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THE EVOLUTION OF UNGULATE LOCOMOTION

Permanent Link: http://ncf.sobek.ufl.edu/NCFE004732/00001

Material Information

Title: THE EVOLUTION OF UNGULATE LOCOMOTION UTILIZING EXTANT TAXA FOR RECONSTRUCING THE MOVEMENT OF EXTINCT FORMS
Physical Description: Book
Language: English
Creator: Carroll, Beth
Publisher: New College of Florida
Place of Publication: Sarasota, Fla.
Creation Date: 2013
Publication Date: 2013

Subjects

Subjects / Keywords: Ungulate
Locomotion
Evolution
Paleontology
Biology
Functional Morphology
Genre: bibliography   ( marcgt )
theses   ( marcgt )
government publication (state, provincial, terriorial, dependent)   ( marcgt )
born-digital   ( sobekcm )
Electronic Thesis or Dissertation

Notes

Abstract: Locomotor behavior is a complex neural and musculoskeletal response to an animal's environment and other external factors. Morphology, behavior, and gait choice are closely interrelated and often coevolve in response to environmental change. Morphological, specifically osteological, correlates of specific behaviors and movement patterns observed in extant taxa provides insight into that of extinct groups in which fossilized bones and trackways provide the only clues. Extant taxa can be useful models for reconstructing the movements and behaviors of extinct forms. The mammalian ungulate clades seen today are a representation of a rich and diverse evolutionary history filled with multiple examples of convergent and parallel evolution in response to similar environmental shifts and behavioral strategies. Modern ungulates (Tubulidentata, Hyracoidea, Sirenia, Proboscidea, Perissodactyla, and Artiodactyla) are useful models for both extinct ungulate groups and unrelated tetrapod vertebrates. While there are limitations, the study of ungulate evolution has uses that are not limited to reconstructing extinct taxa. In addition it has relevance in veterinary care, animal conservation, and robotics.
Statement of Responsibility: by Beth Carroll
Thesis: Thesis (B.A.) -- New College of Florida, 2013
Electronic Access: RESTRICTED TO NCF STUDENTS, STAFF, FACULTY, AND ON-CAMPUS USE
Bibliography: Includes bibliographical references.
Source of Description: This bibliographic record is available under the Creative Commons CC0 public domain dedication. The New College of Florida Libraries, as creator of this bibliographic record, has waived all rights to it worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law.
Local: Faculty Sponsor: Beulig, Alfred

Record Information

Source Institution: New College of Florida
Holding Location: New College of Florida
Rights Management: Applicable rights reserved.
Classification: local - S.T. 2013 C3
System ID: NCFE004732:00001

Permanent Link: http://ncf.sobek.ufl.edu/NCFE004732/00001

Material Information

Title: THE EVOLUTION OF UNGULATE LOCOMOTION UTILIZING EXTANT TAXA FOR RECONSTRUCING THE MOVEMENT OF EXTINCT FORMS
Physical Description: Book
Language: English
Creator: Carroll, Beth
Publisher: New College of Florida
Place of Publication: Sarasota, Fla.
Creation Date: 2013
Publication Date: 2013

Subjects

Subjects / Keywords: Ungulate
Locomotion
Evolution
Paleontology
Biology
Functional Morphology
Genre: bibliography   ( marcgt )
theses   ( marcgt )
government publication (state, provincial, terriorial, dependent)   ( marcgt )
born-digital   ( sobekcm )
Electronic Thesis or Dissertation

Notes

Abstract: Locomotor behavior is a complex neural and musculoskeletal response to an animal's environment and other external factors. Morphology, behavior, and gait choice are closely interrelated and often coevolve in response to environmental change. Morphological, specifically osteological, correlates of specific behaviors and movement patterns observed in extant taxa provides insight into that of extinct groups in which fossilized bones and trackways provide the only clues. Extant taxa can be useful models for reconstructing the movements and behaviors of extinct forms. The mammalian ungulate clades seen today are a representation of a rich and diverse evolutionary history filled with multiple examples of convergent and parallel evolution in response to similar environmental shifts and behavioral strategies. Modern ungulates (Tubulidentata, Hyracoidea, Sirenia, Proboscidea, Perissodactyla, and Artiodactyla) are useful models for both extinct ungulate groups and unrelated tetrapod vertebrates. While there are limitations, the study of ungulate evolution has uses that are not limited to reconstructing extinct taxa. In addition it has relevance in veterinary care, animal conservation, and robotics.
Statement of Responsibility: by Beth Carroll
Thesis: Thesis (B.A.) -- New College of Florida, 2013
Electronic Access: RESTRICTED TO NCF STUDENTS, STAFF, FACULTY, AND ON-CAMPUS USE
Bibliography: Includes bibliographical references.
Source of Description: This bibliographic record is available under the Creative Commons CC0 public domain dedication. The New College of Florida Libraries, as creator of this bibliographic record, has waived all rights to it worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law.
Local: Faculty Sponsor: Beulig, Alfred

Record Information

Source Institution: New College of Florida
Holding Location: New College of Florida
Rights Management: Applicable rights reserved.
Classification: local - S.T. 2013 C3
System ID: NCFE004732:00001


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THE EVOLUTION OF UNGULATE LOCOMOTION: UTILIZING EXTANT TAXA FOR RECONSTRUCING THE MOVEMENT OF EXTINCT FORMS BY BETH CARROLL A Thesis Submitted to the Division of Natural Sciences New College of Florida in partial fulfillment of the requirements for the degree Bachelor of Arts Under the sponsorship of Alfred Beulig Sarasota, Florida May, 2013

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ii A C KNOWLEDG MENTS I would like to thank Dr. Alfred Beulig for sponsoring my thesis and allowing me to ramble ab out ungulates for an hour a w eek as well as my other two committee members Dr. Amy Clore and Dr. Gordon Bauer I would also like to thank Kristi Giles and everyone else at the Maryland Zoo in Baltimore for allowing me to spend my summer observing and filming the animals. Also, thanks go to Ashley Burke a source of encouragement and advice along with the rest of the South Florida Museum staff, without whom I would not have the opportunity to personally handle ungulate fossils. Thank you Colleen Brandt fo r allowing me to film one of your horseback riding lessons. T hank you Gabi Bug aisky for taking the time to read thro ugh and provide feedback o n one of my early drafts.

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iii TABLE OF CONTENTS Acknowledgments ii Table of Contents i i i List of Figures v Abstract vii i Introduction 1 Chapter 1: What is an Ungulate Anyway? 4 Archaic Ungluates 8 Condylarthra 8 Mesonychia 9 South American Ungulates 10 Paenungulata 12 Tubulidentata 13 Hyracoidea 14 Proboscidea 16 Sirenia 18 Extinct Taxa: Embrithopoda and Desmostylia 21 Fereungulata 22 Cetartiodactyla 23 Perissodactyla 29 Why do we care? 32 Chapter 2: Locomotion 35 Defining Gaits 35

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iv TABLE OF CONTENTS Symmetrical Gaits 35 Asymmetrical Gaits 38 Walking or Running? 40 Foot Posture and Locomotion 45 Chap ter 3: Adaptations 49 Specializations Regarding Habitat and Locomotion 49 Horses: From woodland to grassland 50 Camelids: Strange feet and a pacing gait 57 Cervids and Bovines: Wide feet 61 Compensating for Mass and Size 63 Size 64 Mass/Weight 67 Mini me: Juveniles and dwarf lineages 74 Behavior 76 Migratory vs. Sedentary 80 Fight or Flight 82 Conclusion : Where do we go from here? 84 A caveat or two 84 Future research 88 Glossary 93 References 95

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v LIST OF FIGURES Chapter 1 Figure 1.1 A phylogeny of the extant Mammalia 6 Figure 1.2 A reconstruction of Andrewsarchus 9 Figure 1.3 Skeletal foot morphology of some cursorial litopterns 11 Figure 1.4 A restoration of M. patachonica 12 Figure 1.5 Aardvark ( O. afer) foraging at night 13 Figure 1.6 A pair of rock hyrax ( P. capensis) 15 Figure 1.7 Phylogeny of Proboscidea 16 Figure 1.8 Phylogeny of the sirenians 19 Figure 1.9 Arsinoitherium zitteli skull 21 Figure 1.10 Skeleton of the Desmostylian Paleoparadoxia 21 Figure 1.11 Skeletal pedal morphology of two cetartiodactyls and one Perissodactyl 22 Figure 1.12 Phylogeny of major lineages of Artiodactyla 23 Figure 1.13 A comparison of an artiodactyl astragalus 24 Figure 1.14 Extant cetartiodactyla family tree 25 Figure 1. 15 An inferred evolutionary history of an extant cetacean 28 Figure 1.16 Phylogeny and time periods of Perissodactyla 29 Figure 1.17 Reconstruction of a chalicothere 32 Chapter 2 Figure 2.1 Tripod support in walking symmetrical gaits 36 Figure 2.2 Example of diagonal and lateral two leg support 37

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vi LIST OF FIGURES Figure 2.3 The transverse gallop in relation to interference 39 Figure 2.4 The rotary gallop in relation to interference 40 Figure 2.5 Contrast in proportions and foot posture 46 Chapter 3 Figure 3.1 Pectoral girdle and left forelimb of a dolphin 50 Figure 3.2 The humerus of a horse 53 Figure 3.3 Lateral view of the left forel imb of a horse illustrating the passive stay apparatus in the shoulder region 54 Figure 3.4 A repr esentation of a resting horse with a stifle locked 55 Figure 3.5 Left femora of a tapir, camelid, and rhinoceros 56 Figure 3.6 The right manus of didactyl artiodactyl taxa 58 Figure 3.7 diagrams of tylopod and ruminant feet 58 Figure 3.8 Phylogeny of camelids and adaptations towards the extant C amelid foot morphology 61 Figure 3.9 The elongated hoof of a sitatunga 62 Figure 3.10 Comparison of graviportal and cursorial limb structure 68 Figure 3.11 Some graviportal adaptations in the foreleg of a elephant 69 Figure 3.12 Foot bones of the elephant manus and pes 70 Figure 3.13 A size comparison of an Indricothere, elephant, and human 73 Figure 3.14 Limb flexion and action in a cer atopsid dinosaur, horse, rhi no, and elephant 74 Figure 3.15 A giraffe grazing 76

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vii LIST OF FIGURES Figure 3.16 A okapi grazing 76 Figure 3.17 A moose grazing on metacarpal joints 77 Figure 3.18 A warthog feeding 77 Figure 3.19 Two male sable antelope fighting 77 Figure 3.20 A lesser kudu in the process of lying down in the grass 78 Figure 3.21 A camel scratching an itch 78 Figure 3.22 A Key deer scratching an ear 78 Figure 3.23 A adult gerenuk in the typical standing feeding posture 79 Figure 3.24 A sitatunga resting front hooves on a fence while browsing 79

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viii THE EVOLUTION OF UNGULATE LOCOMOTION: UTILIZING EXTANT TAXA FOR RECONSTRUCING THE MOVEMENT OF EXTINCT FORMS Beth Carroll New College of Florida, 2013 ABSTRACT Locomotor behavior is a complex neural and musculoskeletal response to an choice are closely interrelated and often coevolve in response to environmental change. Morphological, specifically osteological, correlates of specific behaviors and movement patterns observed in extant taxa provides insight into that of extinct groups in which fossilized bones and trackways provide the only clues. Extant taxa can be useful models for rec onstructing the movements and behaviors of extinct forms. The mammalian ungulate clades see n today are a representation of a rich and diverse evolutionary history filled with multiple examples of convergent and parallel evolution in response to similar env ironmental shifts and behavioral strategies. Modern ungulates (Tubulidentata, Hyracoidea, Sirenia, Proboscidea, Perissodactyla, and Artiodactyla) are useful models for both extinct ungulate groups and unrelated tetrapod vertebrates. While there are limitat ions, the study of ungulate evolution has uses that are not limited to reconstructing extinct taxa. In addition it has relevance in veterinary care, animal conservation, and robotics. ________________________ Dr. Alfred Beulig Division of Natural Sciences

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Carroll 1 Introduction Most people are familiar with one particular scene in the movie Jurassic Park the one involving a T rex chasing a jeep. While a high speed chase involving a vehicle and an extinct dinosaur already stretches the imagination, to most, the idea that Tyrannosaurus rex was a fearsome and speedy hunter does not seem quite as much of a leap. But how fast could T rex actually run? Top sprint speeds for these large theropods have been estimated as slow as 7 meters per second (m/s) and as fast as 18 20 m/s. A slightly more reasonable speed calculated using mathematical models in a study done by Farlow et al (1995) was determined to be around 10 m/s. value without context but it can provide a clearer picture into aspects of the behavior and ecology of these animals. Locomotor capabilities of an animal are closely tied to predator prey interactions, migratory behavior, diet, and habitat. Ten m/s might easily have been fast enough for a T rex to hunt it s chosen prey such as ceratopsids, which were in some cases equally massive. However, if ceratopsian dinosaurs were able to gallop much like modern day rhinoceroses (11 m/s), as some studies suggest (Paul and Christiansen, 200 0), a sprint of 10 m/s might not be fast enough. The locomotor capabilities of both T rex and their possible ceratopsid prey, has implications toward the long debated question of whether T rex were primarily scavengers or hunters.

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Carroll 2 These types of questions are not unique to the studies of dinosaur locomotion. In 1878, Eadward Muybridge was the first to utilize photography to answer a single question concerning horse locomotion. Do horses have all four hooves off of the ground at any point during either a tro t or a gallop? The answer was a resounding yes (Leslie, 2001) Muybridge was able to conduct his experiment with a set up of cameras and, most importantly, a living horse. The still frame rdings, but the process of using technology to record and break down the specifics of an There is, however, an additional problem when it comes to studying extinct organisms. There are no mastodons readily available to be recor ded and studied as they locomote, just as there are no T rex that may be encouraged to run in front of a camera chasing a jeep. A complete fossilized skeleton and perhaps fossilized trackways are the most one can hope for when studying the locomotor behavi or of extinct taxa. As a result, inferences must be made from what fossils are available as well as model systems. These model systems can be articulated and moveable skeletons of the animal in question, mathematical and computer generated models, or even related extant taxa. Variables that are found to correlate significantly well with speed across a wide range of extant animals in both a phylogenetic sense as well as a morphological sense are useful when making inferences concerning extinct animals, even when there are no extant animals that are closely related (Christiansen, 2002).

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Carroll 3 Understanding the evolution and morphology of locomotor behavior in extinct and extant ungulates as a response to environmental conditions has implications beyond simply reco nstructing the habits of fossil taxa. Ungulates are ideal for such studies due the rich and diverse morphologies and behaviors of extant forms and even more diverse extinct groups. A number of ungulate lineages have relatively complete fossil records as we ll The various ungulate clades are rife with examples of parallel and convergent evolution. Understanding the natural motion of ungulates is important for veterinary care, conservation, and animal welfare. The mechanics of tetrapod locomotion has been ap plied to the field of robotics as well and the development of computer modeli ng technology (Theodor, 2001; F ischer & Blickhan, 2006; Hackert et al., 2006; Maloiy et al., 2009; Sellers et al., 2009; Waldron et al., 2009; Biancardi & Minetti, 2012) In the f ollowing pages, I will be addressing the evolution of ungulate locomotion as can be inferred from a number of extant and extinct taxa. In the first chapter I will provide accounts of the various ungulate clades with a selection of significant characters an d notable taxa. The second chapter will cover the major concepts and terms in the study of locomotion and gait analysis. Chapter three will be focused on locomotor, behavioral, and morphological adaptations including the interaction of such and in response to environmental pressures. To conclude, I will indicate some important limitations of using extant taxa to make inferences about fossil forms such as an incomplete fossil record and behavioral variability. In the conclusion I will also present possible f uture avenues of investigation.

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Carroll 4 Chapter 1 What is an Ungulate anyway? In the simplest terms, ungulates are hoofed mammals. These animals have evolved to stand on the distal most phalange s that are encased externally in a nail like hoof. Traditionally, th e Ungulata included only Artiodactyls (even toed) and Perissodactyls (odd toed) unguligrade animals. Orders like Proboscidea (elephants groups, the true ungulates and subungulate s, were orig inally presumed closely related (Ferguson, 1997; Huffman, 2013). More recently, fossil and genetic analysis have revealed a more complicated picture. Groups found to have a common ancestor with hooves or related to other hoofed lineages were fo lost not only hooves but hind limbs entirely to better navigate an aquatic environment, are now considered as a part of the order Artiodactyla which has been renamed Cetartiodactyla to reflect th e change. Both fossil and DNA evidence agree to the inclusion, though the exact relationships within this new group remain a point of contention (Ferguson, 1997; Lecointre & Le Guyader, 2006; Meredith et al., hewissen & Madar, 1999; Phillips & Penny, 2001; Price et al., 2005; Archibald, 2012; Gatesy et al., 2012; Zhou et al., 2012; Huffman, 2013) The inclusion of DNA evidence has further scattered the different lineages once thought closely related under the n ow inaccurate infraorder Ungulata.

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Carroll 5 The Cenozoic is largely considered the age of the mammals. After the Cretaceous Paleogene (KPg) mass extinction event that wi ped out the non avian dinosaurs mammals experienced a dramatic intraordinal radiation and incr ease in species diversity to fill the now empty niches. The framework for the diversity we see today took root even before the end of the Cretaceous. In Eutheria the placental mammals, DNA evidence shows a deep, pre KPg, split among three super orders tha t appear to be divided almost geographically: Afrotheria (African placentals), Xenarthra (South America), and Boreoeutheria (northern hemisphere). Boreoeutheria further split into the Euarch ontoglires and Laurasiaeutheria (Phillips & Penny, 2001; Lecointre & Le Guyader, 2006; Meredith et al., 2011; Archibald, 2012) Of the extant ungulate clades, Paenungulata (Proboscidea, Hyracoidea, and Sirenia) remain grouped together, but are considered part of Afrotheria whereas the Artiodactyla (including Cetacea ) are in the Laurasiaeutheria (Phillips & Penny, 2001; Lecointre & Le Guyader, 2006; Meredith et al., 2011; Archibald, 2012). (see figure 1.1)

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Carroll 6 Figure 1.1 A phylogeny of the extant members of Mammalia. Ungulates are indicated with stars. Adapted from Lecointre & Le Guyader (2006)

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Carroll 7 While the order Ungulata is no longer a valid taxon the term is still valuabl e not only Artiodactyla and Perissodactyla, but Proboscidea, Hyracoidea, Sirenia, and Cetacea as well as a number of extinct Orders (Condylarthra, Embrithopoda, Desmostyli a, Notoungulata, and Litop terna) (Ferguson, 1997; Lecointre & Le Guyader, 2006; Meredith et al., Penny, 2001; Price et al., 2005; Jehle, 2006a; Archibald, 2012; Gatesy et al., 2012; Zhou et al., 2012; Huffman, 2013; Polly & Speer, n.d.) The or der Tubulidentata (aardvarks) is considered an ungulate group by most, but it is unclear how closely these animals r elate to the rest of Afrotheria (Polly & Speer, n.d.; Ferguson, 1997; Shoshani, 2001c; Huffman, 2013). lost secondarily in several lineages. Other lineages never even evolved hooves in the traditional sense. Chalicotheres, an extinct Family of Perissodactyla, sported large c laws on their front feet presumably used for tearing down vegetation when browsing (Prothero, 2001; Janis et al., 2012; Huffman, 2013; Polly & Speer, n.d.). The different groups are also not nearly as closely related phylogenetically as previously thought nor is the relationship as simple. Still, despite this, or in some cases because of it, the ungulate orders are full of examples of convergent and parallel evolution. Both extinct and extant ungulates display a wide disparate range of habitat, behavior, and morphology while at the same time demonstrating remarkably similar adaptations.

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Carroll 8 Archaic Ungulates Condylarthra Protungulatum, a small rat sized and most likely omnivorous mammal, is to a highly controversial grouping of archaic ungulates whose descendants make up all of the ungulate orders. Some authors have even questioned whether Protungulatum is even a placental mammal (Archibald et al., 2011). Overall the category Condylarthra i s a problematic one. Traditionally all archaic ungulates were filed under the catch all title of Condylarthra. The relationships between the various condylarth families are not consistently resolved and not all of t he groups had the same ancestor (Ferguson 1997; Jehle, 2006a; Lambert et al., 2008 ; Archibald et al., 2011) There has since been some redefining of Condylarthra resulting in a more specific group of taxa included ( Lambert et al., 2008 ), but there is still little consensus on what it actually m eans to be a condylarth or whether this term is a valid one or not (Jehle, 2006a; Archibald et al., 2011). Condylarthra might be a paraphyletic or even polyphyletic group consisting of several clades (Ferguson, 1997; Jehle, 2006a; Lambert et al., 2008 ; Arc hibald et al., 2011). The distribution of archaic ungulate fossils supports diversification of mammals taking place before the extinction of the dinosaurs and disputes the idea of mammalian radiation occurring only after the K Pg boundary. Fossil Protoungu latum indicates the presence of these early ungulates in North America by the Late Cretaceous, approximately 300,000 years before the extinction of non avian dinosaurs at the latest Because the status of Protungulatum as a placental

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Carroll 9 mammal is still under debate, it would be premature to show a definitive pre Cenozoic radiation of placentals, but the dispersal of ungulates while dinosaurs still roamed is clear (Archibald, 2011) Regardless, condylarths were widespread by the Paleocene and various condylarth lineages could be found in Eurasia, Africa, N orth America, and South America (Ferguson, 1997; Jehle, 2006a; Lambert et al., 2008 ; Archibald et al., 2011). There is even evidence of these early ungulates reaching Antarctica and Australia in the early Terti ary (Ferguson, 1997). There are a great number of different condylarth lineages exhibiting a wide variety of morphologies and diets. Many were forest dwelling and most were clawed, th ough some taxa possessed hooves ( Lambert et al., 2008 ) All of these ea rly groups are united in their relatively primitive characteristics as compared to their descendants and later ungulates. Mesonychia The mesonychids are best known for being an order of primarily carnivorous hoofed mammals. Thes e ungulates were more likely scavengers than pursuit predators, however (Janis & Wilhelm, 1993) Figure 1.2 depicts the triisodontine arctocyonid Andrewsarchus, a carnivorous ungulate found in Asia during the middle Eocene Jehle, 2006b) Andrewsarchus is widely considered to be the la rgest known member of Mesonychiidae but Figure 1. 2 A reconstruction of Andrewsarc hus Retrieved April 11, 2013 from http://www.abc.net.au/beasts/f actfiles/factfiles/andrewsarchus .htm

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Carroll 10 there is some question whether these large mammals were mesonychids at all or rather members of Artiodactyla or a separate group altogether (Jehle, 2006b; et al., 2012) Mesonyx, an Eocene predator roughly the size of a wolf, has a more stable membership in the family Mesonychiidae et al., 2012) Due to dental and othe r morphological characters, mesonychids were traditionally considered either closely related to or the ancestors of modern whales Mesonychia, once thought of as a sister tax on to C etacea, has also been included in Artiodactyla by some. However, DNA sequen ce analysis has since indicated that the similarities between mesonychids and cetaceans to be a result of convergent evolution. Mesonychia is now an order in its own right with three possible families, Mesonychidae, Hapalodectidae, and Triisodontidae (The ; Theodor, 2001; Jehle, 2006b; Foss & Prothero, 2007; Argot, 2012; Gatesy et al., 2012) South American Ungulates After the overall fragmentation of Gondwa na and for most of the Cenozoic, the South American continent was isolated from the other landmasses. Up until the formation of the Panama land bridge 2.5 million years ago that connected North and South America, the mammals of South America evolved indepe ndently. Condylarths and other archaic ungulate groups led to a variety of ungulate orders unique to South America (Ferguson, 1997; Tudge, 1997; Lambert et al ., 2008 ; Gelfo & Lorente, 2012) All of these orders are now extinct, but some persisted up until around

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Carroll 11 10,000 years ago (Tudge, 1997; Lambert et al ., 2008 ) The precise cause for the extinction of the ungulate groups endemic to South America is not precisely known. The introduction of new predators and competing species with the formation of the Pana manian land bridge and faunal interchanges may have played a role. It is also likely a combination of factors were the cause and these probably varied between different regions and different species. The South American ungulate clades evolved not only uniq ue adaptations, but also a surprising number of characteristics similar to or parallel to ungu lates found on other continents (Ferguson, 1997; Tudge, 1997; Lambert et al ., 2008 ; Gelfo & Lorente, 2012). Thoatherium and Diadiaphorus endemic to South America and belonging to the family Prototheriidae were standing on a single monodactyl hoof 20 million years before horses did the same (Ferguson, 1997; Lambert et al ., 2008 ). The possible four or more orders of South American hoofed mammal are loosely co mbined into Meridiungulata and/or Panameriungulata, but the delineations between these groups and relationships between the orders within them is still quite unclear. Two of the better known orders are the litopterns and notoungulates. Litopterns have be en assigned to the meridiungulates by some authors (Tudge, 1997) and the panameriungulates by others ( Lambert et al ., 2008 ; Gelfo & Lorente, 2012). The grassland environment is found in South America Figure 1 .3 Skeletal pedal morphology of some fast running litopterns (cursorial South American ungulates) Adapted from Lambert et al (2008)

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Carroll 12 roughly 15 million years earlier than elsewhere and as a result many liopterns were well adapted for running, most with either three or one toe(s). ( See figure 1.3) Some litopterns were horse like in appearance such as the family Prototheriidae, (Ferguson, 1997; Tudge, 1997; Lambert et al ., 2008 ). Another litop tern, Macrauchenia was very similar to camelids in size and appearance, (See figure 1.4) but ran on three toes and possessed a proboscis like that of the modern tapir (Ferguson, 1997; Tudge, 1997; Lambert et al ., 2008 ) The order notoungulata is usuall y included in the meridiungulates. This order was very diverse morphologically, including forms similar in appearance to hippopotamuses, rhinos, rodents, lagomorphs, and eve n giant sloths or chalicotheres (Ferguson, 1997; Tudge, 1997; Lambert et al ., 2008 ) The sizes of these animals ranged from that of a pig to that of a rhinoceros ( Lambert et al ., 2008 ) Having been isolated for nearly 60 million years, the ungulates of South America include some noteworthy examples of convergent and parallel evolution. Paenungulata Paenungulata (sometimes referred to as Uranotheria) is a Superorder of ungulates originating in Africa. Tubulidentata (aardvarks) are considered closely related to Paenungulata by some authors, but are thought more closely related to condyla rt hs by others (Shoshani, 2001c; Lecointre & Le Guyader, 2006; Archibald Figure 1.4 A restoration of M. patachonica by R.B. Horsfall, 1913 Retrieved April 11, 2013 from http://en.wikipedia.org/wik i/Macrau chenia

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Carroll 13 2012). Of the Paenungulata, Hyracoidea is generally considered to have diverged first. The remaining paenungulates make up the Tethytheria: Proboscidea and Sirenia along with the exti nc t Embrithopoda and Desmostylia (Phillips & Penny, 2001; Shoshani, 2001b; Shoshani, 2001a;Lecointre & Le Guyader, 2006; Archibald 2012) Taxeopody, the serial arrangement of the carpal bones, is a major postcranial synapomorphy. Contrasting the plesiomor phic condition (diplarthry) in which one carpal bone articulates with two bones below it, in taxeopody the bone on top articulates with on ly one bone directly beneath it (Shoshani, 2001b; Shoshani, 2001a; Lecointre & Le Guyader, 2006) Tubulidentata Th e aardvark ( Orycteropus afer ) is the only living species of the Afroth erian order Tubulidentata (See f igure 1.5) (Ferguson, 1997; Shoshani, 2001c; Lecointre & Le Guyader, 2006; Phillips & Penny, 2010; Archibald, 2012; Huffman, 2013) These insectivorous an imals are of a moderate size with a body length of 120 170 cm, tail length of 45 60 cm, and a weight of 50 100 kg. The forelimbs are proportionately shorter than the hind and the forefeet are highly specialized with four digits sporting powerful hoof like claws well adapted for shoveling dirt when digging. The hind feet have five clawed digits and two foot pads, the m etatarsal pad and calcanean pad (Shoshani, 2001c; Lecointre & Le Guyader, 2006) Aardvarks are Figure 1.5 Aardvark ( O. afer ) foraging at night Retrieved March 17, 2013 from http://www.arkive.org/aardvark /orycteropus afer/image G34770.html copyright N. J. Dennis

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Carroll 14 digitigrade when walking, but the pads on the re ar feet allow the animal to take a plantigrade position when crouching. The oldest known fossils from the order Tubulidentata date back to the lower Oligocene (30 34 Ma) (Shoshani, 2001c; Lecointre & Le Guyader, 2006) However, the skeletal characters o f this order are highly conserved, the genus Orycteropus having changed very little in the last 20 million years. Early Miocene representatives of this genus from eastern Africa 19 million years ago are nearly identical to the modern aardvark. It is quite appropriate to label the aardvark a Tubulidentata evolution and of interordinal relationships within Eutheria it is plausible that this taxon has its origins much earlier than the fossil record shows, perhaps in the Paleocene (about 65 Ma). It is even possible that this lineage extends back 70 million years and into the Cretaceous (Shoshani, 2001c) Hyracoidea Small size and superficial resemblances led early naturalist s to file hyraxes into the rodent category, but closer inspection of morphology of these tail less animals have since told a different story. Due to convergent morphological similarities, hyraxes have been at some point associated not only with Rodentia, b ut also with Perissodactyla, Notoungulata, Artiodactyla, or Tubulidentata among others. Skeletal characters and DNA support the current consensus that they are the closest extant terrestrial relatives of Proboscidea (Shoshani, 2001a; Lecointre & Le Guyader 2006)

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Carroll 15 The fossil record of these ungulates extends back roughly to the Eocene (55 50 Ma) of Africa. Over their evolutionary history there have been two families in Hyracoidea, Pliohyracidae and Procaviidae. Today, none of Pliohyracidae and only three genera of Procaviidae remain. Only four species are commonly recognized: the southern tree hyrax ( Dendrohyrax arboreus ), the western tree hyrax ( Dendrohyrax dorsalis ), the bush or yellow spotted hyrax ( Heterohyrax brucei ), and the rock hyrax ( Procavia cap ensis ) (Shoshani, 2001a; Lecointre & Le Guyader, 2006) (See Figure 1.6) The overall size of extant hyraxes is approximately that of a rabbit, ranging from 40 50 cm in length and 2.5 3.5 kg. This small size is a secondary trait, however. The extinct Eocene Titanohyrax was at least the size of a large goat, p erhaps even the size of a tapir (Shoshani, 2001a; Witte et al., 2002; Lecointre & Le Guyader, 2006) Having secondarily become smaller, modern hyraxes have retained some of the limb adaptations seen in l arger cursorial ungulate forms, including the absence of a clavicle (Witte et al., 2002). The four toed plantigrade forefeet and three toed digitigrade hind feet found in extant hyraxes are secondarily derived from non plantigrade ungulate stock. In additi on to the acquisition of plantigrady, hyrax feet are highly specialized for climbing with elastic pads kept moist by sweat glands that help to in crease traction on steep slopes (Fischer, 1994; Shoshani, 2001a; Lecointre & Le Guyader, 2006) Primarily herbi vorous, hyraxes inhabit a wide range of Figure 1.6 A pair of rock hyrax ( Procavia capensis ) at the Maryland Zoo in Baltimore. Photo by Beth Carroll, 2013

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Carroll 16 terrestrial and arboreal habitats. Rock hyraxes ( P. capensis ) are most well known for their rupicolous habits (Lecointre & Le Guyader, 2006) Proboscidea Proboscidea is one of two ex tant groups belonging to the Tethytheria. This clade includes extant elephants and their extinct relatives. Of a diverse lineage consisting of approximately 28 genera encompassing 165 species, the oldest of which date back to the late Paleocene (about 55 M a), only three species remain Figure 1.7 Phylogeny of the Proboscidea. Major trends observed are; increase in size, increase in trunk length, increase in tusk size, and a shift from four (upper and lower) to two tusks, upper only. Adapted from Shoshani (2001)

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Carroll 17 today (Shoshani, 2001b; Lecointre & Le Guyader, 2006) Originating in Africa, proboscideans have at some point occupied every continent with the exception of Antarctica and Australia, habitats ranging from snow and ice to dese rt (Shoshani, 2001b). Elephants today are limited to Africa and Asia. (See figure 1.7) African elephants, genus Loxodonta can be divided into two ecotypes. Loxodonta africana savanna elephants (also called bush elephants) are the largest of extant terre strial mammals, weighing of 4 7 tonnes (4000 7000 kg) and reaching a maximum height of approximately 4 meters at the shoulder (Shoshani, 2001b; Lecointre & Le Guyader, 2006; Ren et al., 2008; Ren & Hutchinson, 2008; Kokshenev & Christiansen, 2010). With a maximum shoulder height of 3 meters and weight of 2 4 tonnes, the smaller of the two African elephants is the forest, or dwarf, elephant ( L. cyclotis) (Shoshani, 2001b). The forest and savanna elephants are considered separate species by some (Shoshani, 20 01b; Kokshenev & Christiansen, 2010) while other authors are more reluctant (Hutchinson et al., 2006) relegating the two to the subspecies level (Lecointre & Le Guyader, 2006). As the common names suggest, L. africana inhabit savanna and grassland regions while L. cyclotis live in forested regions. Beyond habitat, there are also morphological features distinguishing the two. Ear and tusk shape, cranial pneumatization, and mandible len gth are among those differences (Shoshani, 2001b). The number of toenails found in adults for both fore and hind feet also differs, but as toenail number is variable between individuals as well as species, this character is not entirely reliable (Shoshani, 2001b; Miller et al., 2008).

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Carroll 18 The forest dwelling Asian elephants ( Eleph as maximus ) are in general smaller in size than their African cousins, weighing roughly 2 5 tonnes and 2 3.5 meters in height. E. maximus exhibit anatomical differences as well including back shape, ear shape, and limb proportions among others. The differ ing morphology and behavior of Asian and Africa n elephants indicate not only di ssimilar ecological adaptations but evolutionary histories as well (Shoshani, 2001b; Kokshenev & Christiansen, 2010) There are at least three recognized subspecies of Asian ele phant: the mainland ( E. m. indicus) the Sri Lankan ( E. m. maximus ), and the Sumatran ( E. m. sumatranus ) (Shoshani, 2001b; Lecointre & Le Guyader, 2006). Sirenia The second extant group of Tethytheria are the only living herbivorous marine mammals. The earliest Sirenia appears in the fossil record is the Eocene (40 Ma) and the two extinct families of Sirenia (Prorastomidae and Protosirenidae) se em to be confined to that epoch (Lecointre & Le Guyader, 2006; Domning, 2012; Benoit et al., 2013). (See Figur e 1.8)

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Carroll 19 Sirenia now only consists of two families, the Trichechidae (manatees) and the Dugongidae (dugongs) represented by on ly two genera and four species (Domning, 2012). The three extant species of manatees all belong to the genus Trichechus and inh abit the Atlantic basin: the Amazonian manatee ( T. inunguis), the West African manatee ( T. senegalensis ), and the West Indian manatee ( T. manatus ). There are two subspecies of T. manatus the Florida manatee ( T. manatus latirostris ) and the Antillean manat ee ( T. manatus manatus ) (Domning, 2012). Manatees generally range from 2.8 meters up to 4 meters in length, and can reach weights of 1500 kg. (Reid, 2002; Reid, 2005; Lecointre & Le Guyader, 2006). Figure 1.8 Simplified phylogeny of the sirenians. Adapted from Domning ( 2012 )

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Carroll 20 Within historic times, there have been two species of dug ong, the modern dugong ( Dugong dugon seacow ( Hydrodamalis gigas). Perhaps the largest sirenian that has ever lived, a nd weighed around 4 tons. This sirenian was also the representative of a lineage that had adapted to the cooler waters of the North Pacific unlike other sirenians. Subsisting on a diet of kelp, this large seacow was quite literally toothless, having lost n ot only teeth, but also phalanges from its flippers. H. gigas was hunted to extinction by humans, the last known ind ividual killed in the year 1798 (Lecointre & Le Guyader, 2006; Domning, 2012). Sirenians have adapted to a n obligatory aquatic lifestyle an d as a result share many similar traits to Cetacea. Convergent with whales and other cetaceans, sirenians have lost the hind limbs and have formed swimming paddles out of the forelimbs. Unlike cetacea, the hands in sirenia form swimming paddles without th e hyperphalangy seen in cetacea (Lecointre & Le Guyader, 2006; Gatesy et al., 2012) A powerful tail with horizontal flukes used to propel the animal through the water is another similar trait shared by the two aquatic lineages. However, the shape of the ta il differs, more so in the manatee. The manatee tail is round. In dugongs, the tail is bifurcated into two lobes, more si milar to that seen in cetaceans (Lecointre & Le Guyader, 2006; Domning, 2012)

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Carroll 21 Extinct Taxa: Embrithopoda and Desmostylia Both E mbrithopoda and Desmostylia are extinct groups of mammal that are as a result, are included in the Tethytheria (Ferguson, 1997; Domning, 2012; Benoit et al., 2013; Polly & Sp eer, n.d.) The most well known and for a while only, example of Embrithopoda is Arsinoitherium a large horned mammal that bears a strong resemblance superficially to the Rhinoceros. (See Figure 1.9) Unlike the rhino, however, the two massive horns on its head are bony in origin. This trait is one example of convergence between Perissodactyla and Embrithopoda, a group most closely related to Proboscidea (Polly & Speer, n.d.; Ferguson, 1997) Desmostylia are another stem Tethytheres group (Ferguson, 1 997; Domning, 2012; Benoit et al., 2013; Polly & Speer, n.d.) Functionally, these animals were amphibious, most likely dwelling in fresh water (Ferguson, 1997;Benoit et al., 2013; Polly & Speer, n.d.) These odd mammals with stumpy yet fully formed robus t limbs and shovel like jaws have structurally been compared analogously with the hippopotamus, however the desmostylian lifestyle may have been more like that of sea lions. While capable of moving about on land, they may only have Figure 1.9 photograph of a skull of Arsinoitherium zitteli Retrieved Ap ril 11, 2013 from http://commons.wikime dia.org/wiki/File:Arsinoi therium_zitteli_skull.JPG ( Wikimedia commons ) Figure 1.10 Skeleton of the Desmostylian Paleoparadoxia Retrieved from http://www.slac.stanford.edu/history/pa leo.shtml

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Carroll 22 done so in order t o rest or mate (Polly & Speer, n.d.; Ferguson, 1997) ( See figure 1.10) It is unclear how exactly Desmostylia relates to both Sirenia and Proboscidea, but it is possible this group is mor e closely related to the latter (Ferguson, 1997) Fereungulata subdivision of the Laurasiatheria. Fereungulata consists of the orders Perissodactyla, Cetartiodactyla, Carnivora, and Pholidota. Carnivora and Pholidota (pangolins) make up the group Ferae. The prec ise relationships between Ferae, Perissodactyla, and Cetartiodac tyla are not yet fully resolved (Lecointre & Le Guyader, 2006; Archibald, 2012). As the focus of this thesis is ungulates, I will only be addressing the characteristics of Perissodactyla and C etartiodactyla out of the orders belonging to Fereungulata. The main characteristic distinguishing between Perissodactyla and Cetartiodactyla is in a very superficial way the number of toes present. ungulates usually have one or three digits (toes). Cetartiodactyla (those Figure 1.11 Anterior views of the left foot of two cetartiodactyls ( a: cow, Bos taurus b: wild boar, Sus scrofa ) and one p erissodactyl (c: tapir, Tapirus terrestris ) ( as: astragalus, cal : calcaneus, cbd : cuboid, cun: cuneiform cun3: third cuneiform, mtt : metatarsus; mtt3 : third metatarsal, nav : navicular bone fi : fibula, ti : tibia) The vertical line indicates the supporting axis. Adapted from Lecointre & Le Guyader (2006)

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Carroll 23 The anatomical basis for having an even or odd number of toes comes down to the axis of symmetry in the foot and which is the weigh t bearing digit. (See figure 1.11) In Perissodactyls, the middle digit (digit III) bears the majority of the weight. This arrangement is termed mesaxonic. Conversely, in the paraxonic Cetartiodactyl foot has a limb axis that passes between digits IV and II I (Ferguson, 1997; Prothero, 2001; Theodor, 2001; Lecointre & Le Guyader, 2006; Huffman, 2013). Cetartiodactyla The even toed ungulates are currently the most diverse group of living mammals. This large order has over 200 extant species worldwide (13 8 of which belong to the family Bovidae ) and a great many more extinct forms. (Ferguson, Figure 1.12 Phylogeny and fossil occurrences of major lineages of Artiodactyla during the Cenozoic Era. Epochs and radiometric ages are marked on the left. Numbered boxes indicate the higher taxonomic cat egories listed: 1, Ruminata; 2. Tylopoda; 3, Suiformes; 4, Pecora; 5, Oreodonta. MYA, millions of years ago. Adapted from Theodor (2001)

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Carroll 24 1997; Theodor, 2001; Lecointre & Le Guyader, 2006; Huffman, 2013) See Figure 1.12 for a phylogeny of the major Cenozoic lineages of Artiodactyla. The earliest artiodac tyl was likely the rabbit sized Diacodexis from the early Eocene (approx. 55 Ma). (Hermanson & MacFadden, 1996; Theodor, 2001; Clifford, 2010). T o avoid confusion, in this thesis terrestrial Cetartiodactyl group when referring to whales and their including both terrestrial and aquatic taxa. In addition to a paraxonic foot, one defining postcranial feature of Cetartiod actyla is a highly derived double trochleated astragalus with pulley shaped articulating surfaces on eit her side (Ferguson, Lecointre & Le Guyader, 2006; Huffman, 2013) (See Figure 1.13) Also called a double p ulley astragalus, this shape allows the ankle to rotate freely along the parasaggital plane, but restri cts lateral motion of the joint This ankle morphology unique to Artiodactyla is considered an adaptation to d ecrease the risk of dislocation when the animal is engaging in high speed terrestrial running It is important to note that while modern cetaceans have lost this character along with the rest of the posterior limbs, archaic whales shar ed the double pulley morphology Huffman, 2013) Figure 1.13 The specialized astragalus of artiodactyls with its double pulley, compared with a carnivore. An astragal us of (a) a dog, Canis and (b) a pig, Sus Bar, 1 cm. Adapted from Theodor (2001)

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Carroll 25 The order Cetartiodactyla can be further divided into three or four suborders: Tylopoda, S uiformes (or Suina), Ruminantia (Ferguson, 1997; Lecointre & Le Guyader, 2006; Huffman 2013) and some combine hippopotamuses and cetaceans into a fourth suborder Cetancodonta (Huffman, 2013). See Figure 1.14 for a phylogeny of the extant Cetartiodactyla. The modern family Camelidae is the only remaining family of the suborder Tylopoda Camelidae can be split into tribe Camelini, the Old World camelids (Bactrian camels and dromedaries), and tribe Lamini, the New World camelids (alpacas, guanacos, llamas, and vicuas). Tylopoda also includes extinct forms such as the Oromerycidae, Oreodo nta, and Protoceratidae (Theodor, 2001; Janis et al., 2002; Lecointre & Le Guyader, 2006; Clifford, 2010). Extant tylopods are characterized by fused metapodials that are splayed distally, secondary digitigrade stanc e and accompanying digital foot pad, and the loss of digits I, II, and V ( Theodor, 2001; Lecointre & Le Guyader, 2006) The Suiformes, sometimes called Suina, consists of Suidae (pigs, hogs, warthog, babirusa, et c.) and Tayassuidae (peccaries) (Theodor, 2001; Lecointre & Le Guyader, 2006; Huffman 2013) The oldest known swine fossil dates back to the Figure 1.14 The extant Cetartiodactyl family tree. Branch lengths are not proportional to time. Mod i fied from and r etrieved April 11, 2013 from http://www.ultimateungulate.com/Cetartiodactyla.ht ml Huffman, 2013

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Carroll 26 lower Eocene (50 Ma) (Lecointre & Le Guyader, 2006). Living Suiniformes have four toes on each foot, with the hoofs of digits III and IV supporting all of the body weight and digits II and V barely t ouching the ground (Lecointre & Le Guyader, 2006) The Tayassuidae are an exception, having o nly three toes on the hind foot (Huffman, 2013) The lar gest suborder of Artiodactyla, Ruminantia consists of six extant families and a number of extinct forms. Th e living ruminant families include the Bovidae (cattle, antelope, and goats), Antilocapridae (pronghorn), and Giraffidae (giraffe and okapi) (Ferguson, 1997; Theodor, 2001; H uffman, 2013) Two infraorders of Ruminantia are recognized, the Tragululina (Tragulidae) and Pecora (the remaining extant ruminant families). All ruminants have metapodials that have fused into a single cannon bone, well developed digits III and IV formin g hooves, and digits I, II and V vestigial or absent (Huffman, 2013) The possible fourth suborder Cetancodonta includes Cetacea (whales, dolphins, etc.) and their closest land dwelling relatives Hippo potamidae. The Hippopotamidae are a semi aquatic orde r with two living species : the hippopotamus ( Hippopotamus amphibius ) and the pygmy hippopotamus ( Choeropsis liberiensis ). The pygmy hippo and hippo vary greatly in size, reaching weights of 180 kg to 3200 kg respectively (Lecointre & Le Guyader, 2006; Huff man, 2013) Both species of hippopotamus exhibit short stubby legs wit h four webbed toes on each foot (Lecointre & Le Guyader, 2006; Huffman, 2013).

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Carroll 27 The position of Cetacea (whales, dolphins and porpoises) among mammals is a question that has been extensi vely researched utilizing both genetic and morphological dat a either separately or combined ( Ferguson, 1997; Hulbert, 2001; Lecointre & Le Guyader, 2006; Meredith et al., Geisler, 1999; Thewissen & Madar, 1999; Phillips & Pen ny, 2001; Price et al., 2005; Archibald, 2012; Gatesy et al., 2012; Zhou et al., 2012; Huffman, 2013 ) This group includes the largest animal known to have existed, the blue whale ( Balaenoptera musculus ), reaching roughly 24 33 meters in length a nd weighi ng 100 136 tonnes (Lecointre & Le Guyader, 2006; Arkive, 2013) The two modern suborders, Odontoceti (toothed whales) and Mysticeti (baleen whales), can trace their evolutionary history back to a collection of extinct whales, collectively referred to as Ar chaeocetes (Lecointre & Le Guyader, 2006; Huffman, 2013; Polly & Speer, n.d.) The earliest well known fossil whale, Pakicetus dates back to the Eocene around 50 Ma (Fordyce, 2001; Hulbert, 2001; Lecointre & Le Guyader, 2006; Polly & Speer, n.d.) However specializations to an aquatic lifestyle extend even further back into the artiodactyl lineage and the common ancestor shared by Hippopotamidae and Cetacea. The presence of an involucrum, the thickening of the medial wall of the auditory bulla, is a trait generally associated with a specialization for hearing underwater. This character is present in both the cetacean Pakicetus and Indohyus a member of the Raoelli dae the sister taxon to Cetacea (Gatesy et al., 2012) Figure 1.15 for an illustrated depictio n of an inference of a potential evolutionary history of a modern whale. In the Oligocene we see the first members of modern whales Mysticeti and Odontoceti (Polly & Speer, n.d.).

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Carroll 28 Figure 1.15 A phylogenetic blueprint for a modern whale ( Balaenoptera mu sculus ). The topology traces the inferred evolutionary history of an extant cetacean. Branch lengths are not proportional to time. Modified from Gatesy et al. (2012)

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Carroll 29 Perissodactyla Despite a diverse 55 million year evolutionary history including the la rgest land mammal to have ever lived (an Eocene rhinoceros, Indricotherium also called Paraceratherium that weighed up to 15 20 metric tons) only three families and 17 or so species remain today, most of which are on the brink of extinction (Paul & Christ iansen, 2000; Prothero, 2001; Lecointre & Le Guyader, 2006; Huffman, 2013; Polly & Speer, n.d.). ( See Figure 1.16) Figure 1.16 Time periods in which the different families of Perissodactyls roamed the earth. Retrieved from http://research.amnh.org/paleontology/perissodactyl/evolution/intro

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Carroll 30 Though intraordinal relationships of some extinct groups are still unclear, the order Perissodactyla is commonly broken down into three ma in suborders: Hippomorpha (equines and the extinct Palaeotheriidae), Ceratomorpha (rhinoceroses, tapirs, and extinct relatives), and Ancylopoda (the extinct Chalicotheres) (Ferguson, 1997; Huffman, 2013, Norris et al., n.d.). There is some debate as to ho w the extinct Chalicotheriidae and Brontotheriidae fit in. Prothero (2001) included chalicotheres into a group with rhinoceroses and tapirs, calling this new grouping Moropomorpha. Brontotheres (also called titanotheres) have been closely allied with or in cluded in Hippomorpha (Ferguson, 1997; Hermanson & MacFadden, 1992) by some authors, or put into their own individual suborder Titanotheriomorpha by others (Prothero, 2001), while still others choose to leave this question unresolved (Norris et al., n.d.). Of the lineages in Equidae, only one genus ( Equus ) remains. This genus encompasses the domestic horse, zebras, and donkeys. With the exception of the plains zebra ( E. burchelli ) all wild equines are rare. The ancestor to domestic horses ( E. caballus) Pr E. ferus przewalskii ) was until recently extinct in the wild and surviving only in zoos ( Ferguson, 1997; Bouman, 2002) Conservationists have been able to reintroduce some of the population into the wild, but the subspecies remains hig hly endangered. (Bouman, 2001) It is interesting to note that by 9 Ma, the multiple horse lineages that were native to North America, the continent on which equines originated and experienced the greatest radiation, were extinct. The wild mustangs seen tod ay were reintroduced when domestic horses

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Carroll 31 were br ought over in ships from Europe (Norris et al., n.d.; Prothero, 2001; Lecointre & Le Guyader, 2006). There is only one genus ( Tapirus ) remaining of Tapiridae but Tapirus dates back approximately 20 million years of the family's 41 mil lion year evolutionary history (Ferguson, 1997; Norris et al., n.d.). There are five modern species of tapir found in rainforests of southeast Asi a and Central and South America (Ferguson, 1997; Prothero, 2001; Lecointre & Le G uyader, 2006; Huffman, 2013; Norris et al., n.d.). Tapirs are generally considered to be evolutionarily conservative in regards to dentition and postcranial features, however they exhibit highly specialized skulls concerning the development of a proboscis (Norris et al., n.d.) These animals retain three and four toes on the fore and hind feet respectively (Lecointre & Le Guyader, 2006) families belonging to the superfamily Rhinoc erotoidea. Furthermore, we do not see true rhinos until about 40 Ma, relatively more recent than the other perissodact yl groups that we find 55 46 Ma ( Cerdeo, 1998; Norris et al., n.d.). Rhinos have an extremely diverse evolutionary history with huge vari ation in habitat, body type, size, and morphology. There were several rhinoceros lineages that developed proboscis similar to tapirs or proboscideans. Habitats ranged from grassland, to wooded, to amphibious. The majority of extinct rhinos did not have hor ns, though horns did evolve independently several different times (the earliest of which was 28 Ma) in several lineages with myriad morphologies (Ferguson, 1997; Cerdeo, 1998; Prothero, 2001; Norris et al., n.d.)

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Carroll 32 Today, four genera and five species belo nging to the family Rhinocerotidae remain, all of which have one or two horns and three toes on each foot. These extant species include the African white rhino ( Ceratotherium simum ) and black rhino ( Diceros bicornis) the Indian rhino ( Rhinoceros unicornis ) and Javan rhino ( R. sondaicus ), and the Sumatran rhino ( Dicerorhinus sumatrensis ). All of these spe cies are endangered in the wild (Prothero, 2001; Huffman, 2013). Chalicotheres are probably some of the more bizarre extinct perissodactyls. These odd br owsing herbivores were mostly horse like, but with elongated forelimbs ar med with large keratinous claws (Ferguson, 1997; Prothero, 2001; Janis et al., 2012; Norris et al., n.d.; Polly & Speer, n.d.) These secondarily derived claws were quite large and w ere most likely used to tear down branches and foliage for easier browsing. (See figure 1.17) With the large claws on their front feet, shorter hind limbs, and much longer forelimbs, chalicotheres probably walked on their knuckles similar to gorillas (Pro thero, 2001) Why do we care? The ungulates clades are rife with instances of convergent and parallel evolution both within and between groups. There are representatives of at least one clade usually several, inhabiting a wide range of environments. Body size, morphology, diet, behavior, sociality, and physiology are also very diverse. A good portion of extant ungulates Figure 1.17 Reconstruction of the chalicothere Anisodon grande from the Middle Miocene of Europe. Retrieved April 11, 2013 from http://en.wikipedia.org/wiki/Chalic othere (Wikimedia commons)

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Carroll 33 are exceedingly derived and specialized for their lifestyle. The fossil record is fairly complete for some of these groups (ie. horse s), allowing for a deeper perspective in time. Furthermore, parallels can also be drawn for extinct groups with no living relatives. Ceratopsid dinosaur locomotion is considered functionally similar to rh inoceros locomotion based on comparisons to the trai ts and capabilities of modern rhinos and elephants (Johnson & Ostrom, 1995; Paul & Christiansen, 2000; Christiansen, 2002) By studying ungulates both ext ant and extinct, we can further understand the complex interplay of environmental change and th e acqui sition of traits and we can reconstruct the lifestyles, behaviors, and mechanics of fully extinct groups (ie. non avian dinosaurs). Ungulates are interesting not only from a scientific perspective, but in a practical sense as well. Proper care and underst anding of these animals is important economically along with improvements of animal welfare, health, and conservation. Hoofed mammals are a source of sustenance (red meat, milk, gelatin, etc.), clothing (wool, leather), fragrances, sport, transportation of people an d goods, and even companionship (Theodor, 2001; Maloiy et al., 2009) Ungulates are often key members of their ecosystems. The now extinct steppe bison ( Bison priscus ) appears to have been a keystone species of the late Pleistocene (Julien et al. 2012). Aardvarks play a vital role in their ecosystem, building burrows for other species and limiting damage inflicted by termites (Rathburn, 2011). Elephants also are considered a keystone animal; some authors go so far as to say a super keystone anima l (Shoshani, 2001b). Various ungulate species, non domestic and occasionally domestic, are valuable prey items for both human and non human carnivores.

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Carroll 34 Understanding the evolution, morphology, and behavior of these animals is beneficial to conservation of endangered species in the wild of both the ungulates themselves as well as their predators. In a captive setting, be it a zoo, farm, reserve, or even the local equestrian center, veterinary care can only improve with this information. Gait analysis has b een utilized as a clinical tool to assess soundness in racehorses as well as captive Indian rhinos ( Pfistermller et al., n.d. ) Degenerative joint diseases, arthrosis or osteoarthritis for example, are not limited to humans. Affliction of the joints is qu ite common in a variety of animals with a wide range of body size (Weissengruber et al., 2006; Prothero, 2001) Familiarity with the appearance of a typical walk for the species in question is necessary to spot possible illness. An arthritic warthog walks differently from an arthritic zebra (personal observations) and both animals would walk differently from an individual with healthy joints. A limp or other deviation from a normal footfall pattern could be a sign of injury as well as disease, but a subtle favoring of a foot or leg is sometimes difficult to detect unless the observ er has a baseline to work from

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Carroll 35 Chapter 2 Locomotion Defining Gaits Locomotion is often a more complex behavior than most give it credit for. The purpose of such a behavior see ms straightforward: to travel a distance through space from point A to point B. It may have a secondary use in activities such as avoiding predators, obtaining food, or finding a mate. The behavior itself is a complex combination of the neural and musculos keletal systems and the way in which they interact with environmental factors (Hackert et al. 2006). For tetrapods, there are a number of possible combinations of limb movements These different gaits, patterns of limb movement, are cyclical, and divisibl e into strides, or the interval between two successive touchdowns of the same foot (Sluijs et al., 2010). Gaits are classified into two overall categories having to do with footfall timing: symmetrical and asymmetrical (Hildebrand, 1980; Pfau et al., 2011) Symmetrical Gaits In symmetrical gaits, the pairs of fore and hind feet have footfalls evenly spaced in time (Hildebrand, 1980; Pfau et al. 2011). Some common symmetrical gaits are the walk, trot, and pace (Robilliard et al ., 2007). There are a vari ety of footfall patterns that can be used in walking gaits. Milton Hildebrand (1980) defines walking as any gait in which each foot is in contact with the ground more than half the time of a gait cycle. This definition has since become somewhat problematic (Biknevicius & Reilly, 2006). The details of this

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Carroll 36 dilemma will be discussed in further detail below. Single foots involve all four feet striking the ground evenly spaced in time. Couplets are when the footfalls of one forefoot and one hind foot are coupl ed in time. A lateral sequence refers to when foot striking the ground directly after the hind foot is on the same side of the body, such as the left hind followed by the left fore foot. The pattern is a diagonal sequence if the forefoot striking the groun d directly after a hind foot is on the opposite side of the body; the left hind foot followed by the right forefoot. Combinations of these terms are used to describe footfall patterns that are usually considered walks at slower speeds: lateral sequence si ngle foot, diagonal couplet, lateral couplet, etc. At faster speeds, the pairs of feet in either the lateral or diagonal couplet strike the ground synchronously; these gaits are calle d the pace or trot respectively (Hildebrand, 1980) Stability is a majo r factor in determining gait selection. In almost all symmetrical gaits (excluding the trot and pace), an animal has only one foot off of stability of a tripod depends on the area enclosed, and on the position of the tripod relative to (Hildebrand, 1980) For single foot gaits, it has been shown that lateral sequence gaits have a more stable tripod than do diagonal sequence gaits. (see figure 2.1 ) Figure 2.1 Support provided by tripods for walking symmetrical gaits, in lateral (left) and diagonal (right) sequence. The spot is the center of gravity. Adapted from Hildebrand (1980)

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Carroll 37 At the pace or trot, however, only two legs are in contact with the ground at a time. The area of the tripod is no longer of consequence as no tripod is created. (See Figure 2.2) In this case, the diagonal trot is more stable than the lateral pace. I n a trot, the line of support created by the two limbs in contact with the ground passes almost directly gravity. The pace is less stable, especially at lower speeds. With the two supporting legs on the same side of the body th e animal has a tendency to roll (Hildebrand, 1980). Camels are among the only mammals that routinely pace (Sluijs et al., 2010; Janis et al., 2002). While several long legged mammals such as the giraffe also have a pace like walk, also called the wal king pace, seen in camels, this pace like walk like walk is actually a modified and faster version of the usual lateral sequence walking gait seen in most mammals (Janis et al., 2002). The pacing gait in came lids is generally believed to have evolved et al. 2010). Camelids have also evolved adaptations to counteract the reduction of lateral stability that results from moving ipsilateral pairs of limbs at the same time (Sluijs et al., 2010; Janis et al., 2002) These adaptations will be discussed in further detail in a later section. Most tetrapods trot if they have a running gait, however some breeds of horses have been selectively bred for t heir natural capacity to pace as well as or Figure 2.2 Example of a diagonal (a) and a lateral (b) two leg support in the llama Lama glama Adapted from Van der Sluijs et al. (2010)

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Carroll 38 instead of trot. Some horses can also be trained to perform a pace (Sluijs et al., 2010). Asymmetrical Gaits Gaits in which the footfalls of each pair of feet are unevenly spaced in time are termed asymmetrica l gaits. Where in symmetrical gaits, the ipsilateral legs are considered a pair, in asymmetrical gaits the forelegs are considered a pair and the hind legs a pair (Pfau et al. 2011) The first foot of the pair to strike the ground is the trailing fo ot, the second the leading foot (Hildebrand, 1980) Usually, the leading foot is also the foot that is extended more than its partner and strikes the ground further forward. The magnitude of the lead is measured by the size of the step between the trailing and l eading footfalls (Hildebrand, 1980) The common asymmetrical gaits are the bound, half bound, and gallop. All asymmetrical gaits involve a period of suspension, flight, or aerial phase. Suspension is the moment when all four feet are off of the ground, e ither collected underneath the body (gathered suspension) or stretched out roughly parallel to the ground (extended suspension). Suspensions are sometimes accompanied by flexion or extension of the spine. Usually with a gathered suspension the spine is ven troflexed and extended suspension the spine is dorsoflexed. In the fastest cursor s, both suspensions may be used (Hildebrand, 1980) The bound refers to a gait in which the leads in both pairs of feet are either very small or absent. In the half bound, t he fore lead is evident, but the hind lead is not. Both the bound and half bound utilize both hind feet, the major source of

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Carroll 39 propulsion in quadruped gaits, in unison. This imparts more forward thrust, propelling the animal forward in a series of leaps. How ever, this form of locomotion is energetically costly, usually limiting the animal to running o nly moderate or short distances (Hildebrand, 1980) Hyraxes and smaller artiodactyls are amongst those tha t use bounds and/or half bounds (Hildebrand, 1980) G allops are the most common asymmetrical gait, in which both the fore and hind pairs of feet show a lead. There are two varieties of gallop gait, both of which have selective advantages and disadvantages. The transverse gallop involves both fore and hind pa irs to have the same lead. The alternative, opposite leads in fore and hind pai rs, is termed the rotary gallop (Hildebrand, 1980) Transverse gallops are slightly more stable and favorable for economy of effort than rotary gallops. This gallop is the most common, e specially amongst large cursors (Hildebrand, 1980; Pfau et al., 2011) Reducing limb interference is also a factor that influences the selection of the transverse gallop. (See Figure 2.3) In long legged cursors, if the limbs on one side of the bod y move in unison, the likelihood of the hind fo ot kicking the forefoot is less (Hildebrand, 1980; Pfau et al., 2011) The drawback of the transverse gallop is the necessity to turn on the inside lead. For example, a horse galloping on a right lead must ch ange leads to a left lead before it can turn to the left. A rotary galloper does not experience this problem. Rotary gallops usually have two periods of suspension and this is the part of the Figure 2.3 The transverse gallop in relation to interference. Modified fro m Hildebrand (1980)

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Carroll 40 stride that covers the most ground. Transverse gallops typically only have one suspension and as a result are relatively slower. Overall, the rotary gallop is better for ag ility and quick bursts of speed (Hildebrand, 1980) Some animals, such as the giraffe and some antelopes, cannot avoid interference at either the transverse or rotary gallop. This is due either to their extremely long legs, possibly along with the flexion and extension in their back as they gallop. These animals straddle their hind limbs wider than their forelimbs, so that the hind pass the fore on t he outside instead of colliding (See Figure 2.4) Hildebrand, 1980) Walking or Running? Asymmetrical gaits tend to be classified as runs, whereas symmetrical gaits can be classified as either walks or runs, and some gaits, such as the trot, can be consi dered both. This, understandably, has led to some confusion. It all boils down One tool used to distinguish walks from runs is footfall kinematics based on duty factor, the ratio of the duration of the su pport to duration of the stride (Biknevicus & Reilly, 2006) (Biknevicus & Reilly, 2006; Hoyt et al. 2006; Starke et al., 2009) Utilizing this method only, you find that some gaits occur mainly as either a walk or run, but Figure 2.4 The rotary gallop in relation to interference. Adapted from Hildebrand (1980)

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Carroll 41 others can occur as e ither. A trot is generally considered as a running symmetrical gait, but the duty factor is such that this footfall pattern can be classified as either a walk or a run. A different approach to this question is the biomechanical approach regarding either t he limb dynamics or whol e body center of mass mechanics (Biknevicus & Reilly, 2006; Hoyt et al. 2006; Hutchinson et al. 2006) There are two generally accepted mechanisms with which terrestrial animals modulate locomotor costs in terms of energy. The fi rst is often referred to as an either pendulum, inverse pendulum, or vaulting mechanism (Ren & Hutchinson, 2008). For vaulting mechanics both kinetic the legs like an inver ted pendulum (Cavagna et al., 1977; Hoyt et al ., 2006; Biknevicus & Reilly, 2006) Vaulting mechanics are mostly seen in animals moving at slow speeds, and as a result is considered indi cative of walking (Biknevicus & Reilly, 2006) At a certain speed the metabolic cost of vaulting while still keeping contact with the ground becomes too great, impossible even (Ren & Hutchinson, 2008). It is at this point that quadrupeds tend to switch to the alternative method, bouncing mechanics, implying a transition to r unning as well (Biknevicus & Reilly, 2006; Hoyt et al., 2006) Bouncing mechanics also called spring or spring mass, rely on the storage and recovery of elastic strain energy in limb elements such as ligaments, tendons, and muscles (Cavagna et al., 1977; B iknevicus & Reilly, 2006; Hoyt et al., 2006; Ren & Hutchinson, 2008)

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Carroll 42 Several factors confuse the matter further. Aerial phases are not limited to with either vaulting or bouncing mechanics. The center of mass moves in an inverted pendulum during slow trotting, classifying this gait as a walk. At faster speeds, the trot utilizes bouncing mechanics and is considered a run. The trot incorporates a per iod of suspension at al l speeds (Biknevicus & Reilly, 2006) As a result, the presence of an aerial phase is not exclusive to running and cannot be used to specify between walk or run on its own. Furthermore, does running require an aerial phase? Elephants are known for maintai ning a lateral sequence footfall pattern at all speeds ranging from walking to running (Hutchinson et al. 2006). This gait has been called terms such as amble, rack, pace, groucho running, running walk, and grounded run (Biknevicus & Reilly, 2006; Hutch inson et al. 2006) Elephants are not the only quadrupeds to use a lateral sequence singlefoot gait without an aerial phase. The tlt, a gait used by Icelandic horses, has a similar grounded footfall pattern as the elephant running gait, bu t has purely bo uncing mechanics (Biknevicus & Reilly, 2006; Hutchinson et al. 2006; Ren & Hutchinson, 2008; Starke et al., 2009) Gaits do not need an aerial phase to meet the definition of running, whether that definition is based on biomechanics or duty factor (Biknev icus & Reilly, 2006) Speed must also be considered when determining if the animal in question is walking or running. To make comparisons between species possible, dimensionless speed, or Froude numbers are used. Froude number is a measure of dimensionle ss speed, the ratio between centripetal forces around the foot and the weight of the

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Carroll 43 animal (Fr=velocity 2 /[hip height x acceleration due to gravity]) (Biknevicus & Reilly, 2006; Hutchinson et al., 2006; Ren & Hutchinson, 2008; Ren et al., 2008) Theoretic ally, at a Froude number of 1.0, a shift from vaulting t o bouncing mechanics must occur (Biknevicus & Reilly, 2006; Hutchinson et al., 2006) Typically, though, quadrupeds switch to bouncing mechanics at a Froude number of approximately 0.35, much ear lier than the theoretical limit (Biknevicus & Reilly, 2006) This implies that the determining factor for this vault bounce transition is not the limitation of forces around the limb, but another factor, possibly metabolic cost (Biknevicus & Reilly, 2006). Wh ole body center of mass motion is a combination of fore and hindlimb mechanics. The center of mass for many quadrupeds, and especially ungulates, lies closer to the forelimbs than the hindlimbs. In relation to this, the fore and hindlimb pairs usually ha ve different locomotor functions. The hindlimbs are used primarily for propulsion, and the forelimbs, as they are located in front of the center of mass, are for braking (Clifford, 2010; Ren et al., 2010). Elephants are an exception to this, utilizing both sets of limbs similarly for both braking and propulsion (Ren et al., 2010) With differing functions, it is not unsurprising that fore and hindlimb pairs might not display a biomechanical shift in vault bounce mechanics at the same point. Even in elephan ts, where fore and hindlimbs do not divide propulsive and braking functions, there is still the possibility that limbs do not function identically (Ren & Hutchinson, 2008; Ren et al., 2010). As some elephant studies suggest, fore and hindlimb pairs may u tilize differing locomo tor dynamics at moderate speeds (Ren & Hutchinson, 2008; Ren et al., 2008) At moderate speeds, around Froude

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Carroll 44 number 0.25, elephant hindlimbs begin to exhibit bouncing mechanics with the forelimbs retaining a vaulting mechanism (Ren & Hutchinson, 2008; Ren et al., 2008; Kokshenev & Christiansen, 2012) Around Froude number 1.0, both fore and hindlimb pairs exhibit separate aerial phases even though elephants do not exhibit a whol e body aerial phase in any gait (Ren & Hutchinson, 2008 ) So how does one d istinguish a walk from a run? Walks and runs display fundamentally different mechanics, vau lting and bouncing respectively (Cavagna et al., 1977; Biknevicus & Reilly, 2006) The variability of limb compliance and movement of the center of mass as a result reflect this change in mechanics. An aerial phase is not necessary to obtain the yielding necessary in the limb for bouncing mechanics, so this is not a good indicator. Footfall pattern and the corresponding gait terms are problematic a s well. Several footfall patterns are found with both vaulting and bouncing mechanics. Gait terms are effective as descr iptors of footfall pattern only (Biknevicus & Reilly, 2006) Duty factor, previously utilized by some, is also unreliable when d istingui shing between mechanics (Biknevicus & Reilly, 2006; Hoyt et al. 2006) It provides information about the percentage of time This information is useful, but does not a ccurately nor consistently measure the yielding of the limbs necessary for distinguishing between walking (vault) and running (bounce) mechanics (Biknevicus & Reilly, 2006) Froude number or a measure of the phase difference in external mechanical energy m ost consistently

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Carroll 45 the most reliable when distinguishing betwee n walking and running mechanics (Biknevicus & Reilly, 2006) It is important to remember, however, that locom otor effort is more than gait or limb compliance. Locomotor behavior is a result of neuromuscular responses to environmental and other external factors. Energy conservation is only one reason amongst many for an ani mal to employ a particular gait (Biknevi cus & Reilly, 2006; Hackert et al. 2006) Foot Posture and Locomotion Limb anatomy is intrinsic to understanding locomotor capabilities and behavior. Animals with similar limb proportions tend to exhibit similar joint mobility and motion, though they al so tend to be phylogenetically related (Pike & Alexander, 2002). Investigating the mechanics of extant groups can be used when determining the function of similar structures that are inferred from features of extinct forms (Thomason, 1986; Clifford, 2010). Often, in the case of fossil groups, only skeletal indicators a re available for interpretation (Miller et al., 2008) Traditionally, elongation of the distal limb is associated with fast moving cursorial locomotion. Longer legs result in a longer stride length and more distance travelled with each stride, potentially leading to greater speed. In addition to limb length, other anatomical features have also been considered indicative of cursoriality and fast locomotion; a mobile scapul a, reduced or fused m etapodials and ep ipodials, and hinge like joints (Christiansen, 2002; Clifford, 2010) Further elongation of the limb can be attained by changes to pedal anatomy.

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Carroll 46 (See Figure 2.5) A more erect foot posture such as digitigrade or unguligrade (as opposed to plantigrade) not only adds length, but also provides extra joints and points of compliance along th e functional length of the limb (Clifford, 2010) Following this reasoning only, unguligrade mammals, as the highest on their toes, should be the fastest Then why did canid and felid carnivores not evolve an unguligrade stance rather than only a digitigrade stance? Digitigrade posture seems more than adequate for these animals to be fast enough to catch their prey. The cheetah, the fastest living cursor w ith a maximum sprint of approximately 100 km/hr (~62 mph), possesses a digitigrade stance. The unguligrade pronghorn antelope, the second fastest runner, has a maximum sustained speed of a mar kedly slower 65 km/hr (~40 mph) (Biewener, 2003) Moreover, the limb anatomy of ungulates and carnivores did not co evolve as in the Pliocene. Roughly twenty million years previous in the late Oligocene is when highly cu rsorial herbiv ores first appear (Janis & Wilhelm, 1993; Clifford, 2010) Unguligrade posture to varying degrees evolved independently in multiple mammal groups, so clearly there is some benefit. But, if not speed, then what is the selective advantage of evolving unguli grady as seen in most ungulate groups? The Figure 2.5 Contrast in proportions and foot posture in the left hind le g skeleton of a noncursor (left, plantigrade bear) moderate cursor (cen ter digitigrade dog ), and a highly specialized cursor (right unguligrade deer ). Adapted from Hildebrand (1988)

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Carroll 47 majority of the time animals are walking not running. Truly fast r unning occurs relatively rarely (Christiansen, 2002) Reaching a maximum speed would be a once in a lifetime occurrence for an animal (Hutchinson e t al., 2006). Optimizing energetic efficiency at all gaits, not just the fast moving ones, seems sensible. Longer stride lengths would increase efficiency at any speed or gait be it a walk or run. Lengthened strides created by longer limbs not only imply higher speed, but also the potential to reduce stride frequency at any given speed regardless of gait (Christiansen, 2002; Thompson et al., 2007) This could potentially decrease the number of steps required to transverse a given distance and as a result m inimize the total energy exerted when locomoting (Christiansen, 2002) Increasing limb length also increases the length of tendons and poten tial for elastic energy storage (Christiansen, 2002; Clifford, 2010; Janis & Wilhelm, 1993; Van der Sluijs et al. 2 010) The energy cost of locomotion is dependent on both speed and size of the animal. Generally, the energetic cost of locomotion decreases as body mass increases and increases as runnin g speed increases (Christiansen, 2002; Maloiy et al., 2009) Running gaits have been found to be very energy efficient, suggesting significant contribution of passive rec oil in tendons at higher speeds (Christiansen, 2002) It follows that the longer tendons with a greater capacity for energy storage can contribute more ela stic energy to the succeeding step. Energy conservation, while a major factor, is not the only selection pressure acting on the evolution of ungulate locomotor morphology, patterns, and behaviors. More than a few lineages secondarily lost their unguligrad e posture while some never passed beyond a sub unguligrade stance. Locomotory behavior is a complex

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Carroll 48 interaction between the animal and the environment. The acquisition of locomotory adaptations, be they morphological or behavio ral, is closely tied to habit at (Thomason, 1986; Janis, 1989; Rooney, 1997; Janis et al., 2002; Theodor, 2001; Van der Sluijs et al., 2010; Julien et al., 2012).

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Carroll 49 Chapter 3 Adaptations Specializations Regarding Habitat and Locomotion Habitat is a key influence on the evolution of a s pecies. The environment is the context in which morphology and behaviors are advantageous or deleterious, and as a result are passed down to following generations as more or less efficient adaptations to the habita t Locomotion and the associated morpholo g ical traits are by no means an exception (Thomason, 1986; Janis, 1989; Rooney, 1997; Janis et al., 2002; Theodor, 2001; Van der Sluijs et al., 2010; Julien et al., 2012) Two mammal groups independently transitioned from a terrestrial habitat to an aquatic one. The extant representatives of both Sirenia and Cetacea are obligate swimmers, and share a number of convergent adaptations. Both have secondarily lost their hindlimbs. Some species still have a reduced pelvic girdle, but it is vestigial at best. Both sirenians and cetaceans have highly robust caudal vertebrae to support flat fleshy lobed tails or flukes. These tails are powerful, a nd a major source of propulsion (Fordyce, 2001; Lecointre & Le Guyader, 2006; Domning, 2012; Gatesy et al., 2012) Another adaptation to aquatic life is the transformation of hands into swimming paddles. The underlying bone structure of cetacean and sirenian flippers differs greatly. In cetaceans, (See Figure 3.1) modification of the forelimbs into flippers involved a shorten ing and flattening of the humerus, radius, and ulna. This flattening of the limb bones and the joint connecting them leads to a restriction of

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Carroll 50 movement of the elbow joint. This extreme reduction of mobility place. Further elongation of the cetacean flipper is achieved by hyperphalangy, a condition in which extra ph alanges are added to the digits (Hildebrand, 1988; Fordyce, 2001; Lecointre & Le Guyader, 2006; Gatesy et al., 2012) The forelimbs of sirenians do not exhibit h yperphalangy, nor is the mobility or rotation o f the elbow joint so restricted (Lecointre & Le Guyader, 2006; Domning, 2012). While the majority of ungulates did not undergo a change in habitat and morphology quite as extreme as cetaceans and sirenians, c hanges in habitat still lead to selective changes in morphology as well as locomotory behaviors. Horses: From woodland creatures to grassland dwellers Environmental change is a major contributor to the evolution of the equid manus. A number of morphologi cal traits found in the highly derived modern horses correspond to the expansion of savanna grassland habitat in the late Miocene (Thomason, 1986; Thomason, 1991; Rooney, 1997; Janis et al., 2002). These traits include monodactyly and the development of a passive stay apparatus in the shoulder region. In equids, the development of a fully unguligrade foot posture Figure 3.1 the pectoral girdle and the left forelimb of a dolphin, where the extension of digits II and III by hyperphalangy is notable. Abb reviations: Digits labeled I V, sc : scapula ul : ulna, r : radius, car : carpus. Adapted from Lecointre & Le Guyader (2006)

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Carroll 51 seems closely related to the transition from tridactyly to monodactyly (Thomason, 1986; Rooney, 1997) Mesohippus a three toed genus of early hor se, inhabited North American forests and swamps from the Late Eocene to t he Middle Oligocene (30 40 mya) (Thomason, 1986; Rooney, 1997) These browsing animals already exhibited cursorial adaptations such as an elongated metacarpus and carpal locking mecha nism. With the presence of a digital footpad, Mesohippus still possessed a sub unguligrade foot posture. The side toes, subequal in length to the central digit, and a padded foot would be useful in a closed wooded habitat with a swampy substrate. Selection would favor the added stability required for quick maneuverability and obstacle avoid ance with soft ground underfoot (Thomason, 1986) We see true unguligrady in the Miocene genus Merychippus. These savanna dwelling, grazing proto horses still retained t hree digits, but with the loss of a digital pad and the reduction of the side toes. Size and weight increase accompanied an increase of the impact and concussive forces on the foot in the savanna as compared to the softer wetlands. Selection would favor th e increased compliance and strength of the unguligrade foot. The loss of digits II and IV as seen in Equus is also associated with the transition from a closed to an open habitat. In wooded habitat, stability and dodging ability are vital to predator avoid ance. In open grassland, it is speed and energy efficiency that counts. The side toes increase inerta of the limb, a disadvantage when running. In an open savanna grassland environment, there would be selection aga inst the retention of side toes (Thomason, 1986; Thomason, 1991; Rooney, 1997)

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Carroll 52 Modern equines are highly specialized for an open grassland environment. Several Miocene equid genera developed different and distinctive humerus shoulder morphologies; evolutionary experiments, possibly associated wit h stability of the shoulder region while standing (Hermanson & Macfadden, 1992) As each observed Miocene morphology is unique to a particular group, the limb anatomy of extant horses exhibits a specialized passive stay apparatus characteristic of the line age. In the forelimb, the morphological characters of this adaptation first evolved five million years ago in the late Miocene as seen in the genus Dinohippus. The fully derived condition is first seen in extinct Pliocene members of the genus Equus such as E. caballus (2 3 Ma) (Hermanson & MacFadden, 1992; Hermanson & MacFadden, 1996) Since then the shoulder morphology appears to have undergone very little change. The function of the passive stay apparatu s is one of energy conservation (Hermanson & MacFadd en, 1992; Hermanson & MacFadden, 1996; Janis et al., 2012) Muscles, ligaments, and deep fascial connective tissue comprise a specialized system for maintaining limb posture, preventing flexion of collapse of the shoulder joint. In this system passive, no n tiring collagenous tendons, ligaments, and fascial connective tissue largely replace the role of active muscular action in maintaining stance. The primary identifying osteological characteristics of this apparatus are a well developed intermediate tuberc le located on the proximal end of the humerus and a prominent muscle origin on the supraglenoid tubercle on the scapula.

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Carroll 53 The intermediate tubercle (see figure 3.2 ) on the humerus brachii, limiting the range of stretch i n the tendon and therefore preventing extreme flexion of the shoulder during weight bearing (Thomason, 1991; Hermanson & MacFadden, 1992) (See figure 3.3) The development of a passive stay apparatus is thought related to the adaptive shift from a wooded t o a grassland savanna habitat. Grazing requires the animal to spend much of the day feeding, standing in open terrain easily visible to predators. An energy conserving non fatiguing structure would be greatly a dvantageous in this environment (Hermanson & M acFadden, 1992; Hermanson & MacFadden, 1996; Janis et al., 2012) Not only would it facilitate standing f or extended periods, but also should predator avoidance become necessary, the individual animal would have the energy to flee swiftly. Figure 3.2 The humerus of a horse, Equus caballus viewed proximally, cranially, and laterally. Abbreviations: GT greater tubercle ; INT intermediate tubercle; LT lesser tubercle. Adapted from Hermanson & Macfadden (1992)

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Carroll 54 A passive stay apparatus evolved in the equine hind limb as well. The mechanism is different, however, due to fundamental structural and functional differences between the fore and hind limbs. Generally, the morphological and anatomical changes seen in the fore and hind pairs are similar. Hind limbs tend to be more derived than the forelimbs, hindlimbs evolving certain characteristics before similar changes are seen in the forelimbs. The retention of a more primitive foot posture or number of digits, for example, is ofte n seen in the forelimbs as compared to the hind. This can be seen in hyraxes. Hyraxes exhibit a digitigrade hindlimb posture and a plan tigrade posture in the forelimb (Clifford, 2012) The passive stay apparatus in horses follows this pattern. The equine h Here it is the knee (also called the stifle) that has been specialized. The patella Figure 3.3 Lateral view of the left forelimb of a horse, E. caballus illustrating the role of the internal tendon of biceps brachii in preventing collapse (flex ion) of the shoulder. Resistance to stretch of this tendon, particularly between the supraglenoid tubercle (ST) and the intermediate tubercle (INT), prevents shoulder flexion without active muscle recruitment. Similar mechanisms around the more distal join ts on the limb also account for passive stance Adapted from Hermanson & Macfadden (1992)

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Carroll 55 of the one hind leg is bent with the hoof pointed downward (See Figure 3.4) (Hermanson & MacFadden, 1996; Janis et al., 2012) The derived condition of the enlarged medial trochlear r idge is first observed in the Miocene equid genus Protohippus about 12 Ma. The analogous shoulder passive stay is not observed until around 5 Ma. The hindlimb passive stay evolved noticeably earlier in equids than the corresponding forelimb mechanism. The selective advantage of knee locking concerns energy conservation while standing for extended periods as well as possibilities of an earlier unknown function. The earlier presence of a locking mechanism in the hindlimb has been attributed to biomechanical differences between the fore and hind limbs such as posture, weight b earing, and locomotory function (Hermanson & MacFadden, 1996) A similar knee locking mechanism can be found in other clades in addition to equines. Among the extant perissodactyls, th e rhinoceros exhibits a highly prominent medial trochlear ridge on the distal femur. Rhinos independently evolved this trait separately from equids. This anatomy might be representative of being able to balance over one hip while resting the other leg as s een in horses, but it is unknown if this behavior is actually employed by rhinos (Janis et al., 2012) Tapirs represent the more primitive morphotype, lacking the derived medial trochlear Figure 3.4 A representation of a domestic horse ( Equus caballus ) in a resting position with the stifle of the right back leg locked. Art by Beth Carroll, 2013

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Carroll 56 ridge (Hermanson & MacFadden, 1996; Janis et al., 2012) (See Figure 3.5) Figure 3.5 Cranial and distal views of left femora from a tapir ( Tapirus veroensis from the late Pleistocene of Florida), a camelid ( Hemiauchenia macrocephala from the early Pleistocene of Florida), and a rhinoceros ( Teleoceras proterum from the l ate Miocene of Florida). Tapirs and camelids exhibit the primitive condition for the medial trochlear ridge. Although early rhinocerotoids have plesiomorphic medial trochlear ridges, derived rhinoceratoids such as Teleoceras have an enlarged medial trochl ear ridge comparable to that of the modern horse. Abbreviations: EF extensor fossa; MTR medial trochlear ridge; LTR lateral trochlear ridge. Adapted from Hermanson & MacFadden (1996) A similar locking mechanism can be observed in the stifle of some arti odactyls, primarily ruminants, though it is not quite as highly developed as that seen in equines and rhinos (Hermanson & MacFadden, 1992; Hermanson & MacFadden, 1996; Janis et al., 2012) Unlike the unique shoulder morphology of equines, a passive stay a joint is not so clear cut. The ruminant artiodactyls are usually savanna or grassland

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Carroll 57 dwelling species and, unlike the non ruminant horses, spend a large portion of the day lying down in a period of rest associated wi th the ruminant digestive cycle (Hermanson & MacFadden, 1996; Janis et al., 2012) The degree of asymmetry in the femur caused by an enlarged medial trochlear ridge correlates, in general, with body mass, the asymmet ry increasing as m ass increases (Hermanson & MacFadden, 1996; Janis et al., 2012) However, size alone is not the only contributing factor. The femoral asymmetry associated with the medial trochlear ridge is more prominent in taxa showing a preference for open habitat, reg ardless of size. It has been proposed that this asymmetry in the knee could be indicative of taxa that not only prefer open habitat, but hab itually employ a galloping gait (Janis et al., 2012) Camels and elephants both are relatively large ungulates inhab iting open terrain, but neither of these taxa demonstrate the highly pronounced medial trochlear ridge and resulting high degree of knee asymmetry. The gallop is not a gait either of these taxa enga ge in habitually if at all (Janis et al., 2012) It is qui te possible the enlarged medial trochlear ridge was originally an adaptation to increasing size and an open habitat that in equines was secondarily developed i nto a passive locking mechanism (Hermanson & MacFadden, 1996; Janis et al., 2012) Camelids: Wha t strange feet you have.... well the better to out pace you with, my dear. The extant members of Tylopoda are unique among the ungulates in not only their pedal morphology, but also their locomotion. Camelids are secondarily digitigrade with splayed toes and a wide elastic footpad. Hooves have been reduced

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Carroll 58 to toenails (See Figure 3.6 and Figure 3.7) (Theodor, 2001; Janis et al., 2002; Lecointre & Le Guyader, 2006; Foss & Prothero, 2007; Clifford, 2010; Van der Sluijs et al., 2010; Huffman, 2013) The two tribes of Camelidae Camelini (Old World camels) and Lamini (New World camelids) share ancestors endemic to the Eocene of North America (Theodor, 2001; Janis et al., 2002; Foss & Prothero, 2007; Van der Sluijs et al., 2010; Huffman, 2013) The early members of the family Camelidae were small with elongated legs and a derived two toed hoofed foot (Theodor, 2001; Van der Sluijs et al., 2010). The ancestors of the Camelini migrated into Eurasia during the Pliocene and in the Pleistocene the first lamoids (me mbers of the Lamini) arrived in South America. During the Pleistocene, the North A merican camelids became extinct (Theodor, 2001; Lecointre & Le Guyader, 2006; Foss & Prothero, 2007; Van der Sluijs et al., 2010; Huffman, 2013). Fig ure 3.6 Didactyl artiodactyl taxa. A, Antilocapra a pronghorn, right manus in dorsal view. B, Lama a cameline camelid, right manus in dorsal view. C, Poebrotherium manus in dorsal view. D, Daeodon entelodont, right manus in dorsal view. Abbreviations: mk metacarpal keel. Scale bars equal 5 cm Adapted from Clifford (2010) Figure 3.7 Schematic diagrams of longitudinal sections of the feet of a tylopod (a) llama and a ruminant (b) sheep. (elp: elastic pad, hf: hoof, ks: keratinized sole, pha1: proximal phalange) Adapted from Lecointre & Le Guyader (2006)

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Carroll 59 The digitigrade stance an d wide footpad found in all extant camelids is generally assumed to be an adaptation for habitats with soft or uneven terrain (Theodor, 2001; Janis et al., 2002;Biancardi & Minetti, 2012; Huffman, 2013) or as an adaptation for the running pace seen only in camels (Janis et al., 2002; Van der Sluijs et al., 2010). In addition to the wide footpad, other characteristics of camelid morphology are considered adaptations to mitigate the inherent lateral instability of pacing. These include narrow chest and hips, broad flat ribs, and enlarged attachment sites for muscles that help prevent collapse on the unsupported side. The narrow torso, wide feet, and long legs also allow for a very narrow stance with the feet contacting the ground close to the midline (Janis et al., 2002; Van der Sluijs et al., 2010; Pfau et al., 2011) However, due to differences in habitat and locomotory behavior of both groups of camelids, the matter may be more complex than simply assigning footpads to the acquisition of pacing. Old World camels utilize a pace like walk at slow speeds and a faster running pace. It is the running pace that is unique to camels. Usually camels are more reluctant to gallop and seldom do so. With the proper incentive to gallop, camels use the transverse gallop (Van der Sluijs et al., 2010; Pfau et al., 2011). A pacing gait is just one trait of camels that make them well suited for efficiently traversing large distances of arid and open land in search of resources such as food or water (Maloiy et al., 2009; Van d er Sluijs et al., 2010; Pfau et al., 2011). New World camelids, the Lamini, share many of the above stated traits that would lead some authors to say they are well adapted anatomically for the p acing gait (Janis et al. 2002; Pfau et al., 2011). Despite be ing seemingly well adapted,

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Carroll 60 lamoids transition smoothly from a pace like walk to a transverse gallop with no clear intermediate gait. Neither a trot nor a pace are utilized by lamoid camelids (Van der Sluijs et al., 2010; Pfau et al., 2011). This may be re lated to habitat. New World camelids are mainly sedentary inhabiting mountainous habitats. Guanacos have some migrational strategies, but they do not travel as far as other migratory species. As compared to Old World camels, New World camelids have ample a nd well distributed resources of food and water, and have le ss need to cover long distances (Van der Sluijs et al., 2010) One hypothesis to explain these discrepancies is that all Camelidae secondarily lost trotting as an intermediate gait and camels late r evolved the pace as a more efficient m ethod of travel than the gallop (Pfau et al., 2011) This secondary acquisition of the pacing behavior possibly happened convergently within two camelid subfamilies, the Camelin ae and the extinct Protolabinae (See Figure 3.8) (Janis et al., 2002) Two other camelid lineages, Stenomylinae and Miolabinae, show similar convergence of the foot morphology seen in extant camelids, but did not attain the fully derived condition (Janis et al., 2002). It is interesting to n ote, however, that the fully derived pedal morphology generally associated with a running pace occurred during the late Oligocene and early Miocene. This is prior to the spread of savanna grasslands seen in North America during the late Miocene (Janis et a l., 2002) While there is a likely connection between environmental and habitat change, the acquisition of digitigrade footpads, and pacing in camels, the precise relationship between these factors remains unclear.

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Carroll 61 stress, come winter everyone will want a pair! The digitigrade footpad found in camelids has been postulated as an advantage in habitats with a soft substrate or uneven terrain underfoot such as sand or rocks (Theodor, 2001; Janis et al., 2002;Biancardi & Minetti, 2012; Huffman, 2013). Other artiodactyls have evolved specializations to adapt to this problem as well, but without losing their hooves or unguligrade posture. Rangifer tarandus commonly known as reindeer in Europe and caribou in North Americ a, have hooves that are especially well adapted for traversing snowfields. The broad hooves provide a wide walking surface on which weight can Figure 3.8 Phylogeny of camelids. The rectangles show chronological ranges of taxa. Key: Unshaded (white) rectangle, no foot morphological adaptations towards extant c amelid condition; lightly rectangles, numerous morphological features like that of extant camelids, but not with full suite of morphological adaptations; and black rectangles, foot morphology unequivocally like that of extant camelids. Adapted from Janis et al. (2002)

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Carroll 62 be evenly distributed. They function as natural snowshoes, preventing the animal from sinki ng too deeply into cru sted snow (Foss & Prothero, 2007; Stefoff, 2007; Huffman, 2013). The exact mechanism of creating this uniform distribution of weight is not completely clear. One perspective is that the hooves are splayed widely to create a greater surface area of contact (Stefoff, 2007). Contrastingly, it has also been postulated that adducting of the phalanges holds the two hooves uniformly together. This adduction would avoid an uneven distribution of weight and resulting het erogeneous sinking into the snow (Foss & Proth ero, 2007). The palmar interosseous muscles of reindeer are relatively well developed as compared to other deer, and as a result are able to adduct the digits more extensively. Well developed palmar interossei and the extreme adduction of digits could be a n adaptation for walking with hooves on soft substrates (Foss & Prothero, 2007) Bohlininae, an extinct Miocene giraffid, has deep metapodial troughs indicative of well developed interosseous muscles such as seen in reindeer. It has been hypothesized that these giraffids inhabited areas with soft substrates that would be easy to sink into, most l ikely muddy or sandy lakeshores (Foss & Prothero, 2007) There are other species that have evolved hooves modified for walking on particular terrains. Sitatunga ( Tragelaphus spekeii ) are a type of antelope that inhabit marshes of Central and Western Africa. The hooves of this species are very elongated with flexible toe joints (see figure 3.9) as an adaptation for wa lking on the soft swampy ground (Beth Carroll, p ersonal Figure 3.9 A sitatunga ( T. spekeii ) at the Maryland Zoo in Baltimore. Note the elongated hoof shape. Photo by Beth Carroll, 2012

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Carroll 63 observation, Foss & Prothero, 2007; Huffman, 2013). Klipspringers ( Oreotragus oreotragus), small mountain dwelling antelopes, took the opposite route and have shortened hooves perfect for scaling rock faces (Foss & Prothero, 2007; Huffman, 2013). Moose ( Alces alces ) have multiple limb adaptations related to their peculiar stilt locomotion and habitat preference for swamps and bogs (Breda, 2008; Huffman, 2013) Stilt locomotion is when the distal portion of the uplifted leg remains rigid. Generally in cervids the distal metapodials are elongated. In Alces it is the proximal portion of the leg, including humerus and radius that is elongated. Fusion of the tarsal bones ( cuneiform and navico cuboid ) is also greater in Alces than found in the generalized ruminant. Greater fusion of the tarsal bones and elongation of the proximal limb both increase power of the foot and are consistent with the rigidity of the distal leg during stilt locomotion. Stilt locomotion and very long legs are ideal when moving thro ugh deep snow or water. The phalanges are relatively long and the specific morphology if the third phalanx in the foot allows for a wider spreading of the toes. Wider feet are a possible adaptation for walking on soft ground as well as swimming (Breda, 200 8) Compensating for Mass and Size Size and mass (and correspondingly weight) are two vital factors that influence evolution of locomotor behaviors and t he related physical adaptations (Clifford, 2010) Mechanical, physiological, ecological, and structur al constraints are the main selective pressures acting on the locomotor apparatus (ie. bones, muscles,

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Carroll 64 tendons, etc). Within these energy efficiency acts as an additional selective pressure (Hackert et al. 2006) Size and mass of the animal do not exist i n a vacuum, and it is the size and mass in the context of the surrounding environment that is pivotal. The largest land mammals were the sauropod dinosaurs. The largest of these, and the heaviest land animal known, was the titanosaurian sauropod Argentino saurus Argentinosaurus lived during the upper Cretaceous, approximately 85 Ma. These massive her bivores weighed up to 78,000 kg (Fowler & Sullivan, 2011) The largest terrestrial mammal Indricotherium (= Paraceratherium) weighed only 15,000 20,000 kg (Pa ul & Christiansen, 2000; Prothero, 2001; Janis et al., 2012). The largest extant terrestrial animal is the African elephant weighing in at a mere 7000 kg (Shoshani, 2001b). Gravity is the limiting factor in terms of size and mass for terrestrial animals. The largest animal ever is the extant blue whale ( Balaenoptera musculus ). Because blue whales are in a marine environment, gravity is not as limiting a factor allowing for these enormous ma mmals to reach up to 136,000 kg (Lecointre & Le Guyader, 2006; Arki ve, 2013) Size: Apparently size does matter... Body size is one of the most important in fluences on locomotor evolution (Clifford, 2010). Energy efficiency during locomotion varies with size. Smaller animals are less energy efficient generally than lar ger animals. Smaller animals also use longer relative stride lengths when running than larger animals and smaller mammals run slightly differen tly than larger mammals as well (Paul & Christiansen, 2000; Christiansen, 2002)

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Carroll 65 Obstacles and irregularities of the ground relative to the animal increase as body size decreases (Fischer, 1994). A fallen branch may be navigated by a moderate large sized antelope, such as the 90 110 cm (3 3.7 ft) tall at the shoulder lesser kudu ( Tragelaphus imberbis ), simply by step ping over the obstacle. A smaller Muntiacus reevesi ) with a shoulder height of 40 cm (16 in), would have to l eap over a similar sized branch (Beth Carroll, personal observations, Huffman, 2013). There is considerable d ifference mechanically as well as energetically between a leap and a high step. dik ( Madoqua kirkii shoulder height 35 their hind legs much higher off of the ground with leg tucked up against their rump while walking even over bare ground (Beth Carroll, personal observation). Moderate large sized bovids such as the lesser kudu and dama gazelle also called the addra gazelle ( Nanger dama, s houlder height 90 120cm) (Huffman, 2013) tend to lift their feet highest only when walking over obstacles or through tall grass. On bare soil or short cropped grass they tend to lift their hind fee t roughly as high as their hock (Beth Carroll, personal obs ervation) Sitatunga are roughly the size of the lesser kudu and dama gazelle, (75 125 cm / 2.2 4.1 ft at the shoulder) (Huffman, 2013). Interestingly, sitatunga lift their hind legs high like smaller artiodactyls do whether they are walking through tall gr ass or over bare ground (Beth Carroll, personal observation). This could be related to the tall grasses and reeds of their native marsh habitat. Sitatunga are also strong swimmers and flee into deep water

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Carroll 66 when escaping predators (Huffman, 2013) When wadi ng into water it takes noticeably l ess energy to lift the legs out of the water to reduce drag rather than push against and displace enough viscous (as compared to air) water to take a step (Beth Carroll, personal observation). Scansorial and arboreal ung ulates such as klipspringers, mountain goats, and hyraxes are known as being well adapt ed for climbing rocks and trees ( Lecointre & Le Guyader, 2006; Huffman, 2013) Climbing usually brings to mind primates leaping or brachiating from tree to tree. Yet sim ply watching a mountain goat ( Oreamnos) or rock hyrax one can easily see that it would be more appropriate to describe them as jumpin g and running from rock to rock (Beth Carroll, personal observation) conception of themselves from one surface or support to another (Hildebrand, 1988). The order of spaces seems to always be related to body size (Fischer, 1994). A lot of small scansori a modified for the habitat (Hildebrand, 1988) That is not to say that smaller bodied scansorial or arboreal animals do not possess any adaptations for climbing. Many hooved climbers possess specializations such as shor tened hooves ( Oreamnos and O. oreotragus ) or dewclaws ( Bos grunniens or yak) (Foss & Prothero, 2007; Huffman, 2013). Hyraxes have sweat glands on t heir feet to help with traction (Fischer, 1994; Shoshani, 2001a; Lecointre & Le Guyader, 2006) Animals like the hyrax also often lay out runways or paths (Fischer, 1994; Prothero, 2001). In addition to traction, the surface on which these animals are

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Carroll 67 locomoting may be on an incline or sloped and so the animal is fighting gravity as well (Huffman, 2013). Mass/ Body size goes hand in hand with body mass. Generally, larger mammals are more energy efficient when running than smaller mammals; locomotor cost decreases with body mas s while it increases with spee d (Christiansen, 2002) While energetically more efficient, large body mass has structural significance. The force of and influence on structural support (Paul & Christiansen 2000) and the locomotor constraints differ between large and small organisms, even through the lifetime growth of a single individual (Miller et al., 2008). A common assumption is that limb bones, long bones more specifically, are the primary support for the body (Kokshenev & Christiansen, 2010). The bone of larger, heavier animals are usually more robust to counteract the greater stresses acting on the skeleton (Alexander & Pond, 1992; Kreutzer, 1992; Miller et al., 2008) Graviportal stance is usually assumed to be an adaptation for immense size and weight. Elephants are the usual example given for this conformation, but rhinos and hippos are usually considered graviportal animals as well. Straight, robust, and columnar limbs primar ily characterize Gra viportality ( See figures 3.10 and 3.11) (Hermanson & MacFadden, 1996; Shoshani, 2001b; Alexander & Pond, 2002; Hutchinson et al. 2006; Weissengruber et al., 2006; Miller et al., 2008; Ren et al., 2008; Ren & Hutchinson, 2008; Clifford, 2010; Kokshenev & C hristiansen, 2010)

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Carroll 68 Figure 3.10 In graviportal animals, like elephants (A) and sauropod dinosaurs (B), the limb bones are essentially loaded as vertical columns. In cursorial animals, like the horse (C), the limb bones are loaded as inclined beams rather than vertical columns. This is p articularly obvious for the humerus and femur. Adapted from McGowan, 1999

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Carroll 69 Graviportal limb structure as an adaptation to compensate for great mass is an attractive prospect for explaining the oddities of elephant locomotion such as a the lack of an aerial phase and running walk. However, the situation is not nearly so simple (Alexander & Pond, 2002; Hutchinson et al., 2006; Ren et al., 2008; Ren & Hutchinson, 2008; Kokshenev & Christiansen, 2010) Weight alone cannot be the reason. Giraffes ( Giraffa camelopardalis) can weigh roughly 1.2 2 tonnes (Dagg, 19 71; Alexander & Pond, 2002; Lecointre & Le Guyader, 2006) That is not too much H. amphibius ) 1.5 3.2 tonnes (Theodor, 2001; Alexander & Pond, 2002; Lecointre & Le Guyader, 2006; Huffman, 2013) Yet giraffes have very long, slender, cursorial legs. If weight were the primary influence determining graviportality or cursoriality, giraffes should also have thick limbs. It should also be noted that the long, relatively straight graviportal legs of elephants differ markedly from the short, not as straight gravip ortal legs of rhinos and hippos (Alexander & Pond, 2002; Weissengruber et al., 2006) Figure 3.11 Some graviportal adaptations if the right foreleg of a Indian elephant Elephas Adapted from Hildebrand, 1988

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Carroll 70 One feature shared by elephants, rhinos, hippos, and even large tetrapod dinosaurs is a fibrous and fatty pad of tissue underlying th e digits (Ferguson, 1997; Miller et al., 2008). The elephant foot is highly specialized, the numerous elements of which are tightly bound and function as a unit much like a hoof. The skeletal structure of the elephant digits in both manus and pes are in a subunguligrade or unguligrade posture, but the presence of the footpad renders ele phants functionally plantigrade (Weissengruber et al., 2006; Miller et al., 2008) While functionally the same, the bones of the manus and pes differ in their underlying conf ormation. (See Figure 3.12) The manual digits are in a more upright, columnar orientation whereas the digits of the pes are more horizontal creating a tripod of support. The elephant pes has been Figure 3.12 Bones of the elephant manus and pes (specim ens A and B, respectively). Manus (a) cranial, (b) caudal, (c) medial and (d) lateral views. Digits are labelled I V: acc accessory carpal; C1 4, carpals I to IV; ic intermediate carpal; meta metacarpals; pp prepollex; rad radius; rc radial carpal; u c ulnar carpal; uln, ulna. Pes (e) cranial, (f) caudal, (g) medial and (h) lateral views. Digits are labelled I V as for the manus; cal calcaneus; cen centrale; b meta metatarsals; ph prehallux; tal talus; T1 4, tarsals I to IV; tib tibia. Phalanges (1 3, variable between digits) and paired sesamoids are shown but not labelled. Adapted from Miller et al. ( 2008)

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Carroll 71 heeled s et al. support in both the manus and the pes termed the prepollex and prehallux respectively. While cartilaginous, the prepollex and prehallux (collectivel y termed predigits become progressively more mineralized with age (presumably with size and weight as well) and they are considered to fulfill a primarily supportive role and prevent compression and potentially collapse of the footpad during locomotion (Miller et al., 2008) Another oddity of elephant posture is the comparatively straight legs (Alexander & Pond, 2002; Weissengruber et al., 2006) This is best seen in the knee joint. The standing knee posture of most quadrupeds can be described as a half bent one. The femur and tibia in elephants when standing create a 180 degree angle and kn ee in posture and motion than other quadrupeds. The knee posture may correspond to plantigrady as well as weigh t bearing or locomotor patterns (Weissengruber et al., 2006) The knee and limb morphology in most of the extinct proboscideans is similar to ele phants, but there are some early exceptions, notably Moeritherium and Numidotherium implying different gaits in these taxa. It is possible the specialized knee seen in modern proboscideans was adopted later than Moeritherium and Numidotherium or in differ ent lineages (Weissengruber et al., 2006)

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Carroll 72 As has been previously mentioned, elephants run with a strange, grounded gait and never have an aerial phase. This lack of suspension is usually associated with the great weight of extant elephants (Alexander & P ond, 2002; Biknevicus & Reilly, 2006; Hutchinson et al. 2006; Weissengruber et al., 2006). Other graviportal and heavy anima ls do have aerial phases though (Alexander & Pond, 2002; Christiansen, 2002; Hutchinson et al., 2006; Ren & Hutchinson, 2008; Cliff ord, 2010) Rhinoceroses are able to achieve a full gallop with limb bones under no more stress than a horse (Alexander & Pond, 2002). Hippopotamuses trot (Beth Carroll, personal observation). Extant elephants are not the largest size that proboscideans h ave achieved but many extinct proboscideans share the limb skeletal morphology seen in extant elephants so it is presumed they moved in a similar manner (Christiansen, 2002; Hutchinson et al., 2006; Weissengruber et al., 2008) The large sauropod dinosaur s and extant elephants share enough limb morphological features that a sauropod proboscidean analogy is often used and they most likely used similar gaits (Paul & Christiansen, 2000; Ren et al., 2010). Some extinct perissodactyl Brontotheres, such as Megac erops that was roughly the size of a modern rhino, also had elephant like limb anatomy, or hindlimb at the very least, and probably employed a grounded running walk when running as elep hants do (Janis et al., 2012) The largest terrestrial mammal was the rhinoceros Indricotherium (= Paraceratherium ) and wei ghed approximately 15 20 tonnes (Paul & Christiansen, 2000; Prothero, 2001; Christiansen, 2002; Janis et al., 2012) That is more than double th 7 tonnes (Shoshani, 2001b). (See fig ure 3.13) If the

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Carroll 73 capability of an aerial phase depended solely on weight, Indricotheres would have been quite earthbound. However, Indricothere limb morphology is significantly different from proboscideans in both limb posture and joint flexion. Indrico there limb posture is similar to other rhinoceroses, including the extant taxa. These extinct giants could at the very least trot if not fully gallop (Paul & Christiansen, 2000; Christiansen, 2002; Janis et al., 2012) Ceratopsian dinosaurs as well have a limb structure more similar to extant rhinos and probably had the same locomotor capabilites as rhinos and other cursors. See Figure 3.14 for a reconstruction comparing the movement of the limb while running in ceratopsids and several large terrestrial ma mmals. An alternate explanation for the incapability of elephants performing a period of suspension while running concerns not weight, but the compliance of the hindlimbs (Kokshenev & Christiansen, 2010) Most running mammals are able to achieve an aerial phase and the hindlimbs are stiffer (less compliant) than the forelimbs. Contrastingly, in elephants the forelimbs are stiffer a nd the hindlimbs more compliant (Kokshenev & Christiansen, 2010) Figure 3.13 A size comparison of Paraceratherium (=Indricothere ), an African savanna elephant, and a human. Retrieved April 15, 2 013 from http://www.itsnature.org/rip/dinosaurs/indricotherium/

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Carroll 74 Mini me: Juvenile animals and dwarf lineages It is clear both size and weight are important factors influencing limb proportions and locomotor capabilities (even if not always how we expect). In mammals, babies and juveniles are simply scaled down versions of their parents, including limb posture and overall pr oportions. This extends to locomotion. Baby elephants employ the same groun ded running walk gait as adults (Hutchinson et al., Figure 3.14 Triceratops or Torosaurus includes anterior view of forelimb and possible point of scapular rotation indicated by a white dot. B, Fast galloping Equus C, Slow galloping juvenile Rhinoce ros D, Ambling Elaphus Adapted from Paul and Christiansen (2000)

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Carroll 75 2006; Phillips, 2006; Miller et al., 2008; Ren et al., 2008; Ren et al., 2010). While the locomotor kinematics and mechanics are the same for small or young animals and larger adults, juveniles have greater athletic abil ities and locomotor performance (Hutchinson et al., 2006; Phillips, 2006; Miller et al., 2008) Younger animals in general tend to be more active than adults (Dagg, 1971; Hutchinson et al., 2006; Phillips, 2006; Miller et al., 2008; Beth Carroll, personal observation). What about evolutionary lineages that have secondarily become smaller? Dwarf lineages are quite common for a number of clades. Extant hyraxes are si gnificantly smaller than some of their ancestors such as Titanohyrax ( Shoshani, 2001a; Witte et al., 2002; Lecointre & Le Guyader, 2006) Even smaller than the extant hyraxes was the Eocene Microhyrax lavocati which was tinier than a modern elephant shrew (Rasmussen & Simons, 2000). Limb proportions are sometimes conserved in small taxa that originated from larger ancestral forms. Pygmy hippos move similarly to the larger hippopotamus (Clifford, 2010; Beth Carroll, personal observation). It is also likel y that dwarf elephants moved similarly to larger elephants so long as they are morphologically similar (Hutchinson et al., 2006; Clifford, 2010). This may not always be the case, though. In the case of hyraxes, the modern taxa descended from larger cursor ial forms and retained many cursorial traits, but conformation that is a geometry more typical of small mammals (Witte et al., 2002). No matter how you look at it, while size and w eight are major influences on the evolution of morphology, there is no simple single manifestation.

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Carroll 76 Behavior As has been previously stated ecology, morphology, and behavior are tightly intertwined evolutionarily. The co evolution of these factors can b e seen not only in locomotory behavior, but other types of behavior as well (Kitchener, 1991) Non locomotor behaviors and activities may employ a larger range of motion in joints than locomotion (Ren et al., 2008). Related species tend to share morpho logy and as a result move in similar ways. Giraffes ( G. camelopardalis) have to spread their forelegs out to the side when drinking or grazing. (See figure 3.15) This is because of their long neck and legs. The okapi ( Okapia johnstoni), st dwelling relative, still has proportionately long legs and a relatively long neck, but not nearly so severe a condition as seen in the giraffe. The okapi, similar to the giraffe as would be expected by their shared ancestry and morphology, also straddle s the forelegs when grazing or drinking. (See figure 3.16) Both giraffids are naturally browsers, but there is a degree of behavioral plasticity seen in all animals. It is reasonable that under certain circumsta nces a browsing animal would coo pt a differ ent behavior for new purpose. Co option is not at all unusual in evolution. The moose, ( A. alces) is a highly specialized browser Figure 3.15 A gira ffe ( G. camelopardalis ) grazing at the Maryland Zoo in Baltimore. Photo by Beth Carroll, 2012 Figure 3.16 A okapi (O. johnstoni) grazing at the Maryland Zoo in Baltimore. Photo by Beth Carroll, 2012

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Carroll 77 (Breda, 2008) Still, moose can be seen grazing, demonstrating behavioral plasticity. With a short neck and long legs, a moose would have difficulty reaching the ground while standing straight. Instead of creating a wider stance, moose instead bend down onto their front legs. The position looks like they are of their forelegs but they are actually restin g their weight on their metacarpal joint or wrist. (See figure 3.17) Warthogs have short necks that necessitates this wrist kneeling behavior when feeding. Age and size does not change matters and both baby and adult warthogs bend their fore legs while ea ting (See Figure 3.18 ) (Beth Carroll, personal observation). Bending down to reach the ground is only one application of this movement. The mechanics of a single movement can be applied to a wide variation of behaviors. The sable antelope ( Hippotragus niger) bends onto the forelegs while drinking or grazing, even though their neck is long enough that they can usually reach. H. niger is most known for exploiting this maneuver during intraspecific combat for access to mates. When fighting the two males w ill clash with their horns, drop to their metacarpal joints, and wrestle (See Figure 3.19) Figure 3.17 A moose grazing on metacarpal joints. Retrieved from April 11, 2013 from http://www.nps.gov/features/yell/sl idefile/mammals/moose/Page 4.htm Photo by J Schmidt, 1977 Figure 3.18 A common warthog ( Phacochoerus africanus ) feeding at the Maryland Zoo in Baltimore. Photo by Beth Carroll, 2012 Figure 3.19 Two male sable antelope ( H. niger ) fighting, one is kneeling on the ground on metacarpal joints. Retrieved April 11, 2013 from http://www.africanwildlifeguide.com/specie s gu ide/mammals/antelope/sable antelope

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Carroll 78 (Kitchener, 1991; Huffman, 2013) Several other bovids such as wildebeest ( Connochaetes spp.) and oryx ( Oryx spp.) also fight in this manner (Kitchener, 1991). Th e position with weight forward on forelegs bent at the wrist is also a standard movement when lyin g down in many ungulates. To lie down, giraffes and many other cursors bend first their front legs resting their weight on their metacarpal joint s and then tu ck their hind legs (Dagg, 1971; Beth Carroll, personal observation) Figure 3.20 depicts a male lesser kudu ( T. imberbis ) in the process of lying down. Cursorial ungulates ranging in si ze from gazelles to giraffes lie down in a similar if not the same way. There are only so many ways to move a particular type of joint. Similarly, there are only so many ways to scratch an itch when you have four hooves and nothing to scratch against. Figures 3.21 and 3.22 show a bactrian camel ( Camelus bactrianus ) and K ey deer ( Odocoileus virginianus clavium ) respectively Figure 3.20 A lesser kudu ( T. imberbis ) in the process of lying down in the grass at the Maryland Zoo in Baltimore. Photo by Beth Carroll, 2012 Figure 3.21 A Bactrian camel ( C. bactrianus ) scratching an itch, at the Maryland Zoo in Baltimore. Photo by Beth Carroll, 2012 Figure 3.22 A Key deer ( O. virginianus clavium ) scratching an ear, at the Lowry Park Zoo in Tampa. Photo by Beth Carroll, 2013

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Carroll 79 Both animals are balancing with one back leg lifted to scratch an irritation. Reaching a leg towards the head is no t a standard locomotor behavior (Beth Carroll, personal observation) Reaching high leaves is another situation in which more mobility or different types other than those involved in locomotion would be needed. It is common knowledge that giraffes evolved long necks that are useful for exploiting the upper branches of trees so as to avoid competition for resources (Dagg, 1971; Theodor, 2001; Huffman, 2013) The gerenuk ( Litocranius walleri) is often called the e to its slender elongated neck (Janis et al., 2002; Huffman, 2013) Gerenuks, as exclusive browsers, have anot her similarity to giraffes. Gerenuks have evolved a behavioral adaptation to assist in reaching the leaves on high branches. They will stand upright on their hind legs and rest a foreleg against the tree or branch for bala nce (See figure 3.23) (Huffman, 20 13) Other ungulates, while not adapted for such, will sometimes show similar behavior and resourcefulness to reach that perfect leaf, such as the female sitatunga in figure 3.24 (Beth Carroll, personal observation) Left: Figure 3.23 Adult female gerenuk ( L. walleri walleri ) in the typical standing feeding posture. Retreived April 10, 2013 from http://www.ultimateungulate.com/Images/Litocra nius_walleri/L_walleri3.html Photo copyright 2001 by B. Huffman Right: Figure 3.24 A sitatunga ( T. spekeii ) resting front hooves on the fence to the enclosure while browsing at the Maryland Zoo in Baltimore. Photo by Beth Carroll, 2012

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Carroll 80 Migratory vs. Sedentary: Is the grass always greener on the other side of the mountain? Migratory behavior is closely tied to locomotion as a response to seasonal changes in habitat and resources, and migrating mammals may cover long distances in search of food (Van der Sluijs et al., 2010; Julien et al ., 2012). Caribou ( R. tarandus ) are generally nomadic, but undergo extensive seasonal migrations in the spring and fall. Caribou have been recorded to tra verse 5,000 km in a single year (Huffman, 2013) Migration is the movement awa y from the home range to another area prompted by seasonal changes and with a retu rn back to the home range again (Julien et al., 2012) and similar terms. Dispersal is the movement from one geographical area to another without return (Julien et al., 2012) As migration usually involves nearly continuous movement once begun until suitable resources are reached. This constant movement is quite different energetically from daily behaviors relat ed to breeding or self maintenance. As a result, a different suite of adaptations, both physical and behavioral, are needed specifically for sustained travel. In contrast, dispersal does not have a predetermined destination or a continuous trek. Dispersa l generally does not require any specific specializations. It should also be noted that migratory species may become sedentary if the conditions are suitabl e and resources remain abundant (Julien et al., 2012) For migrating animals, economy of motion an d energy conservation is essential. Old World camels are well adapted for covering great distances in search

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Carroll 81 of food or water through semi arid habitats. It has been postulated that their unique pacing gait is an adaptation for traveling large distances (M aloiy et al., 2008; Van der Sluijs et al., 2010). Comparatively, New World camelids such as the guanaco and v icuas live in mountainous valleys and plains with rather good distributions of water. As was mentioned previously, lamoids are either sedentary or only marginally migratory. Lamini do not have an intermediary gait equivalent to the pace, and this may be a result of the differing ecological conditions betw een the two groups of Camelidae (Van der Sluijs et al., 2010) Similar to the New World Lamini, giraffids have also lost an intermediary gait and retain only a lateral sequence walk and rotary gallop (Dagg, 1971) Notably, the two extant species of giraffid are both sedentary, despite inhabiting markedly different habitats. Giraffes are non territor ial and occupy open and sparsely wooded savannas. individual jungle territories roughly 2.5 5 square kilometers (Theodor, 2001; Huffman, 2013) The lack of intermediate gait in giraffes h as not been thoroughly investigated, but there may be a correlation between the absent intermediate gait and sedentary lifestyle. African and Asian elephants move generally the same, but there are some subtle differences in locomotor mechanics that coul d be explained by differences in ecology and migratory activity (Kokshenev & Christiansen, 2010) African elephants live in open grassland and savanna environments and undertake regular seasonal migrations. These elephants keep to a walk most of the time a nd are extremely energy efficient with regards to locomotion. This may be in some way related to

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Carroll 82 energy con servation for extended journeys (Kokshenev & Christiansen, 2010; Ren et al., 2010) Asian elephants tend to be found in more forested areas and seem to take fewer if any migrations that cover shorter distances than their African counterparts (Kokshenev & Christiansen, 2010) Dissimilar environments and migratory behavior could reflect on the mechanics of even daily locomotor activities. The different e cological conditions have been proposed as a possible reason for the slight locomotor and morphological differences betw een African and Asian elephants (Hutchinson et al., 2006; Kokshenev & Christiansen, 2010) Fight or Flight: Are you threatening me, ca Predator avoidance is as much a selection pressure as the consumption of food. The choice between a rotary or transverse gallop has been associated in some species not only with e nvironmental constraints, but with predator avoidance as well. Gazelles are found in open grassland habitats where transverse gallops tend to be more favorable. Gazelles, however, utilize a rotary gallop, relying on maneuverability as well as speed to escape pursuing predato rs (Biancardi & Minetti, 2012) Lim b adaptations to skeletal morphology and the resulting motions that are useful for locomotion can be beneficial for defense also. Alces have an oddly spherical femoral head as compared to other deer with symmetrical distal trochlea. This specialized femur allows for a wider range of lateral movement of the proximal leg whereas alternatively the cylindrical femoral head typical of most deer limits movement strictly to a sagittal plane. The structure in Alces loco motion over uneven ground.

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Carroll 83 Increased range of lateral movement in the hip is also the source of the fairly unique posterolateral kick Alces use to defend a gainst predators such as wolves (Breda, 2008) Nearly identical limb structure is found in the genus Cervalces an extinct relative of Alces. Due to these shared specialized characters, one can infer that Cervalces moved in the same way as the modern moose, and probably defended against predators with the same posterolat eral kick (Breda, 2008)

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Carroll 84 Conclusio n Where do we go from here? Structural and behavioral adaptations for locomotion and other behaviors are adaptation s that have co evolved in response to the surrounding environment. The interactions and trends of these characteristics as observed in extant taxa are valuable clues for the reconstruction of the behavior and ecology of extinct animals. With this, we can piece together the puzzle of what life on our planet used to be like, an image that would otherwise be lost. A caveat or two Unfortunately, this process is slightly more complicated than the average jigsaw puzzle. Of extinct animals, fossilized bones are all a paleontologist has to work with. Soft tissue features: muscles, tendons, etc. must be inferred from the marks they might have left on t he bone and most soft tissues like organs or hair do not leave such scars (Riess & Frey, 1991; Lauder & Thomason,1995; Weishampel & Thomason, 1995; Witmer & Thomason, 1995) Occasionally a trace fossil such as a trackway will provide an idea of foot shape, stride length, and footfall pattern, but (Thompson et al., 2007). Furthermore, the fossil record itself is incomplete as only a fraction of the organisms that have lived died un der the exact circumstances and location in which the remains would undergo fossilization. Scientists or collectors have recovered even fewer of these bones. Preservation and completeness of a fossilized organism are also not guaranteed. Very few fossils t hat are recovered are

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Carroll 85 complete or articulated. Piecing together a single fossil skeleton is a difficult puzzle in an d of itself. Returning to our jigsaw puzzle analogy, recreating a clear image of an extinct species and habitat is putting together a jigsa w with a few added challenges. It must be done without knowing what the picture is supposed to be, how many pieces you have, if there are pieces missing, when you will find more, or how the pieces are supposed to fit together. You also cannot assume all of the pieces you do have are undamaged and have not changed shape during the intervening years. Through the integration of paleontological studies of fossils and the biological studies of extant taxa, the number of proverbial puzzle pieces is growing, and w hile we may never have a perfectly complete picture, our understanding will be more complete than previously. The total picture obtained from a complete fossil is not always necessary to make valid inferences and portions are individually useful. The data collected from reconstructing the biomechanics of extinct taxa has been used to further our understanding of not only extant forms concerning mechanics or veterinary care, but has also been applied to non organic fields such as robotics (Rischer & Blickha n, 2006; Hackert et al., 2006; Sellers et al., 2009; Waldron et al., 2009; Biancardi & Minetti, 2012). In the areas where the fossil record is fairly complete as is the understanding of the biomechanics of extant taxa, such as is the case with equines, ca ution is still necessary when making interpretations of osteology and possible correlations. Behavior, including locomotion, is under neural control. Changes in neural output

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Carroll 86 can alter muscle activity patterns and as a result altering stride with few visib le structural alterations (Lauder & Thomason, 1995) The same movement or behavior can also have multiple purposes (Lauder & Thomason, 1995; Witmer & Thomason, 1995; Hermanson & MacFadden, 1996; Breda, 2008) The plasticity and variation of behavior shoul d also be taken into account. Living populations are often used as model s of related extinct taxa, but this direct modeling is not always reliable. Extant bison populations have severely curtailed home ranges due to human populations and as a result the mi gratory or sedentary behaviors exhibited even in wild herds may be at least in part artificial. Historically, bison are considered migratory, or at the very least highly nomadic. Up into the Holocene, the extinct steppe bison ( Bison priscus ) was widespread across the Eurasia. It has been previously assumed B. priscus were migratory as is generally attributed to their modern counterparts, but isotope analysis of fossilized tooth indicates B. priscus had a diet pa rtially consisting less nutritious lichens (Julien et al., 2012) This is more consistent with a non migratory population in a limited territory such as the modern European ( B. bonasus) and Canadian (B. bison athabascae ) b ison populations. These two sedentary groups have severely restricted ranges due to human populations and feed on low energetic plants during cold seasons rather than seasonally migrating to more nutrient rich food sources. The historically assumed migrato ry behavior of the more wide ranging American bison ( B. bison bison ) is also under debate.

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Carroll 87 Physically, bison are more suited for open grassland, but with partial exception of the American bison, populations have been pushed into more wooded habitat. The v ariability seen in diet and behavior of modern groups implies an equal or greater amount of variab ility in fossil species as well (Julien et al., 2012) The assumption of uniform behavior for closely related species is misleading. In fossil groups that ha ve no close extant relatives any assumptions based on generalized traits is even trickier. It is always best to collect as much direct data from the fossils themselves and contemporaneous geologic and paleoenvironmental clues, such as looking at isotopes i n B. priscus tooth enamel to determine diet (Julien et al., 2012) Assumptions can result in misinterpretations of the data, but it should be noted that in cases where something cannot be observed directly, such as inferences of soft tissue in fossil speci es, a certain degree of speculation is required (Witmer & Thomason, 1995). Ignoring one aspect of the myriad influences on the selection and evolution of morphology and behavior can result in an attractive, yet inaccurate explanation. If one were to look would be explained merely with their immense weight. It is only when extinct forms are included, namely a far heavier Indricothere still able to trot, that weight is revealed to be only part of the equation. Overall, a balanced, multidisciplinary, direct approach including not only extinct and extant species, but also ecological factors and with an awareness of the limitations of such studies seems the best strategy when addressing questions s uch as functional interpretations of fossil taxa.

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Carroll 88 Future research There are a number of possible avenues for future research. In only a small number of species are the biomechanical specifics of locomotion studied in depth. Our knowledge of comparatively well understood taxa will also increase and change as new technology becomes available. An interesting parallel to be explored further is the loss of an intermediate gate in both camelids and giraffids. Neither the New World camelids nor the giraffids (g iraffe and okapi) demonstrate an intermediate gait. The form of gallop employed by lamoids and giraffids, transverse and rotary respectively, are not the same. Habitat choice of these taxa do not coincide either; mountainous valleys (lamoids), savanna gras slands (giraffes), and jungle (okapi) (Dagg, 1971; Theodor, 2001; Van der Sluijs et al., 2010; Huffman, 2013) There is a possible relationship between a sedentary lifestyle and the loss of an intermediate gait, but there have been no targeted investigatio n into this thus far. Also unsolved, is why giraffes prefer a rotary gallop when camelids prefer the transverse (Pfau et al., 2011). However, a deeper look at Okapi would be necessary for such a study. The forest dwelling Okapi are morphologically the more archaic of the living giraffids and would provide insight into extinct giraffids (Theodor, 2001) Gait preference in relation to predator avoidance would also be a line of research to pursue. Chasing prey is a major factor influencing predators just as av oiding being eaten is a major influence on prey animals (Lingle, 1992; Hermanson & MacFadden, 1996; Sellers et al., 2009) Certain large animals such as elephants do not need to worry overmuch about predators once they reach adulthood due to

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Carroll 89 their size (Sh oshani, 2001b) Elephants also rarely run (Ren et al., 2010) Other animals, such as the rhinoceros, respond to potential threats by charging. Rhinos, having rather poor vision, need only a hint of provocation to rush forward, investing co nsiderable energy into a gallop (Prothero, 2001) Some ungulates rely on either outmaneuvering or outrunning pursuers and the choice between these two strategies has been found to have a correlation with gallop choice (Biancardi & Minetti, 2012) Some animals when fleeing predators also use gaits such as the bound or pronk. Pronking, also called stotting, involves all four feet leaving the ground and landing simultaneously. A number of artiodactyls such as the springbok ( Antidorcas marsupialis) and the mule deer ( Odocoileus hemionus ) are known to utilize this strange gait as a display responding to a threat (Lingle, 1992; Peters & Brink, 1992) Osteological correlates in association with any of these gaits or avoidance strategy could be valuable for reconstructing anti preda tory behavior in extinct taxa. Some behaviors are not directly related to locomotion, but involve movement of many of the same joints. One such movement or behavior is lying down. As was described in the previous chapter, most cursorial ungulates lay down on the ground first by bending their front legs, resting on their metacarpal joint and then fold their hind legs (Dagg, 1971; Beth Carroll, personal observation) Elephants, however, lower the posterior half first by bending their back legs. Sliding out straightened fro nt limbs controls their descent (Beth Carroll, personal observation). The method employed by elephants may be related to their straight, columnar graviportal limbs. Rhinoceroses despite being generally considered graviportal, have a limb st ructure

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Carroll 90 more similar to other cursorial perissodactyls and run like them as well. Unlike other cursorial perissodactyls, such as the horse, rhinos lay down by bending their back legs first then their front legs, with a similar back to front method seen in elephants and unlike the front to back manner in horses and many other ungulates (Beth Carroll, personal observation). Weight may be a factor regarding how an animal chooses to lay down, but it would be interesting to investigate how much of a role if any weight actually plays. Looking at the hippopotamus and other large or heavy ungulates could make a more inclusive comparison. It would also be prudent to determine how weight distribution and the full range of joint motion involved in both the lounging be havior and leg extension while running can be compared. Aardvarks would be another intriguing clade to investigate. As a living fossil, the modern aardvarks give an interesting perspective on some early Afrotherian ungulates. These animals are also the on ly modern clawed form of ungulate. There may be some comparisons that could be drawn with other, larger extinct, clawed ungulates such as Chalicotheres. Aardvarks also have interesting defense behaviors when confronted with predators. When in defense mode, aardvarks will stand upright on their hind feet and use their thick, muscular tail to help support them. This position is similar to that seen in kangaroos and some comparisons could be drawn there. Aardvarks will also tuck their head between their front legs and roll into a k icking somersault when cornered (Shoshani, 2001c) Somersaulting itself is a very atypical behavior for extant ungulates and the mechanics and evolution of this behavior would be interesting to study.

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Carroll 91 There are multiple instances of parallel evolution in response to similar environments. Cetacea and Sirenia, for example. Studying early groups of these clades may give insight into the transition from a terrestrial to fully aquatic habitat. These two groups share many very similar trait s such as the transformation of forelimbs into flippers, but the underlying structure of this change differs. Both cetaceans and sirenians made the transition first to freshwater habitats and then later to saltwater. Several cetacean families of river dolp hin made the parallel transition back to freshwater from a marine habitat. The sirenian manatee also transitioned back from marine to freshwater. The timing of these shifts from terrestrial to aquatic and from freshwater to marine and back could provide in formation on factors in the aquatic ecosystem that may provoke these changes (Domning, 2012; Gatesy et al., 2012; Benoit et al., 2013) A second example of a similar evolutionary response to environmental change is the development of monodactyly. Equine mo nodactyly has been extensively studied and the mode rn horse is the only extant taxon exhibiting this characteristic. Equines were not the only group to acquire monodactyly, nor the earliest. The extinct South American litopterns evolved a monodactyl foot r oughly 20 million years earlier than horses. This earlier occurrence of monodactyly in South America is attributed to grasslands appearing 15 million years earlier than elsewhere, but the timing is not exact and there may be other factors involved (Ferguso n, 1997; Lambert et al 2008) Numerous additional prospective questions and routes of inquiry remain beyond what I have mentioned here, all of which have implications regarding our

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Carroll 92 understanding the complex relationship between behavior, morphology, locom otion, and ecology of extinct and extant forms. There are some limitations such as the incompleteness of the fossil record and amount of speculation involved in making inferences of soft tissue when none is present. However, even a partial reconstruction o f the vast biological diversity and environment that once covered the planet has more contemporary and practical uses in veterinary care, animal conservation, and robotics. Improvement of the tools necessary for such investigations is a beneficial byproduc t as well, such as improved computer programs for modeling gaits and movement of reconstructed digital forms. Ungulates are an ideal model and focus of studies of quadruped locomotor behavior and evolution due not only to the incredible diversity of body s izes and forms, but the numerous instances of parallel and convergent evolution in response to similar environmental changes.

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Carroll 93 GLOSSARY Arboreal adapted for living in trees Contralateral on opposite sides of the midline of the body Convergent evolut ion the independent acquisition of similar biological traits in unrelated or distantly related evolutionary lineages Cursorial adapted for running Duty factor the ratio of the duration of the support to duration of the stride Froude number a measure of dimensionless speed. T he ratio between centripetal forces around the foot and the weight of the animal (Fr=velocity 2 /[hip height x acceleration due to gravity]) Fossorial adapted for digging Graviportal having straight thick, columnar limbs, usuall y associated with bearing great weight Infraorder a taxonomic category that ranks below a suborder Intermediate gait a gait usually performed at moderate speed such as the pace or trot Ipsilateral on the same side of the midline of the body Keystone animal a species that, relative to population size, has a disproportionate effect on its environment Mesaxonic the axis of symmetry and weight bearing in the foot passes through the third digit Parallel evolution the independent acquisition of simila r biological traits in two closely related evolutionary lineages Paraphyletic a taxonomic group that contains some, but not all, of the descendants sharing a common ancestor Paraxonic the axis of symmetry and weight bearing in the foot passes between t he third and fourth digit Plesiomorphic the ancestral condition of a trait

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Carroll 94 Polyphyletic a taxon containing unrelated groups descended from more than one common ancestor Scansorial adapted for climbing Superorder a taxonomic category that ranks abov e an order Synapomorphy a biological trait shared by all of the descendants of a common ancestor Taxon (plural: taxa) a group of one or more populations of organism

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Carroll 95 REFERENCES Archibald, J. D. (2012). Eutheria (placental mammals). Els, Archibald, J. D., Zhang, Y., Harper, T., & Cifelli, R. L. (2011). Protungulatum, confirmed cretaceous occurrence of an otherwise paleocene eutherian (placental?) mammal. Journal of Mammalian Evolution,18 (3), 153 161. Alexander, R. M., & Pond, C. M. (1992). Locomotion and bone strength of the white rhinoceros, ceratotherium simum. Journal of Zoology, 227 (1), 63 69. doi: 10.1111/j.1469 7998.1992.tb04344.x Argot, C. (2012). Postcranial analysis of a carnivoran like archaic ungulate: The case of arctocyon primaevus (arcto cyonidae, mammalia) from the late paleocene of france. Journal of Mammalian Evolution, 1 32. "ARKive Images of Life on Earth" (On line). Blue Whale (Balaenoptera musculus) Accessed March 21, 2013 at http://www.arkive.org/blue whale/balaenoptera musculus/ Benoit, J., Adnet, S., El Mabrouk, E., Khayati, H., Ali, M. B. H., Marivaux, L., Tabuce, R. (2013). Cranial remain from tunisia provides new clues for the origin and evolut ion of sirenia (mammalia, afrotheria) in africa. PloS One, 8 (1), e54307. Biancardi, C. M., & Minetti, A. E. (2012). Biomechanical determinants of transverse and rotary gallop in cursorial mammals. The Journal of Experimental Biology, 215 (Pt 23), 4144 4156 doi: 10.1242/jeb.073031; 10.1242/jeb.073031 Biewener, A. A. (2003). Animal locomotion Oxford University Press, USA. Biknevicius, A. R., & Reilly, S. M. (2006). Correlation of symmetrical gaits and whole body mechanics: Debunking myths in locomotor biod ynamics. Journal of Experimental Zoology Part A: Comparative Experimental Biology, 305A (11), 923 934. doi: 10.1002/jez.a.332 Bouman, I. 2002. "ARKive Images of Life on Earth" (On (Equus ferus przewalskii). Accessed March 22, 20 13 at http://www.arkive.org/przewalskis horse/equus ferus przewalskii/ Breda, M. (2008). Palaeoecology and palaeoethology of the plio pleistocene genus cervalces (cervidae, m ammalia) in eurasia. Journal of Vertebrate Paleontology, 28 (3), 886 899. doi: 10.1671/0272 4634(2008)28[886:PAPOTP]2.0.CO;2

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Carroll 96 Cavagna, G. A., Heglund, N. C., & Taylor, C. R. (1977). Mechanical work in terrestrial locomotion: Two basic mechanisms for minimi zing energy expenditure. American Journal of Physiology Regulatory, Integrative and Comparative Physiology, 233 (5), R243 R261. Cerdeo, E. (1998). Diversity and evolutionary trends of the family rhinocerotidae (perissodactyla). Palaeogeography, Palaeoclim atology, Palaeoecology, 141 (1 2), 13 34. doi: 10.1016/S0031 0182(98)00003 0 C hristiansen P. (2002). Locomotion in terrestrial mammals: The influence of body mass, limb length and bone proportions on speed. Zoological Journal of the Linnean Society, 136 (4 ), 685 714. doi: 10.1046/j.1096 3642.2002.00041.x Clifford, A. B. (2010). The evolution of the unguligrade manus in artiodactyls. Journal of Vertebrate Paleontology, 30 (6), 1827 1839. doi: 10.1080/02724634.2010.521216 Dagg, A. I. (1971). Giraffa camelopa rdalis. Mammalian Species, (5, Giraffa camelopardalis), pp. 1 8. Domning, D.P. (2012) Sirenia (Dugongs and Manatees). In: eLS. John Wiley & Sons, Ltd: Chichester. DOI:10.1002/9780470015902.a0001576.pub3 Farlow, J. O., Smith, M. B., & Robinson, J. M. (199 5). Body mass, bone "strength indicator," and cursorial potential of tyrannosaurus rex. Journal of Vertebrate Paleontology, 15 (4), 713 725. Ferguson, S. (1997). Natural history collections: Ungulates Retrieved 3/9, 2013, from http://www.nhc.ed.ac.uk/index.php?page=493.170 Fischer, M. S. (1994). Crouched posture and high fulcrum, a principle in the locomotion of small mammals: The example of the rock hyrax (procavia capensis) (mammalia: Hyracoi dea). Journal of Human Evolution, 26 (5 6), 501 524. doi: 10.1006/jhev.1994.1030 Fischer, M. S., & Blickhan, R. (2006). The tri segmented limbs of therian mammals: Kinematics, dynamics, and self stabilization?a review. Journal of Experimental Zoology Part A: Comparative Experimental Biology, 305A (11), 935 952. doi:10.1002/jez.a.333 Fordyce, R. E. (2001). Cetacea (whales, porpoises and dolphins). Els, Foss, S. E., & Prothero, D. R. (2007). The evolution of artiodactyls Baltimore: Johns Hopkins University Press.

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Carroll 97 Fowler, D. W., & Sullivan, R. M. (2011). The first giant titanosaurian sauropod from the upper cretaceous of north america. Acta Palaeontologica Polonica, 56 (4), 685 690. Gatesy, J., Geisler, J. H., Chang, J., Buell, C., Berta, A., Meredith, R. W. McGowen, M. R. (2012). A phylogenetic blueprint for a modern whale. Molecular Phylogenetics and Evolution, Gelfo, J. N., & Lorente, M. (2012). The alleged astragalar remains of didolodus ameghino, 1897 (mammalia, panameriungulata) and a critic of isolated bone association models. Bulletin of Geosciences, 87, 2 Hackert, R., Schilling, N., & Fischer, M. S. (2006). Mechanical self stabilization, a working hypothesis for the study of the evolution of body proportions in terrestrial mammals? Comptes R endus Palevol, 5 (3 4), 541 549. doi: 10.1016/j.crpv.2005.10.010 Hermanson, J. W., & Macfadden, B. J. (1992). Evolutionary and functional morphology of the shoulder region and stay apparatus in fossil and extant horses (equidae). Journal of Vertebrate Pale ontology, 12 (3), pp. 377 386. Hermanson, J. W., & MacFadden, B. J. (1996). Evolutionary and functional morphology of the knee in fossil and extant horses (equidae). Journal of Vertebrate Paleontology, 16 (2), pp. 349 357. H ildebrand M. (1980). The adapti ve significance of tetrapod gait selection. American Zoologist, 20 (1), 255 267. doi: 10.1093/icb/20.1.255 Hildebrand, M. (1988). Analysis of vertebrate structure (3rd ed. ed.). New York: Wiley. Hoyt, D. F., Wickler, S. J., Dutto, D. J., Catterfeld, G. E. & Johnsen, D. (2006). What are the relations between mechanics, gait parameters, and energetics in terrestrial locomotion? Journal of Experimental Zoology Part A: Comparative Experimental Biology, 305A (11), 912 922. doi: 10.1002/jez.a.335 Huffman, B. (2 013). The ultimate ungulate page. Retrieved 3/9/2013, 2013, from http://www.ultimateungulate.com Hulbert, R. C. (2001). The fossil vertebrates of florida Ga inesville: University Press of Florida. Hutchinson, J. R., Anderson, F. C., Blemker, S. S., & Delp, S. L. (2005). Analysis of hindlimb muscle moment arms in tyrannosaurus rex using a three dimensional musculoskeletal computer model: Implications for stanc e, gait, and speed. Paleobiology, 31 (4), 676 701.

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