Comparative Cranial Ecomorphology and Functional Morphology of Semiaquatic

Faunivorous Crurotarsans

A dissertation presented to

the faculty of

the College of Arts and Sciences of Ohio University

In partial fulfillment

of the requirements for the degree

Doctor of Philosophy

Waymon L. Holloway

December 2018

© 2018 Waymon L. Holloway. All Rights Reserved. 2

This dissertation titled

Comparative Cranial Ecomorphology and Functional Morphology of Semiaquatic

Faunivorous Crurotarsans

by

WAYMON L. HOLLOWAY

has been approved for

the Department of Biological Sciences

and the College of Arts and Sciences by

Patrick M. O’Connor

Professor of Biomedical Sciences

Joseph Shields

Interim Dean, College of Arts and Sciences 3

ABSTRACT

HOLLOWAY, WAYMON L., Ph.D., December 2018, Biological Sciences

Comparative Cranial Ecomorphology and Functional Morphology of Semiaquatic

Faunivorous Crurotarsans

Director of Dissertation: Patrick M. O’Connor

Crurotarsi are a clade of archosauromorphs ranging in age from the Middle

Triassic to Recent that includes two semiaquatic, faunivorous subclades: Crocodylia and the predominantly late-Triassic Phytosauria. Phytosaurs and crocodylians exhibit generally similar overall body morphology, and each exhibits a range of narrow to broad rostral cranium morphotypes. These morphological similarities lead to the commonly adopted hypothesis that the two clades exhibited a number of ecological and behavioral similarities. One such hypothesized ecological similarity is that phytosaurs utilized a range of food item types that was the same as that utilized by extant crocodylians. In particular, phytosaurs possessing slender rostra with a high aspect ratio were previously hypothesized to have been strictly or primarily piscivorous, much like extant crocodylians with slender, high aspect ratio rostra that have been described as piscivorous. However, a review of available literature reporting on direct observations and other dietary data in extant crocodylians revealed that no extant crocodylian taxa are either strictly piscivorous or lacking at least one population that consumes teleosts as a primary food source. Instead of being correlated with consumption of a specific food type, then, rostrum morphology in extant crocodylians appears to be correlated with the relative size of food items that can be consumed by a given individual. Cranium shape, 4 jaw musculature, and biomechanical performance were assessed in both phytosaurs and extant crocodylians to test hypotheses of morphological and functional similarities of the cranium between these two clades. Results of these analyses were interpreted in the context of prey:predator size ratios correlating with rostrum morphology in extant crocodylians in order to better constrain inferred diet ranges and variation among phytosaur taxa. In general, phytosaurs were more similar to crocodylians with very high aspect ratio rostra in most facets of cranium shape than crocodylians with lower aspect ratio rostra. This trend supports the interpretation that the diets of phytosaurs were probably most like those of extant crocodylians with high aspect ratio rostra. However, no overlap in any tested aspect of cranium shape was found between phytosaurs and crocodylians, precluding an inference of phytosaur diet as being the same as any sampled crocodylian taxon. The topology, individual origin and insertion area size proportions, and individual muscle force proportions of phytosaur and extant crocodylian jaw musculature all exhibited a great deal of consistency, regardless of variation in rostrum morphology among the sampled taxa. Clear indicators of greater jaw musculature similarity among particular taxa that would support inferences of dietary similarities between those taxa were thus not found. Biomechanical modeling revealed that bite forces produced by phytosaurs generally surpassed those of extant crocodylians, though the crania of most phytosaurs performed worse, from a structural perspective, than most extant crocodylians. These results, though somewhat conflicting, indicate that phytosaurs were typically able to produce higher bite forces than similarly sized extant crocodylians but were less capable of withstanding the resultant force experienced by the cranium 5 during performance of a maximally powerful bite or when biting a hard object. These diverse results, synthesized into a single conclusion, indicate that smaller phytosaurs with relatively narrow, gracile rostra were probably restricted to utilizing food items even smaller, relative to their own size, than do any extant crocodylians. Larger phytosaurs and those with somewhat more robust, if also narrow, rostra were probably capable of utilizing food items of a prey:predator size ratio similar to or exceeding those utilized by extant crocodylians with relatively low rostrum aspect ratios. These new inferences highlight the complexity of interactions between cranium shape and jaw muscle performance that result in differences in trophic niche occupation. Better appreciation for these interactions will allow for a greater understanding of the mechanisms that lead to phenomena such as niche partitioning. Furthermore, more accurately constrained reconstructions of phytosaur ecology will enable further investigations into the complex ecosystem structure and changes during the Late Triassic.

6

DEDICATION

To my Mother, Patricia, who has always supported and encouraged my education, from

its beginning to now; my wife and love, Katharine, for her tireless support, assistance, and motivation throughout this work; Molly, my loving inspiration, that this work may be

a worthy tribute to her memory; and Frankie, for keeping me company as I write this.

7

ACKNOWLEDGMENTS

I would like to acknowledge my advisor, Patrick O’Connor, for the massive amount of guidance and support that he provided throughout my graduate career and committee members John Cotton, Shawn Kuchta, Susan Williams, and Lawrence Witmer for their invaluable input and efforts to improve this work. Discussions and technical assistance from my lab mates, other Ohio University Ecology and Evolutionary Biology program graduate students, and C. Holliday and K. Sellers of the University of Missouri greatly helped me throughout this process. Specimen access and CT scanning was facilitated by C. Pugh and B. Keene of Holzer Clinic; R. Irmis and C. Levitt-Bussian of

UMNH; B. Parker, A. Marsh, and M. Smith of PEFO; J. Payne of Summit Healthcare; M.

Brown and C. Sagebiel of TMM; and Liz Daigle of ARA Wilson Parke. L. Witmer, C.

Brochu, J. Maisano, S. Pierce, and E. Gold provided additional CT scan data. Financial support for this work was provided through an Osteopathic Heritage Foundations

Graduate Research Fellowship, Ohio University Graduate Student Senate Original Work

Grant, and College of Arts and Sciences Graduate Student Research Fund.

8

TABLE OF CONTENTS

Page

Abstract ...... 3 Dedication ...... 6 Acknowledgments ...... 7 List of Tables...... 10 List of Figures ...... 11 Chapter 1: Introduction ...... 13 Phylogenetic Relationships of Phytosauria ...... 13 Occurrence of Phytosauria ...... 15 Hypothesized Ecology of Phytosauria ...... 20 Research Outline...... 31 Chapter 2: Geometric Morphometric Analysis of Cranium Shape Variation in Crurotarsans in an Ecomorphological Context ...... 35 Introduction ...... 35 Rostrum Morphotypes ...... 37 Geometric Morphometric Characterization of Shape ...... 40 Materials and Methods ...... 43 Taxon Sampling ...... 43 Cranial Shape and Landmark Placement ...... 47 Analytical Approaches ...... 49 Results ...... 52 Principal Coordinates Analyses ...... 52 Statistical Analyses ...... 62 Discussion ...... 67 Conclusions ...... 74 Chapter 3: Comparative Cranial Myology of Phytosaurs and Extant Crocodylians ...... 77 Introduction ...... 77 Anatomical Abbreviations ...... 81 Materials and Methods ...... 81 Taxon Sampling ...... 81 Muscle Attachment Site Identification...... 86 9

Three-dimensional Muscle Reconstructions ...... 90 Comparative Analyses ...... 90 Principal Components Analyses ...... 93 Results ...... 94 Muscle Topology ...... 94 Comparative Assessments ...... 114 Principal Components Analyses ...... 121 Discussion ...... 135 Conclusions ...... 147 Chapter 4: Comparative Cranial Biomechanics of Phytosaurs and Extant Crocodylians in the Context of Prey Utilization...... 149 Introduction ...... 149 Materials and Methods ...... 153 Taxon Sampling ...... 153 Specimen Modelling ...... 155 Three-dimensional Lever Mechanics ...... 157 Finite Element Analysis ...... 158 Results ...... 160 Three-dimensional Lever Mechanics ...... 160 Finite Element Analysis ...... 163 Discussion ...... 176 Conclusions ...... 189 Chapter 5: Conclusions ...... 193 New Inferences about Phytosaur Ecology ...... 194 Future Directions ...... 204 References ...... 209 Appendix: Detailed Table of Dietary Data For Extant Crocodylians ...... 256

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LIST OF TABLES

Page

Table 1. Summary of documented feeding of extant crocodylian taxa upon prey taxa. ... 30 Table 2. Taxa sampled for geometric morphometric analyses...... 44 Table 3. Summary of hypotheses tested in this study, part 1...... 73 Table 4. Specimens included in muscle reconstruction analyses...... 84 Table 5. Overview of reconstructed jaw muscle attachment locations...... 97 Table 6. Individual jaw muscle metrics...... 117 Table 7. Summary of hypotheses tested in this study, part 2...... 145 Table 8. Specifications of specimen models used for biomechanical analyses...... 155 Table 9. Results of biomechanical analyses...... 160 Table 10. Axial components of calculated bite forces...... 162 Table 11. Summary of hypotheses tested in this study, part 3...... 187

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LIST OF FIGURES

Page

Figure 1. Previously proposed cladistic hypotheses of Archosauromorpha...... 14 Figure 2. Supertree comprising recent cladistic hypotheses of Phytosauria...... 16 Figure 3. Global distribution of unambiguous phytosaur specimens...... 17 Figure 4. Examples of rostrum morphotypes in Crocodylia and Phytosauria...... 38 Figure 5. Illustration of geometric morphometric landmark placement...... 49 Figure 6. PCA results of the full cranium landmark dataset...... 53 Figure 7. PCA results of the rostrum landmark dataset...... 56 Figure 8. PCA results of the post-orbital cranium landmark dataset...... 60 Figure 9. Results of Procrustes ANOVA for covariation of shape and specimen group. . 63 Figure 10. Results of Procrustes MANOVA for homogeneity of allometric slopes...... 66 Figure 11. Specimen models used for cranial myological reconstructions...... 82 Figure 12. Examples of identified jaw muscle attachment sites...... 87 Figure 13. Origin of mAMES in phytosaurs...... 98 Figure 14. Insertions of mAMES, mAMEM, mAMEP, and mAMP in phytosaurs...... 100 Figure 15. Origin of mAMEM in phytosaurs...... 101 Figure 16. Origin of mAMEP in phytosaurs...... 103 Figure 17. Origin of mAMP in phytosaurs...... 104 Figure 18. Origin of mPSTs in phytosaurs...... 105 Figure 19. Insertions of mPSTs, mPSTp, mPTd, and mPTv in phytosaurs...... 107 Figure 20. Origin of mPSTp in phytosaurs...... 108 Figure 21. Origin of mPTd in phytosaurs...... 110 Figure 22. Origin of mPTv in phytosaurs...... 111 Figure 23. Origin of mDMs in phytosaurs...... 113 Figure 24. Origin of mDMp in phytosaurs...... 115 Figure 25. Insertions of mDMs and mDMp in phytosaurs...... 116 Figure 26. Muscle origin surface area proportions...... 119 Figure 27. Muscle insertion surface area proportions...... 119 Figure 28. Maximum muscle force proportions...... 121 Figure 29. PCA and PPCA results of full muscle origin surface area dataset...... 122 Figure 30. PCA and PPCA results of origin area dataset without mDM...... 124 12

Figure 31. PCA and PPCA results of origin area dataset without mPSTp or mDM...... 126 Figure 32. PCA and PPCA results of full muscle insertion surface area dataset...... 127 Figure 33. PCA and PPCA results of insertion area dataset without mDM...... 129 Figure 34. PCA and PPCA results of insertion area dataset without mPSTp or mDM. . 130 Figure 35. PCA and PPCA results of full maximum muscle force dataset...... 132 Figure 36. PCA and PPCA results of muscle force dataset without mDM...... 133 Figure 37. PCA and PPCA results of muscle force dataset without mPSTp or mDM. ... 135 Figure 38. FEA results for Alligator mississippiensis...... 164 Figure 39. FEA results for Tomistoma schlegelii...... 165 Figure 40. FEA results for Gavialis gangeticus...... 166 Figure 41. FEA results for Parasuchus angustifrons...... 168 Figure 42. FEA results for Ebrachosuchus neukami...... 169 Figure 43. FEA results for Pravusuchus hortus...... 171 Figure 44. FEA results for Machaeroprosopus pristinus...... 172

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CHAPTER 1: INTRODUCTION

Phytosauria are a clade of reptiles that included the largest, most common non- marine faunivores during the Late Triassic, until their end-Triassic extinction (e.g., Hunt,

1989; Hurlburt et al., 2003). However, nearly all inferences of phytosaurian ecology stem from hypotheses based on purely qualitative observations of specimen morphology and superficial comparisons of phytosaurs to extant taxa (e.g., Hunt, 1989). Quantitative and large-scale comparative studies of phytosaurs have, thus far, been lacking, leaving those hypotheses of phytosaur ecology largely untested. Because of their phylogenetic relationships with clades such as Dinosauria and Crocodylomorpha, phytosaurs promise to provide important data on the origins and ancestral states of those more commonly studied taxa. Additionally, as a major component of much of the global terrestrial ecosystem during the Late Triassic, phytosaurs likely played an important role in the biosphere during periods of recovery following the end-Permian mass extinction and leading into the Late-Triassic mass extinction. Better constrained reconstructions of phytosaur ecology will allow for a better understanding of ecosystem structure and changes during a time of relatively high faunal community instability.

Phylogenetic Relationships of Phytosauria

Phytosauria are an extinct, monophyletic, and stem-based subclade of Crurotarsi, a node-based clade including Phytosauria, Ornithosuchidae, Prestosuchus, Suchia, and all descendants of their common ancestor, and Phytosauria is the outgroup to all other crurotarsans (Fig. 1; Sereno & Arcucci, 1990). Historically, Phytosauria was also considered a subclade of the stem-based, archosaurian clade Pseudosuchia, defined as all 14

Figure 1. Previously proposed cladistic hypotheses of Archosauromorpha. (A) Brusatte et al. (2010); (B) Nesbitt (2011); (C) Ezcurra (2016). Hypothesized relationships between Phytosauria (bold) and Archosauria emphasized. Named nodes indicated with black circles, and named stems indicated with black crescents.

archosaurs more closely related to crocodiles than to birds, and were considered the outgroup to all other pseudosuchians (Gauthier & Padian, 1985). The taxa comprising these two clades were historically the same. However, because Crurotarsi is node-based and Pseudosuchia is stem-based, the two were redundant but not synonymous (Brochu,

1997; Senter, 2005). Thus, both clades were valid and appeared interchangeably in the literature (e.g., Kubo & Benton, 2007; Irmis, 2007; Parker, 2007; Brusatte et al., 2008;

Desojo & Arcucci, 2009; Stocker, 2010a). A phylogenetic analysis and reassessment of early archosaurs by Nesbitt (2011) found Phytosauria to be the outgroup to Archosauria, excluding phytosaurs from the definition of Pseudosuchia and expanding the composition of Crurotarsi to include phytosaurs and all archosaurs. A more recent analysis by Ezcurra

(2016) recovered Phytosauria in its historical phylogenetic relationship within

Archosauria, as a subclade of Pseudosuchia and the outgroup to all other pseudosuchians. 15

Phytosauria includes the genus Diadongosuchus, the outgroup to all other phytosaurs (Stocker et al., 2017), and the subclade Parasuchidae (Fig. 2; Stocker, 2010a;

Stocker, 2012; Stocker & Butler, 2013; Butler et al., 2014; Kammerer et al., 2015).

Parasuchidae is a node-based clade comprising the subclade Mystriosuchinae and the

‘Paleorhinus-grade’ genera Wannia, Ebrachosuchus, and the speciose Parasuchus

(Kammerer et al., 2015). Mystriosuchinae is a node-based clade that consists of the subclade Leptosuchomorpha and at least four non-leptosuchomorph genera, including

Brachysuchus, Angistorhinus, Rutiodon, and Protome (Stocker, 2010a; Stocker, 2012;

Stocker & Butler, 2013; Kammerer et al., 2015). Leptosuchomorpha is a node-based clade comprising the subclade Mystriosuchini (Kammerer et al., 2015; Stocker et al.,

2017) and at least three non-mystriosuchinine genera, including Leptosuchus,

Smilosuchus, and Pravusuchus (Stocker, 2010a; Stocker, 2012; Stocker & Butler, 2013).

Mystriosuchini includes the genera Nicrosaurus, Mystriosuchus, Redondasaurus, and the speciose genus Machaeroprosopus (Stocker, 2010a; Stocker, 2012; Stocker & Butler,

2013; Kammerer et al., 2015).

Occurrence of Phytosauria

Phytosaurs are known unambiguously from Late Triassic deposits (Fig. 3) including: the Dockum Group of eastern New Mexico (Hunt & Lucas, 1993; Hunt, 2001) and Texas (Case, 1920, 1922, 1929; Case & White, 1934; Stovall & Wharton, 1936;

Langston, 1949; Stocker, 2009); Popo Agie Formation of Wyoming (Williston, 1904;

Lees, 1907; Mehl, 1913, 1915, 1928b); Chinle Formation of Arizona (Mehl, 1916, 1922,

1928a; Camp, 1930; Long & Murry, 1995; Parker & Irmis, 2006; Stocker, 2010a, 2012), 16

Figure 2. Supertree comprising recent cladistic hypotheses of Phytosauria. Based on: Diadongosuchus–Wannia, Stocker et al. (2017); Wannia–Pravusuchus, Kammerer et al. (2015); Nicrosaurus kapffi–Machaeroprosopus, Hungerbühler (2002); Machaeroprosopus mccauleyi–Mystriosuchus, Kammerer et al. (2015); Mystriosuchus planirostris–M. westphali, Hungerbühler (2002). Named nodes indicated with black circles, and named stems indicated with black crescents.

Utah (Lucas, 1898; Morales & Ash, 1993; R. Irmis pers. comm; A. Milner, pers. comm.), and northern New Mexico (Hunt, 1993; Ziegler et al., 2003a, b; Irmis et al., 2007; Nesbitt

& Stocker, 2008); Blomidon Formation of Nova Scotia (Olsen et al., 1989); Lockatong,

Stockton, and Passaic formations of New Jersey (Huene, 1913; Colbert, 1965; Baird,

1986); New Oxford and Passaic formations of Pennsylvania (Hunt & Lucas, 1989; Doyle 17

Figure 3. Global distribution of unambiguous phytosaur specimens. Paleomap of the Late Triassic (222.6 Ma) continental arrangement modified from Scotese (2013). Localities from which unambiguous phytosaur specimens were collected (stars) based on Stocker & Butler (2013) and Stocker et al. (2017).

& Sues, 1995); Vinita, Bull Run, and Falling Creek formations of Virginia (Weems,

1979, 1980; Sues et al., 1994); Pekin and Cummock formations of North Carolina (Hunt

& Lucas, 1989; Olsen & Huber, 1998); Blasensandstein (Kuhn, 1933, 1936, 1938),

Stubensandstein (Jaeger, 1828; Meyer, 1861, 1863; Huene, 1911, 1923; Westphal, 1963;

Hungerbühler & Hunt, 2000; Hungerbühler, 2002), and Arnstadt (Huene, 1923) formations of Germany; Dachsteinkalk Formation of Austria (Buffetaut, 1993); Calcare di Zorzino and Argilliti di Riva di Solto formations of northern Italy (Renesto &

Paganoni, 1998; Gozzi & Renesto, 2003; Renesto, 2008); Grés de Silves Formation of

Portugal (Mateus et al., 2014); Morocco (Dutuit, 1977a, b; Fara & Hungerbühler, 2000); the United Kingdom (Huene, 1908; Galton, 2007; Maisch & Kapitzke, 2010); France

(Godefroit & Cuny, 1997); Luxembourg (Godefroit et al., 1998); Switzerland (Huene,

1911); Poland (Dzik, 2001); Lithuania (Brusatte et al., 2012); Turkey (Buffetaut et al., 18

1988); the Falang Formation of China (Stocker et al., 2017); Hin Lat Formation of

Thailand (Buffetaut & Ingavat, 1982); lower (Chatterjee, 1978) and upper (Hungerbühler et al., 2002) Maleri Formation of India; Tashinga Formation of Zimbabwe (Barret et al.,

2017); Isalo II or Makay Formation of Madagascar (Dutuit, 1978); and Caturrita

Formation of southern Brazil (Kischlat & Lucas, 2003). Highly fragmentary material that is potentially phytosaurian has also been reported from the Østed Dal Member of the

Fleming Fjord Formation of Greenland (Jenkins et al., 1994) and the upper Lunz

Formation of Austria (Butler, 2013). Phytosaurs have not been reported from the similar- aged Santa Maria, Ischigualasto, or Los Colorados formations of Argentina and Brazil or the Elliot Formation of southern Africa, despite those deposits being well-sampled

(Stocker & Butler, 2013). The lack of reported phytosaur material from regions including

Russia, Australia, and Antarctica may be a result of the scarcity of Late Triassic terrestrial deposits in those regions, rather than the genuine absence of phytosaurs in those areas (Brusatte et al., 2012).

The earliest known phytosaur material is a well-preserved, nearly complete specimen from the middle Ladinian of China (Stocker et al., 2017). Other putative Early–

Middle Triassic phytosaur specimens are either not diagnostic or were destroyed during

World War II (e.g. Jaekal, 1910; Hunt & Lucas, 1991a; Buffetaut, 1993). Potentially phytosaurian mandibular material reported from the earliest Jurassic of the United

Kingdom (Maisch & Kapitzke, 2010) requires confirmation of both identification and stratigraphic position (Stocker & Butler, 2013), and isolated teeth from the earliest

Jurassic of France (Huene & Mauberge, 1954) cannot be confidently identified as 19 phytosaurian because of the lack of dental synapomorphies of Phytosauria and their similarity to dentition of some Jurassic marine crocodyliforms (Barrett & Xu, 2012).

Specimens of the phytosaur genus Redondasaurus are known from the lowermost portion of the Wingate Sandstone in the United States (Morales & Ash, 1993; Lucas et al., 1997;

Lucas & Tanner, 2007b), the best known of which—the so-called “last phytosaur”— is preserved in the underside of an overhang of Wingate Sandstone in Utah as a natural mold of the dorsal surface of the skull (Morales & Ash, 1993). The Wingate Sandstone is currently considered to be latest Rhaetian in age (Lucas & Tanner, 2007a, 2007b; Lucas et al., 2011), extending the confirmed fossil record of phytosaurs into the terminal

Triassic and giving the clade a temporal range of middle Ladinian–latest Rhaetian (c.

240–201.5 Ma).

Because of their nearly global distribution (Fig. 3), relatively narrow temporal range, and relatively high diversity, phytosaurs have been used as biostratigraphic and biochronological index taxa for much of the time since their discovery. The most commonly used scheme in recent years utilizes land-vertebrate faunachrons (LVFs;

Lucas & Hunt, 1993; Lucas, 1998, 2010) that emphasize a stratigraphic sequence of taxa from Paleorhinus and Angistorhinus to Redondasaurus to correlate and relatively date stratigraphic units. Many of the taxa that are key components of those faunachrons are currently considered paraphyletic or polyphyletic as they were conceived when the faunachron scheme was devised, and the biostratigraphic and biochronological utility of taxa that are not monophyletic is unclear (Stocker & Butler, 2013). Additionally, attempts to correlate stratigraphic units over large geographic distances or correlate marine units 20 with terrestrial ones can yield unclear or misleading results (Irmis et al., 2010). Because of the paucity of other data for the Late Triassic that would typically be used to date stratigraphic units (Mundil et al., 2010), accurate biostratigraphic correlations are important (Stocker & Butler, 2013). Better characterization of the morphological changes throughout Phytosauria and paleoecological data on phytosaurs are needed to increase the utility of phytosaurs as index taxa. Such paleobiological data can also be used to better clarify and contextualize depositional, fossil, and other environmental data of the strata from which phytosaurs are known.

Hypothesized Ecology of Phytosauria

Nearly all deposits from which phytosaur specimens are known represent fluvial or floodplain depositional settings (e.g. Sues & Fraser, 2010). However, some specimens of the European genus Mystriosuchus and potential phytosaurian material from Austria are known from near-shore marine deposits (Buffetaut, 1993; Renesto & Paganoni, 1998;

Gozzi & Renesto, 2003; Renesto, 2008). Phytosaurs have a near-global distribution through at least 45º of latitude in the northern hemisphere of Late Triassic Pangaea (Fig.

3; Brusatte et al., 2012; Stocker & Butler, 2013). Most phytosaur specimens from the southern hemisphere of Late Triassic Pangaea are from the eastern coastal margins of the supercontinent. Only a single phytosaur specimen, from modern South America, is known from southwestern Pangaea (Kischlat & Lucas, 2003). Climatic modelling reconstructed most of the areas of phytosaur distribution in the northern hemisphere and southeastern Pangaea, along the margins of the Tethys Ocean, as the “summerwet” biome 21

(i.e. annual monsoonal) and southwestern Pangaea, where phytosaurs are almost entirely absent, as arid (i.e. dry year-round) (Sellwood & Valdes, 2006).

Phytosaurs were large, quadrupedal sauropsids with an overall morphology often described as crocodylian-like (e.g. Hunt, 1989; Stocker & Butler, 2013). Because of this overall, superficial similarity in morphology (e.g., Hunt, 1989; Hungerbühler, 2002) and the similarity in depositional environment (e.g., Kuhn, 1938; Buffetaut, 1993) between phytosaurs and extant crocodylians, the ecology of phytosaurs has long been hypothesized to be similar to that of extant crocodylians. However, such inferences largely ignore the morphological diversity within and between Phytosauria and

Crocodylia that is readily apparent at scales below the overall, whole body level that may reflect functional differences in aspects of anatomy related to ecology. The dorsal aspects of phytosaur torsos were covered with diamond-shaped or triangular osteoderms, arranged in two paramedian rows, and more osteoderms loosely covered their limbs

(Stocker & Butler, 2013). Unlike crocodylians or any other archosauriforms, phytosaurs exhibit a “gular shield” comprising multiple overlapping and interlocking osteoderms on the ventral aspect of the neck (Long & Murry, 1995; Stocker & Butler, 2013). Like many extant crocodylians, phytosaurs, with the exception of the Middle Triassic species

Diadongosuchus fuyuanensis (Stocker et al., 2017), possess longirostrine skulls, but the rostrocaudal length of the phytosaur facial skeleton is primarily composed of a premaxilla that is much longer than the maxilla. This morphology is unlike the condition in crocodylians and the plesiomorphic archosauriform condition of a maxilla that is rostrocaudally longer than the premaxilla (Nesbitt, 2011). Also unlike crocodylians and 22 the plesiomorphic archosauriform condition, the position of the external nares along the rostrum in phytosaurs is non-terminal (Nesbitt, 2011). Extant crocodylians possess a very caudally elongate retroarticular process, whereas the retroarticular process of phytosaurs is smaller and more similar to those of other archosauriforms (e.g., Gozzi & Renesto,

2003; Stocker et al., 2017). Phytosaurs possess antorbital fenestrae, which are evolutionarily lost in crocodylians, presumably for mechanical reasons related to feeding behavior and trophic ecology (Rayfield et al., 2007). The bony palate of extant crocodylians also likely provides mechanical benefits related to feeding behavior and trophic ecology (Rayfield et al., 2007). Phytosaurs do not possess a bony secondary palate of the same morphology as those of extant crocodylians. Instead, the choanae are approximately directly ventral to the nares and are surrounded by the maxilla, vomer, and palatine, the last of which fuse with the midline vomer and pterygoid structures. The bony plate comprised by the phytosaur palatine is quite thin, potentially reducing its mechanical benefit to the cranium, compared to that of the crocodylian bony palate.

Phytosaurs possess faunivorous dentition comprising teeth that are conical, D-shaped in cross-section, or mediolaterally compressed, and several phytosaur taxa exhibit heterodonty with more than one of those dental morphologies in a bi- or tri-partite dentition along the tooth row (Hungerbühler, 2000), unlike the relatively homodont dentition possessed by extant crocodylian taxa,.

Life history and paleoecological data on phytosaurs is very limited. Some partial cranial specimens have been proposed to represent juvenile material (Camp, 1930;

Langston, 1949; Fara & Hungerbühler, 2000; Stocker & Butler, 2013), but the only study 23 to investigate phytosaur ontogeny focused on vertebral neurocentral fusion patterns

(Irmis, 2007). Histological studies involving phytosaurs have been few, primarily occurring within larger-scale archosauriform histological studies (e.g., de Ricqlès et al.,

2003; Werning et al., 2011). Femoral histology (de Ricqlès et al., 2003; Bronowicz,

2009) indicates somewhat slow growth rates (Houssaye, 2012), and osteoderm histology indicates a maximum lifespan of at least two decades for phytosaurs (Scheyer et al.,

2014). Body mass and total length estimates for phytosaurs have been based on measurement data on Alligator specimens (Hurlburt et al., 2003), but potential metric differences between the two clades, such as average tail length being longer in phytosaurs

(Renesto & Lombardo, 1999), call into question the accuracy of such estimates. Although parental care is common in extant archosaurs (Hopson, 1977) and appears to have been practiced by at least some extinct archosaurs (Norell et al., 1995; Tanaka et al., 2015), no evidence of nest-building behavior or parental care is known for phytosaurs (Lucas &

Hunt, 2006). Morphological variation, particularly related to the presence or absence of a rostral crest, between phytosaur taxa has been suggested as evidence of sexual dimorphism (Zeigler et al., 2003a, b; Hunt et al., 2006). However, many of the proposed sexual dimorphs were not recovered as sister taxa in more recent phylogenetic analyses

(Stocker, 2010a; Butler et al., 2012). Many other taxa proposed to represent coexisting morphs (Abel, 1922; Hungerbühler, 2002; Kimmig & Spielmann, 2011) were either not recovered as sister taxa in recent phylogenetic analyses (Stocker, 2010a; Butler et al.,

2012), do not appear to co-occur stratigraphically (Stocker & Butler, 2013), or both.

Although some proposed coexisting morphs within Mystriosuchini are supported as sister 24 taxa (Hungerbühler, 2002; Parker & Irmis, 2006) and occur within a single assemblage

(Zeigler et al., 2003a, b), evidence for sexual dimorphism is lacking. It seems unlikely that morphological variations that are not supported to represent sexual dimorphism in non-mystriosuchinine phytosaurs would represent such dimorphism in Mystriosuchini.

A small number of studies have focused on the sensory systems of phytosaurs.

The presence of a vomeronasal or Jacobson’s organ in phytosaurs has been variably proposed (Camp, 1930) and rejected (Senter, 2002). The presence of a pineal foramen has been proposed for several phytosaur specimens (Jaekel, 1910; Camp, 1930; Langston,

1949), though nearly all cranial specimens clearly lack this feature. A large excavation of the internal dorsal surface of the braincase was reported for Wannia (Lessner & Stocker,

2017), Parasuchus hislopi (Chatterjee, 1978), Smilosuchus (Camp, 1930), and

Machaeroprosopus (Cope, 1888; Mehl, 1928; Holloway et al., 2013) but not for

Parasuchus angustifrons or Ebrachosuchus (Lautenschlager & Butler, 2016). This excavation has been variably described as having housed a cartilaginous portion of the supraoccipital (Hopson, 1979), portions of the dural venous sinus or paratympanic sinus

(Lautenschlager & Butler, 2016), and a large pineal organ (Jaekel, 1910; Langston, 1949;

Holloway et al., 2013; Lessner & Stocker, 2017), and it is likely that some combination of these structure would have filled such a space. Phytosaur endocranial morphology is largely similar to that of extant crocodylians and has been interpreted as the result of sensory system convergence related to ecological convergence between the two groups

(Lautenschlager & Butler, 2016; Lessner & Stocker, 2017). However, several non- crocodyliform pseudosuchians that clearly had a non-semi-aquatic faunivore ecology 25

(Lehane, 2005; Kley et al., 2010) also exhibit overall endocranial morphology similar to phytosaurs and extant crocodylians (Holloway et al., 2013). This trend indicates that pseudosuchian endocranial morphology is not clearly correlated with ecology and endocranial morphological similarity likely represents symplesiomorphy, rather than convergence (Holloway et al., 2013). The dorsal position of the orbits and nares has been used to infer that phytosaurs used the defensive or ambush predatory behavior of staying nearly submerged in water for extended periods of time, similar to such behavior of extant crocodylians (Chatterjee, 1978). The alert, resting head posture for

Machaeroprosopus mccauleyi would place the eyes and nares on similar horizontal planes and allow for seeing above the water surface and breathing with much of the rest of the head submerged below water (Holloway et al., 2013). Extensive facial innervation by the trigeminal nerve and the presence of sensory pits along the rostrum were interpreted as evidence of rostral mechanoreceptive sensitivity in phytosaurs, similar to that of Alligator (Lessner & Stocker, 2017). The only myological reconstruction of phytosaurs examined a single taxon and hypothesized adaptations for supporting large skulls, powerful jaw abduction, rapid jaw adduction, limited lateral head movements, and overall feeding mechanisms similar to extant crocodylians (Anderson, 1936). Swimming

(Stocker & Butler, 2013) and terrestrial footprint (Parrish, 1986; Olsen & Huber, 1998;

Padian et al., 2010) ichnofossils have been used as evidence of phytosaur locomotor capabilities, but interpretations of these fossils are often controversial (e.g., Parrish, 1986;

Olsen & Huber, 1998; Padian et al., 2010; Stocker & Butler, 2013). 26

The previously inferred link between rostrum morphology and divisions in trophic ecology in extant crocodylians was extrapolated as the rationale for hypotheses of piscivorous, generalist, and tetrapod predatory trophic roles for various phytosaur taxa, based on rostrum morphological variation within Phytosauria (Hunt, 1989). However, many of the proposed ecological divisions among extant crocodylians fail to account for the biogeography, evolutionary history, and extinct members of that group. Among the many problems with inferring phytosaur diet variation on the basis of comparisons to diet variation in extant crocodylians is that the latter is often oversimplified during such comparisons. All extant species of Crocodylia are opportunistic feeders in the first months after hatching, primarily utilizing insects, crustaceans, bivalves, small teleosts, and frogs as food items (Grenard, 1991; Grigg & Kirshner, 2015). Juveniles first begin to utilize additional food item types, such as larger crustaceans, actinoptergyian fishes, and amphibians, as well as small sauropsids like lizards, during their first year of life

(Grenard, 1991). Through ontogeny, most species begin to additionally utilize increasingly large, robust, and durable food item types, including large tetrapods such as turtles, birds, and small- to large-sized mammals (Grigg & Krishner, 2015). Increasing utilization of larger and more durable food item types throughout the life cycle of extant crocodylians is often stated to be correlated to both ontogenetic changes in the morphology and function of the skull and teeth (Gignac & Erickson, 2015; Gignac &

Erickson, 2016) and continually increasing overall body size (Dodson, 1975; Grenard,

1991; Abercrombie et al., 2001; Gignac & O’Brien, 2016). However, functional aspects of skull ontogeny, such as bite force, have not been shown to vary in association with 27 major shifts in food item type utilization (Erickson et al., 2003; Erickson et al., 2012).

Additionally, ontogenetic dietary shifts have been observed to vary between populations of crocodylian species, with individuals in some localities not fitting the trends typical of crocodylians in general. In at least some populations of some taxa, the proportion of prey types like tetrapods decreases, crustaceans and actinopterygian fish increases, and insects and gastropods remains consistent in stomach contents through juvenile stages of ontogeny (e.g., Platt et al., 1990). Reliance of crocodylian taxa on particular prey species has also been shown to either remain consistent (Villegas & Schmitter-Soto, 2008) or vary on temporal scales ranging from seasons (e.g., Schaller & Crawshaw, 1982;

Whitaker & Whitaker, 1984; Magnusson et al., 1987; Luiselli et al., 1999; Laverty &

Dobson, 2013; Shirley et al., 2017) to decades (Giles & Childs, 1949; Valentine et al.,

1972), depending on the species and location. Even at larger body sizes, when many crocodylian taxa utilize relatively large and durable food types, smaller items like insects and gastropods are present in the stomach contents of nearly all crocodylians, with the presence of at least some insects resulting from primary ingestion (e.g., Jackson et al.,

1974).

Other functional aspects of adult crocodylian skull morphology have been investigated in the context of behavior performance assumed to be important for food item acquisition. In particular, the length:width aspect ratio of the rostrum has been shown to correlate with underwater drag, such that long, slender rostra produce less drag than others (Thorbjarnarson, 1990; Thorbjarnarson, 1993), and mechanical resistance to bending and torsion correlates with shorter, broader rostra more resistant to those forces 28

(McHenry et al., 2006; Pierce et al., 2009). These trends have been interpreted to support generalizations that crocodylian taxa with shorter, broader rostra, including Caiman and

Alligator, rely less on fast-moving aquatic food item types, such as actinopterygian fish, than do taxa with longer, narrower rostra, including Gavialis and Tomistoma. However, at least some populations of taxa with short, broad rostra have subsurface foraging success rates significantly greater than their success rate at or above the water surface

(e.g., Nifong et al., 2014). Many taxa that possess a wide range of rostrum aspect ratios capture fish using rapid, lateral head movements similar to those utilized by taxa with long, slender rostra (e.g., Graham, 1968; Medem, 1981; Thorbjarnarson, 1989) or employ herding-type fishing behaviors that make capturing fish easier (e.g., Messel et al., 1981;

Schaller & Crawshaw, 1982; Whitaker & Whitaker, 1984). Additionally, regional variation in the diet of some extant crocodylians species has been observed (e.g.,

McNease & Joanen, 1977; Delaney & Abercrombie, 1986; Barr, 1997), including a nearly complete reliance on fish as the sole food type in a population of Crocodylus niloticus, a taxon with an intermediate rostrum aspect ratio, in an area largely devoid of other prey types (Graham, 1968). Conversely, some noted prey items of Tomistoma schlegelii, a taxon with a high aspect ratio, include the long-tailed macaque Macaca fascicularis (e.g., Bezuijen et al., 2001). Within the range of T. schlegelii, these macaques occur in higher densities in peat swamp forests than in other lowland forests along rivers

(MacKinnon et al., 1996). Faunal assemblages of those peat swamp forests are impoverished, compared to nearby freshwater swamp forests, particularly in terms of fish diversity and abundance (MacKinnon et al., 1996), and although both forest types are 29 present within much of the range of T. schlegelii, peat swamp forests are the primary habitat of that species (e.g., Bezuijen et al., 2001; Stuebing et al., 2006). The ecology of these T. schlegelii populations indicates that food availability is not likely a primary factor linking at least some populations of some species to their habitat but that availability of specific prey items, in this example, one outside the range of prey types predicted to be utilized by a taxon based on rostrum morphology, might be. Such an apparent preference for a specific prey item is almost certainly not the case for all populations of all crocodylian taxa, however, as regional variations in the diet of other taxa typically reflect differences in faunal composition between localities (Gorzula &

Seijas, 1989).

Reviewing 207 references to direct observations of food consumption in extant crocodylian taxa, in the form of either records of successful prey capture attempts, stomach content analyses, or fecal content analyses, revealed that no extant crocodylian species is strictly piscivorous, and similiarly, no extant crocodylian species excludes fish from their diet, even as large-bodied adults (Table 1). Rather than extant crocodylian diet variation resulting from a correlation between rostral morphology and the taxonomic identification of prey items, such diet variation appears to result from a limit on the maximum size of prey items, relative to the size of the crocodylian individual, that correlates to rostral morphology. Extant crocodylian taxa possessing rostra with high aspect ratios, such as Gavialis gangeticus and Tomistoma schlegelii, are generally limited to prey that are small relative to themselves, including invertebrates, fish, and small mammals, whereas taxa possessing rostra with lower aspect ratios, such as Alligator 30 mississippiensis and Melanosuchus niger, can utilize those same relatively small prey types and include relatively larger prey types like large mammals. Although absolute limits to the maximum prey size that can be taken by a crocodylian of a given size and rostrum morphology almost certainly depends on several additional extrinsic factors, as indicated by the observation of a ~3.5 m T. schlegelii taking a ~20 kg adult male proboscis monkey (Nasalis larvatus) (Galdikas & Yeager (1984), the typical maximum of such prey size does seem to fall within a fairly narrow range. These findings are generally in line with the interpretation of crocodylian rostral ecomorphology by

Table 1. Summary of documented feeding of extant crocodylian taxa upon prey taxa.

31

McHenry et al. (2006) based on functional inferences.

Data on trophic ecology and prey type utilization in phytosaurs is limited, but the relationship between rostrum morphology and diet variation appears to be similarly complex to that exhibited by extant crocodylians. The only gut contents known for phytosaurs include fish in the gut of Diadongosuchus, the only short-snouted phytosaur

(Stocker et al., 2017), and partial remains of two types of medium-sized archosauromorphs in the gut of Parasuchus hislopi (Chatterjee, 1978), a taxon previously interpreted as strictly piscivorous based on rostral morphology (Hunt, 1989). Fossils of two large paracrocodylomorphs preserve evidence of phytosaur bites (Drumheller et al.,

2014), although it is unclear whether those bites were the result of predatory, scavenging, or defensive behavior on the parts of the phytosaurs. These data indicate that any similarity in diet variation that can be inferred between phytosaurs and extant crocodylians is less likely to be based on the taxonomic identity of prey items, such as categories including “piscivorous,” than the relative sizes of predator and prey.

Research Outline

The potential utility of phytosaurs for providing information about the evolution and paleobiology of Archosauromorpha, evolution of the early Mesozoic terrestrial ecosystem, and trophic system structure in the period of biotic recovery following the end-Permian mass extinction and prior to the end-Triassic mass extinction is substantial.

A better understanding of the functional aspects of phytosaur morphological variation will allow for a more complete picture of phytosaur evolution and appreciation for phytosaurs as key components of their ecosystems. This dissertation is the first broad 32 study of phytosaur functional anatomy and will characterize morphological variation in phytosaur crania in a comparative, ecomorphological context.

Functional morphology is often correlated with ecology in extant organisms because it is a key factor in the effectiveness of an organism to perform given behaviors, which influences the ecological niche that organism can effectively exploit (Reilly &

Wainwright, 1994). Cranial morphology often reflects many aspects of ecology in tetrapods, including diet, feeding behaviors, locomotion, and other habitat use, because of complex relationships between morphological, phylogenetic, and ecological dimensions of evolution and diversification (e.g., Barlow et al., 1997; Haas & Richards, 1998;

Sztencel-Jabłonka et al., 2009; Álvarez et al., 2013; Kraatz et al., 2015). Chapter 2 of this volume describes the quantification of shape and shape variation of the crania of phytosaurs and a range of non-avemetatarsalian archosauromorphs, including crocodylians, to rigorously test hypotheses of morphological convergence between

Phytosauria and Crocodylia. Quantifying the nature and magnitude of cranial morphological variation within and between phytosaurs and extant crocodylians enables more accurate comparisons of morphology between the two, resulting in better constrained inferences of phytosaur trophic ecology.

Osteological morphology is intimately linked with the morphology and function of associated soft tissues, such as muscles (Witmer, 1995). Using osteological correlates to reconstruct myology allows the function of structures such as limbs (e.g., Burch, 2014) and jaws (e.g., Sharp, 2014; Button et al., 2016; Taylor et al., 2017) to be studied in extinct taxa. The morphology and arrangement of cranial musculature, particularly jaw 33 adductor muscles, greatly affect feeding processes and, thus, have important dietary and ecological effects (Lautenschlager, 2013). Chapter 3 of this volume describes reconstructed jaw musculature of phytosaurs and compares these reconstructed muscles with those of extant crocodylians in a topological framework and through statistical analyses. This modeling and analysis of jaw musculature in phytosaurs and extant crocodylians enables further comparisons of bite force, jaw closure rate, gape, and other physical influences on feeding processes and provides quantitative data to support more accurate reconstructions of phytosaur feeding behavior and diet.

The potential range of food types that can be utilized by an animal is limited by the food item mechanical properties that can be overcome by the bite force produced by the jaw muscles and the ability of the cranium to withstand the resultant forces from applying that bite force to the food item (e.g., Bright, 2014; Button et al., 2014; Button, et al., 2016; Nabavizadeh, 2016). Chapter 4 describes the use of data on the cranial skeletal architecture and jaw musculature of phytosaurs and extant crocodylians to estimate bite force and model the mechanical response of the cranium to loading during a simulated bite in specimens of each clade. This analysis focuses on a wide phylogenetic and morphological range of phytosaur and extant crocodylian taxa. The results of this analysis provide quantitative data that allow for accurate constraint of the maximum mechanical properties of food types that phytosaurs can be inferred to have utilized. The goal of this dissertation is to establish the study of phytosaur morphology for purposes beneficial to but outside of biostratigraphic correlation. This research provides some of the first quantitative data on phytosaur ecology and the evolution of phytosaur functional 34 morphology and will enable greater appreciation for broader evolutionary patterns within

Archosauromorpha. 35

CHAPTER 2: GEOMETRIC MORPHOMETRIC ANALYSIS OF CRANIUM SHAPE

VARIATION IN CRUROTARSANS IN AN ECOMORPHOLOGICAL CONTEXT

Introduction

Understanding the evolutionary processes that affect phenotypic diversity is a primary goal of evolutionary biology research (Adams & Nistri, 2010; Mallarino &

Abzhanov, 2012). Phenotypic diversity stems from several processes, including natural selection, sexual selection, physical constraints, developmental constraints, and trait interactions, and the evolutionary diversification of phenotypes often occurs from the confluence of many of these factors (Schluter, 1996; Owens et al., 1999; Ricklefs, 2004;

Berner et al., 2008; Ward & Mehta, 2010; Sanger et al., 2011; Mallarino & Abzhanov,

2012). One approach to gaining a better understanding of the role of phenotypic variation in the diversification of evolutionary lineages is to test hypotheses of patterns and potential causes of morphological diversity in highly variable structures (Fitzpatrick,

1985; Schluter & McPhail, 1992; Hunter, 1998; Wainwright, 2007; Bleiweiss, 2009;

Monteiro & Nogueira, 2010; Close & Rayfield, 2012). The anatomical structure with perhaps the greatest morphological diversity among craniates is the cranial portion of the skull. Cranial morphological diversity evolves in response to a host of influencing forces, including: functional considerations of the primary sensory apparatus (Asahara et al.,

2016; Kaucka & Adameyko, 2017; Verde Arregoitia et al., 2017); the morphology and function of the central nervous system (Hanken & Thorogood, 1993; Kaucka &

Adameyko, 2017); ecological functions such as food acquisition (Metzger & Herrel,

2005; Markey & Marshall, 2007; Motta et al., 2008; Asahara et al., 2016; Verde 36

Arregoitia et al., 2017), defense (Packer, 1983; Reichel et al., 2009; Stankowich & Caro,

2009), and locomotion (Reichel et al., 2009; Verde Arregoitia et al., 2017; Vidal-García

& Keogh, 2017); displays and other inter- and intraspecific functions (Packer, 1983;

Sullivan et al., 2003; Reichel et al., 2009; Stankowich & Caro, 2009; Jasinoski & Abdala,

2017), and numerous others. The evolutionary, developmental, and morphological complexity of the cranium makes it both a challenging subject in the study of the evolution of phenotypic diversity and a unique system for testing hypotheses of the interactions of a large number and wide variety of selective forces, physical constraints, and developmental processes (Hanken & Thorogood, 1993; Motta et al., 2008; Verde

Arregoitia et al., 2017).

Of all influences on cranial morphological variation, dietary strategy and feeding ecology is, perhaps, the most widely studied (e.g., Metzger & Herrel, 2005; Markey &

Marshall, 2007; Motta et al., 2008; Asahara et al., 2016; Verde Arregoitia et al., 2017).

Food preference, foraging behavior, and other aspects of dietary resource acquisition and utilization are correlated with cranial morphology in a wide range of extant taxa, including teleosts (Wainwright & Richard, 1995; Wyckmans et al., 2007), amphibians

(Emerson, 1985; Vidal-García & Keogh, 2017), squamates (Stayton, 2005; Metzger &

Herrel, 2005; da Silva et al., 2016; Klaczko et al., 2016), turtles (Foth et al., 2017), mammals (Tschapka et al., 2008; Asahara et al., 2016; Verde Arregoitia et al., 2017), and birds (Zusi, 1975; Livezey, 1989; Mallarino et al., 2012; Tokita et al., 2016; Pecsics et al., 2017). A relationship between cranial morphology and both food preference and acquisition behavior has been proposed in extant crocodylians (e.g., Iordansky, 1973; 37

Langston, 1973; Pooley, 1989; Busbey, 1995; Marugán-Lobón & Buscalioni, 2003;

McHenry et al., 2006; Foth et al., 2015), and rostrum morphology appears to be linked to the maximum relative size of prey that can be utilized (see “Hypothesized Ecology of

Phytosauria” in Chapter 1 of this volume). Cranial morphology has also been used to support dietary inferences about extinct taxa (e.g., Livezey, 1989; Zanno & Makovicky,

2011; Asahara et al., 2016; Foth et al., 2017). Many studies have sought to infer food item preference or acquisition behavior of extinct taxa based on morphological similarities between those taxa and extant crocodylians. This approach is widely used in studies of extinct crocodyliforms (e.g., Buffetaut, 1979; Denton et al., 1997; Hua &

Buffetaut, 1997; Hastings et al., 2010; Stout, 2012; Cidade, 2017; Sena et al., 2017) and more distantly-related taxa with similar craniofacial morphology (e.g., marine reptiles:

Massare, 1987; dinosaurs: Sereno et al., 1998; Rayfield et al., 2007; champsosaurs:

Ksepka et al., 2005; temnospondyls: Fortuny et al., 2011). Inferences about phytosaur trophic ecology have long been made on the basis of qualitative assessments of their overall, superficial morphological similarity to extant crocodylians (e.g., Hunt, 1989;

Hungerbühler, 2002).

Rostrum Morphotypes

Aspect ratio of the rostrum is an often used metric for categorizing and defining crocodylian cranial morphology (Fig. 4). Crocodylians were divided into the following morphotypes by Busbey (1995): longirostrine, with a long, mediolaterally narrow rostrum; brevirostrine, with a short rostrum; platyrostral, with a mediolaterally broad, dorsoventrally flat rostrum; and oreinirostral, with a mediolaterally compressed, domed 38

Figure 4. Examples of rostrum morphotypes in Crocodylia and Phytosauria. Line drawings of: the longirostrine (A), generalized (B), and brevirostrine (C) crocodylians Gavialis gangeticus (UF 118998), Crocodylus rhombifer (MNB AB- 50.0171), and Melanosuchus niger (RVC-JRH-FBC1), respectively, in dorsal view; the dolichorostral (D) and brachyrostral (E) phytosaurs Ebrachosuchus neukami (BSPG 1931 X 501) and Pravusuchus hortus (UMNH VP 28293), respectively, in dorsal view; and the dolichorostral (F), altirostral (G), and brachyrostral phytosaurs (F) Machaeroprosopus pristinus (PEFO 382), Leptosuchus studeri (UMMP 14267), and Machaeroprosopus mccauleyi (PEFO 31219), respectively, in lateral view. Dolichorostral and altirostral phytosaur morphotypes are similar, apart from a partial rostral crest in the latter, and many brachyrostral phytosaurs exhibit full rostral crests. Drawings not to scale.

39 rostrum. To describe fossil crocodyliform specimens, Brochu (2001) proposed the following morphotypes: generalized, falling between longirostrine and brevirostrine in length and width; ziphodont, with a deep, laterally compressed rostrum similar to the oreinirostral morphotype; and duck-faced, with a long, very broad platyrostral rostrum.

The terms meso-, longi-, and brevirostral were used by Marugán-Lobón & Buscalioni

(2003) to categorize skull morphology based on lateral, rather than dorsal, view, using ratios of brain case, orbit, and rostrum length to define the categories.

Phytosaur rostrum morphology was categorized by Hunt (1994) as either: dolichorostral, which is similar to the crocodylian longirostrine morphotype (sensu

Busbey, 1995); brachyrostral, which is similar to the crocodylian generalized morphotype

(sensu Brochu, 2001) or a more elongate version of the brevirostrine morphotype (sensu

Busbey, 1995); and altirostral, which is defined as a narrow rostrum with a partial or full bony pre-narial crest, otherwise essentially identical to the dolichorostral morphotype

(Hunt et al., 2006), and similar in appearance to the crocodyliform oreinirostral morphotype (sensu Brochu, 2001). Some phytosaur taxa outside the altirostral morphotype category, such as the brachyrostral Machaeroprosopus mccauleyi (Ballew,

1989; Holloway et al., 2013), also possess rostral crests. Thus, the relationship between rostral crests and overall rostral morphology, as seen in dorsal view, the utility of such crests for defining a distinct rostral morphotype, and the ultimate application of such crest morphotypes to making inferences of phytosaur diet is unclear. Phytosaurs such as those of the dolichorostral morphotype, have been hypothesized to have been strictly piscivorous, due to proposed morphological similarity to extant crocodylian taxa like 40

Gavialis (Hunt, 1989). However, the only known phytosaur gut contents are associated with specimens of this rostral morphotype and consist of the prolacertiform sauropsid

Malerisaurus and a partial rhynchosaur (Chatterjee, 1978; Chatterjee, 1980)—both of which were small to moderately-sized, terrestrial tetrapods (e.g., Chatterjee, 1980; Hunt

& Lucas, 1991b).

The benefits of using extant crocodylians as comparative bases for analogies and inferences of diet in phytosaurs include the commonality of faunivory as the dietary strategy of all extant crocodylians (e.g., Grenard, 1991; Grigg & Kirshner, 2015), differences in food item type utilization by individual taxa (Ross & Magnusson, 1989), relatively narrow habitat range occupied by extant crocodylians (e.g., Grigg & Kirshner,

2015), relatively large body size range of extant crocodylians (e.g., Grigg & Kirshner,

2015), and well-documented prey item utilization of many individual taxa (e.g., Table 1;

Grenard, 1991; Grigg & Kirshner, 2015). These ecomorphological data on extant crocodylian rostral morphological variation are important and useful bases for inferring aspects of dietary ecomorphology in extinct taxa.

Geometric Morphometric Characterization of Shape

Despite the utility of rostral morphotypes for broadly categorizing crocodylian and phytosaur specimens, such categories are not taxonomically definitive for crocodylians because of overlap in skull shape between taxa (Busbey, 1995), and their taxonomic relevance for phytosaurs is unclear (Long & Murry, 1995; Stocker, 2010).

Furthermore, the characterization and quantification of morphology through the use of traditional metrics like length and width is of limited statistical utility because such 41 measurements are often interdependent, affected by allometry, or possess other artifacts or biases (Adams et al., 2004). More recently developed computational geometric morphometric methods eliminate biases including interdependence of variables, account for allometric effects on shape, and capture far more subtle aspects of shape variation than could typically be recognized through traditional morphometrics, allowing for more rigorous tests of biological hypotheses and better supported conclusions (e.g., Pierce et al.

2008; Abdel-Rahman et al., 2009; Breno et al., 2011; Pearcy & Wijtten, 2011).

Geometric morphometrics (GM) also allows for graphical representation of shape variation, rather than a table of measurements, which can aid in the depiction of morphological patterns (Adams et al., 2004). Rather than relying on comparisons of distances and ratios between end-points or angles, as in traditional methods, GM relies on a set of landmarks assigned to points on each specimen that are then used to represent the full geometry of those specimens and enable the interpretation of shape differences in multivariate space (Zelditch et al., 2004). A further benefit of GM is that landmark data for two-dimensional (2D) GM analyses can be derived from photographs of specimens, which are more accessible for a large number of specimens than are linear measurements.

Landmarks for GM analysis are positioned on biologically or geometrically homologous points on all sampled specimens and quantified as Cartesian coordinates (Zelditch et al.,

2004). Additional points called semi-landmarks are often placed by defining landmark endpoints and placing a specific number of semi-landmarks along a curve between them

(Zelditch et al., 2004). After rescaling and aligning specimen landmarks to achieve a standard equal specimen size and eliminate artifacts of rotational differences in specimen 42 positions, landmark coordinates can be investigated for differences in relative position, indicating specimen shape variation, free from confounding factors (Zelditch et al.,

2004).

Previous studies have analyzed 2D GM data to investigate crocodylian and crocodyliform craniofacial morphospace occupation patterns and their implications for ecomorphologically and taxonomically informative aspects of shape variation (Sadlier &

Makovicky, 2008; Pearcy & Wijtten, 2011), mechanical performance (Pierce et al.,

2008), and the diversity, disparity, and tempo of craniofacial shape evolution throughout

Crocodyliformes (Wilberg, 2012). Whereas Wilberg (2012) found that rostral length and width explain the most variation in crocodyliform craniofacial shape, other studies have consistently found that those same measurements, traditionally used to define crocodylian morphotypes, are not the factors most variable between species (Pierce et al., 2008;

Sadlier & Makovicky, 2008; Pearcy & Wijtten, 2011). The present study investigates the morphospace occupation of extant crocodylians and phytosaurs, comparing the two clades to one another in the context of other non-avemetatarsalian archosauromorphs. I hypothesize that: (1) variation in extant crocodylian rostrum and overall cranial morphology, as seen in dorsal view, can be primarily described by differences in aspect ratio; (2) variation in phytosaur rostrum and overall cranial morphology, as seen in dorsal view, cannot be described by the same differences in aspect ratio that describe variation in crocodylian rostrum and overall cranial morphology; and (3) phytosaurs and extant crocodylians occupy significantly different regions of rostrum and overall cranium shape space. This third hypothesis is important for testing the viability of attempts to infer 43 phytosaur diet variation based on perceived similarities of rostral and cranial morphology between phytosaurs and extant crocodylians. This study will provide both a framework for testing relationships among morphology, ecology, and phylogeny and a foundation for further investigating functional implications of morphological similarity and disparity.

Materials and Methods

Taxon Sampling

Data were collected from 127 specimens of 93 non-avemetatarsalian archosauromorph taxa (Table 2). The dataset comprises 13 specimens of nine phytosaur taxa, 18 specimens of 17 extinct crocodylian taxa, 45 specimens of 19 extant crocodylian taxa, 5 specimens of 5 non-crurotarsan archosauromorph taxa, and 46 specimens of 43 non-crocodylian pseudosuchian taxa. Because crocodylian cranium shape variation is typically described in terms of features seen in dorsal view and phytosaur crania are generally compared to crocodylian crania within that same context, 2D specimen data collected for this study comprised dorsal view images. Dorsal view images of volumetric models derived from computed tomography data of 44 specimens of 25 taxa were obtained, dorsal view photographs were taken of 14 specimens of 13 taxa, and the remaining specimens were sampled from published figures or photographs available electronically through collections records. Images of volumetric models were obtained with an orthographic view and the specimen aligned such that the plane of the dorsal skull roof (i.e. the bones dorsal and lateral to the neurocranium, typically comprising the frontal, postorbital, parietal, and squamosal bones between the caudal margin of the orbit and dorsocaudal margin of the skull) was parallel to that of the viewport. Photographs of 44

Table 2. Taxa sampled for geometric morphometric analyses. For taxa represented by a particular specimen, that specimen number is given, along with the source of the specimen image (i.e. photograph of physical specimen taken by WLH, screenshot of volumetric specimen model taken in orthographic view by WLH, or photograph included in a published figure). For taxa represented by an anatomical reconstruction or photograph included in a published figure, the reference for that figure is also given.

45

Table 1. Continued.

46

Table 2. Continued.

47 specimens were taken with specimens aligned such that the plane of the skull roof was parallel to that of the camera, with a scale bar placed at the same distance from the camera as the specimen skull roof. Photographs were then imported to Adobe Photoshop

CS6 (Adobe Systems Inc., San Jose, CA, USA) and the “Lens Correction” filter was used to adjust the images to account for distortion caused by the camera lens, with the straightness of the scale bar serving as an indicator for image distortion.

The use of specimen images collected from the literature raises potential concerns about the lack of consistency in how those images were obtained by other authors. Some of the taxa sampled are also not known from complete specimens, and data on those taxa were derived from published reconstructions based on multiple specimens. The phytosaur landmark data also derived almost entirely from specimens that were taphonomically deformed and digitally altered to correct for such deformation. Many morphometric analyses of paleontological specimens have to account for potential additional variables such as these (e.g., Arbour & Brown, 2014). In the case of the present study, the analyses and comparisons are based on gross shape, rather than specific morphological details or features. Therefore, the probability that the results of this study are invalid due to shapes being misrepresented because of minor specimen deformation, slight variations in camera position, or small inaccuracies in specimen reconstructions is reduced (Arbour & Brown,

2014; Collins & Gazley, 2017).

Cranial Shape and Landmark Placement

Using tpsUtil64 (©2018, F. James Rohlf), specimen images were compiled into a tps file that was then imported into tpsDig2 (©2017, F. James Rohlf) for landmark 48 placement and scaling. Nine fixed landmarks and 28 sliding semilandmarks were placed on each specimen image in an arrangement designed to capture gross two-dimensional cranial and rostral morphology in dorsal view (Fig. 5). For each specimen, the left lateral half was sampled, or if the right lateral half was better preserved, it was sampled and then reflected to appear as the left lateral half. Landmark placement was chosen to best represent gross cranium shape and outline, rather than detailed shapes of individual cranial elements or features. For example, landmarks were placed to capture the general shape of the entire rostrum but not the morphology of the maxilla and premaxilla that comprise the rostrum. Fixed landmarks were placed at: (1) the dorsocaudal midline terminus of the parietal, (2) the caudal-most point of the squamosal, (3) the lateral margin of the postorbital at the point where it intersects the caudal margin of the orbit, (4) the specimen midline at the coronal plane of the caudal margin of the orbit, (5) the lateral margin of the quadrate-quadratojugal suture, (6) the lateral margin of the specimen at the coronal plane of the caudal margin of the orbit, (7) the lateral margin of the specimen at the coronal plane of the rostral margin of the orbit, (8) the rostral margin of the interpremaxillary suture, and (9) the specimen midline at the coronal plane of the rostral margin of the orbit. Curves were drawn along curvatures of the cranium between pairs of fixed landmarks, and a set number of semilandmarks were placed at equidistant intervals along each curve. Semilandmarks were treated using the minimum Procrustes distance sliding method (Bookstein, 1997) in subsequent analyses. Two sliding semilandmarks were placed along the caudal margin of the parietal, between landmarks 1 and 2; four along the lateral margin of the skull roof, between landmarks 2 and 3; four along the 49

Figure 5. Illustration of geometric morphometric landmark placement. Examples of landmark (orange circles) and sliding semi-landmark (blue circles) locations on Machaeroprosopus pristinus (PEFO 382).

lateral margin of the cranium, between landmarks 5 and 6; two along the lateral margin of the cranium, between landmarks 6 and 7; and sixteen along the lateral margin of the cranium, between landmarks 7 and 8.

Analytical Approaches

Landmark data were imported into R (R Core Team, 2013), and functions in the package geomorph (Adams & Otárola-Castillo, 2012; Adams et al., 2018) were used for analyses. A General Procrustes Analysis (GPA) was used to standardize the coordinate landmark data, removing artifacts caused by size, rotation, and position differences of specimens in images (Dryden & Mardia, 1998; Joliffe, 2002; Pearcy & Wijtten, 2011).

Shape, in this context, is the residual mismatch and irreducible distance among homologous landmarks (Fernández-Montraveta & Marugán-Lobón, 2017), and these standardized landmark data were used in subsequent analyses. The centroid sizes of specimen landmark configurations, which correspond to the squared root of the sum of the squared distances from each landmark to the centroid (Bookstein, 1991), were used as proxies for size. Specimen landmark data were classified, based on the phylogenetic 50 relationships of the represented taxa (Fig. 1), into one of three groups: Phytosauria,

Crocodylia, and all other non-avemetatarsalian Archosauromorpha included within neither Phytosauria nor Crocodylia.

A Principal Coordinates Analysis (PCA) was performed to plot the position of each specimen in shape space, relative to a calculated mean shape for all specimens. A

Procrustes ANOVA was performed to test for covariation of specimen shape and specimen group. Shape was tested for allometric effects using both the procD.allometry

Procrustes ANOVA function specifically for allometry and a second Procrustes ANOVA using the procD.lm function to test for covariation of shape and size in the entire sample.

A Procrustes MANOVA using the procD.allometry function was performed to test for homogeneity of specimen group allometric slopes, which would indicate an allometric effect common to all groups. Another Procrustes MANOVA using the procD.lm function was performed to test for covariation of shape and size by specimen group.

Morphological disparity, defined as Procrustes variance, was calculated for each group to test for significant differences between the ranges of shape space occupied by each group.

A second calculation of morphological disparity was performed that accounted for common allometric effect. The overall level of morphological integration for standardized landmark data was quantified. A calculated integration slope equal to -1 corresponds to self-similarity, which implies that patterns of shape variation are similar across spatial scales (Bookstein, 2015) and indicates the presence of only a single shape module. A slope less than -1 corresponds to data that are disintegrated, indicating the presence of multiple modules, with a slope of zero corresponding to isotropic data. 51

Following the test for morphological integration of the complete cranium landmark dataset, landmark sets corresponding to cranial regions of interest that were hypothesized to be morphological modules were isolated for additional analyses. Specifically, the rostrum was isolated because rostrum morphology is correlated with diet variation in extant crocodylians, and the region of the cranium caudal to the orbit was isolated because that is the location of the braincase and jaw musculature, the morphology of which are potentially related to organismal ecology. Landmarks 7–9 and the 16 sliding semilandmarks between landmarks 7 and 8 were isolated for analysis of specimen rostral shape. A Generalized Procrustes Analysis was performed on this rostral subset of landmarks, and the analyses performed on the standardized full landmark dataset were performed on these standardized rostral landmark data. Landmarks 1–6 and the sliding semilandmarks between landmarks 1 and 2, 2 and 3, and 5 and 6 were isolated for analysis of specimen post-orbital cranial shape. A Generalized Procrustes Analysis was performed on this post-orbital subset of landmarks, and the analyses performed on the standardized full landmark dataset were performed on these standardized post-orbital landmark data. Available data were insufficient to construct a phylogenetic hypothesis of all of the sampled taxa. The lack of such an hypothesis precluded analysis of phylogenetic signal in the shape data and any other analysis of shape evolution requiring input in the form of phylogenetic relationships among all sampled taxa. 52

Results

Principal Coordinates Analyses

Among the results of a PCA conducted on the 37 standardized landmarks was that the first two principal coordinates (PCs) summarized 57.45% and 12.33% of the total variance, respectively (Fig. 6). The first PC axis describes differences in the relative positions of landmarks that primarily represent the ratio of pre-orbital rostral length to overall cranial length or the relative length of the pre-orbital cranium to that of the post- orbital cranium, as well as the degree of concavity in the curvature of the lateral margin of the rostrum immediately rostral to the orbit. The relative length of the pre-orbital to post-orbital cranium and the concavity of the rostrum immediately rostral to the orbit are inverse to values of the PC1 scores. The differences in relative positions of landmarks described by PC2 primarily represent the ratio of skull roof width to overall cranial width, largely pertaining to rostral width and the distance between the midline and lateral margin of the jugal, as well as the degree of concavity in the curvature of the lateral margin of the rostrum immediately rostral to the orbit. The ratio of skull roof width to rostral and overall cranial width and the concavity of the rostrum immediately rostral to the orbit are inverse to the values of PC2 scores.

Specimen distribution along the first two PC axes is such that non- avemetatarsalian archosauromorphs included within neither Phytosauria nor Crocodylia occupy a great range of both positive and negative scores along PC1 and largely occupy the negative to slightly positive range of PC2 scores. A few non-avemetatarsalian archosauromorphs included within neither Phytosauria nor Crocodylia occupied positive 53

Figure 6. PCA results of the full cranium landmark dataset. Specimens of Phytosauria (orange squares), Crocodylia (blue triangles), and other non- avemetatarsalian archosauromorphs included within neither Phytosauria nor Crocodylia (black circles) projected into the shape space. Percentage of the total variance explained by each of the first two PC axes is given along the corresponding plot axis. Deformation grids for the extreme ends of PC1 and PC2 are given along the corresponding axis. Within shape space, the proportion of rostrocaudal length of the rostrum to entire cranium length and the degree of concavity of the lateral margin of the rostrum increase to the left and decrease to the right. The proportion of skull roof width to overall cranium width and the overall difference in width between the rostrum and post-orbital cranium decreases toward the top and increases toward the bottom.

PC2 scores that were considerably greater than the rest of that group, including:

Anatosuchus minor, Kaprosuchus saharicus, and Stomatosuchus inermis. Crocodylian taxa occupied nearly the same range of PC1 scores as other non-avemetatarsalian archosauromorphs outside of Phytosauria, with “longirostrine” taxa occupying negative

PC1 and “brevirostrine” taxa occupying positive PC1. Crocodylian taxa predominantly 54 occupy the positive to slightly negative range of PC2 scores, with the specimens occupying negative scores being those of the extinct taxa Eogavialis africanum and

Gavialis bengawanicus; young juveniles of extant taxa, including Crocodylus acutus,

Osteolaemus tetraspis, Paleosuchus palpeprosus, and Tomistoma schlegelii; and both juvenile and adult Gavialis gangeticus.

Phytosaurian taxa occupy a far smaller and nearly unique region of shape space, compared to other non-avemetatarsalian taxa. The range of PC1 scores occupied by phytosaurs is much smaller than either of the other two specimen groups and is farther along the negative of PC1 than all but the extant crocodylian Gavialis gangeticus; the extinct crocodylians Eogavialis africanum, Gavialis bengawanicus, and Tomistoma calaritanum; the extinct neosuchian Stomatosuchus inermis; and the thalattosuchians

Cricosaurus araucanensis, Mystriosaurus brongniarti, Pelagosaurus typus, and

Steneosaurus gracilirostris. Phytosaurs occupy only positive PC2 scores ranging from just slightly above the mean PC2 score for the entire sample to approximately the median positive PC2 score for the entire sample, minus the specimen with the greatest positive

PC2 score. This combination of PC1 and PC2 score ranges is almost exclusively occupied by phytosaurs, among the three specimen groups, with the only other taxa occupying the phytosaur region of shape space being the fossil crocodylians Euthecodon brumpti and Tomistoma calaritanum. These results indicate that phytosaurs exhibit a greater ratio of pre-orbital to post-orbital cranium length than almost any other non- avemetatarsalian archosauromorphs and a greater ratio of skull roof width to overall cranial width than nearly all other taxa with similar pre-orbital to post-orbital cranium 55 length ratios, including the longirostrine extant crocodylians Gavialis gangeticus and

Tomistoma schlegelii.

Among the results of a PCA conducted on the 19 standardized rostral landmarks was that the first two principal coordinates (PCs) summarized 84.68% and 6.5% of the total variance, respectively (Fig. 7). The first PC axis describes differences in the relative positions of landmarks that primarily represent the ratio of rostral length to the cranial width at the coronal plane of the rostral margin of the orbit, as well as the degree of concavity or convexity in the curvature of the lateral margin of the rostrum. The ratio of rostral length to cranial width at the rostral margin of the orbit is inverse to the values of the PC1 scores, and lower PC1 scores describe a more concave lateral margin of the rostrum. The differences in relative positions of landmarks described by PC2 primarily represent the ratio of the width of the distal rostrum to the cranial width at the rostral margin of the orbit and the location and concavity of taper along the rostral margin. The ratio of distal rostrum width to cranial width at the rostral margin of the orbit, the degree of concavity in the taper of the rostrum, and the distance of the initiation of that taper from the terminus of the rostrum are all negatively correlated with the values of the PC2 scores. High PC2 scores describe rostra that have straight to convex lateral margins, are uniform in width along their length, and do not taper until near the rostral terminus, resulting in rostra that appear broad until terminating in a blunt tip. Low PC2 scores describe rostra that have highly concave lateral margins, narrow substantially along their length, and begin tapering immediately rostral to the rostral margin of the orbit, resulting in rostra that appear as wedges with concave lateral margins. 56

Figure 7. PCA results of the rostrum landmark dataset. Specimens of Phytosauria (orange squares), Crocodylia (blue triangles), and other non- avemetatarsalian archosauromorphs included within neither Phytosauria nor Crocodylia (black circles) projected into the shape space. Percentage of the total variance explained by each of the first two PC axes is given along the corresponding plot axis. Deformation grids for the extreme ends of PC1 and PC2 are given along the corresponding axis. Within shape space, the ratio of rostrum length to the cranium width at the coronal plane of the rostral margin of the orbit and the degree of concavity of the lateral margin of the rostrum increase to the left and decrease to the right. The difference in width of the distal rostrum to the cranial width at the rostral margin of the orbit decreases toward the top and increases toward the bottom, and the location of taper initiation along the rostral margin is more rostrally located toward the top and more caudally located toward the bottom.

The distribution of specimen rostra along the first two PC axes was such that those of non-avemetatarsalian archosauromorphs included within neither Phytosauria nor

Crocodylia occupied the greatest range of both positive and negative scores along both

PC axes, including the greatest and lowest PC2 scores, the greatest PC1 score, and nearly the lowest PC1 score. Crocodylian taxa occupied a range of positive and negative PC1 57 scores that were only slightly closer to the sample mean than those of nearly all of the other non-avemetatarsalian archosauromorphs outside of Phytosauria. “Longirostrine” taxa occupy negative PC1 and “brevirostrine” taxa occupying positive PC1. Crocodylian rostra predominantly occupy the positive to slightly negative range of PC2 scores, with only two specimens described by negative PC2 scores as low or lower than the median negative PC2 score for the entire sample, minus the two specimens with the lowest PC2 scores. The crocodylian specimens described by negative PC2 scores (e.g., Caiman crocodilus (RVC-JRH-FCC1), Crocodylus intermedius (FMNH 75662), Leidyosuchus canadensis (TMM M-45867-1), Lohuecosuchus megadontos (HUE-04498),

Penghusuchus pani (NMNS-055645), Osteolaemus tetraspis (AMNH R116354; FMNH

98936; TMM M-6774), and Toyotamaphimeia machikanensis (KSNM-F7-6; MOU

F00001)) do not have close phylogenetic relationships and share no ontogenetic similarities, apart from a cluster of three juvenile Osteolaemus tetraspis. These same three O. tetraspis specimens are also described by similar PC1 scores, unlike the adult O. tetraspis specimen (AMNH R160901), which is described by a much lower PC1 score and a positive PC2 score.

As with the results of the PCA of the full 37 landmark dataset, the range of PC1 scores occupied by phytosaur rostra is much smaller than either of the other two specimen groups and is farther along the negative of PC1 than all but the extant crocodylians Gavialis gangeticus and Tomistoma schlegelii; the extinct crocodylians

Eogavialis africanum, Euthecodon brumpti, Gavialis bengawanicus, and Tomistoma calaritanum; and the thalattosuchians Cricosaurus araucanensis, Mystriosaurus 58 brongniarti, Pelagosaurus typus, Rhacheosaurus gracilis, and Steneosaurus gracilirostris, and Steneosaurus minimus. Phytosaur rostra occupy a range of PC2 scores that is almost entirely negative to just slightly more positive than the standardized mean and nearly the inverse of the PC2 score range of crocodylians, including “longirostrine” crocodylians. This combination of PC1 and PC2 score ranges is almost exclusively occupied by phytosaurs, among the three specimen groups, with the only other taxa occupying the phytosaur region of shape space being the extant crocodylians Gavialis gangeticus and Tomistoma schlegelii; the extinct crocodylians Euthecodon brumpti,

Gavialis bengawanicus, and Tomistoma calaritanum; and the thalattosuchians

Cricosaurus araucanensis, Mystriosaurus brongniarti, Pelagosaurus typus,

Rhacheosaurus gracilis, and Steneosaurus gracilirostris, and Steneosaurus minimus.

With the exclusion of the rostrum of the phytosaur Ebrachosuchus neukami, which is the only phytosaur rostrum to be described by a PC2 score that is considerably greater than the standardized mean, this overlap in rostrum shape space between phytosaurs and the other two specimen groups is greatly reduced to include only the extinct crocodylian

Tomistoma calaritanum and the thalattosuchians Cricosaurus araucanensis and

Rhacheosaurus gracilis. These results indicate that phytosaurs exhibit a very narrow range of rostrum aspect ratios that is shared with the longirostrine extant crocodylians

Gavialis gangeticus and Tomistoma schlegelii, but the rostrum of all but one phytosaur tapers more greatly than nearly any longirostrine crocodylian, including G. gangeticus and T. schlegelii. 59

Among the results of a PCA conducted on the 18 standardized post-orbital landmarks was that the first two principal coordinates (PCs) summarized 38.54% and

22.28% of the total variance, respectively (Fig. 8). The first PC axis describes differences in the relative positions of landmarks that primarily represent the ratio of skull roof width to the distance between the cranial midline and lateral margin of the jugal. The ratio of cranial width to skull roof width is inverse to the values of the PC1 scores. The differences in relative positions of landmarks described by PC2 primarily represent the proportion of overall length contributed by the distance between the coronal plane of the caudal-most point of the squamosal and those of the dorsocaudal midline terminus of the parietal and lateral margin of the quadrate-quadratojugal suture. The distance of caudal projection of the squamosal beyond the dorsocaudal midline terminus of the parietal and lateral margin of the quadrate-quadratojugal suture increases with PC2 score value.

The distribution of specimen post-orbital cranium shapes along the first two PC axes is such that those of non-avemetatarsalian archosauromorphs included within neither

Phytosauria nor Crocodylia occupy the greatest range of both positive and negative scores along both PC axes, with each quadrant of shape space occupied by several taxa.

Crocodylian taxa occupy both positive and negative PC1 scores, with a very weak trend of “longirostrine” taxa tending to occupy positive PC1 and “brevirostrine” taxa tending to occupy negative PC1. However, there is substantial overlap in the PC1 ranges of these categories, and the concentration of crocodylian taxa increases closer to the standardized mean. With the except of four specimens occupying negative PC2 scores very close to the standardized mean, crocodylian post-orbital crania all occupy positive PC2 scores. 60

Figure 8. PCA results of the post-orbital cranium landmark dataset. Specimens of Phytosauria (orange squares), Crocodylia (blue triangles), and other non- avemetatarsalian archosauromorphs included within neither Phytosauria nor Crocodylia (black circles) projected into the shape space. Percentage of the total variance explained by each of the first two PC axes is given along the corresponding plot axis. Deformation grids for the extreme ends of PC1 and PC2 are given along the corresponding axis. Within shape space, the position of the caudal-most point on the squamosal, relative to the caudal-most point on both the dorsocaudal midline terminus of the parietal and lateral margin of the quadrate-quadratojugal suture is more rostrally located toward the top and more caudally located toward the bottom.

As with the results of the PCAs of the full 37 landmark and 19 rostral landmark datasets, the range of PC1 scores occupied by phytosaur post-orbital crania is much smaller than either of the other two specimen groups, and entirely negative. Although phytosaur post-orbital crania occupy a PC1 score range from close to the standardized mean to among the lowest negative scores of the entire sample, this range is within the 61 limits of the rest of the entire sample. Phytosaur post-orbital crania occupy a range of

PC2 scores that is entirely negative, with no specimens occupying PC2 scores close to the standardized mean. Only a small number of non-avemetatarsalian archosauromorphs included within neither Phytosauria nor Crocodylia occupy negative PC2 values as low as the range occupied by phytosaurs, and excluding the taxon occupying the lowest PC2 score, the notosuchian Simosuchus clarki, phytosaurs occupy the five lowest PC2 scores.

There is also a substantial range of negative PC2 scores separating the phytosaur range from the crocodylian range. The combination of PC1 and PC2 score ranges occupied by phytosaurs is almost entirely devoid of other taxa. The only other taxa occupying the phytosaur region of shape space are the proterochampsid Proterochampsa barrionuevoi, the ornithosuchid Riojasuchus tenuisceps, and the aetosaur Stenomyti huangae. These results indicate that phytosaurs exhibit a far greater amount of shape variation in the post- orbital cranium than in the rostrum or whole cranium. Additionally, the range of cranial width to skull roof width ratios exhibited by phytosaurs was the same as most of

Crocodylia, including several longirostrine, generalized, and brevirostrine extant crocodylians and excluding some longirostrine crocodylians such as Gavialis and

Eogavialis. Phytosaurs also exhibited a ratio of the length of the caudal projection of the squamosal beyond the dorsocaudal midline terminus of the parietal and lateral margin of the quadrate-quadratojugal suture to overall post-orbital cranium length that was greater than all but a few other non-archosaurian archosaurmorphs and far greater than any crocodylian taxa. 62

Statistical Analyses

Analysis of the results of the GPA conducted on the 37 cranial landmark dataset revealed significant covariation between cranium shape and specimen group (Procrustes

ANOVA: df=2, R2=0.21, F=16.42, Z=10.93, p<0.01). The plot of these results (Fig. 9A) illustrate a substantial difference between phytosaurian crania and those of the other two groups and a very small difference between Crocodylia and other non-avemetatarsalian archosauromorphs outside of Phytosauria. The procD.allometry Procrustes ANOVA for allometry detected a significant allometric effect on cranium shape (df=1, R2=0.29,

F=50.70, Z=21.26, p<0.01). Results of the procD.lm Procrustes ANOVA for covariation of cranium shape and centroid size were congruent with those of the procD.allometry analysis (df=1, R2=0.15, F=21.70, Z=12.824, p<0.01). The procD.allometry Procrustes

MANOVA for homogeneity of allometric slopes failed to reject the null hypothesis of parallel slopes (df=121, R2=0.02, F=1.92, Z=1.68, p=0.08). Results of the Procrustes

MANOVA for covariation of cranium shape and centroid size by specimen group found significant covariation between shape and size (df=1, R2=0.15, F=26.28, Z=12.82, p<0.01), shape and group classification (df=2, R2=0.12, F=10.82, Z=7.79, p<0.01), and shape and size by group classification (df=2, R2=0.05, F=4.35, Z=3.64, p<0.01). Cranial morphological disparity was calculated as 1.86x102 for Phytosauria, 7.9x103 for

Crocodylia, and 1.47x102 for other non-avemetatarsalian archosauromorphs. Pairwise absolute differences between group variances were significant in pairings of Crocodylia with each of the other groups (p<0.01) but not the pairing of Phytosauria and other non- avemetatarsalian archosauromorphs outside of Crocodylia (p=0.11). Cranial 63

Figure 9. Results of Procrustes ANOVA for covariation of shape and specimen group. Results from analyses of the full cranium (A), rostrum (B), and post-orbital cranium (C) landmark datasets. Procrustes distance fitted values are plotted for taxonomic groups, as labeled. Red line indicates group Procrustes distance residual means. Ranges along y-axis indicate amount of within-group variances, and distance along x-axis indicates amount of similarity between group mean distance from the sample mean.

morphological disparity, accounting for allometry, was 1.29x102 for Phytosauria, 7.3 x103 for Crocodylia, and 1.26 x102 for other non-avemetatarsalian archosauromorphs.

Pairwise absolute differences in group variances, accounting for allometry, were significant between Crocodylia and each of the other groups (p<0.01) but not between

Phytosauria and other non-avemetatarsalian archosauromorphs outside of Crocodylia

(p=0.914). A global morphological integration slope of -0.58 was calculated for the full cranium landmark data.

Analysis of the results of the GPA conducted on the 19 rostral landmark dataset found significant covariation between rostrum shape and specimen group (Procrustes

ANOVA: df=2, R2=0.15, F=10.72, Z=7.16, p<0.01). The plot of these results (Fig. 9B) 64 illustrate the substantial difference between phytosaurian rostra and those of the other two groups and a very small difference between Crocodylia and other non-avemetatarsalian archosauromorphs outside of Phytosauria. The procD.allometry Procrustes ANOVA revealed a significant allometric effect on rostrum shape (df=1, R2=0.30, F=54.53,

Z=19.96, p<0.01). Results of the procD.lm Procrustes ANOVA for covariation of rostrum shape and centroid size were congruent with those of the procD.allometry analysis (df=1,

R2=0.15, F=21.25, Z=10.63, p<0.01). The procD.allometry Procrustes MANOVA for homogeneity of allometric slopes failed to reject the null hypothesis of parallel slopes

(df=121, R2=0.01, F=1.21, Z=1.00, p=0.33). Results of the Procrustes MANOVA for covariation of rostrum shape and centroid size by specimen group found significant covariation between shape and size (df=1, R2=0.15, F=23.17, Z=10.63, p<0.01), shape and group classification (df=2, R2=0.06, F=4.69, Z=3.45, p<0.01), and shape and size by group classification (df=2, R2=0.04, F=2.96, Z=2.18, p<0.05). Rostrum morphological disparity was 1.79x102 for Phytosauria, 1.12x102 for Crocodylia, and 1.53x102 for other non-avemetatarsalian archosauromorphs. Pairwise absolute differences between group variances were not significant when comparing Phytosauria with Crocodylia (p=0.14) or comparing other non-avemetatarsalian archosauromorphs with either Crocodylia (p=0.19) or Phytosauria (p=0.57). Rostrum morphological disparity, accounting for allometry, was

1.07x102 for Phytosauria, 1.02x102 for Crocodylia, and 1.35x102 for non- avemetatarsalian archosauromorphs. Pairwise absolute differences between group variances, accounting for allometry, were not significant between Phytosauria and

Crocodylia (p=0.91) or between other non-avemetatarsalian archosauromorphs and either 65

Crocodylia (p=0.26) or Phytosauria (p=0.54). A global morphological integration slope of -0.94 was calculated for the rostrum landmark data.

Analysis of the results of the GPA conducted on the 18 post-orbital landmark dataset revealed significant covariation between post-orbital cranium shape and specimen group (Procrustes ANOVA: df=2, R2=0.29, F=25.04, Z=14.71, p<0.01). The plot of these results (Fig. 9C) illustrate a substantial difference between phytosaurian post-orbital crania and those of the other two groups and a very small difference between Crocodylia and other non-avemetatarsalian archosauromorphs outside of Phytosauria. The procD.allometry Procrustes ANOVA for allometry found a significant allometric effect on post-orbital cranium shape (df=1, R2=0.80, F=10.93, Z=8.14, p<0.01). Results of the procD.lm Procrustes ANOVA for covariation of post-orbital cranium shape and centroid size were congruent with those of the procD.allometry analysis (df=1, R2=0.06, F=7.35,

Z=5.78, p<0.01). The procD.allometry Procrustes MANOVA for homogeneity of allometric slopes rejected the null hypothesis of parallel slopes (df=121, R2=0.03,

F=3.30, Z=2.72, p<0.05). The plot of these results (Fig. 10) illustrates that the allometric slopes of phytosaurian and crocodylian post-orbital crania are similar to one another and different from other non-avemetatarsalian archosauromorphs. Results of the Procrustes

MANOVA for covariation of post-orbital cranium shape and centroid size by specimen group found significant covariation between shape and size (df=1, R2=0.6, F=10.13,

Z=5.78, p<0.01), shape and group classification (df=2, R2=0.26, F=23.42, Z=14.22, p<0.01), and shape and size by group classification (df=2, R2=0.02, F=2.26, Z=2.97, p<0.05). Post-orbital cranium morphological disparity was 8.02x102 for Phytosauria, 66

Figure 10. Results of Procrustes MANOVA for homogeneity of allometric slopes. The procD.allometry function was used to test for homogeneity of allometric slopes among specimen groups in the post-orbital cranium dataset. (A) The common allometric component (CAC), the component of shape change most closely aligned with size, relative to log(centroid size), and (B) the first residual shape component (RSC1), relative to CAC. The null hypothesis of parallel allometric slopes is rejected (df=121, R2=0.03, F=3.30, Z=2.72, p<0.05). Phytosaurian (red circles) and crocodylian (green circles) allometric slopes are similar to one another and different from other non-avemetatarsalian archosauromorphs (black circles).

2.37x102 for Crocodylia, and 6.12x102 for other non-avemetatarsalian archosauromorphs.

Pairwise absolute differences between group variances were significant when comparing

Crocodylia with each of the other groups (p<0.01) but not when comparing Phytosauria and other non-avemetatarsalian archosauromorphs outside of Crocodylia (p=0.06). Post- orbital cranium morphological disparity, accounting for allometry, was 6.79x102 for

Phytosauria, 2.25x102 for Crocodylia, and 5.96x102 for other non-avemetatarsalian archosauromorphs. Pairwise absolute differences between group variances, accounting for allometry, were significant between Crocodylia and each of the other groups (p<0.01) but not between Phytosauria and other non-avemetatarsalian archosauromorphs outside 67 of Crocodylia (p=0.38). A global morphological integration slope of -0.69 was calculated for the post-orbital cranium landmark data.

Discussion

Phytosaurs occupy regions of cranium, rostrum, and post-orbital cranium shape space different from those occupied by either crocodylians or other non-avemetatarsalian archosauromorphs (Figs. 6–8). These results can be interpreted in a few ways. The first interpretation is that because phytosaurs are significantly different from other non- avemetatarsalian archosauromorphs, including crocodylians, in terms of overall cranium shape, inferences of phytosaur diet variation based solely on cranial morphological similarity to extant crocodylians cannot be made. The range of phytosaur cranium shape space occupation (Fig. 6) indicates a relatively high pre-orbital:post-orbital cranium length ratio. This region of cranium shape space lies outside the range occupied by crocodylians to the extreme of the longirostrine portion of crocodylian shape space. This relationship between the cranium shape space occupied by the two clades supports a second interpretation: that phytosaur cranial shapes collectively represent an a more extreme version of the longirostrine crocodylian morphotype. Under this interpretation, phytosaur diet variation can be inferred to have been an extreme version of longirostrine crocodylian diet variation. This conclusion would support the previously proposed hypothesis that phytosaurs, particularly those of the dolichorostral morphotype, were primarily piscivorous (Hunt, 1989). The primary problem with this interpretation, however, is that it relies on variation in cranial morphology being essentially a function of only the rostrum:overall cranium length ratio, without regard for rostral width, cranial 68 width, or any other aspect of shape complexity or variation. Results of the PCAs performed on the rostrum and post-orbital cranium region highlighted this problem by illustrating great differences in the profiles of variations in these regions between phytosaurs and crocodylians.

The third interpretation of the results requires the assumption that diet variation covaries with the aspect ratio of the rostrum alone, rather than the shape of the entire cranium. Such an approach is in line with previous hypotheses of the link between rostrum shape and diet (e.g., Iordansky, 1973; Langston, 1973; Pooley, 1989; Busbey,

1995; Marugán-Lobón & Buscalioni, 2003; McHenry et al., 2006; Foth et al., 2015), and it has the advantage of ignoring regions of the cranium that do not physically interact with food items, directly (e.g. the neurocranium). The PCA of the rostrum landmark dataset found the range of aspect ratios, described by PC1, of phytosaur rostra to be the similar to some longirostrine crocodylians, including Gavialis gangeticus and Tomistoma schlegelii (Fig. 7). The third interpretation of these results leads to the conclusion that phytosaur diet variation can be inferred to approximate that of the most longirostrine crocodylians. Although PC2 only explains 6.5% of the total variance in rostrum shape, the range of phytosaur rostrum shape space is greater along PC2 than PC1. Excluding one phytosaur taxon, the range of PC2 scores occupied by phytosaurs only slightly overlaps the scores of a few longirostrine crocodylians, none of which are extant taxa. The relationship between diet variation and the amount and shape of rostral taper described by

PC2 has not been investigated in extant crocodylians. The wider range of PC2 scores occupied by phytosaurs could indicate a stronger relationship between rostral taper and 69 diet variation in phytosaurs than crocodylians. The existence of such an ecomorphological trend in phytosaurs is supported by the distribution of phytosaur taxa along PC2 not being ordered phylogenetically (Fig. 2). Not all phytosaur rostra with the highest aspect ratios have taper shapes similar to those of longirostrine crocodylians, which indicates a difference in the relationship between rostrum aspect ratio and taper shape between these two clades. The nearly complete lack of overlap in shape space of phytosaur and crocodylian rostra indicates an inability to directly infer diet variation in phytosaurs based on covariation of rostrum shape and diet in extant crocodylians. Instead, inferring diet variation in phytosaurs based on rostrum shape alone requires differences in the nature of variation between phytosaurs and crocodylians to be ignored and only dorsal view aspect ratio to be considered. Furthermore, only considering the rostrum when discussing ways that aspects of cranium shape covary with diet variation ignores other functionally important regions of the cranium. One such functionally important region of the cranium is the post-orbital region, where the muscles responsible for the action of the jaws are located.

A potential relationship between post-orbital cranium shape and diet variation has not been previously proposed in extant crocodylians. One reason for this may be the gross similarity of post-orbital cranium shapes within Crocodylia. This point is illustrated by the dense cluster of crocodylian taxa within post-orbital cranium shape space, particularly near the standardized mean of PC1 and within a narrow range of PC2 (Fig.

8). The range of PC2 scores occupied by phytosaur post-orbital crania is entirely distinct from the PC2 score range of crocodylians, owing to the more pronounced caudal 70 projection of the squamosal beyond the dorsocaudal margin of the cranium in phytosaurs.

However, the relationship of the extent of caudal projection of the squamosals to diet variation is unclear and may not be ecologically relevant since the PC2 scores of such ecologically diverse taxa as Proterochampsa barrionuevoi, Protosuchus richardsoni,

Saurosuchus galilee, Desmatosuchus haploceras, Simosuchus clarki, and Stagonolepis olenkae, fall within the range occupied by phytosaurs. The arrangement of crocodylian taxa along post-orbital cranium shape PC1 does not completely match the rostrum morphology categorizations of crocodylians (Busbey, 1995; Brochu, 2001). There are examples wherein many taxa of different rostrum morphotypes, such as Tomistoma calaritanum, Caiman crocodilus and Lohuecosuchus megadontos all occupy approximately the same PC1 scores. However, the general trend is such that most of the longirostrine crocodylian taxa, including Eogavialis africanum, Gavialis gangeticus, and

Tomistoma schlegelii, occupy the highest PC1 scores. Taxa exhibiting some of the broadest rostra, including Alligator mississippiensis and Melanosuchus niger, occupy the lower range of PC1 scores. Comparing phytosaur and crocodylian post-orbital cranium shapes purely on the basis of PC1 scores yields interesting results in that phytosaurs occupy a range of PC1 scores shared with many non-longirostrine crocodylians, including Alligator mississippiensis, Crocodylus moreletii, and Melanosuchus niger. If there is an as-yet-to-be-identified significant relationship between post-orbital cranium shape and diet variation in extant crocodylians, phytosaur diet variation may be inferred to compare more favorably with non-longirostrine extant crocodylian taxa than longirostrine ones. 71

Analyses of all three landmark datasets found a significant allometric effect. This allometric effect was common to all three specimen groups in the overall cranium and rostrum landmark datasets. In the post-orbital landmark dataset, the allometric slope for non-avemetatarsalian archosauromorphs outside of Phytosauria and Crocodylia was found to differ from those of the other two groups (Fig. 10). The common allometry was accounted for in analyses of morphological disparity among specimen groups, and the results of these analyses were unchanged from those that did not account for the common allometric effect. Morphological disparity of phytosaurs was significantly greater than that of crocodylians but not significantly greater than other non-avemetatarsalian archosauromorphs outside of Crocodylia in both the full cranium and post-orbital cranium landmark datasets. The morphological disparity of crocodylians in these datasets was also significantly less than other non-avemetatarsalian archosauromorphs outside of

Phytosauria. These differences in morphological disparity are in contrast to the results of the analysis of the rostrum landmark dataset, which found the morphological disparity of none of the three groups to be significantly different from one another. Despite crocodylians exhibiting rostrum morphological variation comparable to each of the other two groups after accounting for common allometry, the range of post-orbital cranial morphological variation in Crocodylia is sufficiently restricted that overall cranial morphological variation is significantly less in crocodylians than in either of the other two groups. This means that phytosaurs exhibit greater shape variation in regions of the cranium other than the rostrum than do crocodylians. Rostrum shape variation was not significantly greater in phytosaurs than crocodylians, indicating that phytosaur rostra 72 exhibit a range of shapes that is approximately equal to that exhibited by crocodylian rostra, despite crocodylians possessing such varied rostral morphologies as those of

Gavialis and Melanosuchus (Fig. 4) and all of the sampled phytosaurs possessing relatively high length:width aspect ratios. These results indicate a range of phytosaur rostrum shape variation that is at least as great as, though less obvious than, that of crocodylians. Rather than differences in aspect ratio being the primary driver of rostrum shape variation, a combination of lateral rostral margin concavity and degree of taper along the length of the rostrum appears to account for much of the variation in phytosaurs. Phytosaur rostrum shape variation may be even greater than indicated by these results when considering aspects of rostrum shape not incorporated in this study, such as lateral profile.

Crocodylians exhibited greater relative morphological disparity in the rostrum and overall cranium landmark datasets than the other two specimen groups. A majority of the variance in these datasets was explained by aspect ratio, either of the rostrum itself or of the rostrum relative to the entire cranium (Fig. 6–7). Because of these results, the null of the first hypothesis that variation in extant crocodylian rostrum and overall cranium morphology cannot be primarily described by differences in aspect ratio is rejected

(Table 3). Not only were regions of shape space occupied by phytosaurs and crocodylians significantly different from one another in the analyses of rostrum and overall cranium landmark dataset, but phytosaurs also exhibited a much greater range of PC2 scores, relative to their range of PC1 scores, than did extant crocodylians. Instead of being primarily described by differences in aspect ratio, variation in phytosaur cranium shape, 73 as observed in dorsal view, appears to be primarily summarized by post-orbital cranium shape variances (Fig. 8). These findings, therefore, result in a failure to reject the second null hypothesis: that variation in phytosaur and extant crocodylian rostrum and overall cranium shape cannot be primarily described by the same differences in aspect ratio.

Moreover, the shape space regions occupied by phytosaurs in analyses of each of the three landmark datasets were significantly different from those occupied by either of the other two specimen groups (Figs. 6–8). Thus, these analyses result in a failure to reject

Table 3. Summary of hypotheses tested in this study, part 1. Statement of null and alternative hypotheses, the results of analyses pertinent to each hypothesis, and the conclusion drawn from interpretation of those results.

74 the null hypothesis that phytosaurs and extant crocodylians occupy significantly different regions of rostrum and overall cranium shape space.

The implications of the results reported here are that the covariation of diet variation and whole cranium or rostrum shape reported for crocodylians cannot be confidently used to directly infer diet variation in phytosaurs. That said, the results reported here do not entirely preclude any comparisons between phytosaurs and other non-avemetatarsalian archosauromorphs, including extant crocodylians, based on any one aspect of cranial shape. One of the most favorable of such comparisons that can be made is that phytosaur crania, although very different from those of crocodylians or other non- avemetatarsalian archosauromorphs outside of Crocodylia, share a region of shape space, in at least some aspects, with some thalattosuchians and the most longirostrine crocodylians (e.g., Gavialis gangeticus and a few extinct taxa). To the extent that diet variation may covary with some aspect of cranium or rostrum shape common to all of these groups, as defined by the gross shape of the cranium or isolated pre-orbital cranium as observed in dorsal view, the diet variations exhibited by the phytosaurs sampled for this study were probably more similar to those of the longirostrine extant crocodylians

Gavialis gangeticus and Tomistoma schlegelii than to other extant crocodylians.

Conclusions

Crocodylian rostrum and overall cranium shape variation, as seen in dorsal view, is easily defined by differences in aspect ratio (Figs. 4, 6–7). Rostrum and overall cranium shape variation in phytosaurs, on the other hand, is much more greatly affected by differences other than aspect ratio than they are in extant crocodylians. In particular, 75 the range of rostrum shape space occupied by phytosaurs was described less by aspect ratio than was that of longirostrine extant crocodylians. Instead, phytosaur rostrum shape variation was described by much greater differences in the amount and contour of rostral taper than was that of extant longirostrine crocodylians. These findings invalidate covariation of rostrum or overall cranium shape with diet variation in extant crocodylians

(see “Hypothesized Ecology of Phytosauria” in Chapter 1 of this volume) as an appropriate basis for directly inferring diet variation in phytosaurs. Instead, inferences of diet variation in phytosaurs made through comparisons of rostrum or overall cranium shape with extant crocodylians require extrapolation of the ecomorphological trend observed in extant crocodylians in order for it to be applicable to phytosaurs. In this way, phytosaurs may be considered to have occupied the extreme margin of that ecomorphological trend. Based on the results presented here, one such general inference about probable phytosaur diet variation that can be made is that phytosaur diet variation was probably more similar to that of longirostrine extant crocodylians like Gavialis and

Tomistoma than to extant crocodylians within other rostrum morphotype categories.

Furthermore, phytosaurs were probably restricted to utilizing food items that were more extreme versions (i.e. of lower prey:predator size ratios) than those utilized by longirostrine crocodylians. These inferences are probably most applicable to phytosaur genera like Ebrachosuchus and Parasuchus that occupy regions of rostrum shape space closest to those occupied by Gavialis and Tomistoma.

Perhaps the greatest concern with any study of shape such as this one is the accuracy of the specimen images in conveying true specimen shape. The focus on gross shape 76 variation among a very phylogenetically widespread sample in this study probably minimized errors due to inconsistencies in specimen image collection methods (Arbour &

Brown, 2014; Collins & Gazley, 2017). However, future studies of more detailed aspects of the trends reported here should undertake to better standardize the method of specimen image collection. Additionally, further morphometric analyses of shape variation within and between Phytosauria and Crocodylia should consider additional aspects of cranium shape, including lateral profile. As illustrated by the results of the PCAs of rostrum and post-orbital cranial morphology (Figs. 7–8), phytosaur cranial shape variation, as observed in dorsal view, is described by factors that do not describe the majority of such variation in crocodylians. Similarly, phytosaur crania appear to vary in lateral profile in ways and to an extent that those of crocodylians do not. The inclusion of additional dimensions or view angles in future analyses will help to determine whether these apparent difference in variation between Phytosauria and Crocodylia are significant and what, if any, relationship they have to aspects of ecology like diet variation.

77

CHAPTER 3: COMPARATIVE CRANIAL MYOLOGY OF PHYTOSAURS AND

EXTANT CROCODYLIANS

Introduction

The skull is a major anatomical region that serves as a primary point of interaction between an animal and its environment. One such interaction is feeding, during which the functional morphology of the skull serves as an important link between the fundamental range of feeding behaviors that an animal could possibly perform and the realized behaviors that are performed. The variability of success in these realized feeding behaviors can be a strong selective force, influencing the life history, metabolic physiology, habitat exploitation, ecological role, and other aspects of the physical and behavioral phenotype of an evolutionary lineage (e.g., Owen-Smith, 1988; Chapman &

Reiss, 1999; Schwenk, 2000; Button et al., 2016). Thus, a better understanding of feeding behaviors in extinct taxa can provide data on larger evolutionary patterns, trophic roles and interactions, and coevolutionary processes (Reisz & Sues, 2000; Barret & Rayfield,

2006; Lautenschlager, 2013; Barrett, 2014; Button et al., 2016).

Cranial musculature, particularly the jaw adductors, directly affect feeding behaviors by allowing particular jaw motions, bite forces, rates of jaw adduction, and so on (e.g., Schwenk, 2000; Button et al., 2006; Sellers et al., 2017). Muscles rarely preserve as fossils (Kellner, 1996; Briggs et al., 1997), leaving myological data for extinct taxa almost entirely dependent on reconstructions. Muscle reconstructions have a long history in the literature on extinct taxa (e.g., Lull, 1908; Adams, 1919; Anderson, 1936; Haas,

1955; Ostrom, 1961), and this is still a major area of study for better constraining and 78 inferring the feeding behaviors, diets, and evolution of such taxa (e.g., Holliday, 2009;

Lautenschlager, 2013; Button et al., 2016; Nabavizadeh, 2016). Myological reconstructions of extinct taxa typically utilize muscle scars and processes on bones associated with specific muscles, as determined by comparisons to dissections of extant taxa, to estimate the location, size, and organization of muscle origins and insertions

(e.g., Galton, 1974; Holliday, 2009; Lautenschlager, 2013; Button et al., 2016;

Nabavizadeh, 2016). Most modern soft-tissue reconstructions, including those of myology, use the principle of parsimony to infer muscle data for extinct taxa based on comparisons with observable muscle data for extant taxa that phylogenetically bracket the extinct taxon of interest (Bryant & Russell, 1992; Witmer, 1995).

Phytosauria is an extremely important study clade because of its phylogenetic position as the outgroup to all other Crurotarsi, whether that includes all of Archosauria

(Nesbitt, 2011) or all non-phytosaurian Pseudosuchia (Ezcurra, 2016). A greater knowledge of phytosaur ecology, including feeding behaviors and trophic interactions, thus promises to further our understanding of the evolution of an incredibly diverse and long-lived clade. However, phytosaurs have only once been the subject of a myological reconstruction, when Anderson (1936) reconstructed the cranial musculature of an exemplar phytosaur genus based on material of at least three species that were, at the time, considered congeneric but which are currently considered paraphyletic (Stocker &

Butler, 2013; Kammerer et al., 2016).

Previous inferences about phytosaur feeding behaviors have been made on the basis of qualitative comparisons to extant crocodylians with a superficially similar overall 79 morphology (e.g., Hunt, 1989; Hungerbühler, 2002). However, much remains unknown about the diversity and variability of cranial musculature in extant crocodylians, as only a very small number of species have been thoroughly investigated in a systematic, comparative framework. Those species for which thorough anatomical descriptions of jaw musculature are available are: Alligator mississippiensis (e.g., Adams, 1919;

Anderson, 1936; Poglayen-Neuwall, 1953b; Iordansky, 1964; Schumacher, 1973;

Holliday & Witmer, 2007; Holliday et al., 2013); Caiman crocodilus (Lubosch, 1914;

Iordansky, 1964; Lubosch, 1933; Poglayen-Neuwall, 1953b; Schumacher, 1973;

Schumacher, 1985; Cleuren & De Vree, 1992, 2000; Holliday & Witmer, 2007), Caiman crocodilus apaporiensis (Schumacher, 1973); Caiman yacare (van Drongelen &

Dullemeijer, 1982); Caiman latirostris (Bona & Desojo, 2011); Gavialis gangeticus and

Tomistoma schlegelii (Endo et al., 2002); Crocodylus niloticus (Iordansky, 1964);

Crocodilus rhombifer (Schumacher, 1973); and Crocodylus porosus (Lubosch, 1914;

Poglayen-Neuwall, 1953b; Lubosch, 1933; Iordansky, 1964). Although the jaw musculature of ten of the approximately twenty-four extant species of Crocodylia has thus been studied, many studies directly investigated only a single species and made cursory comparisons with data available from other taxa. Most studies that focused on multiple species or genera have done so by making qualitative comparisons of the topology and innervation of individual muscles and muscle groups. No quantitative comparison of cranial musculature exists for extant crocodylians. Thus, existing inferences about the feeding behaviors of phytosaurs, based on properties of jaw musculature, are based on qualitative anatomical comparisons that are themselves based 80 on partial sampling and qualitative comparisons between fewer than half of the extant crocodylian taxa. A true understanding of the functional aspects of feeding in both

Phytosauria and extant Crocodylia cannot be achieved without the benefit of an adequate appreciation for the variability of the anatomy functioning to perform such behaviors in either group.

The present study investigates the range of variability in jaw muscle attachment sites, in terms of location, shape, and surface area, in extant crocodylians and phytosaurs.

It is here hypothesized that: (1) the topology of phytosaur jaw muscle attachments is consistent with that of extant crocodylians, (2) the size proportions of phytosaur jaw muscle origin and insertion surface areas are more similar to one another than they are to those of extant crocodylians, (3) extant crocodylians exhibit trends in origin and insertion surface area size proportions that are correlated with aspect ratio of the rostrum, (4) phytosaurs all exhibit similar origin and insertion surface area size proportions because those sampled here exhibit similar rostrum aspect ratios (see “Results” in Chapter 2 of this volume), (5) the size proportions of phytosaur jaw muscle origin and insertion surface areas are more similar to those of crocodylians with high rostrum aspect ratios than those with lower ratios, (6) the proportions of individual muscle forces in phytosaur jaw muscles are more similar to one another than they are to those of extant crocodylians,

(7) variation in the proportions of individual muscle forces in crocodylian jaw muscles is correlated with rostrum aspect ratios in those taxa, (8) phytosaurs do not exhibit trends in proportions of individual muscle forces that are correlated with aspect ratio of the rostrum, and (9) the proportions of individual muscle forces in phytosaur jaw muscles are 81 more similar to those of crocodylians with high rostrum aspect ratios than those with lower ratios. This study will provide a better understanding of the anatomical and functional morphological bases of feeding behavior variation in extant crocodylians and quantitatively test hypotheses of similarity of such behaviors in phytosaurs.

Anatomical Abbreviations

ptf, post-temporal fenestra; pof, pteroccipital fenestra; qf, quadrate foramen; ptpq, pterygoid process of the quadrate; stf, supratemporal fenestra; ce, coronoid eminence; qfa, quadrate facet of the articular; rap, retroarticular process; emf, external mandibular fenestra; itf, infratemporal fenestra; orb, orbit; sqf, squamosal fossa; opsq, opisthotic process of the squamosal; imDMs, insertion area of m. depressor mandibulae superficialis; imDMp, insertion area of m. depressor mandibulae profundus; CN V, trigeminal (CN V) foramen; ept, epipterygoid; suof, suborbital foramen; cho, internal choana; sutf, subtemporal foramen; ect, ectopterygoid; pt, pterygoid; pal, palatine; sopsq, subsidiary opisthotic process of the squamosal; cpsq, caudal process of the squamosal

Materials and Methods

Taxon Sampling

Four phytosaur and four extant crocodylian specimens were selected for cranial myological reconstruction (Fig. 11). Phytosaur specimens were sampled on the basis of being well-preserved individuals of taxa with a broad phylogenetic distribution and a broad range of rostrum and overall cranium shape (see Chapter 2 of this volume). Extant crocodylian specimens were sampled on the basis of broad phylogenetic distribution 82

Figure 11. Specimen models used for cranial myological reconstructions. Specimen models upon which cranial myological reconstructions were based in (A–D, I– L) dorsal and (E–H, M–P) left lateral views. Specimen models represent the extant crocodylian taxa (A, E) Gavialis gangeticus (UF 118998), (B, F) Tomistoma shlegelii (TMM M-6342), (C, G) Mecistops cataphractus (TMM M-3529), and (D, H) Alligator mississippiensis (OUVC 09640) and the phytosaurian taxa (I, M) Parasuchus angustifrons (BSPG 1931 X 502), (J, N) Ebrachosuchus neukami (BSPG 1931 X 501), (K, O) Pravusuchus hortus (UMNH VP 28293), and (L, P) Machaeroprosopus pristinus (PEFO 382). Scale bars equal 10 cm.

83 among taxa with the greatest rostrum and overall cranium shape similarity to the sampled phytosaurs (see Chapter 2 of this volume), with additional specimens of dissimilar taxa selected as a control. The sample comprised: the phytosaurs Parasuchus angustifrons

(BSPG 1931 X 502), Ebrachosuchus neukami (BSPG 1931 X 501), Pravusuchus hortus

(UMNH VP 28293), and Machaeroprosopus pristinus (PEFO 382); and the extant crocodylians Gavialis gangeticus (UF 118998), Tomistoma shlegelii (TMM M-6342),

Mecistops cataphractus (TMM M-3529), and Alligator mississippiensis (OUVC 09640).

Crania of phytosaur taxa for which suitable mandibular material is not known were modeled with mandibles of congeners or closely related, morphologically similar taxa

(Table 4) in order to approximate the sizes and locations of muscle insertions. In such cases, mandibular models were scaled and deformed to match the dimensions and morphology of the cranium, primarily using alignment of the tooth rows, jaw joints, and relative length of the coronoid process to the jugal/quadratojugal bar as alignment landmarks.

Specimens were CT scanned at different facilities and different scan resolutions

(Table 4). Stacked CT images were manually processed using Avizo 7.0 (Visualization

Sciences Group, SAS, Merignac, France), wherein a surface model of each specimen was created using the grayscale value threshold tool; material representing matrix was excluded from the model and breaks and cracks were virtually filled using segmentation editor tools. Morphological features not preserved in individual specimens, such as portions of the palatine of Ebrachosuchus neukami (BSPG 1931 X 501), were reconstructed by either mirroring features preserved on one side onto the side lacking 84 preservation or using other specimens with intact skeletal anatomy, such as the preserved palatine of Parasuchus angustifrons (BSPG 1931 X 502), as a guide for the morphology of the reconstructed feature. Surfaces were smoothed and rendered in Avizo 7.0 and exported as .obj files that were then imported to Maya 2018 (Autodesk, Inc., San Rafael,

Table 4. Specimens included in muscle reconstruction analyses. Specimens representing each taxon included in this analysis and the parameters of CT scan data acquired for each specimen.

85

CA, USA). Using the sculpt geometry tool and lattice deform in Maya 2018, surface models were deformed to correct effects of taphonomy and better reflect the morphology typical of other (i.e., non-distorted) phytosaur specimens, specifically using conspecifics or congeners, when available. Surface models were bisected along the sagittal midline and the better preserved half was reflected across the sagittal midline using the mirror tool to create bilaterally symmetrical models to be used for later analysis (Fig. 11).

Specimens of phytosaurs belonging to several taxa preserve epipterygoids (e.g.,

Hungerbühler, 2002; Stocker & Butler, 2013; Butler et al., 2014), making it reasonable to infer that all phytosaurs possessed them. However, specimens of two of the phytosaur taxa sampled for this study (P. hortus and M. pristinus) did not preserve an epipterygoid, presumably the result of differential preservation, rather than a natural lack of that element. Epipterygoid morphology for each of these specimens was approximated by isolating the epipterygoid and surrounding bone from the specimen model of

Ebrachosuchus neukami (BSPG 1931 X 501) and deforming that isolated region in Maya

2018 to match the dimensions of the reconstructed target specimen model not preserving an epipterygoid. The overlapping regions from each target model were deleted in

Geomagic Studio (Geomagic Inc., Research Triangle Park, NC, USA) and the two materials were combined. The bridge tool in Geomagic Studio was used to interpolate a three-dimensional structure filling the gap between the two surfaces. The resulting model was again reflected across the sagittal midline in order to retain specimen model bilateral symmetry. 86

Muscle Attachment Site Identification

Anatomical data on phytosaurs were analyzed within the framework of the Extant

Phylogenetic Bracket approach (Bryant & Russell, 1992; Witmer, 1995; Witmer, 1998).

Muscle origin and insertion sites were identified based on comparative data derived from the dissection of a juvenile Alligator mississippiensis specimen, performed by WLH; examination of iodine-contrast-enhanced CT scan data of preserved specimens of extant crocodylians; and a review of literature on both extant (e.g., Anderson, 1936; Merz, 1963;

Iordansky, 1964; Haas, 1973; Bock, 1985; Iordansky, 2000; Endo et al., 2002; Holliday

& Witmer, 2007; Holliday, 2009; Jones et al., 2009; Sereno et al., 2009; Jones et al.,

2012; Gröning et al., 2013; Holliday et al., 2013; Johnston, 2014; Previatto & Posso,

2015; Sellers et al., 2017) and extinct (e.g., Anderson, 1936; Holliday, 2009; Sereno et al., 2009; Button et al., 2016) archosaur, lepidosaur, and testudine cranial musculature.

Reconstructions and analyses of the focal taxa specimens reported here were performed within the context of this reviewed body of literature, rather than performing additional reconstructions and analyses of all phylogenetically bracketing taxa, such as avians and non-archosauromorph sauropsids. In particular, the muscle reconstructions described here are intended to serve as extensions of the work of Holliday (2009).

Individual muscle attachment sites were identified for each muscle, on each specimen, based on general cranial topography, osteological correlates, and obvious surface features (e.g., muscle scars, depressions or fossae, ridges, crests, tuberosities, and other bony landmarks) (Fig. 12). Study specimens of extant crocodylian taxa, were treated the same as the phytosaur specimens in the sense that they were dry skulls and 87

Figure 12. Examples of identified jaw muscle attachment sites. The caudal process of the left squamosal of Machaeroprosopus pristinus (MU 525) in (A) ventromedial and (B) ventral views, illustrating the origin areas of m. adductor mandibulae externus medialis in the squamosal fossa (sqf) and m. depressor mandibulae profundus on the opisthotic process of the squamosal (opsq). The caudal processes of the (C) left and (D) right squamosals of UMNH VP.25564 in caudomedial and lateral views, respectively. The left retroarticular process of TMM M-31173-83 in dorsocaudal view, illustrating the insertion areas of mm. depressor mandibulae superficialis (imDMs) and profundus (imDMp), separated by a strong ridge. The right retroarticular process of Parasuchus bransoni (TMM M-31100-101) in dorsocaudal and dorsocaudomedial views, respectively.

88 muscle reconstructions were inferred from identification of osteological correlates, rather than based on dissections or other soft-tissue observations for those specific specimens.

In cases where muscle attachment sites could not be clearly identified, either due to a lack of distinct osteological landmarks or because of the presence of matrix on the specimen that obscured a given region where a specific muscle attachment would likely be found, areas of attachment were inferred based on the variation in that muscle attachment site for other specimens. An example of this is the boundary of the origin of m. pterygoideus dorsalis (mPTd), which is ambiguous in many of the phytosaur specimens because the dorsal aspect of the palatine is rarely free of matrix in specimens preserving enough of the palatine to demonstrate that boundary. Additionally, in many extant taxa, part of the origin of mPTd is on soft-tissue structures (Holliday et al., 2013) that are not preserved in the phytosaur fossils. In this specific case of mPTd, the morphology of the matrix-free surface model, specifically a depression on the dorsal surface on the pterygoid that is consistent across phytosaur specimens, was used to infer the origin boundary. In other cases, the location and extent of one or more clearly identified muscle attachment areas were used to constrain the location and area of an adjacent muscle attachment. Examples of this are the insertions of m. adductor mandibulae externus medialis (mAMEM), m. pseudotemporalis superficialis (mPSTs), and m. pseudotemporalis profundus (mPSTp), which are difficult to distinguish due to a lack of specific associated osteological morphology but are broadly constrained by the better defined insertions of m. adductor mandibulae externus superficialis (mAMES) and m. adductor mandibular externus profundus (mAMEP). These considerations were used to assign levels of inference to 89 muscle origin and insertion reconstructions, following criteria of Witmer (1995). Levels of inference were reported for both phytosaurian and crocodylian specimens, based on identification of landmarks for muscle attachments. Although such levels of inference are not strictly necessary or relevant for extant taxa for which musculature can be directly observed through means such as dissection of additional specimens, they are reported here in order to provide comparisons of the clarity of muscle attachments in each clade.

The presence of a structure like the cartilago transiliens is not known in phytosaurs, which potentially impacts the accuracy of reconstructions and analyses of those muscles that are associated with the cartilago transiliens in extant crocodylians, particularly mPSTs and m. intermandibularis (Tsai & Holliday, 2011). The lack of data on such a structure in phytosaurs also inhibits accurate reconstruction of the m. intermandibularis (mI). There is a region of potential mI insertion in phytosaurs that is similar in location and appearance to that in extant crocodylians (Holliday, 2009;

Holliday et al., 2013). However, the distinction between such an insertion of mI and the insertion of m. adductor mandibulae profundus (mAMP) is difficult to determine because there is no feature present to mark the boundary between those two muscle insertions. For these reasons, mI was not reconstructed in phytosaurs, and the area of potential mI insertion was included within the area of mAMP insertion. In order to keep the analyses of each clade as comparable to one another as possible, the omission of mI and expansion of the mAMP insertion area to include that of mI was also performed in the reconstructions of the crocodylian jaw muscles. This approach likely affected the 90 contributions of mAMP and mPSTs to analysis results, but the consistency of its application across all taxa likely minimized any resulting bias.

Three-dimensional Muscle Reconstructions

Faces corresponding to identified muscle attachments areas were selected on the specimen surface models using Geomagic Studio. Surface faces in each selected area were duplicated, creating separate materials for the attachment sites. Materials representing origins and insertions for each muscle were combined into a single object, and the bridge tool was used to interpolate a three-dimensional structure between the two plates. The resulting three-dimensional muscle objects were analyzed to ensure that they did not collide with the surface of the modeled skull between the origin and insertion plates. If no collisions or collisions involving only a few faces were found, the attachment plates were accepted. If a surface collision involved several faces, the attachment sites were reevaluated and adjusted to minimize the need for the modeled muscle to wrap around a bone or another muscle in order to span the distance between origin and insertion, as such morphology is uncommon in archosauromorph jaw muscles, with the notable exception of mPTv.

Comparative Analyses

In addition to comparing the general topology of muscle attachments among specimens, comparisons were made between both the surface areas of muscle attachments and the estimated force of muscular contraction of individual muscles. In order to compare raw measurements of muscles across specimens, those specimens must first be scaled to a constant size. The notable differences in cranium morphology between 91 phytosaurs and extant crocodylians preclude scaling criteria including: cranial or cranium roof width, because the generally taller crania of phytosaurs result in a greater overall size per unit of such width in phytosaurs than crocodylians; surface area or volume, because differences in anatomy, such as the presence of a bony-bounded airway within the length of the rostrum possessed by crocodylians but not by phytosaurs, and rostral shape differences among all of the taxa create surface area and volume differences between taxa that have little to do with specimen size; and other clear metrics of linear or quantifiable scaling factors that could be considered repeatable. Due to the lack of an adequate way of standardizing specimen size, comparing raw measurements of muscles across specimens is not an appropriate analytical approach. Instead, for each specimen, the surface area of each muscle origin and insertion was recorded, and from those data, the percent contribution of the origin and insertion of each muscle to the total origin and insertion surface area, respectively, was calculated. These percentages were then compared across specimens to assess the relative contribution of the attachment area of each muscle to the total specimen surface area dedicated to jaw muscle attachments across taxa.

The force of muscular contraction of each jaw muscle was estimated for all specimens, due to the lack of availability of direct measurements of individual muscle forces for any of the sampled specimens. Muscle contraction force calculations require the muscle volume to be known. Because the specimen sample comprised fossil and skeletonized skulls, muscle volume could not be directly measured. Instead, muscle volume was estimated by applying the equation for calculating the volume of a frustum, a 92 cone with its apex cut off parallel to its base, to each muscle (Sellers et al., 2017).

Equation 1 defines the volume of a frustumic muscle:

푙 푉 = M · (퐴 + 퐴 + √퐴 · 퐴 ) M 3 or ins or ins , (1) where lM is the muscle length, Aor is the surface area of the muscle origin, and Ains is the surface area of the muscle insertion (Sellers et al., 2017). Muscles generate force in proportion to their physiological cross-sectional area (PCSA), a function of muscle volume, fiber length, and pennation (Gans, 1982). Thus, to estimate the force of muscular contraction, PCSA was estimated for each muscle, as defined in Equation 2 (Sacks &

Roy, 1982):

푉M PCSA = · cos(θ), (2) 푙f where VM is the muscle volume, lM is the fiber length of the muscle (in terms of fractions of total muscle length), and θ is the angle of pennation. At present, fiber length and pennation angle cannot be known for phytosaur jaw muscles, and of all extant crocodylian taxa, only Alligator mississippiensis has been adequately studied in this respect. Thus, fiber length and pennation data derived from Alligator mississippiensis

(Porro et al., 2011) were used for these values across all sampled taxa. The ratio between

PCSA and force production is specific tension, as defined in Equation 3:

퐹M = PCSA · 푇specific, (3) where FM is the muscle force and Tspecific is the specific tension. Specific tension data derived from Alligator mississippiensis (Porro et al., 2011) were applied across all sampled taxa. The calculated force of each muscle was recorded and used to calculate the percent contribution to the total combined force of all muscles for each specimen. These 93 percentages were then compared across specimens to determine the relative contribution of each muscle to total muscle force across taxa. Direct comparisons, across specimens, of percent contributions of muscle origin surface areas, insertion surface areas, and forces were performed.

Principal Components Analyses

Both PCAs and phylogenetic PCAs (PPCAs) of percent contributions of both muscle attachment areas and muscle forces were performed to determine which characteristics separated the sampled taxa in tangent space. PCAs and PPCAs were performed on each of three sets of muscle data. The first dataset comprised data on all of the described jaw muscles; the second, data on all of the described jaw muscles, excluding depressor mandibulae (mDM); and the third, data on all of the described jaw muscles, excluding depressor mandibulae and pseudotemporalis profundus (mPSTp).

Data were subsampled in this way because although the action of depressor mandibulae contributes to total bite force (Sellers et al., 2017), it is not, by definition, a jaw adductor, and thus, its inclusion with the other described jaw muscles could potentially give rise to misleading results. The very small size and percent force contribution of mPSTp can be reasonably expected to translate into very little action contributing to feeding behaviors that rely on jaw adduction. The results of each PCA of data incorporating mPSTp included a contribution of mPSTp to the PC axes that was seemingly greater than its presumed contribution to feeding behaviors. Analyses of dataset subsamples were performed in order to assess whether or not the inclusion of mDM and mPSTp substantially altered the results. The two muscle bellies of mDM in phytosaurs, mDM 94 superficialis and mDM profundus, were combined for analyses so they could be compared as a group to the singular mDM muscle belly of crocodylians. The calculated

PCSA of pterygoideus dorsalis underestimates the actual cross-section of this muscle in

Alligator mississippiensis, when based on the surface area of the bony part of its origin

(pers. obs.). For the quantitative analyses performed here, a region on the dorsal aspect of pterygoid, bounded by a faint ridge indicating the margins of the muscle belly, was included in the origin surface area of pterygoideus dorsalis.

Results

Muscle Topology

Nearly all of the fossae, crests, tuberosities, and other osteological features that are known to correlate with specific muscle origins and insertions in extant crocodylians could be identified in each of the skeletonized crocodylian specimens and phytosaur. The exact boundaries between some muscles in a few specimens, including those delimiting the origins of m. adductor mandibulae externus medialis (mAMEM) from m. adductor mandibulae externus profundus (mAMEP), were sometimes unclear. However, the consistent location of those attachments across taxa, similarities in the proximities of origins and the those of the corresponding insertions for such muscle pairs, and the general similarity in function of those muscle pairs likely means that the impact of minute inaccuracies of the exact borders between muscles with ambiguous shared borders on subsequent functional analyses is minimal. By and large, however, the borders of muscle attachments were clearly defined and not shared by multiple muscles. For some muscles, phytosaurs exhibited anatomical features clearly related to muscular attachments that are 95 not seen in other taxa but consistent among Phytosauria. An example of this is the sharply delimited fossa (Figs. 11A–C, 14D–E) for the origin of (mAMEM) that is most easily observed in phytosaurs including Pravusuchus hortus and Machaeroprosopus pristinus but not known in taxa within the comparative extant sample. Phytosaurs also possess an epipterygoid, which clearly served as the cranial attachment of m. pseudotemporalis profundus (mPSTp), unlike extant crocodylians which evolutionarily lost that skeletal element, shifting the origin of mPSTp to the lateral bridge of the laterosphenoid.

Examples such as these make scoring osteological correlates of muscles, in terms of levels of inference, as a means of character mapping an extremely complicated and highly subjective procedure. The inclusion of those inference levels is therefore reported here as a general guide rather than a meaningful metric of validity.

With the exception of the m. depressor mandibulae (mDM) group, all of the jaw muscles described here were divided into groups based on their topological relationships with branches of the trigeminal nerve (CN V). These muscle groups comprise the mm. adductor mandibulae externus, posterior, and internus. These groups are further divided into muscle bellies, which comprise: m. adductor externus superficialis (mAMES), mAMEM, and mAMEP within m. adductor mandibulae externus and m. pseudotemporalis superficialis (mPSTs), mPSTp, m. pterygoideus dorsalis (mPTd), and m. pterygoideus ventralis (mPTv) within m. adductor mandibulae internus. The topological relationships of these groups and their constituents remain largely constant throughout the comparative sample, adding confidence in the identifications of their approximate locations in Phytosauria. With a few exceptions, such as extant 96 crocodylians, attachments for the muscle bellies described here also maintain their topological relationship with other soft tissues throughout the comparative sample. Thus, even if the margin of a muscle attachment was unclear due to lack of a well-defined osteological correlate, the position of other features, such as the foramen for CN V and the groove for the stapedial artery (aST) were used to make reasonable inferences of the attachment location and margins of that muscle. The organization of the topological descriptions that follow will be such that descriptions of the muscles identified here will be grouped according to topological relationships with branches of the trigeminal nerve.

Under each of those headings, the name of each muscle will be given, followed by its abbreviation and general levels of inference for its origin and insertion in the format:

Muscle name (muscle name abbreviation–origin inference level/insertion inference level). Table 5 summarizes this information, along with the general attachments of each muscle, across all specimens. Each of the following descriptions only applies to the specimens included in this study.

Mm. adductor mandibulae externus—.

M. adductor mandibulae externus superficialis (mAMES–I/I). In extant crocodylians, mAMES originates on the ventral surface of the quadrate and is separated from m. adductor mandibulae posterior by a rostroventrally oriented ridge that it shares with that muscle origin. This origin location is also the condition in phytosaurs, though the aforementioned ridge is less obvious in some specimens, likely due to taphonomic effects (Fig. 13). In neither clade is the origin of mAMES within the supratemporal fenestra. The insertion of mAMES in crocodylians is a smooth region on the dorsal 97

Table 5. Overview of reconstructed jaw muscle attachment locations. Jaw muscles described in this study, along with the location and general level of inference of each muscle attachment in extant crocodylians and phytosaurs. In phytosaurs, m. depressor mandibulae is divided into two muscle bellies. 98

Figure 13. Origin of mAMES in phytosaurs. (A) Location of the origin attachment area of mAMES, in blue, on the cranium of Machaeroprosopus pristinus (PEFO 382), rendered transparent. Close-ups of the same attachment area, in rostral view, on the crania of (B) Parasuchus, (C) Ebrachosuchus, (D) Pravusuchus, and (E) Machaeroprosopus, with more rostral portions of the cranium cut away. 99 surface of the surangular bounded rostrally by the coronoid eminence left by mAMEP. In phytosaurs, the insertion is a very large, smooth area on the dorsolateral surface of the surangular that is bounded laterally and medially by weak ridges, the latter of which is shared with mAMEM (Fig. 14). Both origin and insertion reconstructions of mAMES are

Level I inferences in all sampled taxa.

M. adductor mandibulae externus medialis (mAMEM–I/I′). The origin of mAMEM in extant crocodylians is a smooth region of the quadrate between the foramen for CN V and the origins of mAMES and mAMEP. In this position, it is excluded from the supratemporal fenestra. This is unlike the condition in phytosaurs. In leptosuchosauromorph phytosaurs, the parietal exhibits a large, caudal process that projects beyond the dorsocaudal margin of the cranium (see Chapter 2 of this volume). In those taxa, the ventromedial surface of the caudal process of the squamosal is almost entirely occupied by a deep fossa with a smooth texture and sharply angle edges that approximates the shape of the process. The origin of mAMES in all phytosaurs is a smooth area on the lateral portion of the dorsal aspect of the posttemporal bar, along the caudal surface of the supratemporal fenestra (Fig. 15). In phytosaur taxa that exhibit a projecting caudal processes of the squamosal, the origin of mAMEM extends onto the medial aspect of the squamosal and terminates caudally within the aforementioned fossa in its ventromedial aspect. The insertion of mAMEM is poorly defined in all taxa but it is generally bounded laterally by mAMES and rostrally by the coronoid eminence left by mAMEP (Fig. 14). This arrangement is slightly easier to determine in phytosaurs because of the presence in some specimens of a weak ridge that marks the boundary between the 100

Figure 14. Insertions of mAMES, mAMEM, mAMEP, and mAMP in phytosaurs. (A) Locations of the insertion attachment areas of mAMES (blue), mAMEM (teal), mAMEP (lavender), and mAMP (green) on the mandible of Parasuchus bransoni (TMM M-31100-419), rendered transparent. Close-ups of the same attachment areas in (B) lateral, (C) dorsomedial, (D) dorsolateral, and (E) rostrolateral (with the surangular removed) views, respectively.

lateral margin of mAMEM and the medial margin of mAMES. Reconstructions of mAMEM origins are Level I inferences in both clades because of the consistency of osteological correlates among lepidosaurs, despite discrepancies in origin position among those taxa and the novel caudal extent of the origin in leptosuchomorph phytosaurs.

Insertion reconstructions are Level I′ inferences because of their reliance on other, better defined muscle insertions to delimit their margins, apart from the weak ridge marking the lateral margin in phytosaurs.

M. adductor mandibulae externus profundus (mAMEP–I/I). The deepest and 101

Figure 15. Origin of mAMEM in phytosaurs. (A) Location of the origin attachment area of mAMEM, in teal, on the cranium of Machaeroprosopus pristinus (PEFO 382), rendered transparent. Close-ups of the same attachment area, in rostrodorsomedial view, on the crania of (B) Parasuchus and (C) Ebrachosuchus. Close-ups of the same attachment area, in caudomedial and caudoventromedial view, respectively, on the crania of (D) Pravusuchus, and (E) Machaeroprosopus.

smallest of the three bellies of mm. adductor externus, mAMEP, originates on the caudomedial surface of the supratemporal fenestra in crocodylians and caudal surface of that fenestra in phytosaurs, on the medial portion of the dorsal aspect of the posttemporal 102 bar (Fig. 16). In all taxa, this area is indicated by a smooth surface, and in leptosuchomorph phytosaurs, it is found within a trough that is highly pronounced in mystriosuchinines. The boundaries of this trough clearly indicate demarcations between the origin of mAMEP and those of mAMEM, laterally, and mPSTs, medially. In all taxa, mAMEP inserts on a rugosity on the dorsal surface of the surangular, the coronoid eminence, that is rostral to the insertion of mAMES (Fig. 14). Origin and insertions reconstructions are all Level I inferences.

Mm. adductor mandibulae posterior—.

M. adductor mandibulae posterior (mAMP–I/I). In both crocodylians and phytosaurs, mAMP originates on the lateral surface of the quadrate (Fig. 17). In both clades, the lateral margin is along a ridge shared with the medial margin of mAMES, and the medial extent is no farther medial than the medial terminus of the pterygoid process of the quadrate. The insertion is within the medial mandibular fossa in both clades (Fig.

14). Both the origin and insertion reconstructions are Level I inferences.

Mm. adductor mandibulae internus—.

M. pseudotemporalis superficialis (mPSTs–I/I′-II′). In extant crocodylians, mPSTs originates from the caudolateral surface of the laterosphenoid and is excluded from the supratemporal fenestra. The only exception to this pattern determined here was in

Gavialis, which has a much larger supratemporal fenestra than other extant crocodylians and wherein the origin of mPSTs is along the medial margin of that fenestra. The general crocodylian pattern is unlike the condition in phytosaurs, which is such that mPSTs attaches to a smooth area on the medial surface of the supratemporal fenestra demarcated 103

Figure 16. Origin of mAMEP in phytosaurs. (A) Location of the origin attachment area of mAMEP, in lavender, on the cranium of Machaeroprosopus pristinus (PEFO 382), rendered transparent. Close-ups of the same attachment area, in rostrodorsolateral view, on the crania of (B) Parasuchus, (C) Ebrachosuchus, (D) Pravusuchus, and (E) Machaeroprosopus, with the skull roof and postorbital bar cut away in the latter two.

from the origin of mAMEP by a very weak ridge and/or change in curvature of the supratemporal fenestra margin (Fig. 18). The rostral extent of the origin is bounded by the laterosphenoid buttress in all taxa, and this position is further supported by its relativity to the fenestra for CN V. In some phytosaurs, most notably Ebrachosuchus, the 104

Figure 17. Origin of mAMP in phytosaurs. (A) Location of the origin attachment area of mAMP, in green, on the cranium of Machaeroprosopus pristinus (PEFO 382), rendered transparent. Close-ups of the same attachment area, in rostrolateral view, on the crania of (B) Parasuchus, (C) Ebrachosuchus, (D) Pravusuchus, and (E) Machaeroprosopus, with more rostral portions of the cranium cut away. 105

Figure 18. Origin of mPSTs in phytosaurs. (A) Location of the origin attachment area of mPSTs, in pink, on the cranium of Machaeroprosopus pristinus (PEFO 382), rendered transparent. Close-ups of the same attachment area, in lateral view, on the crania of (B) Parasuchus, (C) Ebrachosuchus, (D) Pravusuchus, and (E) Machaeroprosopus, with more lateral portions of the cranium cut away.

rostral extent of the origin occupies a very well-defined space surrounded on three sides by a U-shaped crest that separates it rostroventrally from the epipterygoid and caudally 106 from an area directly rostral to mAMEP. The insertion of mPSTs is on the rostral portion of the medial mandibular fossa in extant crocodylians. In phytosaurs, mPSTs appears to insert on the medial aspect of the surangular, medial to the coronoid eminence left by mAMEP (Fig. 19). A reasonable alternative insertion in phytosaurs is the rostral portion of the medial mandibular fossa, as in crocodylians. Origin reconstructions of mPSTs are

Level I inferences in all taxa. Reconstructions of mPSTs insertions are Level I′ inferences in crocodylians and Level II′ inferences in phytosaurs because of the discrepancies in insertion location among extant archosaurs and lack of a clear osteological correlate in this clade.

M. pseudotemporalis profundus (mPSTp–I/I′). In phytosaurs, the origin of mPSTp is the lateral surface of the epipterygoid (Fig. 20), and it inserts on the surangular, rostromedially to the coronoid eminence left by mAMEP. The origin of this muscle in crocodylians is a small, clearly-defined fossa in the lateral bridge of the laterosphenoid, but the insertion is unclear. This ambiguity in crocodylians is because mPSTp in that clade frequently merges with those of the medial surfaces of adjacent muscles. For consistency in comparisons with phytosaurs, the insertion of mPSTp in crocodylians has here been inferred as a small region rostral to the insertion of mPSTs and rostromedial to that of mAMEP, as is the case in phytosaurs (Fig. 19). Reconstructions of mPSTp origins are Level I inferences in phytosaurs, because of their possession of an epipterygoid, and in the crocodylian specimens presented here, because of the reasonably well-defined fossa in the laterosphenoid marking their attachment. However, the reliance on 107

Figure 19. Insertions of mPSTs, mPSTp, mPTd, and mPTv in phytosaurs. (A) Locations of the insertion attachment areas of mPSTs (pink), mPSTp (purple), mPTd (orange), and mPTv (red) on the mandible of Parasuchus bransoni (TMM M-31100- 419), rendered transparent. Close-ups of the same attachment areas in (B) dorsomedial, (C) dorsomedial, (D) rostroventromedial, (E) lateral, and (F) ventromedial views, respectively.

108

Figure 20. Origin of mPSTp in phytosaurs. (A) Location of the origin attachment area of mPSTp, in purple, on the cranium of Machaeroprosopus pristinus (PEFO 382), rendered transparent. Close-ups of the same attachment area on the crania of (B) Parasuchus, (C) Ebrachosuchus, (D) Pravusuchus, and (E) Machaeroprosopus, in dorsolateral, lateral, caudolateral, and lateral view, respectively.

109 surrounding muscle insertions to locate and constrain the insertion of mPSTp in all of the taxa causes those inferences to be Level I′.

M. pterygoideus dorsalis (mPTd–I/I). In both clades, mPTd originates on the dorsal aspect of the palatine and on the pterygoid, just rostroventral to the foramen for

CN V (Fig. 21). The pterygoid origin rostroventral to the foramen for CN V is a smooth, very shallow fossa in most specimens. The rostral extent of the palatine origin is somewhat ambiguous but generally appears to be in a recess near the coronal plane of the rostral margin of the antorbital fenestra in phytosaurs and a similarly shaped recess in crocodylians. In crocodylians, there is a very small area for muscle attachment between this recess and the suborbital fenestra. The relative size of the suborbital fenestra in phytosaurs is considerably less than in crocodylians. In Machaeroprosopus, that fenestra is extremely small, and in Pravusuchus, it is almost entirely absent. The caudal extent of the mPTd origin in phytosaurs is therefore not likely the rostral margin of the suborbital fenestra, but rather, a large, steep ridge near the suture between the ectopterygoid and palatine. This ridge creates the appearance of a shallow fossa for nearly the entire dorsal aspect of the palatine in phytosaurs, and it is in this fossa that mPTd originates. In both crocodylians and phytosaurs, mPTd inserts on a smooth area on the medial surface of the articular and retroarticular processes (Fig. 19). Both origin and insertion reconstructions of mPTd are Level I inferences.

M. pterygoideus ventralis (mPTv–I/I). In crocodylians, mPTv originates along the caudoventral edge of the pterygoid as is generally bounded by weak ridges. In phytosaurs, this muscle originates along the caudoventral edge of the ectopterygoid, and 110

Figure 21. Origin of mPTd in phytosaurs. (A) Location of the origin attachment area of mPTd, in orange, on the cranium of Machaeroprosopus pristinus (PEFO 382), rendered transparent. Close-ups of the same attachment area, in dorsal view, on the crania of (B) Parasuchus, (C) Ebrachosuchus, (D) Pravusuchus, and (E) Machaeroprosopus, with more dorsal portions of the cranium cut away.

its boundaries are marked by curvature changes and ridges along the ventral and dorsal aspects of the ectopterygoid (Fig. 22). In non-leptosuchomorph taxa, the rostral extent of this origin on the ventral aspect of the ectopterygoid is quite extensive, and it is decreasingly so in leptosuchomorphs and mystriosuchinines. On the dorsal aspect of the ectopterygoid, the same large, steep ridge that is the caudal boundary for mPTd is the rostral boundary for mPTv. In both crocodylians and phytosaurs, the insertion is on the 111

Figure 22. Origin of mPTv in phytosaurs. (A) Location of the origin attachment area of mPTv, in red, on the cranium of Machaeroprosopus pristinus (PEFO 382), rendered transparent. Close-ups of the same attachment area, in ventrolateral view, on the crania of (B) Parasuchus, (C) Ebrachosuchus, (D) Pravusuchus, and (E) Machaeroprosopus. 112 ventrolateral surface of the retroarticular process and angular in both clades (Fig. 19).

The transition in texture from the smooth fossa of the attachment area to the surrounding bone marks the margins of the insertion. Reconstructions of both origins and insertions are Level I inferences.

Mm. depressor mandibulae—.

M. depressor mandibulae (mDM–I/I-III). The only muscle innervated by the facial nerve (CN VII) that is described here is mDM. The origin of mDM in crocodylians is a smooth area on the caudomedial surface and caudal margin of the squamosal and the caudal margin of the exoccipital. Phytosaurs possess two distinct muscle bellies of mDM, with the origin of one being a fleshy attachment on the caudomedial surface and caudal margin of the squamosal, a similar location as mDM in crocodylians (Fig. 23). The orientation of this origin, relative to the overall axes of the skull, is different in leptosuchomorph phytosaurs, wherein it is on a smooth area on the ventral edge of the caudal process of the squamosal. This origin also extends onto the lateral surface of the squamosal, caudal to the otic notch. The margins of this attachment on the lateral surface of the squamosal are farther rostral and dorsal in Pravusuchus than the two non- leptosuchomorph taxa and farther in those directions in Machaeroprosopus than any of the other phytosaurs. In leptosuchomorph phytosaurs, the ventral boundary of this origin is the crest of the subsidiary opisthotic process of the squamosal, which projects caudoventrally from the caudal process of the squamosal. The origin of the second belly is a highly rugose area on the opisthotic process of the squamosal, which is a ventrally projecting process off the ventral aspect of the caudal process of the squamosal and 113

Figure 23. Origin of mDMs in phytosaurs. (A) Location of the origin attachment area of mDMs, in pink, on the cranium of Machaeroprosopus pristinus (PEFO 382), rendered transparent. Close-ups of the same attachment area on the crania of (B) Parasuchus, in caudolateral view, and (C) Ebrachosuchus, (D) Pravusuchus, and (E) Machaeroprosopus, in caudoventrolateral view.

114 extremely large in leptosuchomorphs (Figs. 11B,D; 24). In crocodylians, mDM inserts on a smooth area on the dorsal surface of the retroarticular process. In phytosaurs, both bellies of mDM insert on the smooth areas on the caudodorsal surface of the retroarticular process (Figs. 11E–G, 25). These two insertions are separated by a pronounced ridge that extends from the caudal margin of the quadrate facet of the articular to the caudal extent of the retroarticular process, with the insertion for the belly originating from the caudal or ventral margin of the squamosal inserting lateral to this ridge and the belly originating from the opisthotic process of the squamosal inserting medial to it. Reconstructions of the origins and insertions of mDM in both clades are Level I inferences, though one of the phytosaur mDM bellies originates from a novel location on the opithotic process that is identified by novel osteological features (e.g., rugosities) that are often correlated with muscle attachments. For that reason, the reconstruction of the origin of that muscle belly, and arguably the reconstruction of the entire muscle belly, is a Level III inference.

Comparative Assessments

Muscle origin and insertion surface areas, and thus muscle forces, varied considerably throughout the sampled taxa, apart from between Parasuchus angustifrons and Ebrachosuchus neukami (Table 6). These results are not unexpected given the relative overall size similarity between those two specimens compared to the great amount of size dissimilarity among the other sampled specimens. Direct comparison of the surface areas of individual muscle origins, represented as proportions of the total surface area of all muscle origins of each specimen, revealed more overall similarity within Phytosauria and within Crocodylia than between any two members of different 115

Figure 24. Origin of mDMp in phytosaurs. (A) Location of the origin attachment area of mDMp, in pink, on the cranium of Machaeroprosopus pristinus (PEFO 382), rendered transparent. Close-ups of the same attachment area, in caudolateral view, on the crania of (B) Parasuchus, (C) Ebrachosuchus, (D) Pravusuchus, and (E) Machaeroprosopus.

clades (Fig. 26). The most notable differences in muscle origin surface area proportions among crocodylians were: greater proportions of mAMEP and mPSTs and a lower proportion of mPTd in Gavialis, a greater proportion of mPTd and a lower proportion of mAMP in Mecistops, and a greater proportion of mAMP and lower proportions of 116

Figure 25. Insertions of mDMs and mDMp in phytosaurs. (A) Locations of the insertion attachment areas of mDMs (dark pink) and mDMp (light pink) on the mandible of Parasuchus bransoni (TMM M-31100-419), rendered transparent. Close-ups of the same attachment areas in (B) caudodorsal and (C) caudodorsomedial views, respectively.

mAMES and mDM in Alligator. Among phytosaurs, the most notable differences were: a greater proportion of mPTv in Parasuchus, a lower proportion of mAMES and mAMEP in Pravusuchus, lower proportions of mAMP and mDMp in Machaeroprosopus, and greater proportions of mAMEM and the mDMs in both Pravusuchus and

Machaeropropus. Excluding the largest and smallest origin area of each muscle in the sample, some differences between phytosaurs and crocodylians are apparent. In general, surface area size proportions of the origins of mPTv and the mDM group were considerably larger in phytosaurs than crocodylians and mAMES and mPTd were larger 117 in crocodylians. The origin area proportion of mAMES varied more in phytosaurs, and mAMP varied more in crocodylians. In general, mAMEM, mAMEP, mPSTs, and mPSTp origin areas were consistent throughout the sample.

Direct comparison of the surface areas of individual muscle insertions, as proportions of the total surface area of all muscle insertions of each specimen, demonstrated more overall similarity within Phytosauria, apart from M. pristinus, and

Table 6. Individual jaw muscle metrics. Origin surface areas, insertion surface areas, and maximum forces of individual jaw muscles and the percent contribution of each to the total for each category in each of the sampled taxa.

118

Table 6. Continued.

within Crocodylia than between any two members of different clades (Fig. 27). The most notable difference in muscle insertion surface area proportions among crocodylians were: a greater proportion of mPTd and lower proportions of mAMES and mAMP in Gavialis and both a greater proportion of mAMEM and a lower proportion of mDM in Alligator.

Among phytosaurs, the most notable differences were: greater proportions of mAMEM and mDMs in Pravusuchus and both greater proportions of mAMES and mAMP and a 119

Figure 26. Muscle origin surface area proportions. Barplot of the proportion of each jaw muscle origin surface area to the total surface area of all jaw muscle origins, per sampled specimen.

Figure 27. Muscle insertion surface area proportions. Barplot of the proportion of each jaw muscle insertion surface area to the total surface area of all jaw muscle insertions, per sampled specimen. 120 lower proportion of mPTv in Machaeroprosopus. Excluding the largest and smallest insertion area of each muscle in the sample, some differences between phytosaurs and crocodylians are apparent. In general, surface area size proportion of the insertion of mPTv was considerably larger, and that of the mDM group was slightly larger, in crocodylians than phytosaurs, and mAMES was considerably larger in phytosaurs. The insertion area proportion of the mDM group varied more in crocodylians, and both mAMP and mPTv varied more in phytosaurs. In general, mAMEP, mPSTs, and mPSTp insertion areas were consistent throughout the sample.

Comparison of individual muscle forces, as proportions of the total muscle force of each specimen, revealed a great deal of similarity in most individual muscle forces, across all taxa (Fig. 28). Gavialis demonstrated a lower force proportion of mAMES and slightly greater proportion of mPSTs force than other taxa, Mecistops demonstrated a lower force proportion of mAMP and greater proportion of mPTd force than other taxa,

Alligator demonstrated a lower force proportion of the mDM group, Parasuchus demonstrated a slightly greater force proportion of mPTv, and Machaeroprosopus demonstrated both greater proportions of mAMES and mAMP and lower proportions of mPTd and mPTv than other taxa. Both Parasuchus and Ebrachosuchus had lower mAMEM force proportions and slightly greater mAMEP proportions than the rest of the taxa, except for Gavialis. This similarity may be either indicative of other similarities between these taxa or simply the result of somewhat unclear boundaries between the origins and insertions of these two muscle bellies in Parasuchus and Ebrachosuchus, as their combined muscle force approximated that in all of the other taxa. 121

Figure 28. Maximum muscle force proportions. Barplot of the proportion of the estimated muscular force contribution of each jaw muscle to the total muscular force, per sampled specimen.

Principal Components Analyses

Muscle Origin Surface Areas—. Among the results of a PCA conducted on the surface area proportions of all muscle origins was that the first two principal components (PCs) summarized 31.86% and 28.17% of the total variance, respectively (Fig. 29).

Contributions of mAMEM, mAMEP, mAMP, mPSTs, mPSTp, and mPTd to PC1 were similarly low; the contributions of both mAMES and mDM to PC1 were approximately triple those of the low contributions; the contribution of mPTv to PC1 was approximately five times those of the low contributions; the contributions of mAMES, mAMEM, and mPTV to PC2 were negligible; the contributions of mAMP, mPSTp, and mDM to PC2 were similarly low; and the contributions of mAMEP, mPSTs, and mPTd to PC2 were each approximately quintuple that of the low contributions. The overall effect of these 122

Figure 29. PCA and PPCA results of full muscle origin surface area dataset. PCA biplot of taxa and contributions of jaw muscle origin surface area proportions to the first two PC axes in the full muscle dataset (left) and PPCA biplot of taxa and jaw muscle origin surface area proportions in the full muscle dataset (right).

contributions was that mAMES, mAMEM, mPTv, and mDM contributed more to PC1 than PC2, with the contribution of mPTv to PC1 being greater than the contribution of any other muscle to either PC axis; mAMEP and mPTd contributed more to PC2 than

PC1; and mAMEM, mAMP, and mPSTp contributed little to either PC axis. Along PC1, extant crocodylians occupied positive PC score values and phytosaurs, negative ones.

Along PC2, Tomistoma occupied a PC score approximately equal to the sample mean,

Pravusuchus occupied a slightly negative score, Parasuchus and Ebrachosuchus occupied slightly positive scores of similar value, Machaeroprosopus occupied a positive

PC score value approximately one-third that of Gavialis, and Mecistops and Alligator occupied similar negative PC values. The combination of PC scores was such that all of the crocodylians occupied a relatively narrow range of PC1 scores and a very wide range of PC2 scores, whereas all of the phytosaurs occupied relatively narrow score ranges along both PC axis. All of the phytosaurs occupied PC2 score values much closer to the 123 sample mean than any crocodylian, apart from Tomistoma. The two clades occupied discrete regions of tangent space. Results of a PPCA of this dataset included the crocodylians and phytosaurs occupying discrete regions of tangent space (Fig. 29).

Crocodylians occupied negative PC2 scores and a wide range of positive and negative

PC1 scores, and phytosaurs occupied negative PC1 scores and a range of PC2 scores from positive to slightly negative. The relationship and distance between the two clades in tangent space approximate the results of the PCA.

Results of a PCA conducted on the surface area proportions of all muscle origins, excluding the mDM group, included the first two PCs summarizing 33.28% and 29.03% of the total variance, respectively (Fig. 30). The contributions of mAMP and mPSTp to

PC1 were negligible, contributions of mAMEM and mPTd to PC1 were similarly low, contributions of mAMES and mPTv to PC1 were both approximately double the low contributions, and contributions of mAMEP and mPSTs to PC1 were both approximately quadruple the low contributions. The contributions of mAMES, mAMEP, mAMP, and mPSTs to PC2 were similarly low; contributions of mAMEM, mPTd, and mPTv to PC2 were approximately double those low contributions; and the contribution of mPSTp was approximately quadruple those low contributions. The overall effect of these contributions was that mAMES, mAMEP, and mPSTs contributed more to PC1 than

PC2; mAMEM, mAMP, mPSTp, and mPTd contributed more to PC2 than PC1; and mPTv contributed greatly to both PC axes. Along PC1, Gavialis occupied a score value on the extreme negative end of the sample; Tomistoma, Alligator, Mecistops, and

Machaeroprosopus all occupied a relatively narrow range of score values just to either 124

Figure 30. PCA and PPCA results of origin area dataset without mDM. PCA biplot of taxa and contributions of jaw muscle origin surface area proportions to the first two PC axes with the mDM group removed from the full muscle dataset (left) and PPCA biplot of taxa and jaw muscle origin surface area proportions with the mDM group removed from the full muscle dataset (right).

side of the sample mean; and the other phytosaurs occupied a similar positive score values farther from the sample mean. Along PC2, Pravusuchus and Machaeroprosopus occupied score values near the sample mean; Gavialis, Parasuchus, and Ebrachosuchus occupied a narrow range of relatively high positive score values; and Tomistoma,

Mecistops, and Alligator occupied a fairly wide range of negative score values. The combination of PC scores was such that the crocodylians occupied a relatively wide range of scores along both PC axes and the phytosaurs occupied comparatively narrow ranges along both axes. The two clades occupied discrete regions of tangent space.

Results of a PPCA of this dataset included the crocodylians and phytosaurs occupying discrete regions of tangent space (Fig. 30). Crocodylians occupied positive PC2 scores and a wide range of positive and negative PC1 scores, and phytosaurs occupied a range of

PC scores from negative to slightly positive along each axis. The relationship and 125 distance between the two clades in tangent space approximate the results of the PPCA of the full muscle origin dataset.

Among the results of a PCA conducted on the surface area proportions of all muscle origins, excluding mPSTp and the mDM group, was that the first two PCs summarized 38.04% and 27.24% of the total variance, respectively (Fig. 31). The contribution of mAMP to PC1 was negligible, contributions of mAMEM and mPTd to

PC1 were similarly low, contributions of mAMES and mPTv to PC1 were approximately double that of the low contributions, and contributions of mAMEP and mPSTs to PC1 were approximately quadruple that of the low contributions. The contributions of mAMEM, mAMEP, mAMP, and mPSTs to PC2 were similarly low; the contribution of mAMES to PC2 was approximately double the low contributions; and the contributions of mPTd and mPTv to PC2 were approximately quintuple the low contributions. The overall effect of these contributions was that mAMEP and mPSTs contributed more to

PC1 than PC2; mAMP, mPTd, and mPTv contributed more to PC2 than PC1, mAMEM contributed a low amount to both PC axes; and mAMES contributed a moderate amount to both PC axes. Although the positions of taxa in tangent space were different in this analysis from the analysis of the muscle origin dataset that only omitted the mDM group, the relative position and distance between the two clades in tangent space was similar between the two analyses. The PC scores resulting from a PPCA of this dataset were nearly identical to those resulting from the PPCA of the dataset including all muscle origins (Fig. 31). 126

Figure 31. PCA and PPCA results of origin area dataset without mPSTp or mDM. PCA biplot of taxa and contributions of jaw muscle origin surface area proportions to the first two PC axes with mPSTp and the mDM group removed from the full muscle dataset (left) and PPCA biplot of taxa and jaw muscle origin surface area proportions with mPSTp and the mDM group removed from the full muscle dataset (right).

Muscle Insertion Surface Areas—. Among the results of a PCA conducted on the surface area proportions of all muscle insertions was that the first two PCs summarized 53.78% and 31.38% of the total variance, respectively (Fig. 32). The contributions of mAMEM, mAMEP, mPSTs, and mPSTp to PC1 were similarly low and the contributions of mAMES, mAMP, mPTd, mPTv, and mDM to PC1 were approximately quadruple those low contributions. The contributions of mAMES, mPTv, and mDM to PC2 were negligible; the contributions of mAMP and mPTd to PC2 were similarly low; the contributions of mAMEM and mPSTs PC2 were approximately double those low contributions; and the contributions of mAMEM and mPSTp to PC2 were approximately triple and quadruple those low contributions, respectively. The overall effect of these contributions was that mAMES, mAMP, mPTd, mPTv, and mDM contributed more to

PC1 than PC2 and mAMEM, mAMEP, mPSTs, and mPSTp contributed more to PC2 than PC1. Along PC1, extant crocodylians occupied positive PC score values and 127

Figure 32. PCA and PPCA results of full muscle insertion surface area dataset. PCA biplot of taxa and contributions of jaw muscle insertion surface area proportions to the first two PC axes in the full muscle dataset (left) and PPCA biplot of taxa and jaw muscle insertion surface area proportions in the full muscle dataset (right).

phytosaurs, negative ones. Along PC2, Parasuchus and Ebrachosuchus occupied PC scores near the sample mean, Gavialis and Tomistoma occupied similar positive scores,

Mecistops and Alligator occupied similar negative scores that were approximately the same in absolute value as those of Gavialis and Tomistoma, Pravusuchus occupied a negative PC score value approximately double the distance from the sample mean as the score occupied by Alligator, and Machaeroprosopus occupied a positive score approximately double that of Tomistoma. The combination of PC scores was such that all of the crocodylians occupied positive PC1 scores and a range along the PC2 axis from moderately negative to moderately positive scores, whereas the phytosaurs occupied a relatively narrow range of negative PC1 scores and a wide range of PC2 scores. The two clades occupied discrete regions of tangent space. Results of a PPCA of this dataset included the crocodylians and phytosaurs occupying discrete regions of tangent space

(Fig. 32). Crocodylians occupied negative PC1 scores and a wide range of positive and 128 negative PC2 scores, and phytosaurs occupied positive PC1 scores and a narrower range of PC2 scores from positive to slightly negative.

Results of a PCA conducted on the surface area proportions of all muscle insertions, excluding the mDM group, included the first two PCs summarizing 51.69% and 35.16% of the total variance, respectively (Fig. 33). The contributions of mAMEM, mAMEP, mPSTs, and mPSTp to PC1 were similarly low; the contributions of mAMP and mPTd to PC1 were approximately triple those of the low contributions; and the contributions of mAMES and mPTv to PC1 were approximately quadruple those of the low contributions. The contributions of mAMES and mPTv to PC2 were negligible; the contributions of mAMP and mPTd to PC2 were similarly low; the contributions of mAMEM, mAMEP, and mPSTs were approximately double those of the low contributions; and the contribution of mPSTp to PC2 was approximately triple those of the low contributions. The overall effect of these contributions was that mAMES, mAMP, mPTd, and mPTv contributed more to PC1 than PC2 and mAMEM, mAMEP, mPSTs, and mPSTp contributed more to PC2 than PC1. Along PC1, extant crocodylians occupied negative PC score values and phytosaurs, positive ones. Along PC2,

Parasuchus and Ebrachosuchus occupied slightly positive scores near the sample mean,

Pravusuchus occupied a the greatest positive score, Mecistops and Alligator occupied positive scores intermediate between the sample mean and the score value of Mecistops,

Machaeroprosopus occupied a negative score value that was the farthest from the sample mean, and Gavialis and Tomistoma occupied negative scores that were approximately one-third the distance from the sample mean as that of Machaeroprosopus. The 129

Figure 33. PCA and PPCA results of insertion area dataset without mDM. PCA biplot of taxa and contributions of jaw muscle insertion surface area proportions to the first two PC axes with the mDM group removed from the full muscle dataset (left) and PPCA biplot of taxa and jaw muscle insertion surface area proportions with the mDM group removed from the full muscle dataset (right).

combination of PC scores was such that phytosaurs occupied positive PC1 scores and a wide range of positive and negative PC2 scores, whereas crocodylians occupied negative

PC1 scores and a narrower range of positive and negative PC2 scores. The two clades occupied discrete regions of tangent space. Results of a PPCA of this dataset included the crocodylians and phytosaurs occupying discrete regions of tangent space (Fig. 33).

Crocodylians occupied a very narrow range of negative PC1 scores and positive PC2 scores, and phytosaurs occupied a wider range of positive PC1 scores and negative PC2 scores.

Results of a PCA conducted on the surface area proportions of all muscle insertions, excluding mPSTp and the mDM group, included the first two PCs summarizing 58.4% and 29.35% of the total variance, respectively (Fig. 34). The contributions of mAMEM, mAMEP, and mPSTs to PC1 were similarly low and the contributions of mAMES, mAMP, mPTd, and mPTv to PC1 were approximately 130

Figure 34. PCA and PPCA results of insertion area dataset without mPSTp or mDM. PCA biplot of taxa and contributions of jaw muscle insertion surface area proportions to the first two PC axes with mPSTp and the mDM group removed from the full muscle dataset (left) and PPCA biplot of taxa and jaw muscle insertion surface area proportions with mPSTp and the mDM group removed from the full muscle dataset (right).

quadruple those of low contributions. The contributions of mAMES and mPTv to PC2 were negligible, the contributions of mAMP and mPTd to PC2 were similarly low, the contribution of mAMEP to PC2 was approximately double that of those low contributions, and the contributions of mAMEM and mPSTs to PC2 were approximately triple those low contributions. The overall effect of these contributions was that mAMES, mAMP, mPTd, and mPTv contributed more to PC1 than PC2, and mAMEM, mAMEP, and mPSTs contributed more to PC2 than PC1. Although the exact positions of taxa in tangent space were slightly different in this analysis from the analysis of the muscle insertion dataset that only omitted the mDM group, the relative positions of taxa to one another changed very little, and the relative positions of the two clades in tangent space was similar between the two analyses. The PC scores resulting from a PPCA of this dataset were practically identical to those resulting from the PPCA of the insertion dataset that excluded only mDM (Fig. 34). 131

Estimated Muscle Forces—. Results of a PCA conducted on the estimated force proportions of all described jaw muscles included the first two PCs summarizing 43.71% and 20.89% of the total variance, respectively (Fig. 35). The contributions of mAMEM, mAMEP, mPSTs, mPSTp, and mDM to PC1 were similarly low; the contributions of mAMES, mPTd, and mPTv to PC1 were approximately double those of the low contributions; and the contribution of mAMP to PC1 was approximately triple those of the low contributions. The contributions of mAMES, mAMEM, mAMP, mPSTp, and mPTv to PC2 were negligible; the contributions of mAMEP and mPTd to PC2 were similarly moderate; and the contributions of mPSTs and mDM to PC2 were approximately double and triple those moderate contributions, respectively. The overall effect of these contributions was that mAMES, mAMP, and mPTv contributed more to

PC1 than PC2; mAMEP, mPSTs, and mDM contributed more to PC2 than PC1; mAMEM contributed little to either PC axis, and mPTd contributed similarly to both PC axes. Along PC1, nearly all taxa occupied score values near the specimen mean, except for Gavialis, which occupied a high positive score value, and Machaeroprosopus, which occupied a negative score similar in distance from the specimen mean to that of Gavialis.

Along PC2, Tomistoma occupied a score near the specimen mean; Pravusuchus occupied a negative score slightly below the specimen mean; Parasuchus, Ebrachosuchus, and

Mecistops occupied a narrow range of positive score values; Alligator occupied a higher positive score value; and Gavialis and Machaeroprosopus occupied similar negative score values similar in distance from the specimen to that of Alligator. The combination of PC scores was such that the two clades occupied generally different regions of tangent 132

Figure 35. PCA and PPCA results of full maximum muscle force dataset. PCA biplot of taxa and contributions of individual jaw muscle force proportions to the first two PC axes in the full muscle dataset (left) and PPCA biplot of taxa and individual jaw muscle force proportions in the full muscle dataset (right).

space, but the ranges of the clades overlapped a bit within positive PC2 space, near the specimen mean along PC1. Results of a PPCA of this dataset included crocodylians and phytosaurs occupying discrete regions of tangent space (Fig. 35). Crocodylians occupied negative PC1 scores and a wide range of positive and negative PC2 scores, and phytosaurs occupied positive PC1 scores and a narrower range of PC2 scores from moderate positive values to a negative value near the specimen mean. The two clades were slightly separated, though Tomistoma was near the region of tangent space occupied by phytosaurs.

Among the results of a PCA conducted on the force proportions of all described jaw muscles, excluding the mDM group, was that the first two PCs summarized 47.11% and 19.72% of the total variance, respectively (Fig. 36). The contributions of mAMEM, mAMEP, mPSTs, and mPSTp to PC1 were similarly low, and the contributions of mAMES, mAMP, mPTd, and mPTv to PC1 were approximately triple those low 133

Figure 36. PCA and PPCA results of muscle force dataset without mDM. PCA biplot of taxa and contributions of individual jaw muscle force proportions to the first two PC axes with the mDM group removed from the full muscle dataset (left) and PPCA biplot of taxa and individual jaw muscle force proportions with the mDM group removed from the full muscle dataset (right).

contributions. The contributions of mAMP, mPSTs, and mPTv to PC2 were similarly low; the contributions of mAMES, mAMEP, mPSTp, and mPTd to PC2 were approximately triple those low contributions; and the contribution of mAMEM to PC2 was approximately nine times those low contributions. The overall effect of these contributions was that mAMP and mPTv contributed more to PC1 than PC2; mAMEM, mAMEP, and mPSTp contributed more to PC2 than PC1; mPSTs contributed little to either axis; and mAMES and mPTd contributed similarly to both PC axes. Along PC1, nearly all taxa occupied score values near the specimen mean, except for

Machaeroprosopus, which occupied a high positive score value, and Gavialis, which occupied a negative score of slightly less distance from the specimen mean than that of

Machaeroprosopus. Along PC2, Tomistoma occupied a score near the specimen mean;

Pravusuchus, Mecistops, and Alligator occupied a narrow range of positive score values;

Parasuchus and Ebrachosuchus occupied a narrow range of negative score values 134 slightly farther from the sample mean than the Pravusuchus, Mecistops, and Alligator group; and Gavialis and Machaeroprosopus occupied similar negative score values approximately one-third the distance from the sample mean as Parasuchus and

Ebrachosuchus. The combination of PC scores was such that the two clades occupied generally different regions of tangent space, but the ranges of the clades overlapped a bit within positive PC2 space, near the specimen mean along PC1. Results of a PPCA of this dataset included crocodylians and phytosaurs occupying discrete regions of tangent space

(Fig. 36). Although the PC scores of taxa in this analysis were slightly different from those in the full muscle force dataset, their positions in tangent space, relative to one another, remained largely unchanged, and the relative positions of, and distance between, the two clades were very similar to the results of that previous analysis.

Results of a PCA conducted on the force proportions of all described jaw muscles, excluding mPSTp and the mDM group, included the first two PCs summarizing 51.03% and 34.11% of the total variance, respectively (Fig. 37). The contributions of mAMEM, mAMEP, and mPSTs to PC1 were similarly low; the contributions of mPTd and mPTv to

PC1 were approximately double those low contributions; and the contributions of mAMES and mAMP to PC1 were approximately triple those low contributions. The contributions of mAMES, mAMP, mPSTs, and mPTv to PC2 were similarly low; the contribution of mPTd to PC2 was approximately double those low contributions; and the contributions of mAMEM and mAMEP were approximately nine times those low contributions. The overall effect of these contributions was that mAMES, mAMP, and mPTv contributed more to PC1 than PC2; mAMEM and mAMEP contributed more to 135

Figure 37. PCA and PPCA results of muscle force dataset without mPSTp or mDM. PCA biplot of taxa and contributions of individual jaw muscle force proportions to the first two PC axes with mPSTp and the mDM group removed from the full muscle dataset (left) and PPCA biplot of taxa and individual jaw muscle force proportions with mPSTp and the mDM group removed from the full muscle dataset (right).

PC2 than PC1; mPSTs contributed little to either PC axis; and mPTd contributed similarly to both PC axes. Although the exact positions of taxa in tangent space were slightly different in this analysis from the analysis of the muscle force dataset that only omitted the mDM group, the general arrangement of taxa in tangent space was similar between the two analyses, and the relative positions of the two clades in tangent space changed very little. The PC scores resulting from a PPCA of this dataset were practically identical to those resulting from the PPCA of the insertion dataset that excluded only mDM (Fig. 37).

Discussion

In general, the topology of jaw muscle origins and insertions in phytosaurs is similar to that in extant crocodylians (e.g., Anderson, 1936; Iordansky, 1964; Iordansky,

2000; Endo et al., 2002; Holliday, 2009; Holliday et al., 2013; Sellers et al., 2017).

However many of the similarities between these two clades are also shared with avians 136

(Merz, 1963; Bock, 1985; Sereno et al., 2009; Previatto & Posso, 2015), other archosaurs

(Holliday, 2009; Sereno et al., 2009; Button et al., 2016), lepidosaurs (Anderson, 1936;

Haas, 1973; Holliday & Witmer, 2007; Holliday, 2009; Jones et al., 2009; Gröning et al.,

2013; Johnston, 2014), and testudines (Jones et al., 2012), indicating that such similarities are the result of plesiomorphy, rather than convergence. For those origins and insertions that exhibit different topologies in phytosaurs and crocodylians, phytosaurs possess attachment sites very similar to the lepidosaur (Anderson, 1936; Haas, 1973; Holliday &

Witmer, 2007; Holliday, 2009; Jones et al., 2009; Gröning et al., 2013) and testudine conditions (Jones et al., 2012), indicating that such topologies are the plesiomorphic state from which the crocodylian topologies ultimately diverged. In terms of muscle origins, the primary differences between phytosaurs and crocodylians are the locations of mAMEM, mPSTs, and mPTd. In phytosaurs, the origin of mAMEM is lateral to the origin of mAMEP and located along the lateral portion of the caudal margin of the supratemporal fenestra (Fig. 15). This location is similar to that in lepidosaurs (Anderson,

1936; Haas, 1973; Holliday & Witmer, 2007; Jones et al., 2009; Gröning et al., 2013) and unlike the condition in extant crocodylians, wherein the origin of mAMEM is ventrolateral to that of mAMEP and excluded from the margin of the supratemporal fenestra (e.g., Holliday, 2009; Holliday et al., 2013; Sellers et al., 2017). Similarly, the origin of mPSTs is along the medial margin of the supratemporal fenestra in phytosaurs

(Fig. 18), unlike its exclusion from the fenestra in extant crocodylians (e.g., Holliday,

2009; Holliday et al., 2013; Sellers et al., 2017), apart from Gavialis. The location of the mPSTs origin in phytosaurs is similar to its location in lepidosaurs (Anderson, 1936; 137

Haas, 1973; Holliday & Witmer, 2007; Jones et al., 2009; Gröning et al., 2013).

Reconstructing the mPSTs origin within both the confines of a U-shaped crest on the laterosphenoid and a smooth area on the medial surface of the supratemporal fenestra in phytosaurs causes that origin to have a shape that is, particularly in Ebrachosuchus, considerably more sinuous than in other taxa (Fig. 18). A more typical shape of this origin can only be reconstructed if the rostral extent is located caudal to the area within the U-shaped crest, in a location immediately rostromedial to mAMEM. However, such a reconstruction requires the origin to cross a weak ridge separating this alternative rostroventral margin from the supratemporal fenestra. The reconstruction of the phytosaur mPSTs origin presented here represents the most contiguous, but not necessarily the only plausible, topology. Additionally, because phytosaurs possessed an epipterygoid, the origin of mPSTp in that clade is in the plesiomorphic location, on the lateral aspect of the epipterygoid. In extant crocodylians, the origin of mPSTp is located on the laterosphenoid because crocodylians evolutionarily lost the epipterygoid (Holliday

& Witmer, 2009).

The location of the mPTd origin does not differ between phytosaurs and crocodylians in the same way that those of mAMEM and mPSTs do. Instead, the size of the suborbital fenestra is very different between crocodylians, which have very large fenestrae, and phytosaurs, which have considerably smaller fenestrae, and this difference in fenestra size results in a much larger area available for muscle attachment on the dorsal aspect of the phytosaur palatine. The greater palatine surface area of phytosaurs allows for a palatine portion of the origin of mPTd that is more like that of lepidosaurs 138

(Anderson, 1936; Haas, 1973; Jones et al., 2009; Gröning et al., 2013) than crocodylians

(e.g., Holliday, 2009; Holliday et al., 2013; Sellers et al., 2017). The suborbital fenestra also acts as the primary boundary separating the palatine and pterygoid portions of the mPTd origin in extant crocodylians. The boundary separating these portions of the mPTd origin in phytosaurs is considerably less clear as a result of the much smaller suborbital fenestra in that clade.

The origin of mDM differs considerably between phytosaurs and crocodylians.

Phytosaurs, unlike crocodylians or any other sauropsid used for comparison in this study, possess two muscle bellies of mDM. The existence of two bellies of mDM in phytosaurs was previously proposed by Anderson (1936), and that interpretation is supported here.

As Anderson (1936) did not provide nomenclature for the two bellies of mDM in phytosaurs, the belly with the dorsal-most origin is here referred to as m. depressor mandibulae superficialis (mDMs) and the belly with the ventral-most origin, m. depressor mandibulae profundus (mDMp). When these muscles are three-dimensionally reconstructed, mDMs lies superficial to mDMp. Developmental data cannot be used to clarify homology of these muscle bellies between phytosaurs and other sauropsids.

However, general similarities between phytosaurs and other sauropsids, in terms of the location and osteological correlates of the origins, indicate that the phytosaur mDMs and mDM of other taxa are probably homologous, and the phytosaur mDMp is a novel muscle belly. Although the origin of mDM in Gavialis extends into a fossa on the caudal margin of the squamosal, the majority of this origin in all of the extant crocodylians sampled here is on the caudomedial surface of the squamosal. In phytosaurs, the origin of 139 mDMs extends from the medial to lateral aspects of the caudal process of the squamosal.

This lateral extension is particularly pronounced in phytosaurs with large caudal processes of the squamosal like Pravusuchus and Machaeroprosopus. The attachment of this muscle to the lateral face of the squamosal is reminiscent of the condition in testudines, but the origin of mDM does not appear to also extend onto the medial aspect of the squamosal in testudines (Jones et al., 2012).

In terms of jaw muscle insertion topology, phytosaurs appear very similar to extant crocodylians. The primary difference between the two clades results from the difference in morphology of the surangular. In crocodylians, the surangular is a relatively cylindrical bar that exhibits a small area for the insertion of mAMES on its dorsal aspect.

In contrast, the phytosaur surangular is a large plate of bone that is ventrolaterally declined, and provides a much larger area of attachment for mAMES. The relative size and orientation of the insertion of mAMES in phytosaurs is similar to lepidosaurs

(Anderson, 1936; Haas, 1973; Jones et al., 2009; Gröning et al., 2013), turtles (Jones et al., 2012), and avians (Holliday, 2009; Sereno et al., 2009). The insertion of mPSTs in phytosaurs is somewhat ambiguous, and its reconstruction is a Level II inference because of the lack of clear osteological correlates for this insertion and inconsistency in its location among extant archosaurs. Phytosaur mandibular morphology does allow for a mPSTs insertion location similar to those of crocodylians, though an insertion location more similar to squamates and avians (Anderson, 1936; Merz, 1963; Haas, 1973; Bock,

1985; Holliday & Witmer, 2007; Holliday, 2009; Jones et al., 2009; Previatto & Posso,

2015) would also be accommodated by phytosaur mandibular morphology. 140

A few differences exist between the phytosaur jaw muscle topology proposed by

Anderson (1936) and the one presented here. These differences include the topology of the origin of mAMES and of the two mDM muscle bellies. According to Anderson

(1936), the origin of mAMES extended from the rostral surface of the quadrate, where it is reconstructed here, to the lateral surface of the squamosal through a smooth depression in the caudodorsal corner of the infratemporal fenestra. The presence of mAMES origin on the lateral surface of the skull would be extremely unusual, if not novel, for a diapsid with temporal fenestrae morphology resembling that of a phytosaur (Holliday, 2009;

Jones et al., 2009; Holliday et al., 2013; Gröning et al., 2013; Sellers et al., 2017). Such a lateral attachment area also appears to be precluded by the presence of a substantial gap between the clearly identifiable bounds of the mAMES origin on the rostral surface of the quadrate and the caudodorsal margin of the infratemporal fenestra (Fig.12). The smooth depression present in the caudodorsal corner of the infratemporal fenestra in phytosaurs is, instead, interpreted here as either being related to fascia associated with the fenestra, thus far unidentified neurovascular structures, or both.

Two muscle bellies of mDM in phytosaurs were reconstructed by Anderson

(1936). The primary differences between the reconstructions of the mDM muscle bellies by Anderson (1936) and those presented here are the locations of the insertion of each muscle belly. Anderson (1936) proposed that what is here termed mDMs had a fleshy origin attachment and a tendinous insertion on the caudal terminus of the retroarticular process. This interpretation was based on the reported presence of rugose striations in that region of the retroarticular process (Anderson, 1936). Additionally, Anderson (1936) 141 stated that what is here termed mDMp had a tendinous origin on the opisthotic process of the squamosal and a fleshy insertion on the caudodorsal surface of the retroarticular process. In such an arrangement, the muscle belly with the fleshy origin attachment would have a tendinous insertion, and the one with the tendinous attachment would have a fleshy insertion. That interpretation is not supported here for three reasons: (1) none of the phytosaur mandibles sampled in this study or additionally examined for comparative assessment were observed to possess textural differences between the bulk of the caudodorsal surface of the retroarticular process and the region near the caudal terminus of that process (Fig. 12); (2) the topology proposed by Anderson (1936) would require the origin with a Level I inference reconstruction to pair with an insertion with a Level III inference reconstruction and the origin with a Level III inference reconstruction to pair with an insertion with a Level I inference reconstruction, meaning that neither muscle belly could be confidently assumed to be homologous to mDM of other sauropsids; and

(3) the caudodorsal surface of the extensive medial expansion of the articular is separated from the caudodorsal surface of the retroarticular process by a substantial crest (Fig. 12), surfaces both medial and lateral to this crest exhibit similar surface textures consistent with fleshy muscle attachments, and the location of the mDMp insertion on that medial expansion would allow the origin with a Level I inference reconstruction to pair with the insertion with a Level I inference reconstruction and the origin with a Level III inference reconstruction to pair with an origin with a Level III inference reconstruction. The topology proposed by Anderson (1936) would require both muscle bellies to have split from a plesiomorphic mDM and migrated to novel attachment locations. The topology 142 proposed here would instead require mDM to remain largely unchanged as mDMs while a smaller subset of fibers separated and gave rise to mDMp, which attached to origin and insertion locations that were both novel.

The comparisons of muscle origin and insertion surface area proportions demonstrated greater intra-clade than inter-clade similarities (Figs. 25–26). The primary differences between the two clades, in terms of muscle origin surface area proportions, were greater proportions of mPTv and mDM and lower proportions of mAMES and mPTd in phytosaurs than crocodylians. In terms of muscle insertion surface area proportions, the primary differences between the two clades were greater proportions of mAMES and mAMP and a lower proportion of mPTv in phytosaurs than crocodylians.

Interestingly, despite all of the various differences in attachment area proportions within and between the two clades, the proportions of individual muscle forces were largely similar across all taxa (Fig. 28). The most notable exceptions to this overall similarity were a greater proportion of mAMP force, slightly greater proportion of mAMES force, and lower proportion of mPTd force in Machaeroprosopus and a slightly lower proportion of mAMES force in Gavialis, compared to the rest of the sample. These results indicate that the interplay between variations in origin surface areas, insertion surface areas, and muscle length, which was not compared across specimens because of the lack of an appropriate scaling metric, ultimately result in similar proportions of muscle force produced by each muscle. The general trend of relative maximum prey:predator size ratios seen in extant crocodylians (see “Hypothesized Ecology of

Phytosauria” in Chapter 1 of this volume) does not appear to be correlated with any trend 143 in proportions of jaw muscle origin sizes, jaw muscle insertion sizes, or force produced by individual jaw muscles in that clade.

The results of each PCA and PPCA consistently demonstrated that proportions of muscle origin areas, muscle insertion areas, and individual muscle forces were more similar within phytosaurs and extant crocodylians than between each group. These findings were evidenced by the difference in the regions of tangent space occupied by members of each clade (Figs. 28–36). In particular, the PCAs and PPCAs of muscle origin and insertion surface area size proportions resulted in phytosaurs and crocodylians occupying regions of tangent space that were clearly separated from one another. The

PCA and PPCA of individual muscle force proportions found that the regions of tangent space occupied by each clade did slightly overlap. However, that overlap was so small, relative to the magnitude of the range of tangent space occupied by each clade, that the probability of it being statistically significance is doubtful. In analyses of all three metrics, removing mDM from the dataset altered the positions of taxa, somewhat, but the relative relationships of the taxa and clades to one another in tangent space changed very little. Removing mPSTp from the dataset had very little impact on the results of any of the three analyses. The results of these analyses are largely consistent with those of the direct comparisons of origin surface area proportions, insertion surface area proportions, and muscle force proportions. This consistency is particularly apparent between the direct comparison and PCA of muscle force proportions, which both found general similarities between most taxa, except for Gavialis and Machaeroprosopus, each of which fell outside the range of similarity in opposite directions. No substantial variation within 144 either Crocodylia or Phytosauria was found in these analyses. There was also no observed similarity between members of one clade and an individual member of the other clade that was greater than the similarity between the two groups as a whole. Because of the lack such findings, the ability to derive meaningful inferences about phytosaur feeding behavior from comparisons to extant crocodylians, on the basis of proportions of jaw muscle origin sizes, jaw muscle insertion sizes, and force production of individual jaw muscles, is null.

Jaw musculature topology in phytosaurs generally reflects what seems to be the plesiomorphic topology for Sauropsida, or at least for Diapsida, based on similarities to the topology of lepidosaurs and testudines (Anderson, 1936; Haas, 1973; Holliday &

Witmer, 2007; Holliday, 2009; Jones et al., 2009; Jones et al., 2012; Gröning et al., 2013;

Johnston, 2014). Whereas the overall topology of crocodylian jaw musculature generally retains the plesiomorphic condition, some divergence from that condition can be seen in specific muscle attachments in extant crocodylians. Noted differences in muscle topology between crocodylians and phytosaurs result in a failure to reject the null hypothesis that topology of phytosaur jaw muscle attachments is consistent with that of extant crocodylians (Table 7).

The relative proportions of muscle origin and insertion surface areas varied throughout the sample, but within each clade, there was relative consistency. This correlation between the proportions of origin and insertion surface areas and clade membership can be seen in the results of direct comparisons, PCAs, and PPCAs of these datasets. As a result of this correlation, the null hypothesis that size proportions of jaw 145 muscle origin and insertion surfaces areas are consistent between phytosaurs and extant crocodylians is rejected (Table 7). Moreover, apart from a slightly lower size proportion of both attachments of mDM in Alligator than other crocodylians, no trend in origin or

Table 7. Summary of hypotheses tested in this study, part 2. Statement of null and alternative hypotheses, the results of analyses pertinent to each hypothesis, and the conclusion drawn from interpretation of those results.

146 insertion size proportions were seen among crocodylians. These results lead to a failure to reject the null hypothesis that jaw muscle origin and insertion surface area size proportions are not correlated with rostrum aspect ratio in extant crocodylians. Similarly, apart from some differences in proportions of attachment sizes in Machaeroprosopus, compared to other phytosaurs, origin and insertion surface area size proportions were very consistent across all phytosaurs. All of the phytosaurs sampled here also exhibit relatively similar rostrum aspect ratios (see “Results” in Chapter 2 of this volume).

Because of these results, the null hypothesis that phytosaurs exhibit no difference in jaw muscle origin and insertion surface area size proportions, regardless of similarities in rostrum aspect ratio among taxa, is not rejected. Because of the lack of correlation of jaw muscle origin and insertion surface area size proportions and rostrum aspect ratio in extant crocodylians, the same attachment size proportions in phytosaurs are not more or less similar to those of extant crocodylians with any particular rostrum aspect ratio. These results lead to a failure to reject the null hypothesis that size proportions of phytosaur jaw muscle origin and insertions surface areas are no more or less similar to those of extant crocodylians with a particular rostrum aspect ratio than any other extant crocodylians.

Relative proportions of individual jaw muscle forces were very consistent across all taxa, excluding slight differences in the proportions of muscle force of a small number of muscles in both Gavialis and Machaeroprosopus. This consistency results in a failure to reject the null hypotheses that the proportions of individual jaw muscle forces are consistent between phytosaurs and extant crocodylians and individual jaw muscle force proportions are not correlated with rostrum aspect ratio in extant crocodylians (Table 7). 147

Because of this consistency, the null hypothesis that phytosaurs exhibit individual jaw muscle force proportions that are unrelated to rostrum aspect ratios among taxa, is not rejected. The PCAs and PPCAs of individual jaw muscle force proportions found a very slight overlap in tangent space between some phytosaurs and some extant crocodylians.

However, the phytosaurs that were closest to the crocodylians in tangent space were more much more similar to Alligator than Gavialis and only slightly more similar to

Tomistoma than Alligator. Thus, the similarities between phytosaurs and extant crocodylians in these results are inconsistent with the rostrum aspect ratios of the crocodylians. This lack of a clear trend results in the failure to reject the null hypothesis that individual jaw muscle force proportions in phytosaurs are no more or less similar to those of extant crocodylians with particular rostrum aspect ratios than those of any other extant crocodylians.

Conclusions

In general, very little variation was observed in the topologies, relative sizes of origins and insertions, and force production of individual jaw muscles among the taxa sampled here. Apart from some minor differences seen in one or two taxa, very little difference exists in the jaw musculature of phytosaurs and extant crocodylians. Those differences that were apparent seem to be the results of retention of the plesiomorphic condition in phytosaurs and divergence from that condition in crocodylians. Thus, the analyses presented here resulted in no clear support for basing hypotheses of feeding behavior and trophic ecology variation in phytosaurs on comparisons with jaw musculature of specific extant crocodylians that exhibit particular feeding behavior and 148 trophic ecology. However, only a small subset of the factors contributing to jaw function in these taxa were assessed and compared.

Comparisons between jaw muscles in phytosaurs and crocodylians, or between any faunivorous taxa, will benefit greatly from the development of an appropriate set of criteria for scaling specimens of greatly different shapes to one another. The current inability to scale specimens to one another prohibits meaningful comparisons of many aspects of muscle topology that have important impacts on the function of the jaws and the feeding behaviors affected by that function. For example, muscle length is an important factor in the balance between power and speed of jaw adduction. However, without a way to scale specimens, muscle length cannot be compared across taxa of widely different shapes, precluding comparisons of jaw closure rate and gape between individual taxa and across clades. Additionally, because the percentage contribution of a muscle to total muscle force, as was described here, is not necessarily the same as its percentage contribution of bite force, further comparisons between the relative contributions of individual muscles to bite force may yield different results from those presented here. Continued investigations of the relationships between the topology, size, power, and speed of an individual jaw muscle and the overall action of the jaws in taxa such as crocodylians that do not orally processes food will greatly benefit interpretations of the differences in jaw musculature between phytosaurs and extant crocodylians observed here. In a broader context, any study of Mesozoic paleoecology would similarly benefit from such advances in the ability to derive clear meaning from comparisons between extinct and extant sauropsids. 149

CHAPTER 4: COMPARATIVE CRANIAL BIOMECHANICS OF PHYTOSAURS

AND EXTANT CROCODYLIANS IN THE CONTEXT OF PREY UTILIZATION

Introduction

The concept of organismal performance is rooted in the field of ecomorphology, wherein performance is a measure of ability to perform ecologically relevant actions that impact the fitness of an organism (Arnold, 1983; Lande & Arnold, 1983). The biomechanical performance of the vertebrate skull is often correlated with feeding behavior and diet variation. Bite force, for example, is considered a measure of potential dietary breadth based on food hardness (e.g., Aguirre et al., 2003; Anderson et al., 2008;

Dumont et al., 2009; Santana et al., 2010; Smith et al., 2015). Finite element analysis

(FEA) is a computational modeling technique that has been increasingly used by biologists to explore, estimate, and hypothesize the mechanical performance of specific structures. FEA subdivides a large, complex problem, such as the structure of a cranium and application of muscle forces, into smaller, simpler parts called elements. The simpler equations that model such elements are then assembled into a larger system of equations that model the entire problem. Using concepts of mechanical performance developed in the field of engineering, wherein structures are evaluated in terms of their strength and/or efficiency, FEA can be applied to investigations of the mechanistic links between morphology and performance that produce correlations seen in ecological studies (e.g.,

Dumont et al., 2009; Panagiotopoulou, 2009; Tseng et al., 2011; Figueirido et al., 2014;

Button et al., 2016). Thus, FEA can help reveal the mechanisms underlying ecologically relevant variation in organismal morphology. Examples of such applications of FEA 150 include studies of the feeding mechanics of extant and extinct vertebrates (Alexander,

2006; Barret & Rayfield, 2006; McHenry et al., 2006; Thomassen et al., 2007; Schultz et al., 2014; Button et al., 2016; Sellers et al., 2017).

Applying force to a structure produces stress within that structure, which in turn causes the structure to change shape. Strain is the amount of shape change, in terms of length, or deformation, in the direction of the applied force, divided by the initial length of the shape. Von Mises stress is a criterion in determining whether a material like bone will yield under application of force Juvinall & Marshek, 2005). The non-uniform distribution of von Mises, or any other, stress in a structure indicates regions where deformation, and likelihood of failure, is greatest by identifying those regions with the highest stress concentration. The maximum stress value in that structure indicates at what applied load magnitude deformation will occur. In conservative elastic systems, such as crania, the work done by an externally applied force is identical to the elastic strain energy of the system. The total strain energy in a structure under load, thus, indicates the efficiency and stiffness of that structure, as well as the amount of deformation that will occur under the applied load. In order to compare maximum stress and total strain energy across finite element models (FEMs), those models must first be scaled to one another.

Comparisons of performance measures based on structural strength, such as maximum stress, require that force per unit area be held constant, whereas comparisons of total strain energy performance require that force per unit volume be held constant (e.g.,

Dumont et al., 2009; Slater & Van Valkenburgh, 2009; Slater et al., 2009; Dumont et al.,

2011; Neenan et al., 2014; Smith et al., 2015). For such comparisons, specimen models 151 may be scaled to one another according to surface area and volume, depending on the metric being compared, and then tested with the same total load. However, for comparisons involving specimens with disparate shapes, such scaling can be difficult because of the differences in surface area:volume ratios inherent in structures of sufficiently different shapes. This is the case for comparisons between crania, wherein differences in ratios of height, length, width, bone thickness, and so on make scaling models to yield identical force:surface area ratios or force:volume ratios difficult or impossible. In such cases, comparisons between FEMs can still be appropriately made by scaling the results of each analysis. Any remaining differences in stress and strain between models are entirely due to differences in shape, and contour plots of stress and strain distribution can be compared (e.g., Dumont et al., 2009; Slater & Van

Valkenburgh, 2009; Slater et al., 2009; Dumont et al., 2011; Neenan et al., 2014; Smith et al., 2015). Unfortunately, many FEAs of biological systems contain artificially high stresses and strains at specific points due to kinematic constraints, point loads, sharp corners, and so on because the theory of elasticity admits stress and strain singularities, points at which stress or strain is infinite, due to such idealizations (Dumont et al., 2009).

These modeling artifacts are highly localized and do not impact stress values in other regions of the model (Cook & Young, 1985), but they do make extracting exact maximum von Mises stress values from the FEA difficult (Dumont et al., 2009). Thus, although a maximum von Mises stress value can be obtained, the location of the corresponding point in the model is typically at the constraints or some other region outside of those that make for meaningful comparisons. Strain energy, on the other hand, 152 is theoretically infinite at points admitting stress or strain singularities, but the strain energy contained in a finite volume of material encompassing such points is finite

(Dumont et al., 2009). Total strain energy, therefore, is not sensitive to the presence of model idealizations and is a more reliable and informative metric of overall model performance with respect to work efficiency (Dumont et al., 2009).

The crania of extant crocodylians exhibit several characteristics, such as dorsoventral flattening, hypothesized to be adaptations for aquatic ambush predation

(Iordansky, 1973), and extant crocodylians produce the highest measured bite forces among extant tetrapods (Erickson et al., 2003). Bite force production in extant crocodylians is consistent across taxa with disparate rostrum or tooth morphology

(Erickson et al., 2012) and diet range (see Chapter 1 of this volume). The combination of morphology and performance of the crania of extant crocodylians is in contrast to the cranium morphology of other tetrapods that produce high bite force, which is typically a dorsoventrally tall cranium hypothesized to be resistant to dorsoventral bending of the rostrum (e.g., Molnar, 1998; Metzger & Herrel, 2005; Tseng & Stynder, 2011;

Schaerlaeken et al., 2012). Phytosaurs exhibit the dorsoventrally tall cranium morphology typical of tetrapods, particularly those that produce high bite force, yet they are also hypothesized to have occupied a semiaquatic niche similar to that occupied by extant crocodylians. Therefore, the biomechanical performance of phytosaur crania represents a system in which to test the hypothesized adaptive significance of the extant crocodylian cranium morphology. Additionally, comparing cranium biomechanical performance in phytosaurs with that of extant crocodylians will help constrain the potential ecological 153 niche and dietary variation ranges of phytosaurs. It is here hypothesized that: (1) phytosaurs produced bite forces comparable to those produced by extant crocodylians, regardless of rostrum morphology; (2) increased maximum von Mises stress in the rostrum of extant crocodylians is positively correlated with increased rostrum aspect ratio; (3) the region of the cranium with the greatest stress concentration in both phytosaurs and extant crocodylians is the pre-orbital cranium; (4) the structural efficiency of the cranium is negatively correlated with increased rostrum aspect ratio in extant crocodylians, (5) the structural efficiencies of phytosaur crania are consistently more similar to extant crocodylians with higher rostrum aspect ratios than those with lower rostrum aspect ratios. This study will yield novel information about the functional bases of dietary variation in extant crocodylians and the likely dietary niche of phytosaurs.

Materials and Methods

Taxon Sampling

Four phytosaur and three extant crocodylian specimens were selected for biomechanical analyses. Phytosaur specimens were sampled on the basis of being well- preserved individuals of taxa with a broad phylogenetic distribution and a broad range of rostrum and overall cranium shape (see Chapter 2 of this volume). Extant crocodylian specimens were sampled on the basis of broad phylogenetic distribution among taxa with the greatest rostrum and overall cranium shape similarity to the sampled phytosaurs (see

Chapter 2 of this volume), with an additional specimen of a morphologically dissimilar taxon selected as a baseline for comparison. The sample comprised: the phytosaurs

Parasuchus angustifrons (BSPG 1931 X 502), Ebrachosuchus neukami (BSPG 1931 X 154

501), Pravusuchus hortus (UMNH VP 28293), and Machaeroprosopus pristinus (PEFO

382); and the extant crocodylians Gavialis gangeticus (UF 118998), Tomistoma shlegelii

(TMM M-6342), and Alligator mississippiensis (OUVC 09640).

Cranial specimens of two phytosaurs, Parasuchus angustifrons and Pravusuchus hortus, do not preserve the rostral terminus of the rostrum. Rostrum terminus morphology for each of these specimens was approximated by isolating the rostrum terminus from specimen models of closely related taxa and deforming that isolated region in Maya 2018 to match the dimensions and morphology of the reconstructed target specimen model not preserving a rostral terminus. Criteria including the position of the maxilla-premaxilla suture in the two specimens being combined and the distance between the rostral margin of the nares and rostral terminus of the rostrum in several other closely related specimens were used to constrain the length of rostrum added to each specimen model. Then, in

Geomagic Studio (Geomagic Inc., Research Triangle Park, NC, USA), the overlapping region from each target model was deleted, the two materials were combined, and the bridge tool was used to interpolate a three-dimensional structure filling the gap between the two surfaces. The resulting model was again reflected across the sagittal midline in order to retain specimen model bilateral symmetry. To the specimen model of

Parasuchus angustifrons, the rostrum tip of P. bransoni (TMM M-31100-101) was added, and to the specimen model of Pravusuchus hortus, the rostrum tip of another non- mystriosuchinine leptosuchomorph (TMM M-31173-120) was added. 155

Specimen Modelling

Cranium models used for biomechanical modeling were the same as those used previously for reconstructions and comparisons/analyses of cranial musculature (see

Chapter 3 of this volume). One specimen model included in the myological reconstructions, that of Mecistops cataphractus (TMM M-3529), was not included in the biomechanical analyses reported herein. Because complex models are computationally expensive and a model surface resolution of 300,000 faces is required to obtain stable

FEA results in a comparative context (McCurry et al., 2015), each surface model was down-sampled using the “Decimate” tool in Geomagic Studio (Geomagic Inc., Research

Triangle Park, NC, USA) to approximately 300,000 surface faces (Table 8). The

“Remesh” tool in Geomagic Studio was used to achieve a uniform tessellation for each model and reduce the number of potential errors encountered when generating a polyhedral mesh. Surface meshes were then imported to Strand7 R3 (G1D Computing

Pty Ltd, Sydney, Australia) where surface model errors were eliminated using the

“Autoclean” tool. Surface meshes were then converted to linear-four-noded tetrahedral meshes using the “Automesh” tool in Strand7 R3. The resulting solid meshes matched the

Table 8. Specifications of specimen models used for biomechanical analyses. Taxonomic identification of specimen models utilized in biomechanical analyses, the number of faces (or plates) of each surface model, the number of four-noded tetrahedral bricks comprising each solid mesh created from each surface model, and the volume of each solid mesh.

156 input geometry of each specimen and comprised between 1,285,000 and 1,791,500 four- noded tetrahedral bricks, depending on the surface area:volume ratio of each specimen.

The dimensions of all models are: x is positive in the left lateral direction, y is positive in the dorsal direction, and z is positive in the rostral direction.

Isolated muscle attachment surface face models created as part of the previous analysis of jaw musculature (see Chapter 3 of this volume) were visualized along with the corresponding down-sampled surface face specimen model used for solid mesh generation above in Geomagic Studio. The boundaries of the full-resolution muscle attachment surface models were then traced onto the down-sampled specimen models.

The surface area of each down-sampled muscle attachment resulting from that tracing was always greater than the surface area of the full-resolution counterpart but never by more than 0.5 mm2. Because of small variations resulting from mesh down-sampling and remeshing, muscle attachment areas are not perfectly symmetrical, in terms of the arrangement of surface faces within the areas of muscle attachment, but the size consistency between full-resolution and down-sampled muscle attachment surface models meant that bilateral pairs of down-sampled muscle attachment models were approximately the same in surface area. Down-sampled muscle attachment surface models were imported to Strand7 R3, where they were traced to select bricks of solid mesh models. These selected bricks were assigned to unique property groups that were then tessellated to create surface face models of each muscle attachment area that were aligned to the geometry of the solid mesh model. 157

Three-dimensional Lever Mechanics

Calculation of bite force first requires calculation of the moment of each muscle about the jaw joint. The moment arm of a muscle is the perpendicular distance from the muscle force vector to the axis of rotation. Equation 4 describes the calculation of moments about the jaw joint axis (JJA):

퐌JJA = 퐮JJA · (퐫M × 퐅M), (4) where MJJA is the moment about the JJA; uJJA is the unit vector describing the JJA; rM locates the muscle insertion, and thus the muscle force vector, relative to one of the jaw joints; and FM is the vector describing the magnitude and orientation of muscle force

(Sellers et al., 2017).

Output forces in lever systems like jaws act perpendicularly to the plane common to the axis of rotation and the output moment arm. Equation 5 describes the relationship of moments about the jaw joint axis to bite force:

퐌JJA = 퐮JJA · (퐫B × 퐅B), (5) where rB locates the bite point, relative to the jaw joint, and FB is the magnitude and orientation of bite force (Sellers et al., 2017). The total moment about the JJA was calculated using the results of these calculations on data for each muscle. Bite force is the quotient of total moment about the JJA and the perpendicular distance from the bite point to the JJA. In this study, bite force was calculated using FEA, which, when applied to an experimental design similar to that used in this study, was shown by Sellers et al. (2017) to produce results almost identical to those of traditional three-dimensional lever 158 mechanics. The component of force in each dimension was recorded in addition to overall magnitudes.

Finite Element Analysis

Rather than modeling muscle forces as a collection of single vectors at the centers of muscle attachment areas, calculated muscle force (see Chapter 2 of this volume) was distributed over the entire surface area of each muscle origin. In this model setup, each free face of each tetrahedral brick representing a muscle origin had an equal portion of the total force of that muscle applied to it, directed at the centroid of the muscle insertion.

The distribution of muscle forces was calculated with the use of the computation toolkit

BoneLoad version 7 (Davis et al., 2010) and these calculated applied loads were incorporated into biomechanical models by zipping the surface faces output by BoneLoad to the tetrahedral mesh of each specimen. All solid meshes were assigned material properties of Alligator mandibular cortical bone (Zapata et al., 2010) in Strand7 R3. Two unilateral biting scenarios were modelled by constraining a single node at the tip of either the rostral-most or caudal-most left lateral tooth (or the rostral margin of the alveolus for that tooth) of each specimen. In all four modelled scenarios, a single node in the center of the articular surface of each quadrate was also constrained. Nodes were constrained in all three translational and all three rotational degrees of freedom. Bite force for each biting scenario was estimated by measuring the node reaction force at the bite point constraint.

Methods similar to these were shown by Sellers et al. (2017) to produce bite force estimates consistent with both those obtained from calculations reliant on direct measurements of muscles in cadaveric specimens (Gignac & Erickson, 2016) and in vivo 159 measurements of bite force (Erickson et al., 2003). Bite force efficiency was compared across specimens and biting scenarios by comparing the ratio of bite force to muscle force, such that a value of 1 meant that the bite force equaled the total force produced by the jaw muscles.

The distribution of von Mises stress in FEMs of each specimen in each biting scenario was recorded as a contour plot, wherein warm colors indicate regions of high stress and cool colors indicate low stress. Maximum von Mises stress calculated in each analysis was determined to correspond to constraints placed at the jaw joints and bite points. Excluding bricks comprising regions of constraints and measuring the maximum von Mises stress in the remaining regions of the model often resulted in points of highest maximum stress being found in regions outside those of the highest stress regions indicated by the contour plot. This outcome was interpreted as being the result of stress singularities at some sharp corners or other feature that could not be identified, rather than a meaningful indication of the maximum stress in the weakest anatomical region.

Maximum von Mises stress was, therefore, not recorded or compared between specimens.

Instead, stress distribution contour plots were visualized with the same range of scale values to allow models to be visually compared to one another in terms of regions of stress concentration and relative maximum von Mises stress values. Additionally, total strain energy was calculated in each analysis, recorded, and compared across specimens by standardizing the results of each specimen model analysis to those of the Alligator mississippiensis model analysis on the basis of force:volume ratios. Equation 6 describes scaling maximum von Mises stress: 160

1/3 2 푉퐵 퐹퐴 푈퐵′ = ( ) ( ) 푈퐵, (6) 푉퐴 퐹퐵 where UB′ is the scaled strain energy, VB is the volume of the model being scaled, VA is the volume of the A. mississippiensis model, FA is the force or load applied to the A. mississippiensis model, FB is the force or load applied to the model being scaled, and UB is the computed strain energy in the model being scaled (Dumont et al., 2009). The combination of the results of these analyses were used to determine regions of specimen models where failure would occur under a high enough load, and the relative strength of each model in terms of the order in which they would fail as the scaled applied force increased, and the efficiency of each model in terms of the amount of deformation that results from the given applied load.

Results

Three-dimensional Lever Mechanics

The node reaction force at the bite point constraint, and thus the estimated bite force in this analysis, demonstrated a considerable range throughout the sample and between modeled biting scenarios (Table 9). In both biting scenarios, Gavialis and

Table 9. Results of biomechanical analyses. Calculated bite force (bite point node reaction force) and total strain energy of each model as calculated by FEA, the ratio of calculated bite force to total muscle force for each model, and the total strain energy of each model scaled by the volume of that model volume, for each of the rostral and caudal unilateral bite point scenarios.

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Tomistoma exhibited similar enough bite forces that the differences between the two could likely be explained by size differences between these specimens (see Chapter 3 of this volume), and they demonstrated similar bite force efficiencies. The bite force and bite force efficiency of Alligator were much greater than those of either Gavialis or

Tomistoma in both biting scenarios. Both the bite force and bite force efficiency of

Parasuchus were the lowest of these measurements among phytosaurs in both biting scenarios. In both metrics, the values for Ebrachosuchus were only slightly greater than those for Parasuchus, likely in keeping with the former being a slightly larger specimen than the latter. The bite forces of both Parasuchus and Ebrachosuchus in the rostral biting scenario fell intermediate within the range of those of the crocodylians, despite these phytosaur specimens being approximately the same size or slightly larger than the largest crocodylian specimen. In the rostral biting scenario, the bite force efficiency of

Parasuchus was only slightly greater than that of Tomistoma and much lower than that of

Alligator. In the caudal biting scenario, the bite force of Parasuchus was 202% that of

Gavialis but only 77.5% that of Alligator, and the bite force efficiency of Parasuchus fell similarly within the range of those of the crocodylians. The bite force of Ebrachosuchus in the caudal biting scenario was 138% that of Parasuchus and 107% that of Alligator, and its bite force efficiency compared similarly to those taxa. The bite forces of

Pravusuchus and Machaeroprosopus were similar to one another in both biting scenarios, with that of Machaeroprosopus being slightly greater in the rostral biting scenario and that of Pravusuchus being slightly greater in the caudal biting scenario. The bite force of

Pravusuchus in the rostral biting scenario was 143.63% that of Alligator, and in the 162 caudal biting scenario, the bite force of Machaeroprosopus was 246.77% that of

Alligator. In the rostral biting scenario, the bite force efficiency of Pravusuchus was similar to that of Alligator, and the bite force efficiency of Machaeroprosopus was similar to that of Parasuchus. In the caudal biting scenario, the bite force efficiency of

Machaeroprosopus was the same as that of Alligator, and the bite force efficiency of

Pravusuchus was nearly double that of any other taxon, except for Ebrachosuchus, which demonstrated a bite force efficiency approximately two-thirds that of Pravusuchus. Bite force typically refers only to the dorsoventral component of that force, and that was the metric reported here as bite force (Tables 9–10). However, the mediolateral and rostrocaudal components of total force potentially represent the magnitude of shear stress in a food item during a bite. In the rostral bite point scenario, all phytosaurs exhibited far greater mediolateral and rostrocaudal components of force than any of the crocodylians

(Table 10). In the caudal bite point scenario, phytosaurs exhibited greater mediolateral and rostrocaudal components of force than did crocodylians, except for Alligator, which exhibited larger magnitudes of these forces than Parasuchus.

Table 10. Axial components of calculated bite forces. Mediolateral (Fx), dorsoventral (Fy), and rostrocaudal (Fz) axis components of bite point node reaction forces calculated by FEA for each of the specimen models in each of the bite point scenarios. Fy is considered to represent bite force in this study.

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Finite Element Analysis

Rostral Bite Point Scenario—. Distribution of von Mises stress was nearly identical on both the left and right sides of the cranium in the majority of examined taxa. Some phytosaurs exhibited slight asymmetry, however, near the terminus of the rostrum. Stress was spread almost uniformly across the entire cranium of Alligator, except for the skull roof, braincase, and lateral margins of the rostrum, where stress values were near zero, and the ectopterygoid and pterygoid, where stress concentrations were slightly greater

(Fig. 38A–D). This pattern largely contrasts those seen in any of the other taxa, all of which exhibited relatively high stress concentrations along the dorsal and ventral aspects of the rostrum. The lateral margins of the rostrum exhibited stress values near zero in all taxa. In Alligator, the greatest stress concentration was on the caudal margin of the pterygoid, just rostrolateral to the caudal pterygoid flange and caudolateral to the choanae, and the second greatest concentration was along the lateral margin of the ectopterygoid. These same regions exhibited high stress concentrations in Tomistoma

(Fig. 39A–D). However, the greatest stress concentration in Tomistoma was along the caudal margin of the suborbital fenestra, at the suture between the pterygoid and palatine, the second greatest was along the rostromedial margin of the ectopterygoid, and the third highest was approximately midway along the rostrum, on both the dorsal and medial aspects. The regions of high stress concentration in both Alligator and Tomistoma were also the locations of noticeable stress concentrations in Gavialis (Fig. 40A–D). However, the stress magnitudes in these regions in Gavialis were lower than the greatest stress concentration, which comprised a region along the rostral face of the quadrate, 164

Figure 38. FEA results for Alligator mississippiensis. Distribution of von Mises stress in FE models of an Alligator mississippiensis (OUVC 09640) cranium in dorsal (A, E), rostral (B, F), ventral (C, E), and caudal (D, H) views. Arrows show bite point (white) and jaw joint (black) constraint locations in rostral (A–D) and caudal (E–H) bite point scenarios. Colors indicate areas of low stress (cool), high stress (warm), and those exceeding the stress scale (white).

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Figure 39. FEA results for Tomistoma schlegelii. Distribution of von Mises stress in FE models of a Tomistoma schlegelii (TMM M-6342) cranium in dorsal (A, E), rostral (B, F), ventral (C, E), and caudal (D, H) views. Arrows show bite point (white) and jaw joint (black) constraint locations in rostral (A–D) and caudal (E–H) bite point scenarios. Colors indicate areas of low stress (cool), high stress (warm), and those exceeding the stress scale (white).

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Figure 40. FEA results for Gavialis gangeticus. Distribution of von Mises stress in FE models of a Gavialis gangeticus (UF 118998) cranium in dorsal (A, E), rostral (B, F), ventral (C, E), and caudal (D, H) views. Arrows show bite point (white) and jaw joint (black) constraint locations in rostral (A–D) and caudal (E–H) bite point scenarios. Colors indicate areas of low stress (cool), high stress (warm), and those exceeding the stress scale (white).

167 caudoventral aspect of the quadratojugal, and caudoventral aspect of the jugal, and the second greatest stress concentration, which was along the rostrodorsal aspect of the jugal.

The skull roof and braincase exhibited very low stress magnitudes in all crocodylians.

Among the crocodylians, the greatest stress magnitude was seen in Gavialis, the second greatest was seen in Tomistoma, and the third greatest was seen in Alligator. In terms of work, the total strain energy of Alligator was 33.46% lower than that of Gavialis and

68.71% lower than that of Tomistoma.

The greatest concentrations of von Mises stress in Parasuchus were on the dorsal and ventral aspects of the rostrum, approximately one-third of the length from the nares to the terminus; various points along the rostral and caudal aspects of the quadrate and the caudoventral margin of the pterygoid process of the quadrate; on the medial aspect of the jugal; and on the rostroventral aspect of the squamosal, near the suture between the squamosal and parietal (Fig. 41A–D). The stress magnitudes in each region decreased in that order. Those same regions, along with additional regions, exhibited high stress concentrations in Ebrachosuchus (Fig. 42A–D). Stress magnitudes in regions of high stress concentration in Ebrachosuchus decreased in the order of: the dorsal aspect of the rostrum, approximately one-third of the length from the nares to the terminus; dorsal and ventral aspects of the rostrum, near the rostral terminus; various points along the rostral and caudal aspects of the quadrate and the caudoventral margin of the pterygoid process of the quadrate; the caudolateral aspect of the pterygoid; the medial aspect of the jugal; the rostroventral aspect of the squamosal, near the suture between the squamosal and parietal; points along the ventral and rostral margins of the antorbital fenestra; the ventral 168

Figure 41. FEA results for Parasuchus angustifrons. Distribution of von Mises stress in FE models of a Parasuchus angustifrons (BSPG 1931 X 502) cranium in dorsal (A, E), rostral (B, F), ventral (C, E), and caudal (D, H) views. Arrows show bite point (white) and jaw joint (black) constraint locations in rostral (A–D) and caudal (E–H) bite point scenarios. Colors indicate areas of low stress (cool), high stress (warm), and those exceeding the stress scale (white).

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Figure 42. FEA results for Ebrachosuchus neukami. Distribution of von Mises stress in FE models of an Ebrachosuchus neukami (BSPG 1931 X 501) cranium in dorsal (A, E), rostral (B, F), ventral (C, E), and caudal (D, H) views. Arrows show bite point (white) and jaw joint (black) constraint locations in rostral (A–D) and caudal (E–H) bite point scenarios. Colors indicate areas of low stress (cool), high stress (warm), and those exceeding the stress scale (white).

170 aspect of the rostrum, approximately one-third of the length from the nares to the terminus; the lateral margin of the nares; the internarial septum; and the lateral aspect of the jugal, near the rostral margin of the infratemporal fenestra. The region of greatest stress concentration in Pravusuchus was the caudoventral margin of the pterygoid process of the quadrate and adjoining margin of the pterygoid, followed, in decreasing order of magnitude, by a point along the caudolateral aspect of the pterygoid; a point along the medial aspect of the quadrate, near the quadrate foramen; the internarial septum; and a much lower stress region on the dorsal aspect of the rostrum, along its entire length (Fig. 43A–D). In Machaeroprosopus, the region of highest stress concentration was a point along the medial aspect of the quadrate, near the quadrate foramen, followed by a region on the dorsal aspect of the rostrum approximately half the length between the nares and terminus (Fig. 44A–D). The skull roof and braincase of each phytosaur exhibited low to moderate stress magnitudes that were greater than the very low stress magnitudes in that region of each crocodylian. Of the phytosaurs, only

Machaeroposopus exhibited a maximum stress value lower than those of Gavialis or

Tomistoma. Ebrachosuchus exhibited several regions with stress values greater than any region of any other taxon. The stress magnitude contained in the region of greatest stress concentration in Parasuchus was greater than any region of Pravusuchus. In terms of work, the total strain energy of Machaeroprosopus was 66.57% lower than that of

Pravusuchus, 84.5% lower than Parasuchus, and 89.65% lower than Ebrachosuchus.

Across all taxa, Machaeroprosopus had the lowest total strain energy, 39.73% that of

Alligator, and Ebrachosuchus had the highest total strain energy. 171

Figure 43. FEA results for Pravusuchus hortus. Distribution of von Mises stress in FE models of a Pravusuchus hortus (UMNH VP 28293) cranium in dorsal (A, E), rostral (B, F), ventral (C, E), and caudal (D, H) views. Arrows show bite point (white) and jaw joint (black) constraint locations in rostral (A–D) and caudal (E–H) bite point scenarios. Colors indicate areas of low stress (cool), high stress (warm), and those exceeding the stress scale (white).

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Figure 44. FEA results for Machaeroprosopus pristinus. Distribution of von Mises stress in FE models of a Machaeroprosopus pristinus (PEFO 382) cranium in dorsal (A, E), rostral (B, F), ventral (C, E), and caudal (D, H) views. Arrows show bite point (white) and jaw joint (black) constraint locations in rostral (A–D) and caudal (E–H) bite point scenarios. Colors indicate areas of low stress (cool), high stress (warm), and those exceeding the stress scale (white).

Caudal Bite Point Scenario—. Distributions of von Mises stress varied between the left and right sides of the cranium in each of the taxa, such that greater stress concentrations 173 occurred more rostrally on the bite point side and more caudally on the contralateral side.

Stress distribution was fairly uniform in Alligator, except for regions of slightly higher concentration on the bilateral caudal margins of the pterygoids, just rostrolateral to the caudal pterygoid flanges and caudolateral to the choanae; the rostral aspect of the ipsilateral ectopterygoid; the contralateral caudal margin of the suborbital fenestra, near the suture between the pterygoid and ectopterygoid; and a small region on the lateral aspect of the ipsilateral postorbital bar (Fig. 38E–H). Stress magnitudes in those regions decreased in the order in which they were listed. Alligator also exhibited a region of very low stress on the contralateral skull roof, and the maximum stress value seen in any region of the Alligator cranium was far lower than the maximum stress value seen in any other taxon. Tomistoma and Gavialis exhibited more bilaterally uniform stress distributions than Alligator, particularly along the skull roof. The regions of greatest stress concentration in Tomistoma were, in descending order of magnitude: the rostral margin of the ipsilateral ectopterygoid; the bilateral caudal margins of the suborbital fenestrae, near the sutures between the pterygoid and ectopterygoids; the caudal margin of the ipsilateral ectopterygoid; and the bilateral caudal margins of the pterygoids, just rostrolateral to the caudal pterygoid flanges and caudolateral to the choanae (Fig. 39E–

H). In Gavialis the region of greatest stress concentration comprised the bilateral rostral faces of the quadrates, caudoventral aspects of the quadratojugals, and caudoventral aspects of the jugals (Fig. 40E–H). Very slight stress concentrations were also exhibited on the bilateral lateral aspects of the jugals and ipsilateral rostral margin of the ectopterygoid. Of the crocodylians, Gavialis exhibited the greatest stress magnitude. In 174 terms of work, the total strain energy of Alligator was approximately the same as that of

Gavialis and 41.81% lower than that of Tomistoma.

The greatest concentration of von Mises stress in Parasuchus was a point along the ipsilateral rostromedial margin of the pterygoid, near the sutures of the pterygoid with the ectopterygoid and palatines (Fig. 41E–H). Additional areas of stress concentration were, in decreasing order of magnitude: a point along the rostroventral aspect of the contralateral squamosal, small points along the ipsilateral medial margin of the pterygoid, a point along the caudal margin of the ipsilateral antorbital fenestra, and the caudal face of the contralateral quadrate, near the quadrate foramen. Very slight stress concentrations were also exhibited on the medial and dorsolateral aspects of the contra- and ipsilateral jugals, respectively. Ebrachosuchus exhibited high stress concentrations in the same regions as Parasuchus and in approximately the same order of decreasing magnitude but also had high stress concentrations along the rostroventral aspect of the ipsilateral squamosal that matched that of the contralateral squamosal in stress magnitude, regions of similar stress magnitude along the dorsal and ventral aspects of the lateral margin of the ipsilateral orbit, and a region of greater stress magnitude along the rostroventral margin of the ipsilateral jugal (Fig. 42E–H). The region of greatest stress concentration in

Pravusuchus was almost the entirety of the ventral margin of the pterygoid process of the contralateral quadrate, followed by a point along the ipsilateral lateral margin of the pterygoid, near the suture of the pterygoid and ectopterygoid; points along the rostral margin of the ipsilateral subtemporal fenestra, near the suture of the ectopterygoid and jugal, and along the ventral margin of the jugal, near the suture of the jugal and maxilla; 175 points along the rostral and caudal margins of the ipsilateral antorbital fenestra; the ventral margin of the contralateral jugal; the caudal margin of the ventral shelf of the pterygoid process of the ipsilateral quadrate; and the lateral faces of the jugals, bilaterally

(Fig. 43E–H). In Machaeroprosopus, the region of greatest stress concentration was the ipsilateral lateral margin of the pterygoid, near the suture of the pterygoid and ectopterygoid, followed by slight concentrations on the ventral margin of the jugal, near the suture of the jugal and maxilla, and on the caudal face of the quadrate, near the quadrate foramen (Fig. 44E–H). The caudal processes of the bilateral squamosals exhibited very low stress magnitudes in both Pravusuchus and Machaeroprosopus. Stress concentrations along the skull roof of each phytosaur were nearly bilaterally distributed and greater in magnitude than any of the crocodylians. Of the phytosaurs, only

Machaeroposopus exhibited a maximum stress value lower than those of Gavialis or

Tomistoma. Ebrachosuchus exhibited several regions with stress values greater than any region of any other taxon. The stress magnitude contained in the region of greatest stress concentration in Pravusuchus was greater than any region of Parasuchus, and

Pravusuchus exhibited at least three more points with maximum stress magnitudes approximately equal to the greatest stress magnitude in Parasuchus. In terms of work, the total strain energy of Machaeroprosopus was 81.35% lower than that of Parasuchus,

86.47% lower than Ebrachosuchus, and 97.01% lower than Pravusuchus. Across all taxa,

Machaeroprosopus had the lowest total strain energy, 71.76% that of Alligator, and

Pravusuchus had, by far, the highest. Ebrachosuchus had the next highest total strain energy. 176

Discussion

The estimated bite force of the Alligator cranium specimen modeled here very closely matched the bite force predicted for a specimen of that size by the regression of skull length to bite force calculated by Sellers et al. (2017) using FEA. The regression of skull length to bite force estimated from FEA differed from that derived from in vivo bite force measurements such that a specimen of the size presented here is predicted by FEA to have a lower bite force than that recorded in vivo (Sellers et al., 2017). However, the difference between FEA estimated bite forces and in vivo bite force measurements may be largely due to the static loading parameters of the FEMs lacking a momentum contribution from impact forces that would be a component of in vivo measurements

(Sellers et al., 2017). The model analysis results presented here do not demonstrate a similarity in bite force of crocodylian individuals of different taxa but similar size. The

Alligator specimen modeled here was of a similar size to that of the Gavialis specimen

(Fig. 11) and exhibited a much greater bite force than that latter specimen model. These results are counter to the in vivo findings of Erickson et al. (2012), wherein similarly sized crocodylians produced similar bite forces. The relatively low estimated bite forces of the Gavialis and Tomistoma specimens sampled here may not provide sufficient evidence to support rejection of the findings of Erickson et al. (2012), however, because those authors reported the bite force of Gavialis as falling slightly under the specimen size:bite force regression curve for extant crocodylians. The bite force differences between Gavialis and Tomistoma estimated here may have been of a magnitude that could result from size differences between these two specimens. Additionally, the 177 subadult status of the Tomistoma specimen sampled here potentially resulted in ontogenetic artifacts that are not reported in Alligator (Erickson et al., 2003; Gignac &

Erickson, 2016; Sellers et al., 2017).

The phytosaurs all exhibited estimated bite forces that seemed to be proportional to their size, relative to each other, and much greater than similarly sized crocodylians.

The estimated bite forces of Machaeroprosopus and Pravusuchus were similar to one another in both biting scenarios and much greater than any other taxon modeled here

(Table 9). Some of this relatively high bite force may be due to allometry because these two specimens were considerably larger than any other specimen, and

Machaeroprosopus was the larger of the two. However, according to the regression of skull length to FEA-calculated bite force presented by Sellers et al. (2017), the bite forces calculated for Machaeroprosopus and Pravusuchus in the caudal bite point scenario would equal that of an alligator with a skull length of approximately 55 cm. Such a skull length is well into the high end of the size range for Alligator mississippiensis, and the in vivo bite force of such an individual was predicted to be nearly 10,000 N (Erickson et al.,

2003; Sellers et al., 2017). This trend indicates that the bite forces of these phytosaur taxa may have approximated or exceeded that known for any living taxon, after accounting for the contribution of momentum from impact forces to bite force.

In the rostral bite point scenario, the estimated bite forces of Parasuchus and

Ebrachosuchus were greater than those of either Gavialis or Tomistoma (Table 9) despite general rostrum aspect ratio similarities between these phytosaurs and crocodylians (Figs.

4, 7) and a size similarity between these phytosaurs and the Gavialis specimen (Fig. 11). 178

In that scenario, both Parasuchus and Ebrachosuchus had a lower estimated bite force than Alligator, but in the caudal bite point scenario, Ebrachosuchus had a slightly greater bite force than Alligator. These results indicate that Parasuchus and Ebrachosuchus may have been able to utilize food items of greater prey:body size ratios than Gavialis or

Tomistoma but lower ratios than Alligator, if such food items were acquired using bites with the rostral tip. In the rostral biting scenario, the estimated bite force of

Machaeroprosopus was more similar to that of Pravusuchus than to any other taxon, though Machaeroprosopus is slightly larger than Pravusuchus. The bite forces of these two phytosaurs were also greater than any other taxa in the rostral biting scenario, indicating that they may have been able to utilize food items of greater prey:body size ratios than any of the modeled crocodylians, if such food items were acquired using bites with the rostral tip.

In the rostral bite point scenario, Tomistoma, Parasuchus, Ebrachosuchus, and

Machaeroprosopus all had generally similar biting efficiencies (Table 9), indicating a potentially similar utility of the rostrum tip for performing feeding behaviors in these taxa. Interestingly, the biting efficiency of Gavialis, a taxon generally restricted to food items of a relatively low maximum prey:body size ratio (see “Hypothesized Ecology of

Phytosauria” in Chapter 1 of this volume), was lower than any other taxon and approximately half that of any phytosaur in the rostral biting scenario. A greater similarity in estimated maximum relative prey size utilization may, thus, be indicated between the extant crocodylian Tomistoma and the phytosaurs Parasuchus,

Ebrachosuchus, and Machaeroprosopus than between those phytosaurs and Gavialis. 179

Likewise, the similar biting efficiencies of Alligator and Pravusuchus in the rostral biting scenario may indicate similar relative prey size utilization in these taxa, particularly because differences in bite forces between these specimens are probably due to allometry.

Machaeroprosopus and Parasuchus also demonstrated similar biting efficiencies. If the utility of the rostral tip in the performance of feeding behaviors in the taxa modeled here affected the maximum relative prey size those taxa were capable of utilizing, either increased bite force or biting efficiency may indicate an increase in relative prey size because as one increased, the other typically increased as well. However, the relationship between bite force and bite force efficiency is not consistent and its exact nature is unclear. Ambiguity in that relationship is demonstrated by both Machaeroprosopus and

Tomistoma, the former of which had the greatest bite force and one of the lowest bite efficiencies, among phytosaurs in both bite point scenarios, and the latter of which had a lower bite force and greater bite efficiency than Gavialis, in both bite point scenarios.

The caudal bite point scenario results followed a trend similar to those of the rostral bite point results in the crocodylians (Table 9). However, the bite forces and bite force efficiencies of the phytosaurs were considerably greater in the caudal bite point scenario than were those of any crocodylian except for Alligator. The biting efficiency of

Alligator in the caudal bite point scenario was just over double that in the rostral bite point scenario, whereas the other crocodylians exhibited a slightly greater than three-fold increase and the phytosaurs demonstrated a three- to five-fold increase. These results may be intuitive, mechanically, because the increase in lever arm length between the jaw joint axis and bite point from the caudal biting scenario to rostral biting scenario is greater in 180 taxa with longer rostra. This interpretation is supported by the taxa with the most similar rostrum aspect ratios, Gavialis, Tomistoma, and Parasuchus (Fig. 7), having similar magnitudes of increase in biting efficiency from rostral to caudal bite point scenarios and the two taxa with the highest rostrum aspect ratios, Ebrachosuchus and

Machaeroprosopus, having the greatest increases in biting efficiency between bite point scenarios. If maximum bite force is an indicator of maximum relative prey size utilization, Parasuchus, Ebrachosuchus, and Machaeroprosopus may have utilized prey of similar maximum relative size to those utilized by Alligator because of the similarity in bite force across these taxa after considering probable allometric effects. If maximum bite force efficiency is an indicator of maximum relative prey size utilization, Parasuchus may have utilized prey of maximum relative sizes greater than those utilized by

Tomistoma but lower than Alligator, Machaeroprosopus may have utilized prey of maximum relative sizes similar to Alligator, and both Ebrachosuchus and Pravusuchus may have utilized prey of maximum relative sizes greater than Alligator, with

Pravusuchus utilizing prey of the greatest maximum relative size. These results indicate that the maximum relative size of food items that phytosaurs could utilize was almost universally greater than any of the sampled crocodylians, particularly if the primary means of food acquisition or processing was through bites performed in the caudal portion of the tooth row. An exception to this trend is Parasuchus, which probably could not utilize food items of a maximum relative size as great as those that could be utilized by Alligator. 181

Results of the FEAs indicated that the point of failure was remarkably consistent between rostral and caudal bite point scenarios for each crocodylian. The only noteworthy difference in the stress distributions in crocodylians between the two scenarios was the additional stress concentration along the rostrum in the rostral bite point scenario, but that stress concentration was never the point of initial failure under sufficient load. Instead, the ventral quadrate and quadratojugal was where failure would occur in Gavialis, the rostral margin of the ectopterygoid along the caudal margin of the suborbital fenestra was where failure would occur in Tomistoma, and the caudal margin of the pterygoid was where failure would occur in Alligator. The differences in stress magnitude indicate that the Gavialis model was the weakest of these structures, followed by Tomistoma and Alligator, in both bite point scenarios. Alligator exhibited the lowest scaled total strain energy in the rostral bite point scenario, indicating that it is a more efficient, stiffer structure that undergoes less deformation than either of the other crocodylian models under those loading conditions (Table 9). The structural efficiency of

Alligator being greater than either of the other two crocodylians in this bite point scenario may be expected, given the much lower rostrum aspect ratio of the former (Fig. 7).

However, Tomistoma possessed a lower rostrum aspect ratio and exhibited a greater scaled total strain energy than Gavialis in both bite point scenarios. Surprisingly, the total strain energy in the Alligator model was similar to that in the Gavialis model in the caudal bite point scenario, but they both had less total strain energy than the Tomistoma model. Although Gavialis would experience failure at a lower applied force than

Tomistoma in both bite point scenarios, the total strain energy in Tomistoma was much 182 greater than Gavialis in each scenario. These results indicate that the Tomistoma cranium model is a much less efficient structure and would undergo much more overall deformation than the Gavialis model. Gavialis would experience failure at a lower applied force than Alligator in both scenarios. In the caudal bite point scenario, Gavialis and Alligator would undergo approximately the same amount of deformation, indicating that they are equally efficient structures in that bite point scenario. Although work efficiency varied inconsistently across models, the trend of maximum stress magnitudes matched the trend of maximum relative prey:predator size ratios in extant crocodylians and may be a contributing factor to differences in relative prey size ranges in these taxa.

The phytosaurs exhibited clear differences in regions of greatest stress concentration among models. However, much like the crocodylians, these regions, excluding the rostrum, were largely consistent in each taxon for both bite point scenarios.

In the rostral bite point scenario, both Ebrachosuchus and Parasuchus would fail at approximately the mid-length point of the rostrum under sufficient load, with

Ebrachosuchus experiencing failure at a lower applied force than Parasuchus.

Pravusuchus has a much more robust and dorsoventrally tall rostrum than any of the other sampled phytosaurs (Fig. 11), and this factor seems to have limited and more evenly distributed the stress concentration in the rostrum of this taxon, compared to the other phytosaurs. Instead, failure in the Pravusuchus model would initiate along the caudoventral margin of the pterygoid process of the quadrate and adjoining margin of the pterygoid, which was the region of second-greatest stress concentration in Parasuchus and Ebrachosuchus. Failure in Pravusuchus would require a higher load than either 183

Parasuchus or Ebrachosuchus. The Machaeroprosopus model would fail at a point along the medial aspect of the quadrate, near the quadrate foramen, and the load sufficient to induce failure in this taxon would be far greater than that required to cause failure in any of the other phytosaurs. In the caudal bite point scenario, both Ebrachosuchus and

Parasuchus would fail at the location of their greatest stress concentration in the rostral bite point scenario, excluding the rostrum and Pravusuchus would fail in the same place as in the rostral bite point scenario. Machaeroprosopus would fail along the ipsilateral lateral margin of the pterygoid, which is a region that did not exhibit a particularly great stress concentration in the rostral bite point scenario. Failure in the caudal bite point scenario would first occur in Ebrachosuchus, followed by Parasuchus, Pravusuchus, and

Machaeroprosopus, which is the same order of failure as in the rostral bite point scenario.

If the apparent relationship between maximum stress magnitude and maximum relative prey:predator size ratios found in extant crocodylians may be used to infer such prey:predator size ratios in phytosaurs, Ebrachosuchus was probably limited to food items below a relatively low maximum relative prey:predator size ratio, Parasuchus was probably limited to food items of somewhat greater maximum relative sizes than was

Ebrachosuchus, Parasuchus was probably limited to food items of considerably greater maximum relative sizes that Parasuchus but lower than any of the crocodylians, and

Machaeroprosopus was probably limited to food items of maximum relative sizes greater than that of Tomistoma but lower than that of Alligator.

The differences between phytosaurs, in terms of total strain energy in each model, were largely consistent between both bite point scenarios (Table 9). The one exception to 184 this was the total strain energy in the Pravusuchus model under the caudal bite point scenario. The reported total strain energy value for that model is so great as to be highly suspect, although performing the analysis of that model several times, including one attempt that began again at the point of creating a tetrahedral mesh and continued through the rest of the workflow, resulted in the exact same measurement values. The structural efficiency of Pravusuchus, in terms of work and total deformation, under the caudal bite point scenario load conditions was reported here, but uncertainty over the validity of those results remains sufficient to preclude comparing that specimen to the others in the caudal bite point scenario. Apart from that one anomaly, Machaeroprosopus underwent less deformation than Pravusuchus in the rostral bite point scenario, Pravusuchus underwent less deformation than Parasuchus in the rostral bite point scenario, and

Parasuchus underwent less deformation than Ebrachosuchus in both bite point scenarios.

This trend matches several morphological trends, including: the overall bone thickness and robusticity of the cranium, as Ebrachosuchus had a considerably more lightly built cranium with thinner bone than the rest of the phytosaurs (Butler et al., 2014); the rostral extent of the premaxillary sinus, which extends the entire length of the rostrum in

Ebrachosuchus, approximately half the rostral length in Parasuchus, and approximately one-third the rostral length in Pravusuchus and Machaeroprosopus; and the length of the caudal process of the squamosal, which also exhibited extremely low stress concentrations in Pravusuchus and Machaeroprosopus. Thus, differences in cranial structural efficiency among phytosaurs appears to be related to the evolution of multiple morphological features, and ascribing a greater relationship of one such feature to such 185 structural efficiency is not possible. Much like in the crocodylian models, work efficiency in phytosaurs varied inconsistently across taxa of different rostrum morphotypes. Work efficiency in the model of Pravusuchus, an altirostral phytosaur, in the rostral bite point scenario was lower than those of Ebrachosuchus and Parasuchus but greater than

Machaeroprosopus, all of which were dolichorostral phytosaurs. The work efficiency values in Ebrachosuchus, Parasuchus, and Machaeroprosopus were inverse to the order of those specimens in terms of rostrum aspect ratio, but Pravusuchus exhibited a lower rostrum aspect ratio than any of the other modeled phytosaurs (Fig. 11). It does not appear that work efficiency, on its own, is an appropriate proxy for inferring maximum relative prey:predator size ratios of food items that can be utilized in extant crocodylians and is, therefore, unfounded as a basis for inferring such ratios in phytosaurs.

From a structural perspective, the shape of the Ebrachosuchus model was the worst of any model, under both sets of load conditions tested here, followed by the

Parasuchus model. These taxa would both fail and undergo greater total deformation at lower loads than any other taxon, indicating that they likely could not withstand the forces applied to the cranium as a result of biting a relatively hard prey item as well as could the other sampled taxa. Despite being very different from one another, the shapes of the Gavialis, Alligator, and Pravusuchus models were the most similar to one another in terms of structural performance under the load conditions tested here. Although

Gavialis has been observed preying upon turtles and other small terrestrial tetrapods, this phenomenon is not as well-documented in that taxon as it is in Alligator (Table 1). These results indicate that potential differences in prey type utilization between Gavialis and 186

Alligator are likely due to factors other than the relative ability of those taxa to withstand the forces applied to the cranium that result from biting a hard prey item. Pravusuchus seems to have had at least the same capacity for preying upon hard food items as Gavialis and Alligator, based on the similarity of its performance to these taxa. The

Machaeroprosopus model performed superiorly to all of the other models, under both sets of loading conditions, and this taxon was likely capable of preying upon food items that were even harder than those utilized by the sampled extant crocodylians.

The differences in magnitude of the mediolateral and rostrocaudal components of total force production between phytosaurs and crocodylians may reflect differences in biting mechanics that are related to variations in prey type. The bites of phytosaurs, in both bite point scenarios, exhibited far greater mediolateral and rostrocaudal components of force than almost all of the crocodylians. This could indicate that phytosaurs producing lower bite forces that Alligator, for example, may have either utilized prey more susceptible to shear stress than those preyed upon by Alligator or processed food items with behaviors different from those performed by crocodylians.

Bite forces were generally consistent within each clade, after accounting for probable allometric effects, regardless of variations in rostrum morphology among taxa.

The phytosaurs all exhibited bite forces that seemed to be proportional to their size, relative to each other, and much greater than similarly sized crocodylians. Thus, the first null hypothesis that phytosaurs produced bite forces comparable to those produced by extant crocodylians, regardless of rostrum morphology, is rejected (Table 11). In the rostral bite point scenario, Alligator exhibited much lower von Mises stress 187 concentrations along the rostrum than did either of the other crocodylians, which exhibited similar rostrum stress concentrations to one another (Figs. 38–40). Because of

Table 11. Summary of hypotheses tested in this study, part 3. Statement of null and alternative hypotheses, the results of analyses pertinent to each hypothesis, and the conclusion drawn from interpretation of those results.

188 these results, increased maximum von Mises stress in the rostrum of extant crocodylians is here considered to be positively correlated with increased rostrum aspect ratio. The second null hypothesis that maximum von Mises stress in the rostrum does not increase along with the aspect ratio of the rostrum in extant crocodylians is, therefore, rejected.

Although the region of the cranium exhibiting the greatest stress concentration in the rostral bite point scenario in both Parasuchus and Ebrachosuchus was the rostrum, that was not the case in any of the other taxa. Furthermore, points of initial failure were unique to nearly all taxa. These results lead to a failure to reject the null hypothesis that no region of the cranium exhibits consistently greater stress concentrations than any other among the sampled taxa. The work efficiency of the cranium of Alligator was the greatest among crocodylians in the rostral bite point scenario, but it was similar to that of Gavialis in the caudal bite point scenario. In both bite point scenarios, Tomistoma was the least efficient structure among the crocodylian models. The efficiencies of these crania, therefore, do not appear to exhibit a consistent enough trend to consider work efficiency to be negatively correlated with increased rostrum aspect ratio in extant crocodylians.

These results lead to a failure to reject the null hypothesis that there is no correlation between structural efficiency and rostrum aspect ratio in extant crocodylians. The work efficiency of the Machaeroprosopus cranium model was far greater than that of any other taxon in each of the bite point scenarios. No similarities existed among the work efficiencies of the phytosaurs or between the phytosaurs and crocodylians in the rostral bite point scenario. In the caudal bite point scenario, the work efficiency of the

Parasuchus model was within the range of the crocodylians, but those of the other 189 phytosaur models were not. These results lead to a failure to reject the null hypothesis that structural efficiencies of phytosaur crania are not more similar to those of extant crocodylians with a particular rostrum aspect ratio.

Conclusions

Conflicting trends in bite force, bite force efficiency, and structural performance make it unclear which criteria of biomechanical performance in the cranium can best be used as a proxy for maximum relative prey:predator size ratios in extant crocodylians.

This ambiguity makes constraining inferences of such ratios in phytosaurs, based on comparisons to a single aspect of extant crocodylian cranial biomechanics, problematic.

However, the general trend of maximum relative prey:predator size seen in extant crocodylians does seem to be at least somewhat reflected in a combination of bite force production and the performance of the cranium, in terms of maximum stress magnitude.

Based on comparisons to that trend exhibited by extant crocodylians, phytosaurs like

Parasuchus and Ebrachosuchus were likely restricted to prey items below a relatively low maximum prey:predator size ratio, and taxa like Pravusuchus and

Machaeroprosopus were likely better able to utilize prey items with higher prey:predator size ratios that either approximated or exceeded those maximum ratios utilized by extant crocodylians such as Alligator.

In herbivorous mammalian taxa, the ability of the cranium to resist higher stress may be correlated with the performance of discrete periods of biting associated with consumption of relatively hard food items and relatively short periods of oral processing

(Figueirido et al., 2014). Conversely, a greater ability of the cranium to evenly distribute 190 stress may be correlated with the performance of repetitive chewing in extended mastication periods (Figueirido et al., 2014). Despite their moniker, phytosaurs were almost certainly not herbivorous. Still, some parallels may be drawn between the results presented here and those trends described in herbivorous mammals. Specifically, the crania of Ebrachosuchus and Parasuchus exhibited a lower ability to both resist and evenly distribute stress than any of the crocodylians, indicating that those taxa may have been restricted to food items that were both much softer and less durable than those of crocodylians. Pravusuchus may have been restricted to food items that were softer than any of the crocodylians, but it may have been able to engage in the performance of repeated bites on a food item in a manner similar to longirostrine extant crocodylians.

The cranium of Machaeroprosopus exhibited an ability to both resist high stress and evenly distribute stress that was only matched or exceeded by Alligator. These results indicate that Machaeroprosopus may have been able to both utilize food items that were as hard as those that Alligator is able to utilize and engage in the performance of repeated, powerful bite needed to break down larger food items, particularly if interactions with such large and/or hard food items primarily occurred in the caudal portions of the tooth row.

In addition to the usefulness of these interpretations of stress distribution and structural performance for constraining phytosaur food item type utilization, differences between phytosaurs and extant crocodylians in force components that do not translate directly as bite force may be important additional indicators of the mechanical properties of food items that could be utilized by phytosaurs. Force output along the y-axis is 191 recorded as bite force by both in vivo transducer experiments and the FEA results reported here. However, force output along the x- and z-axes may be important for imparting shear stress in food items. Differences between phytosaurs and extant crocodylians in the ability to impart such stress could indicate either substantial differences in the mechanical properties of prey items utilized by these two clades or differences in post-prey capture mechanical processing behaviors used to subdivide larger prey items into smaller units for ingestion. Although some phytosaurs, such as

Ebrachosuchus, possessed somewhat needle-like teeth, many phytosaurs possessed considerably more heterodont dentition than extant crocodylians or even many other faunivorous archosauromorphs, and the teeth of most phytosaurs exhibited features like carinae not seen in the teeth of extant crocodylians (Hungerbühler, 2000). This difference in dentition morphology between the two clades may be related to differences in food item capture behaviors and behaviors to subdivide large food items. Further investigations of the breadth and diversity of phytosaur dentition and the mechanical properties of various food items that would have been potentially available for utilization by phytosaurs are needed to elucidate the significance of each of these morphological and force production distinctions between phytosaurs and extant crocodylians.

Because all of the specimen models analyzed here were modeled using the same parameters and criteria, the results of each can be compared to one another in relative terms (Bright, 2014), with the understanding that the quantified values of the various measurements obtained from these models are likely somewhat different from those that would be obtained through in vivo sampling. Furthermore, relative differences in the 192 performances of the taxa represented here, in terms of both bite force production and structural strength, may be different under different model parameters, such as various loading conditions, gape angles, and so on. Additional analyses must be performed to determine the effects of these model parameter variants on the calculated performance of phytosaur crania. Future in vivo studies of extant crocodylians are also needed to validate the results of the model analyses conducted here, particularly on a range of extant crocodylian taxa outside of Alligator mississippiensis. Although some aspects of the models tested here may perform within acceptable ranges of in vivo measurements, based on the validity of the Alligator model (Sellers et al., 2017), continued efforts are needed to improve load conditions and other model parameters to better account for additional factors, such as cranial sutures (Bright, 2012; Curtis et al., 2013; Jones et al., 2017) and momentum, that contribute to in vivo results. It is currently difficult to decouple the effect of specimen size on bite force and bite force efficiency in specimens with widely varying shapes. A method of scaling bite forces must be developed in order to determine the amount of difference between specimens that is due solely to shape variation and allow for comparisons of bite force production among specimens of varying sizes. The ability to more appropriately infer aspects of phytosaur feeding ecology based on interpretations of the results presented here will continue to benefit from ongoing efforts in these future research directions, as will future efforts to accurately model the feeding ecology of any extinct faunivorous sauropsid.

193

CHAPTER 5: CONCLUSIONS

The link between form and function has been a cornerstone of paleontological research for much of its history (e.g., Gould, 1970; Seilacher, 1970; Hickman, 1988;

Rahman, & Smith, 2014). In particular, the relationship between the shape of the cranial skeleton and trophic ecology in extant taxa has been used as a basis for inferences about the trophic ecology of extinct taxa (e.g., Livezey, 1989; Zanno & Makovicky, 2011;

Asahara et al., 2016; Foth et al., 2017). Such paleoecological hypotheses have been proposed for phytosaurs, a clade known from a cosmopolitan distribution exclusive to the

Late Triassic, built largely on the assumption that similarity in overall form between phytosaurs and extant crocodylians can be used to infer a similarity in specific aspects of trophic ecology, such as diet variation (Hunt, 1989). However, such hypotheses often ignore morphological differences in specific skeletal regions, including the cranium, which could translate to functional differences that affect feeding behaviors and alter the relationship between overall form and function. This dissertation tested previous hypotheses based on qualitative assessments of gross similarity by quantitatively analyzing aspects of cranial morphologic disparity in a functional context. In addition to analyzing morphological differences in the skeleton of the cranium between phytosaurs and extant crocodylians, this dissertation also assessed topological and functional differences in the jaw musculature of these two groups. The jaw musculature and cranium shape of extant crocodylians and phytosaurs were also biomechanically analyzed to determine the functional effects of, and interplay between, variations in these two aspects morphology and anatomy. Each of the studies presented here tested hypotheses of 194 morphological variation, biomechanical function, the links between these two variables, and how each variable is correlated with diet variation in extant crocodylians. The results of these analysis were used to assess the utility of the foundations of functional morphological comparisons between extant crocodylians and phytosaurs. The combination of quantitative morphological and functional approaches presented here allows for a multifaceted consideration of factors underlying diet variation in extant crocodylians and the development of better constrained inferences of such variation in phytosaurs.

New Inferences about Phytosaur Ecology

Geometric morphometric analyses recovered a distribution of extant crocodylians in both overall cranium (Fig. 6) and rostrum (Fig. 7) shape space that was largely consistent with the maximum prey:predator size ratios utilized by those taxa (see

“Hypothesized Ecology of Phytosauria” in Chapter 1 of this volume). These results indicate a relationship between rostrum and overall cranium shape and diet variation in extant crocodylians that is somewhat different from previous hypotheses of a correlation between rostrum morphotype categories and taxonomic identities of prey items utilized by extant crocodylians (e.g., McHenry et al., 2006; Pierce et al., 2009). Phytosaurs did not exhibit overall cranium or post-orbital cranium morphological variation ranges that overlapped with the variation ranges exhibited by extant crocodylians, and only one phytosaur taxon exhibited a rostrum morphology that was within the range of rostrum morphological variation exhibited by extant crocodylians (Figs. 6–8). This lack of overlap between phytosaurs and extant crocodylians in the shape metrics analyzed here 195 indicates that the inference that phytosaurs exhibited prey:predator size ratios that were the same as those observed in any extant crocodylian taxon is unsupported. However, the range of rostrum:overall cranium length ratios exhibited by phytosaurs appears to be an extension of the end of that range in extant crocodylians occupied by longirostrine taxa, and the aspect ratios of phytosaur rostra fell within the range of rostrum aspect ratios seen in longirostrine extant crocodylians including Gavialis gangeticus and Tomistoma schlegelii. These results lead to the conclusion that although food items phytosaurs were capable of utilizing were probably not of the same maximum prey:predator size ratios as those utilized by any extant crocodylian, they were probably most similar to those utilized by longirostrine extant crocodylians. Additionally, the maximum prey:predator size ratios of food items that phytosaurs were capable of utilizing were probably slightly to substantially lower than those utilized by extant crocodylians such as Gavialis and

Tomistoma, as evidenced by the results of these geometric morphometric analysis.

The topology of much of the jaw musculature of phytosaurs resembled that of extant crocodylians. However, the same can largely be said of extant crocodylians and most other sauropsids (e.g., Anderson, 1936; Merz, 1963; Haas, 1973; Bock, 1985;

Holliday & Witmer, 2007; Holliday, 2009; Jones et al., 2009; Sereno et al., 2009; Jones et al., 2012; Gröning et al., 2013; Johnston, 2014; Previatto & Posso, 2015; Button et al.,

2016). The topological similarities between phytosaurs and extant crocodylians, then, are the result of plesiomorphy or shared deep ancestry, rather than convergence upon some functionally constrained topology that would be informative as the basis for ecological inferences. The results of comparisons between the jaw muscle topologies of phytosaurs 196 and extant crocodylians were not such that phytosaurs were found to be appreciably more similar to one crocodylian taxon than another because the crocodylians were all very similar to one another. Comparisons of jaw muscle origin and insertion surface area proportions demonstrated taxa within each clade to be more similar to each other than to taxa of the other clade. Neither clade, as a whole, was found to be more similar to one taxon of the other clade than to other taxa of that other clade. The positions of taxa in tangent space defined by the proportions of jaw muscle origin and insertion surface areas were such that phytosaurs and crocodylians occupied discrete regions of tangent space, and no taxa of either clade were found to be consistently more similar to a particular taxon of the other clade (Figs. 29–34). These results indicate that jaw muscle topology and attachment surface area proportions do not appear to be correlated with diet variation in extant crocodylians. Thus, inferences related to diet variation in phytosaurs cannot be based on comparisons of jaw muscle topology or attachment surface area proportions between phytosaurs and extant crocodylians.

Proportions of maximum muscle force of individual muscles were remarkably consistent across all taxa, with the slight exception of Gavialis and Machaeroprosopus

(Figs. 28, 35–37). Gavialis differed from the rest of the sample in having a slightly lower proportion of force produced by m. adductor mandibulae externus superficialis

(mAMES) and slightly greater proportions of force produced by m. pseudotemporalis superficialis and m. depressor mandibulae. Machaeroprosopus differed from the rest of the sample in having lower proportions of force produced by m. pterygoideus dorsalis and m. pterygoideus ventralis and greater proportions of force produced by mAMES and 197 m. adductor mandibulae posterior. These results indicate that some difference exists between the muscle force proportions of the extant crocodylian with the greatest rostrum aspect ratio, Gavialis, and those of other members of that clade. However, the functional relevance of this difference to aspects of feeding behavior or diet variation is not entirely clear because the rest of the crocodylians were very similar to one another, despite exhibiting different rostrum aspect ratios and utilizing food items of different maximum prey:predator size ratios. If the proportional muscle force production of individual jaw muscles is in some way correlated with maximum prey:predator size ratios in extant crocodylians, it is probable that phytosaurs were capable of utilizing food items of maximum prey:predator size ratios that were unlike those utilized by Gavialis and within the range of those utilized by all other extant crocodylians. Additionally, the maximum prey:predator size ratio of food items that could be utilized by Machaeroprosopus was probably unlike those that could be utilized by any extant crocodylian or any other phytosaur, based on these results.

Biomechanical modeling of phytosaur and extant crocodylian crania estimated the bite force and bite efficiency of these modeled taxa. The bite forces and bite efficiencies of extant crocodylians were such that rostrum aspect ratios were inverse to both bite force and bite efficiency, after accounting for likely allometric effects. That same trend was not seen in the phytosaurs. Instead, the bite forces and bite efficiencies of both Parasuchus and Ebrachosuchus were greater than those of longirostrine extant crocodylians in both rostral and caudal bite point scenarios, and those metrics in Ebrachosuchus were greater than Alligator in the caudal bite point scenario. Although some of these differences in 198 estimated bite force may be the result of size differences among specimens, allometric effects alone were probably insufficient to account for all of that difference because these two phytosaur specimens were approximately the same size to slightly larger than the

Gavialis specimen, which was approximately the same size to slightly larger than the

Alligator specimen. The estimated bite forces of both Pravusuchus and

Machaeroprosopus were considerably greater than any of the other taxa, but these were also the largest specimens sampled. The bite efficiency of these two phytosaurs varied greatly between the two bite point scenarios but generally fell within the higher portion of the efficiency range exhibited by the crocodylians. The results indicate that Parasuchus and Ebrachosuchus were probably capable of producing bite forces high enough for those taxa to utilize food items of maximum prey:predator size ratios and mechanical properties, such as hardness, at least as great as those utilized by longirostrine extant crocodylians. Additionally, Pravusuchus and Machaeroprosopus were probably able to produce bite forces sufficient for those taxa to utilize food items of maximum prey:predator size ratios and mechanical properties that exceeded those utilized by any sampled extant crocodylian.

FEA results indicate that that the rostrum was never the location of initial failure in any extant crocodylian, in either bite point scenario and under sufficient load (Figs.

38–39). The differences in stress distribution and magnitude among crocodylians indicate that the Gavialis model was the weakest of these taxa, followed by Tomistoma and

Alligator, in both bite point scenarios. Stress distribution in the rostrum, therefore, does not appear to be a primary factor limiting the ability of any extant crocodylian to utilize 199 any particular food item. However, the maximum prey:predator size ratios and mechanical properties of food items that can be utilized by extant crocodylian taxa does seem to be inverse to the magnitude of load application that must be applied in order to induce mechanical failure of the cranium in those taxa. Alligator exhibited the lowest scaled total strain energy in the rostral bite point scenario of any crocodylian, indicating that it is a more efficient, stiffer structure that undergoes less deformation than either of the other crocodylian models under those loading conditions (Table 9). Gavialis exhibited a scaled total strain energy that was lower than Tomistoma in both bite point scenarios and similar to Alligator in the caudal bite point scenario. This lack of a clear trend in total strain energy among extant crocodylians that utilize food items with different maximum prey:predator size ratios and mechanical properties casts doubt on the utility of total strain energy comparisons as the basis for inferences about such diet variation in phytosaurs.

The stress distribution patterns seen in crocodylians are in contrast to those exhibited by the phytosaurs Ebrachosuchus and Parasuchus, which would initially fail at approximately the mid-length of the rostrum in the rostral bite point scenario, under sufficient load (Figs. 41A–D, 42A–D). Stress distribution in the rostrum would probably be a primary factor limiting the ability of these taxa to utilize a food item above a certain maximum prey:predator size ratio or with particular mechanical properties. Stress magnitudes in the rostrum were lower in Pravusuchus than any other phytosaur, which was probably an effect of the greater robusticity and dorsoventral height of the rostrum in that taxon, compared to the others (Fig. 11). Similar to the stress distributions in extant 200 crocodylians, initial failure would not occur in the rostrum of either Pravusuchus or

Machaeroprosopus. In both bite point scenarios, Ebrachosuchus was the weakest phytosaur model, followed by Parasuchus, Pravusuchus, and Machaeroprosopus. Failure in Ebrachosuchus, Parasuchus, and Pravusuchus would occur at a lower applied load than any of the crocodylians. Failure in Machaeroprosopus would require a higher applied load than Tomistoma but a lower applied load than Alligator. Comparing the FEA results for phytosaurs and extant crocodylians allows for the inference that the maximum prey:predator size ratios and mechanical properties of food items that could be utilized by most phytosaurs, including the dolichorostral Parasuchus and Ebrachosuchus and the altirostral Pravusuchus, were likely lower than those that can be utilized by any sampled extant crocodylian. The dolichorostral phytosaur Machaeroprosopus, however, was probably able to utilize food items of a maximum prey:predator size ratio and with mechanical properties, such as hardness, that both exceeded those that can be utilized by longirostrine extant crocodylians and were similar to those that can be utilized by other crocodylians, such as Alligator.

The results of analyses presented here offer a greater ability to more confidently constrain the probable range of food items that phytosaurs could utilize, particularly when considering the results of any one analysis. Synthesizing the results of all of the analyses presented here creates a very complex picture of the relationship between functional morphology and diet in extant crocodylians and causes inferences of diet ranges in phytosaurs to be less clear due to the often incongruent trends and indications of different sets of results. For example, the results of geometric morphometric analysis 201 indicate that phytosaurs were capable of utilizing food items of maximum prey:predator size ratios that were lower than, but most similar to, longirostrine extant crocodylians like

Gavialis and Tomistoma. Comparisons of the proportional muscle force production of individual jaw muscles, however, indicate that phytosaurs were capable of utilizing food items of maximum prey:predator size ratios that were unlike those utilized by Gavialis and within the range of those utilized by all other extant crocodylians. Based on those same comparisons, Machaeroprosopus appears to have been able to utilize food items with maximum prey:predator size ratios unlike those that could be utilized by any of the other sampled taxa. Comparisons of bite forces and bite efficiencies indicate that both

Parasuchus and Ebrachosuchus were probably capable of utilizing food items of maximum prey:predator size ratios and mechanical properties, such as hardness, at least as great as those utilized by longirostrine extant crocodylians, and both Pravusuchus and

Machaeroprosopus were probably able to utilize such food items that exceeded those utilized by any sampled extant crocodylian. Stress distribution was very different between crocodylians and phytosaurs, in terms of the stress concentration in the rostrum being a limiting factor of the ability to withstand a great applied load. Comparisons of stress distributions also indicated that Machaeroprosopus was probably able to utilize food items of a maximum prey:predator size ratio and with mechanical properties, such as hardness, that both exceeded those that can be utilized by longirostrine extant crocodylians and were similar to those that can be utilized by other crocodylians, such as

Alligator, whereas those properties of food items that could be utilized by the other phytosaurs were likely lower than those that can be utilized by any extant crocodylian. 202

In general, phytosaurs with cranial morphology similar to that of either

Parasuchus angustifrons or Ebrachosuchus were probably limited to utilizing food items with prey:predator size ratios and mechanical properties, such as hardness, lower than those utilized by Tomistoma and possibly not exceeding those utilized by Gavialis. On the other end of the spectrum, Machaeroprosopus pristinus and other phytosaurs with similar cranial morphology to M. pristinus were probably able to utilize food items with prey:predator size ratios and mechanical properties that spanned a range similar to, or plausibly in excess of, those food items utilized by any of the sampled extant crocodylians. Results of analyses of Pravusuchus generally found it to be variable in its greater similarity to either Machaeroprosopus or Parasuchus and Ebrachosuchus. Thus, trends of similarity between Pravusuchus and any particular extant crocodylian taxa are less clear than those of the other sampled phytosaurs. Still, these results indicate that

Pravusuchus and other phytosaurs with similar cranial morphology were probably able to utilize food items with prey:predator size ratios and mechanical properties, such as hardness, no lower than those of phytosaurs with cranial morphology similar to

Parasuchus and Ebrachosuchus or longirostrine extant crocodylians such as Gavialis and

Tomistoma. It is also plausible that Pravusuchus and other phytosaurs with similar cranial morphology were capable of utilizing food items with prey:predator size ratios and mechanical properties approaching, but not exceeding, those utilized by phytosaurs with cranial morphology similar to Machaeroprosopus or extant crocodylians of the generalized or brevirostrine morphotype, such as Alligator. 203

This dissertation has returned multiple novel results, including those of various geometric morphometric analysis and stress distributions calculated with FEA of a simulated bite, that support previous hypotheses and inferences of a correlation between variation in rostrum morphology and diet in extant crocodylians, although the exact nature of that correlation is considered here to be slightly different from those previous assertions. The analysis described here were also the first to test previously stated hypotheses of diet variation in phytosaurs—specifically that dolichorostral phytosaurs were similar to longirostrine extant crocodylians in being piscivorous (Hunt, 1989)—and the results reported here indicate no support for those hypotheses. One major problem with this previously proposed hypothesis of diet variation in phytosaurs is that it assumes longirostrine extant crocodylians are strictly, or at least primarily, piscivorous and crocodylians within different rostrum morphotype categories are not. Because the foundation upon which this hypothesis is built is inaccurate (Table 1; see also

“Hypothesized Ecology of Phytosauria” in Chapter 1 of this volume), the entire hypothesis appears to be groundless. Additionally, whereas some phytosaurs, such as those with cranium morphology similar to the dolichorostral taxa Parasuchus angustifrons and Ebrachosuchus, probably utilized food items most similar to those utilized by extant longirostrine crocodylians like Gavialis and Tomistoma, those with cranium morphology similar the dolichorostral taxon Machaeroprosopus were probably capable of utilizing food items similar to those utilized by extant crocodylians of the generalized or brevirostrine morphotype, such as Alligator. Additionally, the altirostral phytosaur Pravusuchus was not shown to demonstrate any aspect of functional 204 morphology that distinguished it from the range of dolichorostral taxa and would support an inference of an appreciable difference in diet between altirostral and dolichorostral phytosaurs.

Future Directions

Although some conclusions may be drawn from the general trends and similarities in aspects of functional morphology of phytosaurs and extant crocodylians analyzed here, further research and additional investigations along these lines will certain aid in clarifying the relationship between form and function in the extant crocodylian feeding apparatus. In turn, such work will benefit efforts to interpret morphological variations observed in a wide variety of extinct sauropsids, in an ecological context, based on comparisons to extant crocodylians. For example, studies of cranial morphologic variation in extant crocodylians do not often include extinct taxa, severely limiting inferences of evolutionary or adaptive significance of such variation. The inclusion of extinct taxa (e.g., Toyotamaphimeia machikanensis, Eosuchus lerichei, Crocodylus thorbjarnarsoni, etc.) in such analyses will allow for more robust conclusions that incorporate aspects of change on the temporal scale, such as ecological shifts.

The geometric morphometric analyses presented here are good examples of studies that could benefit from a broader base of knowledge resulting from more robust approaches for testing hypotheses of cranium shape variation in extant crocodylians. For example, morphometric analyses of crocodylian cranium shape almost always focus on the preorbital skeleton and ignore potential variation in the post-orbital cranium. As demonstrated in this volume, shape variation in the post-orbital cranium of extant 205 crocodylians does not fit the same trend as that seen in variation of rostrum shape.

However, some general trends in post-orbital shape within Crocodylia were seen that could be functionally significant. Unfortunately, determining the exact nature of that trend was outside the scope of the present study. Variation in cranium shape exhibited in phytosaurs was largely described by variables including post-orbital cranium shape, but the lack of information about the functional or ecological implications of post-orbital cranium variation in extant crocodylians hindered comparisons between the two clades on this basis. Phytosaur cranial shape variation is also largely described by differences in rostrum height among taxa. Geometric morphometric analyses of crocodylian cranium shape have, as yet, not addressed the potential of rostrum height variation among crocodylian taxa for impacting crocodylian trophic ecology, meaning that comparisons to phytosaurs in these terms hindered. Future studies of cranial morphologic variation in extant crocodylians must address aspects of cranium shape that go beyond comparisons of rostrum aspect ratio, such as post-orbital cranium shape and rostrum height variation.

The vast majority of anatomical or functional morphologic—and even ecological—studies of extant crocodylians focus on a small number of taxa, most often

Alligator mississippiensis. Although the ability to study wild specimens of other crocodylian taxa is probably limited by protection of those taxa put in place because of conservation efforts, captive individuals represent an acceptable, if less than ideal, alternative source of anatomical information that is currently lacking. For example, the jaw musculature of relatively few taxa has been studied in detail, and that of even fewer taxa has been described using modern digital dissection techniques (e.g., Metscher, 2009; 206

Jeffery et al., 2011). This lack of a broad sample means that much of the potential range of variation in jaw muscle topology within extant Crocodylia is unknown, and the resulting ability to interpret and contextualize the wide variety of jaw muscle topologies observed among extinct archosauromorphs is at a severe disadvantage. Far more work is needed to fill in the information gaps regarding variation in jaw musculature topology among extant crocodylians.

In addition to the benefits that would derive from additional future research on crocodylians, many functional morphology studies would benefit from continued advances in various methodological aspects. For instance, the ability to meaningfully compare the biomechanical performance of different taxa would not be possible without a means of scaling either the specimen models or the calculated results of analysis.

However, there is currently no satisfactory way of scaling models or results for specimens of such widely differing shape as crocodylian and phytosaur crania. Bite force production, for example, would seemingly be an extremely useful metric for comparing the ability of disparate taxa to utilize particular food item types, but there is currently no means of scaling these magnitudes that would allow for such direct comparisons between the specimens sampled in this study. Similarly, although calculated maximum stress magnitudes can be scaled among models, doing so relies on surface area as a scaling factor. Such scaling would be appropriate for specimen models that do not demonstrate widely different shapes, but phytosaurs and crocodylians differ so greatly in many aspects of cranium shape (e.g., the presence of a bony-bounded airway that runs nearly the length of the skull in crocodylians but is absent in phytosaurs, the presence of 207 antorbital fenestrae in phytosaurs and their lack in crocodylians, and the presence of a solid bony crest on the rostrum of some phytosaurs) that scaling models based on surface area was not appropriate. Thus, exact values for maximum stress were not able to be reported here. Alternative methods for scaling models and analysis results may be limited, mathematically, but if future research is able to determine an acceptable proxy for current scaling methods, studies of trophic ecology in paleontology would surely greatly benefit.

Potential future directions of research focused on phytosaur ecology are nearly limitless, given that this clade has never before been the focus of a rigorous functional morphology study. The results presented here highlight several aspects of phytosaur anatomy and functional morphology that are of great interest and potentially great utility in furthering efforts to constrain inferences of phytosaur ecology. The functional role of the rostral crest exhibited by some phytosaur species is currently unknown. If phytosaurs did acquire aquatic food items with similar lateral movements of the head that most, if not all, species of extant crocodylians use to capture teleosts, it is seemingly unlikely that a crested phytosaur would be able to perform such a behavior as effectively as one lacking a crest. One means of testing such a hypothesis would be to characterize and quantify the neck musculature of closely related, crested and un-crested phytosaurs and contextualize these results with those of computational fluid dynamics (CFD) analyses of the rostra of those same taxa. The teeth of many phytosaurs are also very morphologically distinct from those of crocodylians. A combined morphometric and biomechanical approach to analyzing the functional implications of these morphological 208 differences in dentition would further clarify any differences in how the two clades may have directly interacted with food items. Beyond studies directly related to phytosaurs, functional morphology studies of other Late Triassic taxa would provide a great deal of information that would contextualize the results presented here. One example of such a study would be to biomechanically model shells, scales, carapaces, osteoderms, and so on, of invertebrates, teleosts, and tetrapods that comprised the faunal communities in which phytosaurs existed. The results of such a study, coupled with the results presented here, would approach the question of trophic system structure during the Late Triassic from both the predator and prey perspective and would allow for far more specific inferences and reconstructions of that structure than an approach from only one of those perspectives. Future studies such as these will continue to build upon the foundation of knowledge resulting from the analyses presented here and undoubtedly allow for a better understanding of ecosystem structure and changes during the time of relatively high faunal community instability following recovery from the end-Permian mass extinction and leading into the Late-Triassic mass extinction.

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APPENDIX: DETAILED TABLE OF DIETARY DATA FOR EXTANT

CROCODYLIANS

Documented feeding of extant crocodylian taxa upon specified prey taxa, as determined from observations of feeding events in the wild, stomach content analyses, and/or fecal content analyses. Numbers in each cell correspond to the following references: (1) Kellog (1929), (2) Giles & Childs (1949), (3) Fogarty & Albury (1968), (4) Chabreck (1971), (5) Neill (1971), (6) Valentine et al. (1972), (7) McNease & Joanen (1977), (8) Delaney & Abercrombie (1986); (9) Wolfe et al. (1987), (10) Delaney (1990), (11) Platt et al. (1990), (12) Elsey et al. (1992), (13) Barr (1997), (14) Rice (2004), (15) Rice et al. (2007), (16) Saalfeld et al. (2011), (17) Nifong & Silliman (2013), (18) Nifong et al. (2015), (19) Nifong (2016), (20) Taylor (1986), (21) Delaney et al. (1999), (22) Gabrey (2010), (23) Elsey et al. (2017), (24) Nifong & Lowers (2017), (25) Platt & Elsey (2017), (26) Weldon & McNease (1991), (27) Nifong et al. (2011), (28) Chamberlain (1930), (29) Elsey et al. (2004), (30) Martin et al. (2008), (31) Folk et al. (2014), (32) Nell & Frederick (2015), (33) Coulson & Coulson (2017), (34) Gabrey & Elsey (2017), (35) Chabreck & Dupuie (1976), (36) Bennet & Bennet (1990a), (37) Bennet & Bennet (1990b), (38) Butler (2009), (39) Rootes & Chabreck (1993), (40) Kinsella (1982), (41) Shoop & Ruckdeschel (1990), (42) Gabrey et al. (2009), (43) Epstein et al. (1983), (44) Huang (1982), (45) Staton & Dixon (1975), (46) Gorzula (1978), (47) Vanzolini & Gomes (1979), (48) Medem (1981), (49) Schaller & Crawshaw (1982), (50) Medem (1983), (51) Magnusson et al. (1987), (52) Fitzgerald (1988), (53) Gorzula & Seijas (1989), (54) Thorbjarnarson (1993), (55) da Silveira & Magnusson (1999), (56) Laverty & Dobson (2013), (57) Barão-Nóbrega et al. (2016), (58) Bontemps et al. (2016), (59) Schmidt (1928), (60) Miller (1918), (61) Guggisberg (1972), (62) Forero-Medina et al. (2006), (63) Varona (1983), (64) Carvalho (1951), (65) Aquino-Ortiz (1988), (66) Santos & Pinheiro (1992), (67) Krieg (1928), (68) Borteiro et al. (2009), (69) Marcgrave & Piso (1648), (70) Klappenbach & Orejas-Miranda (1969), (71) Diefenbach (1979), (72) Weyenbergh (1876), (73) Medem (1958a), (74) Bortero-Arias (2007), (75) Mudrek (2016), (76) Campos et al. (1995), (77) Dutra-Araújo (2017), (78) Jackson et al. (1974), (79) Vanzolini & Gomes (1979), (80) de Assis & dos Santos (2007), (81) Melo Sampaio et al. (2013), (82) Horna et al. (2001), (83) Tovar Serpa (1967), (84) Fountain (1902), (85) de la Ossa et al. (2010), (86) Hornaday (1885), (87) Shortt (1921), (88) Biswas (1970), (89) Whitaker (1975), (90) Singh (1977), (91) Saikia (2013), (92) Whitaker & Basu (1982), (93) Forsyth (1910), (94) Maskey & Schleich (2002), (95) Sind (1922), (96) Bezuijen et al. (1997), (97) Galdikas & Yeager (1984), (98) Galdikas (1985), (99) Rachmawan & Brend (2009), (100) Bezuijen et al. (2010), (101) Waitkuwait (1985), (102) Riley & Huchzermeyer (2000), (103) Pauwels et al. (2007), (104) Shirley et al. (2017), (105) Riley & Huchzermeyer (1999), (106) Luiselli et al. (1999), (107) Schmidt (1919), (108) Waitkuwait (1989), (109) Pauwels et al. (2003), (110) Platt et al. (2007a), (111) Welman & Worthington (1944), (112) Hippel (1946), (113) Cott (1954), (114) Corbet (1959), (115) Corbet (1960), (116) Cott (1961), (117) Graham (1968), (118) Blomberg (1977), (119) Hutton (1987), (120) Wallace & Leslie (2008), (121) Stevenson- 257

Hamilton (1917), (122) Pauwels et al. (2017), (123) Attwell (1954), (124) Piennar (1969), (125) de Sola (1930), (126) Soberón et al. (2001), (127) Schmidt (1924), (128) Platt et al. (2002), (129) Finger (2004), (130) Platt et al. (2006), (131) Platt & Rainwater (2007), (132) Cedeño-Vázquez et al. (2016a), (133) Cedeño-Vázquez et al. (2016b), (134) Tellez et al. (2017), (135) Platt et al. (2016), (136) Platt et al. (2007b), (137) Seijas (1998), (138) Humboldt (1907), (139) Medem (1958b), (140) Antelo et al. (2008), (141) Tárano (2007), (142) Álvarez del Toro (1974), (143) Thorbjarnarson (1988), (144) Cupul-Magaña et al. (2008), (145) Villegas & Schmitter-Soto (2008), (146) Platt et al. (2013), (147) Alonso-Tabet et al. (2014), (148) Casas-Andreu & Barrios-Quiroz (2003), (149) Beltrán-López (2015), (150) Cervantes et al. (2017), (151) Thorbjarnarson (1989), (152) Cupul-Magaña et al. (2015), (153) Dugan et al. (1981), (154) Aprill (1994), (155) Plotkin & Zannella (1994), (156) Ortiz et al. (1997), (157) Cupul-Magaña et al. (2005), (158) Caldwell (1986), (159) Casas-Andreu & Méndez de la Cruz (1993), (160) Richards & Wasilewski (2003), (161) Webb et al. (1982), (162) Tucker et al. (1996), (163) Johnson (1973), (164) van Weerd (2010), (165) Ross (1977), (166) Burgin (1980), (167) Pernetta & Burgin (1983), (168) Neill (1946), (169) Taylor (1979), (170) Webb et al. (1991), (171) Sah & Stuebing (1996), (172) Stuebing & Mohd Sah (1992), (173) Messel et al. (1981), (174) Allen (1974), (175) Webb (1977), (176) Santiapillai (2000), (177) Shelford (1916), (178) Whiting & Whiting (2011), (179) Webb et al. (1978), (180) Messel et al. (1980), (181) Kar & Bustard (1983a), (182) Samarasinghe & Alwis (2017), (183) Kar & Bustard (1981), (184) Kar & Bustard (1983b), (185) Daniel, 2002, (186) Daltry et al. (2003), (187) Bezuijen, 2010, (188) Sam et al. (2015), (189) Abdulali (1938), (190) McCann (1940), (191) Whitaker & Whitaker (1984), (192) Mobaraki (1999), (193) Whitaker (1999a), (194) Whitaker (1999b), (195) Mobaraki (2000), (196) Bhatnagar & Mahur (2010), (197) Mobaraki (2015), (198) Minton (1966), (199) Whitaker (1978), (200) Joshi et al. (2011), (201) Ranjitsinh (1989), (202) da Silva et al. (2011), (203) Smoothbore (1897), (204) Brander (1927), (205) da Silva et al. (1994), (206) Simcox (1905), (207) Bhattarai (2015). 258

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