of the axial neural spine (Figures 2.7-2.12; see also Campione and Holmes 2006, Tsuihiji and Makovicky

2007).

The head support and combat hypotheses predict that the syncervical evolved either in concert with, or after the appearance of 1) large head size or 2) cranial weaponry in ceratopsians, respectively. Ancestral character state optimizations clearly show that the syncervical evolves first in small-bodied non-ceratopsid neoceratopsians that have average sized heads for both ceratopsians and terrestrial amniotes when basal skull length is standardized by femur length

(Figures 2.7-2.12; Table 2.4). Even when absolute head size was examined, the acquisition of large skulls is gradual. There is a significant increase in skull size at the node where a posteriorly inclined axial neural spine evolves (Figures 2.14, 2.15), suggesting that morphological changes in syncervical evolution may have aided in head support. However, data are missing to reconstruct the nodes just before this significant difference, so this significant increase might instead reflect incomplete sampling.

It was not possible to directly test how relative skull size evolves using previously proposed metrics (Ostrom 1966, Sereno et al. 2007, Xu et al. 2006) due to limitations of sample size. Nevertheless, based on the sample size for which vertebral measurements are known, none surpass Ostrom’s (1966) threshold of a basal skull length one-third precaudal vertebral length,

83 except Leptoceratops (50%), which was still not an extreme outlier in the residual analysis. Of the three taxa with trunk lengths, both Psittacosaurus meileyingensis and Chasmosaurus have basal skull lengths greater than 40% trunk length (Sereno et al. 2007). However, Triceratops falls below this threshold, and results from residuals (Table 2.5) suggest that, by this metric, these ceratopsians have typical relative skull sizes compared to other terrestrial amniotes. Even with metrics presented by Ostrom (1966) and Sereno et al. (2007), the data still support our rejection of the head support hypothesis. The threshold proposed by Xu et al. (2006), which defines a large head as 13% total body length, does not allow us to reject this hypothesis as large head size would be plesiomorphic for Ceratopsia (Figures 2.7-2.12). However, this threshold represents the average for terrestrial amniotes (Table 2.2), and ceratopsians are not extreme outliers in the distribution of residuals of basal skull length to total body length (Table 2.5).

Taken together, these analyses falsify the hypothesis that the syncervical evolved to support a large head.

Ancestral state reconstructions indicate that the syncervical also evolves before the appearance of either nasal or orbital horns, which falsifies the hypothesis that intraspecific combat acted as a selective pressure for the origin of the neoceratopsian syncervical. Prominent nasal horns evolved in the ancestor of Ceratopsidae based on character codings for the nasal horn in Xu et al. (2006), and orbital horns optimize in the ancestor of Ceratopsidae and Zuniceratops.

Therefore, we can reject the hypothesis that forces resulting from intraspecific combative behaviors influenced the evolutionary origin of the syncervical.

While these two hypotheses cannot explain the origin of the neoceratopsian syncervical, they may explain subsequent morphological changes during its evolution. For example, ancestral state reconstructions indicate that the anteroposterior expansion of the axial neural spine evolved in concert with the evolution of cranial weaponry and enlarged heads of ceratopsids. A nuchal

84 ligament, which attaches to the anterior cervical vertebrae and the nuchal region of the skull, is the primary skull support structure in tetrapods (e.g., Hildebrand and Goslow 2001). Expansion of the axial neural spine may have increased the attachment site for this ligament, possibly allowing its size and strength to increase, as well. Without further soft-tissue and biomechanical reconstructions of the ceratopsid syncervical, we cannot reject that these other syncervical characters evolved in response to physical demands associated with increased head size or combative behavior. However, unfused syncervicals imply that fusion was not essential to syncervical function, suggesting that other aspects of syncervical anatomy may have been exapted in ceratopsids.

These analyses reject the two widely cited functional hypotheses as selective pressures for the origin of the syncervical, leaving the mechanism for its origin unclear in ceratopsians.

Fused anterior cervical vertebrae are known for some rodents, some cetaceans, armadillos, and a disparate number of other taxa (e.g., Buchholtz 2001, Buchholtz and Schur 2004, Gupta 1966,

Rose and Emry 1983a, 1993). This ecologically disparate group of extant taxa with analogous cervical structures provides important models that may give insight into the function and origin the neoceratopsian syncervical. Many extant taxa with a syncervical are fossorial, and cervical fusion has been suggest to improve digging ability by increasing out-force produced during head-lift digging (e.g., Barnosky 1981, Rose and Emry 1983b). This hypothesis is particularly interesting because some ceratopsians are hypothesized to exhibit fossorial behaviors (Longrich

2010). Alternatively, ceratopsians have a unique suite of cranial morphologies including short, deep jaws with parrot-like beaks that arose early in the clade and suggest feeding strategies that are different from other ornithschians. (e.g., Sereno et al. 2010, Tanoue et al. 2009). It is, therefore, conceivable that feeding ecology may have played a role in the evolution of the syncervical in ceratopsians.

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Table 2.1: Scorings for Auroraceratops into Makovicky (2010)

10 20 30 40 50 60 70

Auroraceratops ?101??1?11 111011000? ?010?01011 100001111 0?00??0111 110?000??0 1?1100?011

80 90 100 110 120 130 140 147

111010?010 110010101 0100?01201 0??0?10101 111??????? ?????00?0? ???000010? 0?0????

Table 2.2: Relative head size in extant taxa shown as percentages

Metric All taxa Mammals Reptiles Body length 13.17% 15.31% 10.24% Precaudal length 30.09% 31.70% 27.90% Trunk length 38.52% 38.74% 38.22% Hindlimb length 51.41% 46.40% 58.26% Femur length 120.15% 113.02% 129.90%

Table 2.3: Goodness-of-fit statistics for one-dimensional models when compared to the volumetric metric.

Total Body Length Trunk Length Precaudal Length Hind limb Length Femur Length r-squared 0.2784*** 0.1839*** 0.2556*** 0.08099* 0.06 AIC -3.09 2.45 -1.69 7.80 9.05 Akaike weight 0.64 0.04 0.32 0.00 0.00 Intercept 1.14E-17 4.14E-18 -2.11E-18 2.55E-18 4.14E-18 Slope 1.01 1.11 1.34 0.77 0.75 CI intercept -0.07 -0.07 -0.07 -0.08 -0.08 0.07 0.07 0.07 0.08 0.08 CI slope 0.53 0.43 0.67 0.07 -0.05 1.49 1.79 2.02 1.47 1.55

Table 2.4: Taxa that fall outside of one and two standard deviations of the mean when skull length is compared to femur length.

Big head Small head 1 SD 1 SD Hippopotamus amphibius Sylvilagus foridanus Caiman crocodilius Cyclura cornuta Dracaena guianensis Physignathus lesueurii Tiliqua scincoides Chlamydosaurus kingi Prestosuchus Basiliscus vittatus Udanoceratops Phrynosoma platyrhinos Pentaceratops Eoraptor Utahceratops Masiakasaurus Pachyrhinosaurus lakustai Carnotaurus Amargasaurus Hypsilophodon Cerasinops

2 SD 2 SD Alligator mississipiensis Rapetosaurus Malawisaurus Stegosaurus stenops Big head (frill) Small head (frill) 1 SD 1 SD Alligator mississipiensis Eoraptor Caiman crocodilius Masiakasaurus Protoceratops Ouranosaurus Centrosaurus Lambeosaurus Triceratops Carnotaurus Chasmosaurus belli Corythosaurus Kosmoceratops Amargasaurus Chasmosaurus russelli Avaceratops Einiosaurus

2 SD 2 SD Pentaceratops Rapetosaurus Utahceratops Malawisaurus Styracosaurus Stegosaurus stenops

Table 2.5: Residuals of ceratopsian taxa with known vertebral chains compared to one standard deviation from the mean.

Total Body Length Trunk Length Precaudal Length 1SD 0.16 0.12 0.15 Psittacosaurus 0.09 0.09 0.04 Leptoceratops - - 0.28 Centrosaurus 0.24 - 0.17 Chasmosaurus 0.20 0.15 0.18 Triceratops 0.28 0.09 0.18

100

Table 2.6: Measurements of fused and unfused syncervical elements used in the analysis

Taxon Specimen AtH logAtH AtL logAtL AxH logAxH AxL logAxL C3L logC3L C3H logC3H Centrosaurus apertus TMP 95.400.250 75.5 1.877946 76.5 1.883661 92.6 1.966610 87.6 1.942504 88.6 1.947433 102 2.008600 Ceratopsidae TMP 83.18.56 70.5 1.848189 60.9 1.784617 88.3 1.945960 93.3 1.969881 87.2 1.940516 87.4 1.941511 Centrosaurus sp. TMP 80.18.274 85.7 1.932980 75.5 1.877946 94.1 1.973589 91.4 1.960946 84.2 1.925312 106.9 2.028977 Centrosaurus sp. TMP 87.18.59 75.9 1.880241 79.6 1.900913 83.5 1.921686 96.8 1.985875 79.8 1.902002 90.7 1.957607 Ceratopsidae TMP 81.19.131 73.8 1.868056 64.6 1.810232 65.3 1.814913 78.8 1.896526 65.1 1.813580 67.7 1.830588 Ceratopsidae TMP 96.176.0141 76.9 1.88592 87.1 1.940018 97.1 1.98721 79.8 1.902002 99.3 1.996949 106 2.025305 P. lakustai TMP 86.55.247 87.7 1.942999 76.5 1.883661 83.9 1.923761 106.7 2.028164 96.6 1.984977 83.1 1.919601 P. lakustai TMP 89.55.1292 90.2 1.955206 93.9 1.972665 P. lakustai TMP 87.55.223 95.3 1.979092 94.1 1.973589 87.4 1.941511 106 2.025305 80.1 1.903632 107.2 2.030194 P. lakustai TMP 88.55.195 89.2 1.950364 110 2.041392 86.5 1.937016 85.1 1.92992 93.9 1.972665 P. lakustai TMP 89.55.665 93 1.968482 82.4 1.915927 103.95 2.016824 98.5 1.99343 86.8 1.938519 92.8 1.967547 P. lakustai TMP 88.55.33 96.8 1.985875 80.4 1.905256 103.8 2.016197 127.6 2.105850 P. sp. TMP 02.76.1 93.38 1.97025 93.7 1.971739 103.54 2.015108 93.02 1.968576 97.84 1.990516 101.28 2.005523 Achelousaurus horneri MOR 591 62.72 1.79740 57.07 1.756407 67.78 1.831101 79.56 1.900694 74.6 1.872738 71.87 1.856547 Achelousaurus horneri MOR 571 77.81 1.891035 69.35 1.841046 85.89 1.933942 94.16 1.97386 82.93 1.918711 94.13 1.973728 Centrosaurus apertus ROM 767 86.39 1.936463 91.05 1.95927 70.11 1.845779 89.75 1.953034 98.69 1.994273 88.92 1.948999 P. lakustai UALVP 53552 86.53 1.937166 76.36 1.88286 103.82 2.016281 97.43 1.988692 84.3 1.925827 109.78 2.040523 Centrosaurus apertus TMP 1991.36.263 72.25 1.858837 62.91 1.798719 P. lakustai TMP 1987.55.315 95.71 1.980957 75.13 1.875813 P. lakustai TMP 1986.55.53 92.8 1.967547 86.86 1.938819 96.24 1.983355 97.5 1.989004 P. lakustai TMP 1986.55.53 75.4 1.877371 97.73 1.990027 Pachyrhinosaurus CMN 10630 125 2.096910 109.8 2.04060 111.5 2.047274 98.8 1.994756 130.8 2.116607 143.3 2.15624 Chasmosaurus belli CMN 2245 76.1 1.881384 85.3 1.930949 71 1.851258 94.8 1.976808 91.3 1.960470 112 2.049218 Abbreviations: At, atlas; Ax, axis; C3, third cervical vertebra; H, centrum height; L, centrum length

100

101

Figure 2.1. An example of a ceratopsid syncervical. The syncervical of Styracosaurus albertensis (CMN 344) in anterior (A), lateral (B), and posterior (C) view. At, atlas; AtNA, atlantal neural arch; Ax, axis; AxNS, Axial neural spine; C3, third cervical vertebra; C3NS, C3 neural spine; ivf, intervertebral foramen; tp, transverse process. Scale bar = 5 cm

101

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Figure 2.2 A diagrammatic view of the measurements taken of fused and unfused syncervicals. Centrum height, width, and length measurements were taken on all vertebrae, and neural spine height was taken on the axis and C3. All other measurements were only taken where shown here on the syncervical. aCH, anterior centrum height; aCW, anterior centrum width; dCL, dorsal centrum length; ivfL, intervertebral foramen length; NSH, neural spine height;

NSL, neural spine length; pCH, posterior centrum height; pCW, posterior centrum width; TPL, transverse process length; vCL, ventral centrum length.

103

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105

Figure 2.3 The isolated, ufused atlases. TMP 87.55.315 (a-f) and TMP 91.36.263 (g-l) in anterior (A, G) left lateral (B, H), ventral (C, I), posterior (D, J), right lateral (E, K), and dorsal

(F, L) views. Anatomical abbreviations: an, atlas neural arch; atp, atlas pleurocentrum; axi, axial intercentrum; co, cotyle; p, peduncle.

105

106

!" ! # " , !"

&' #

!" + * ) #

!$#

!$% # ( ' &

&' #

!$# % $ # #

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106

107

Figure 2.4 The isolated atlas-axis. TMP 86.55.217 in anterior (A), left lateral (B), posterior (C), right lateral (D), dorsal (E), and ventral (F) views. Anatomical abbreviations: at, atlas; ax, axis; axns, axial neural spine.

107

108

! & !#$% % $ !" !#$% !" !"

!" !#

!# # "

!#$% !#$%

!#$% !# !#

108

109

Figure 2.5 The isolated third cervical vertebra. TMP 86.55.53 in anterior (A), left lateral (B), dorsal (C), posterior (D), right lateral (E), and ventral (F) views. Anatomical abbreviations: c3ns,

C3 neural spine; f, fenestra; posz, postzygapophyses; prez, prezygapophyses; tp, transverse process.

109

110

! !"#$ & %&'( % %&'( %&'( !"#$

%)$( *%

!"#$

# " $ %)$( !"#$ !"#$ %&'(

%)$( +

110

111

Figure 2.6 Measurements of fused and unfused syncervical elements. A regression of log- transformed centrum length and height for the atlas (A; R2 = 0.8473, intercept = 0.2631), axis (B;

R2 = 0.1812, intercept = 1.613), and third cervical vertebra (C; R2 = 0.6837, intercept = 0.556) showing the relative size of unfused and fused syncervical elements.

111

112

! # %"&( %"&% %"&& %"&& !"$( !"$# !"$& !"$< !"#( !"$; !"$% )*+!&,-=80,123.456,:23+.9 !"#& )*+!&,-.)/0,123.456,:23+.9 !"$& !"'( !"# !"$ %"& %"! !"#( !"$& !"$( %"&& %"&( )*+!&,-.)/0,123.456,728+9. )*+!&,-=80,123.456,728+9.

" %"!& !"#$%&$'()*"+&+* %"&( !"#$%&$'()*"+&+*,@53A502BC

%"&& ,-(.&)*"+&+* ,-(.&)*"+&+*,@53A502BC !"$( *.924,124/.*D08B/2 !"$& )*+!&,1>,?23.456,)23+.9 !"#(

!"$& !"$( %"&& %"&( %"!& )*+!&,1>,?23.456,928+9.

112

113

Figure 2.7 Character evolution in Ceratopsia without the frill, first phylogeny. The composite phylogeny of Ceratopsia with ancestral character states for relative head size (not including the frill) and discrete characters mapped to test for character coevolution. Bolded taxa had data available for quantifying head size in vertebrates without the frill included. (*) denotes taxa that deviate more than one standard deviation above the average, (**) denotes taxa that deviate more than two standard deviations above the average, and (•) denotes taxa that deviate more than one standard deviation below the average.

113

114

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

" # $ A%&B+2.8? 0.00 : 0.02 @ = " 0.03 : 0.05 0.06 : 0.08 >0.09

114

115

Figure 2.8 Character evolution in Ceratopsia without the frill, second phylogeny. The composite phylogeny of Ceratopsia with ancestral character states for relative head size (not including the frill) and discrete characters mapped to test for character coevolution. Bolded taxa had data available for quantifying head size in vertebrates without the frill included. (*) denotes taxa that deviate more than one standard deviation above the average, (**) denotes taxa that deviate more than two standard deviations above the average, and (•) denotes taxa that deviate more than one standard deviation below the average.

115

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

" # &'%B,3/9=013%5C%D(E% $ 85%FE%;G,08%H0I@ < -0.16 "'%()*+,-./+01 -0.15 : -0.13 A > " # -0.12 : -0.10 " #'%20301%45-*3 -0.09 : -0.07 A > " -0.06 : -0.04 $'%6-7/801%45-*3 A > " -0.03 : -0.01 0.00 : 0.02 ! !'%4,09%(/:,%;<=%,8%01'%#>>?@ A > " 0.03 : 0.05 0.06 : 0.08 >0.09 %%

116

117

Figure 2.9 Character evolution in Ceratopsia without the frill, third phylogeny. The composite phylogeny of Ceratopsia with ancestral character states for relative head size (not including the frill) and discrete characters mapped to test for character coevolution. Bolded taxa had data available for quantifying head size in vertebrates without the frill included. (*) denotes taxa that deviate more than one standard deviation above the average, (**) denotes taxa that deviate more than two standard deviations above the average, and (•) denotes taxa that deviate more than one standard deviation below the average.

117

118 +(&(.(*"/&/* !":'(&%)(3'3)11 B/>%(*"/&/* 9.$,3$%&"'()* ?6+8%+$ 4%.($%&"'()* ?3">6($%&"'()* 9:,)68%,;%/%+ !"#$%&#'() +,"(-".#*"/&/* 4/".,/"$%&"'()* 0457%+$%86#+)6) 0457(=%' 7:;6/<3"'/.%.*3* 7:;1%36%-3.#%.*3* 045)6>6'6&3) 045+#67%+$%86#+)6) 045)6+#+)6) 23"($%&"'()* 0"1"$%&"'()* 9&$,"%($%&"'()* 2#'()6+%,) *%+"(+%&#'("%,) 7&%.($%&"'()* ./(+%&#'("%,) -#,"%&#'("%,) 9*3"$%&"'()* <3'%'(&#'("%,) 0'%"%&#'("%,)1 !"#"$%&"'()* 5&"$363$%&"'()* 8/.3$%&"'()* 96>%&'"$%&"'()* =3.($%&"'()* C"#"$%&"'()* 9&&,3.($%&"'()* E:;/'",%.*3* B'6&#'("%,)1 2#+"'%)(3'3)1 245>#88615 245'3))#8861 9#/<"$%&"'()* ."(;&#'("%,)11 0#+"(&#'("%,)11 +(",/36"$%&"'()* F('&3$%&"'()* E:;6"'/* D%@($%&"'()* =)3.()* A6+6%)(3'3)1 9$,%6(/*"/&/* 7":;6"A/*'"3 7":;$"."@%.*3* C%)7%&#'("%,)1 <@(&#'("%,)1 " # $ ! %

" # %'&()*+,-./*&01&234& $ 50&64&78).5&9.:;&& < -0.18 -0.17 : -0.14 "'&3<=>)?@+>./ -0.13 : -0.10 " I G " # -0.09 : -0.06 #'&A.*./&B0?=* -0.05 : -0.02 I G " $'&C?D+5./&B0?=* -0.01 : 0.02 I G " 0.03 : 0.06 ! !'&B).,&3+E)&7F-&)5&./'&#GGH; 0.07 : 0.10 I G " 0.11 : 0.14 >0.15

118

119

Figure 2.10 Character evolution in Ceratopsia with the frill, first phylogeny. The composite phylogeny of Ceratopsia with ancestral character states for relative head size (including the frill) and discrete characters mapped to test for character coevolution. Bolded taxa had data available for quantifying head size in vertebrates with the frill included. (*) denotes taxa that deviate more than one standard deviation above the average, (**) denotes taxa that deviate more than two standard deviations above the average, and (•) denotes taxa that deviate more than one standard deviation below the average.

119

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

" # &'%()*+,-./*%01%234% $ 5+67%18+//%60%94%:7).6% ;.<=%% "'%3>?@)8A+@./ < -0.18 " J H " # -0.17 : -0.14 #'%B.*./%C08?* -0.13 : -0.10 J H " -0.09 : -0.06 $'%D8E+6./%C08?* -0.05 : -0.02 J H " -0.01 : 0.02 ! !'%C).,%3+F)%:G-%)6%./'%#HHI= 0.03 : 0.06 J H " 0.07 : 0.10 0.11 : 0.14 >0.15

120

121

Figure 2.11 Character evolution in Ceratopsia with the frill, second phylogeny. The composite phylogeny of Ceratopsia with ancestral character states for relative head size

(including the frill) and discrete characters mapped to test for character coevolution. Bolded taxa had data available for quantifying head size in vertebrates with the frill included. (*) denotes taxa that deviate more than one standard deviation above the average, (**) denotes taxa that deviate more than two standard deviations above the average, and (•) denotes taxa that deviate more than one standard deviation below the average.

121

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

%&'()*+,-./*'01'234' " # 5+67'18+//'60'94':7).6' $ ;.<= < -0.16 "&'3>?@)8A+@./ -0.15 : -0.13 J H " # -0.12 : -0.10 " #&'B.*./'C08?* -0.09 : -0.07 J H " -0.06 : -0.04 $&'D8E+6./'C08?* -0.03 : -0.01 J H " 0.00 : 0.02 !&'C).,'3+F)':G-')6'./&'#HHI= ! 0.03 : 0.05 J H " 0.06 : 0.08 >0.09

122

123

Figure 2.12 Character evolution in Ceratopsia with the frill, third phylogeny. The composite phylogeny of Ceratopsia with ancestral character states for relative head size (including the frill) and discrete characters mapped to test for character coevolution. Bolded taxa had data available for quantifying head size in vertebrates with the frill included. (*) denotes taxa that deviate more than one standard deviation above the average, (**) denotes taxa that deviate more than two standard deviations above the average, and (•) denotes taxa that deviate more than one standard deviation below the average.

123

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

%'&()*+,-./*&01&234& " # 5+67&18+//&60&94&:7).6& $ ;.<=&& < -0.18 "'&3>?@)8A+@./ J H " # -0.17 : -0.14 " #'&B.*./&C08?* -0.13 : -0.10 J H " -0.09 : -0.06 $'&D8E+6./&C08?* -0.05 : -0.02 J H " -0.01 : 0.02 !'&C).,&3+F)&:G-&)6&./'&#HHI= 0.03 : 0.06 ! J H " 0.07 : 0.10 0.11 : 0.14 >0.15

124

125

Figure 2.13 Relative head size in amniotes based on previously proposed metrics. The three previously proposed metrics, basal skull length to trunk length (A, B), precaudal length (C, D), and total body length (E, F), compared used residuals showing ceratopsians relative to mammals, reptiles, and other dinosaurs.

125

126

! " %"# !"$ !"# ï '()&#*4/-''*01.)23 &"$ ï

!"# !"$ %"# %"$ '()&#*+,-./*01.)23

# $ %"# !"$ !"# ï '()&#*4/-''*01.)23 &"$ ï

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!"$ %"# %"$ 9"# '()&#*+(27'*:(8;*01.)23 @7AA7'? <1=2>'1? C231,*8>.(?7-,? B1,72(=?>7.?

126

127

Figure 2.14 Absolute head size reconstructed on a phylogeny of Ceratopsia. log-transformed basal skull length is reconstructed on one of the phylogenies showing reconstructions of discrete traits and a heat map of basal skull length values. A graph of reconstructed basal skull length at each node (except those within Psittacosauridae, Leptoceratopsidae, and Protoceratopsidae) is also presented with syncervical character changes noted.

127

128 A ! $ # " +\SVLORSKRGRQ !"#$%&#'() ?7+9%+$ 3=(%>(+$)(4'4) !"#$%"#&'(#)*+, 2568%+$%97#+)7) 2568(;%'

! 25694;7("4+#+)7) 2568#79#>7+$#+)7) 256)7<7'7&4) 256+#78%+$%97#+)7) 256)7+#+)7) -7(%&#'("%,) ?(8(&#'("%,) :'&=(#%&#'("%,) :4'%'(&#'("%,) &HUDVLQRSV !%&3+/8&'.9+&:;<&+7&/0%&#==>? $%&5,6.7/0&34,)2 #%&1/2/0&34,)2 "%&'()*+,-.*/0 @ @ @ *%+"(+%&#'("%,) 0('$*&'(#)*+, " @ = = = ./(+%&#'("%,)0 -#,"%&#'("%,) = " " " 2,.#&'(#)*+, 2'%"%&#'("%,) " # 1($(&#'("%,) -(#&./.&'(#)*+, 1"$.&'(#)*+, !'$*&'(#)*+, A7(<9%&#'("%,) :@(&#'("%,) 2/5'()#&'(#)*+,

$ 4+.$*+, 3#+"'%)(4'4) 3*(*$*,#"(", !">'(&%)(4'4) A%&04BC7,/)2D4,E+8&F'G 4.$*&'(#)*+, && " # 9"5'*,#"(", >3.02 2.91 : 3.01 2.80 : 2.90 2.69 : 2.79 2.58 : 2.68 2.47 : 2.57 2.36 : 2.46 2.25 : 2.35 2.14 : 2.24 < 2.13 C7+7%)(4'4) 2&%'/*",#"(", 2(569(B4)"(70 0#67&#$#8'$,., 356<#9976 356'4))#997 2:";#&'(#)*+, ."(=&#'("%,)0 2#+"(&#'("%,)0 3*#%"./#&'(#)*+, D($(&#'("%,) G%)8%&#'("%,) 2$&%.&'(#)*+, :''=7+%&#'("%,) =*)(.&'(#)*+, <67/#)", <67")#%'$,., F'7&#'("%,)

E#/%&#'("%,) Node Number Node

5 10 15 2.2 Reconstruction 2.6 3.0 " "

128

129

Figure 2.15 Absolute head size including the frill reconstructed on a phylogeny of Ceratopsia. log-transformed basal skull length with the frill included is reconstructed on one of the phylogenies showing reconstructions of discrete traits and a heat map of basal skull length values. A graph of reconstructed skull length at each node (except those within Psittacosauridae, Leptoceratopsidae, and Protoceratopsidae) is also presented with syncervical character changes noted.

129

130 A ! $ # " +\SVLORSKRGRQ !"#$%&#'() <6+8%+$ +,"(-".#*"/&/* 0/".,/"$%&"'()* 1457%+$%86#+)6) 1457(:%'

! 14583:6("3+#+)6) 1457#68#>6+$#+)6) 145)6;6'6&3) 145+#67%+$%86#+)6) 145)6+#+)6) -6(%&#'("%,) <(7(&#'("%,) 9'&=(#%&#'("%,) 93'%'(&#'("%,) &HUDVLQRSV !%&3+/8&'.9+&:;<&+7&/0%&#==>? $%&5,6.7/0&34,)2 #%&1/2/0&34,)2 "%&'()*+,-.*/0 @ @ @ @ *%+"(+%&#'("%,) 4&%.($%&"'()* = = = = " ./(+%&#'("%,)0 -#,"%&#'("%,) " " " " 6*2"$%&"'()* 1'%"%&#'("%,) # !"#"$%&"'()* 1&"$232$%&"'()* 5/.2$%&"'()* 0%.($%&"'()* 92"83($%&"'()* 9?(&#'("%,) 638%&'"$%&"'()*

$ 7)2.()* 2#+"'%)(3'3) +(&(.(*"/&/* !">'(&%)(3'3) F'G&H.7I&D,.00 A%&04BC7,/)2D4,E+8& 72.($%&"'()* && " # ?/8%(*"/&/* 3.18 : 3.31 3.04 : 3.17 2.90 : 3.03 2.76 : 2.89 2.62 : 2.75 2.48 : 2.61 2.34 : 2.47 2.20 : 2.33 < 2.19 @6+6%)(3'3)

>3.32 6$,%3(/*"/&/* 4":;3"=/*'"2> 4":;$"."<%.*2* 245;#8865 245'3))#886 6#/@"$%&"'()* ."(=&#'("%,)0 1#+"(&#'("%,)0 +(",/23"$%&"'()* A($(&#'("%,) D%)7%&#'("%,) 6.$,2$%&"'()* 9''=6+%&#'("%,) B('&2$%&"'()* A:;3"'/* A:;/'",%.*2* C'6&#'("%,)

B#/%&#'("%,) Node Number Node

5 10 15 2.2 Reconstruction 2.6 3.0 3.4 " "

130

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Appendix 2

body mass skull mass Femur Taxon Specimen # Clade (g) (g) Skull FC HC TBL % TBL TL % TL HL L % HL L L % FL PC % PC Sphenodon punctatus ROM R170 R 6.2 47.13 12.46 11.44 347.35 13.57% 111.24 42.37% 70.07 67.26% 35.22 133.82% 145.22 32.45% Pogona vitticeps ROM R8504 R 324 9.5 41.44 11.14 10.13 424.07 9.77% 119.49 34.68% 78.98 52.47% 35.33 117.29% 159.63 25.96% Corucia zebrata ROM R7868 R 374 5.9 46.69 11.1 11.3 573.46 8.14% 184.31 25.33% 92.32 50.57% 35.3 132.27% 210.16 22.22% Heloderma suspectum ROM R269 R 14.8 61.99 14.47 14.16 640.79 9.67% 252.66 24.53% 90.8 68.27% 44.55 139.15% 308.69 20.08% Cyclura cornuta ROM R285 R 6.6 56.25 21.43 16.02 713.29 7.89% 202.04 27.84% 158.55 35.48% 65.49 85.89% 268.04 20.99% Tupinambus teguixin ROM R8380 R 1207 19.3 81.37 17.85 15 715.93 11.37% 203.78 39.93% 163.4 49.80% 57.27 142.08% 284.4 28.61% Simosuchus R 99 44 40 724 13.67% 267 37.08% 234 42.31% 118 83.90% 383 25.85% Dracaena guianensis ROM R377 R 53.1 92.84 17.04 14.58 777.27 11.94% 207.64 44.71% 122.78 75.61% 56.39 164.64% 284.49 32.63% Varanus exanthematicus ROM R7715 R 2460 18.4 74.37 19.63 18.4 820.74 9.06% 257.37 28.90% 123.85 60.05% 56.67 131.23% 368.37 20.19% Varanus salvator ROM R88 R 8.1 77.81 18.11 18.44 1027.05 7.58% 242.24 32.12% 138.01 56.38% 57.14 136.17% 338.24 23.00% Caiman crocodilius ROM R6872 R 22050 550 207 43 37.3 1501.87 13.78% 334.3 61.92% 261.03 79.30% 117.01 176.91% 566.62 36.53% Alligator mississippiensis ROM R690 R 815 301 51 66 1678.43 17.93% 371.28 81.07% 335.27 89.78% 148.25 203.04% 600.66 50.11% Varanus komodoensis ROM R7565 R 45000 141.6 174 58 57 2205.33 7.89% 561.55 30.99% 307.71 56.55% 146.74 118.58% 856.86 20.31% Prestosuchus R 555 195 123 4591 12.09% 1042 53.26% 858 64.69% 420 132.14% 1598 34.73% Phrynosoma platyrhinos ROM R8807 R 16.1 0.4 15.92 124.05 12.83% 50.5 31.52% 41.09 38.74% 17.96 88.64% 60.42 26.35% Basiliscus vittatus ROM R4660 R 112 1.9 35.3 5.82 4.41 446.56 7.90% 76.56 46.11% 95.98 36.78% 40.55 87.05% 103.26 34.19% Chamaeleo calyptratus ROM R7981 R 141 6.3 43.94 9.59 10.16 391.96 11.21% 143.46 30.63% 78.42 56.03% 38.43 114.34% 159.02 27.63% Chlamydosaurus kingi ROM R8521 R 242 2.7 40.95 10.65 9.64 527.83 7.76% 98.14 41.73% 110.97 36.90% 48.25 84.87% 137.58 29.76% Tiliqua scincoides ROM R7535 R 243 4.9 47.87 8.42 6.74 430.9 11.11% 172.71 27.72% 49 97.69% 25.6 186.99% 204.65 23.39% Physignathus lesueurii ROM R8526 R 337 3.9 42.55 483.17 8.81% 100.37 42.39% 116.81 36.43% 48.72 87.34% 135.06 31.50% Varanus salvadorii ROM R7926 R 4839 25.6 111.98 25 23 1745.71 6.41% 353.81 31.65% 178.22 62.83% 81.24 137.84% 464.49 24.11% Peromyscus gossypinus ROM R1947 M 39.5 0.4 26.27 220.78 11.90% 55.32 47.49% 52.83 49.73% 19.25 136.47% 63.68 41.25% Dendrohyrax arboreus 70734 M 86 21 20 479 17.95% 261 32.95% 151 56.95% 68 126.47% 338 25.44% Martes americana ROM R8956 M 829.9 14.2 77.7 13.21 14.4 541.32 14.35% 242.62 32.03% 172.83 44.96% 66.82 116.28% 296.62 26.20% Mustela vison ROM R8876 M 1137 12.8 67.58 15.83 14.77 559.91 12.07% 226.33 29.86% 137.05 49.31% 53.45 126.44% 290.49 23.26% Caluromys lanatus M 5 59.08 11.64 12.5 628.76 9.40% 164.01 36.02% 119.74 49.34% 53.79 109.83% 185.68 31.82%

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Eira barbara 91.2.1.9 M 114 23 24 865 13.18% 322 35.40% 238 47.90% 104 109.62% 416 27.40% Vombatus ursinus 80.11.29.11 M 183 52 62 879 20.82% 465 39.35% 292 62.67% 143 127.97% 536 34.14% Gulo gulo 91.2.1.8 M 144 40 43 910 15.82% 386 37.31% 331 43.50% 144 100.00% 505 28.51% Lontra canadensis ROM R8955 M 46.3 105.06 23.87 26.42 936.19 11.22% 351.13 29.92% 195.08 53.85% 70.72 148.56% 444.13 23.66% Hydrochaeris hydrochaeris ROM 88099 M 645 227 65 53 1117.24 20.32% 614.98 36.91% 464.73 48.85% 211 107.58% 764.98 29.67% Canis lupus ROM R4399 M 19504 420 235 54 53 1427.53 16.46% 581 40.45% 574.66 40.89% 231 101.73% 781.36 30.08% Orycterpous afer 00.11.29.9 M 247 85 58 1536 16.08% 533 46.34% 452 54.65% 197 125.38% 643 38.41% Urus thibetanus ROM R931 M 279 93 99 1610 17.33% 921 30.29% 604 46.19% 319 87.46% 1170 23.85% Tapirus americanus 95.8.13.22 M 355 109 110 1758 20.19% 974 36.45% 687 51.67% 316 112.34% 1200 29.58% Panthera tigris ROM R6804 M 107300 1100 270 90 93 1836.21 14.70% 910.46 29.66% 774.1 34.88% 344 78.49% 1152.01 23.44% Tapirus terrestris ROM 66623 M 2080 380 106 92 1896.14 20.04% 974.16 39.01% 866.01 43.88% 307 123.78% 1225.36 31.01% Hippopotamus amphibius ROM R1171 M 21800 610 193 196 2678 22.78% 1303 46.82% 976.34 62.48% 472 129.24% 1613 37.82% Equus M 502 173 147 3116 16.11% 1384 36.27% 1128 44.50% 464 108.19% 2137 23.49% Camelus dromedarius ROM R3971 M 2370 439 126 162 3174.23 13.83% 1329.17 33.03% 1257 34.92% 463 94.82% 2302.61 19.07% Loxodonta africana ROM R6000 M 6435000 132400 1040 399 416.3 4393.14 23.67% 1796.14 57.90% 2000.47 51.99% 1147.5 90.63% 2240.14 46.43% Ochrotomys nuttalli ROM R6298 M 10 0.4 24.13 143.05 16.87% 39.1 61.71% 40.03 60.28% 14.72 163.93% 44.92 53.72% Glaucomys sabrinus ROM R7051 M 111 1.4 36.85 257.12 14.33% 87.85 41.95% 87.89 41.93% 35.28 104.45% 100.27 36.75% Thomomys talpoides ROM R5570 M 120 2.4 36.21 203.02 17.84% 81.53 44.41% 62.6 57.84% 26.43 137.00% 92.81 39.02% Rattus norvegicus ROM R5644 M 464 4.3 50.9 15.55 12.26 448.56 11.35% 136.63 37.25% 101.77 50.01% 41.34 123.13% 161.53 31.51% Sciurus niger ROM R4091 M 836 9.3 64.51 19.29 16.55 519.24 12.42% 175 36.86% 154.27 41.82% 63.71 101.26% 202.99 31.78% Aplodontia rufa ROM R6571 M 953 23.3 72.95 16 16 297.89 24.49% 163 44.75% 120.92 60.33% 52.75 138.29% 186.94 39.02% Ondatra zibethicus ROM R5612 M 1141 14.9 65.34 17 16 556.1 11.75% 175.9 37.15% 140.96 46.35% 48.44 134.89% 200.35 32.61% Sylvilagus floridanus ROM R3521 M 1324 16.1 74.11 18.51 15.63 448.38 16.53% 237 31.27% 224.9 32.95% 88.7 83.55% 289.27 25.62% Vulpes vulpes ROM R5621 M 3803 56.1 131.39 26 24 933.14 14.08% 317.16 41.43% 333.05 39.45% 129.19 101.70% 436.43 30.11% Procyon lotor ROM R6563 M 4820 65.9 109.76 33.53 28.89 729.8 15.04% 279.73 39.24% 285.38 38.46% 121.28 90.50% 346.83 31.65% Manis pentadactyla ROM R589 M 24.3 86.26 29 36 769.38 11.21% 277.37 31.10% 163.13 52.88% 74.79 115.34% 337.12 25.59% Potos flavus ROM R460 M 35.2 82.58 23 22 733.85 11.25% 226.34 36.48% 204.62 40.36% 88.84 92.95% 272.27 30.33% Dasyprocta fulginosa ROM R453 M 47.5 111.47 34 21 598.47 18.63% 340 32.79% 281.51 39.60% 113.26 98.42% 411 27.12% Ailurus fulgens ROM R663 M 77 104.22 26.21 25.46 911.22 11.44% 327 31.87% 267.35 38.98% 116.77 89.25% 406 25.67% Psittacosaurus meileyingensis ROM 53574 D 150.32 57 47 1069.6 14.05% 333.25 45.11% 381.93 39.36% 142.44 105.53% 485.69 30.95%

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Eoraptor D 104 47 34 1184 8.78% 341 30.50% 379 27.44% 144 72.22% 528 19.70% Buitreraptor D 193 35 30 1340 14.40% 280 68.93% 464 41.59% 146 132.19% 516 37.40% Masiakasaurus D 142 62 26 1850 7.68% 409 34.72% 491 28.92% 197 72.08% 722 19.67% Herrerasaurus D 288 196 48 2489 11.57% 585 49.23% 839 34.33% 352 81.82% 988 29.15% Chasmosaurus D 828 294 5438 15.23% 1825 45.37% 1621 51.08% 920 90.00% 2636 31.41% Majungasaurus D 488 258 113 5577 8.75% 1178 41.43% 1414 34.51% 644 75.78% 2297 21.25% Ouranosaurus D 589 346 173 6854 8.59% 2408 24.46% 1850 31.84% 908 64.87% 3293 17.89% Rapetosaurus D 278 234 205 6983 3.98% 1260 22.06% 1212 22.94% 688 40.41% 4651 5.98% Lambeosaurus D 671 219 7923 8.47% 2318 28.95% 2409 27.85% 1071 62.65% 3550 18.90% Carnotaurus D 485 368 156 7950 6.10% 1865 26.01% 2484 19.52% 1044 46.46% 2993 16.20% Corythosaurus D 687 8042 8.54% 2279 30.14% 2486 27.63% 1061 64.75% 3487 19.70% Malawisaurus D 314 394 224 9524 3.30% 1686 18.62% 2429 12.93% 1067 29.43% 5208 6.03% Amargasaurus D 495 535 358 10009 4.95% 1992 24.85% 1693 29.24% 1032 47.97% 4238 11.68% Suchomimus D 1023 394 224 11236 9.10% 3191 32.06% 2429 42.12% 1067 95.88% 4783 21.39% Stegosaurus stenops USNM 4934 D 414 2986 13.86% 1773 23.35% 1688 24.53% 1045 39.62% 2572 16.10% Parasaurolophus D 3575 2590 1051 1051

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