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Narial Novelty in Mammals: Case Studies and Rules Of NARIAL NOVELTY IN MAMMALS: CASE STUDIES AND RULES OF CONSTRUCTION A thesis presented to the faculty of the College of Arts and Sciences of Ohio University In partial fulfillment of the requirements for the degree Master of Science Andrew B. Clifford August 2003 This thesis entitled NARIAL NOVELTY IN MAMMALS: CASE STUDIES AND RULES OF CONSTRUCTION by ANDREW B. CLIFFORD has been approved for the Department of Biological Sciences and the College of Arts and Sciences by Lawrence M. Witmer Associate Professor, Biomedical Sciences Leslie A. Flemming Dean, College of Arts and Sciences CLIFFORD, ANDREW B. M.S. August, 2003. Biological Sciences Narial Novelty in Mammals: Case Studies and Rules of Construction (pp. 128) Director of Dissertation: Lawrence M. Witmer Both anatomy and function of the enigmatic proboscis of moose and the nasal cavity of saiga are described. Dissection, sectioning, and skeletonisation of study specimens and related outgroups are supplemented with CT scans and other software-generated imaging to describe the structure of apomorphic narial tissues and skeletal modifications. Anatomy is used to assess previously suggested functions of these probosces and to advance new hypotheses based on novel anatomy. Moose noses possess elaborated nostril musculature and nasal cartilages which contribute to a nostril closing mechanism. Saiga have evolved an elaborated nasal vestibule which cleans air destined for lungs. Both probosces modify the bony naris in ways that have justified tapir-like trunks in fossil species. Integrating data from many different probosces, mammals follow limited rules of construction in proboscis- building. Outgroup anatomy constrains proboscis anatomy, and exaptation produces narial novelty. Muscular hydrostats and maxillolabial probosces leave the fewest osteological correlates, limiting proboscis reconstruction. Approved: Lawrence M. Witmer Associate Professor, Biomedical Sciences Dedication To Rosie, who always knew it is not what you take with you when you leave but what you leave behind when you go. She has left behind an immeasurable wealth that shall be cherished forever by everyone that knew and loved her. Acknowledgments I owe my sincerest thanks to so many individuals, many of whom I have never met, who saw fit to donate or provide specimens for the purpose of this research project. In the death of such beautiful animals, they saw the inestimable value to science these animals held. H. Mayle, D. Pratt, and R. Ridgely donated precious time and skill to CT scanning and illustration. J. Sedlmayr, C. Holliday, P. O’Connor, B. Beatty, and T. Hieronymus provided much-needed assistance in specimen preparation. A. Biknevicius and S. Reilly were excellent, patient, and gracious committee members. My advisor, L. Witmer, gave freely many hours of guidance and advice that I hope to carry with me for the rest of my career. Finally, the grounding given to me by my friends and family, their tolerance of my eccentricities, makes this work all the more fulfilling. 6 Table of Contents Page Abstract 3 Dedication 4 Acknowlegments 5 List of Tables 8 List of Figures 9 List of Abbreviations 12 Chapter One: The Enigmatic Nose of Moose (Artiodactyla: Cervidae: Alces alces) 15 Abstract 15 Introduction 17 Materials and Methods 21 Results 22 External anatomy 22 Integument 23 Connective tissue pad 24 Musculature 24 Major nerves and vessels 34 Nasal cartilages 40 Overview of nasal cavity 43 Glands 46 Osteology 47 Discussion 51 Novel aspects of narial anatomy in moose 51 Moose narial anatomy with respect to fossil alcines 56 Functions of moose noses based on anatomical specialisations 58 Chapter Two: Structure and Function of the Nasal Cavity of Saiga (Artiodactyla: 63 Bovidae: Saiga tatarica) Abstract 63 Introduction 65 Materials and Methods 68 Results 69 Overview of nasal cavity 69 Nasal vestibule 70 Main nasal cavity 74 Nasal septum 80 Osteological correlates of the proboscis in saiga 81 Discussion 85 Reorganisation of the nasal cavity 85 Proboscis function in saiga 87 7 Lateral recess homology and function 90 Chapter Three: Rules of Construction in Mammalian Proboscis Building 92 Abstract 92 Introduction 94 Proboscis types within Mammalia 96 Phylogenetic constraint and exaptation 100 Rules of construction in proboscis building 104 Reliable osteological correlates resulting from proboscis building 109 Further tests of construction hypotheses 111 Applications to extinct taxa 113 References 116 Appendix One: Homolgy and Nomenclature of Facial Musculature in Mammals 123 8 List of Tables Page Appendix Table 1. Facial musculature in mammals. Sources for muscles are given in column titles, and muscle groups are given in the leftmost column. Muscles in a single row are homologous. Note the disparities in homology between sources and the disparate nomenclature sometimes used. a—These muscles were grouped separately in a “lateralis nasi group” by Boas & Paulli (1908a, b). b—Except in Carnivora (Evans, 1993). 127 9 List of Figures Figure Page 1.1. Lateral view of male moose (Alces alces) in velvet (a) and lateral view of male moose head (b) showing unique muzzle. (a) Courtesy of M. Reichmann; used with permission. (b) Courtesy of G. and B. Corsi and the California Academy of Sciences; used with permission. 18 1.2. Phylogenetic relationships of taxa and clades referred to in this study. Topology based on Novacek, Wyss & McKenna (1988) and Groves & Grubb (1987). 19 1.3. Superficial dissection of the face of Alces alces shown in (a) left lateral view and in (b) oblique left rostrodorsolateral view, based on OUVC 9559. Scale bars = 10cm. 25 1.4. Deep dissections of the face of Alces alces. Maxillolabial muscles are intact in (a). In (b), the maxillolabial muscles have been reflected to reveal underlying structures, based on OUVC 9559. Scale bars = 10cm. 26 1.5. Drawings of selected computerized tomographic (CT) images of the face of Alces alces (OUVC 9559) showing narial structures in successive transverse sections (a-h). (i) Skull in left lateral view to show the rostrocaudal levels of sections depicted in (a-h). Scale bars = 5 cm. 38 1.6. Oblique left rostrodorsolateral view (a) of a skull of Alces alces with cartilages in place to show the cartilaginous framework of the nose. (b) Skull in left lateral view. Drawings based on OUVC 9559. Scale bars = 10cm. 41 1.7. Medial view of right side of sagittally sectioned head (a) and skull (b) of Alces alces (OUVC 9559) with nasal septum and vomer removed to show internal nasal structures. Scale bars = 10cm. 44 1.8. White-tailed deer (Odocoileus virginianus). Left lateral view of superficial (a) and deep (b) dissections showing musculature of the face and nostril. (c) Medial view of right side of sagittally sectioned head with nasal septum and vomer removed to show internal nasal structures. Skull in left rostrodorsolateral view with nasal cartilages intact (d) and in left lateral view (e). Scale bars = 5cm. 52 1.9. Cladogram of Odocoileus virginianus (a), Cervalces scotti (b), and Alces alces (c) and their skulls in left lateral view to illustrate transformation of the bony naris. Skull in (b) redrafted from Scott (1885). 57 10 2.1. Left lateral views of reconstructions of AMNH 202492 using Amira. (a) Lateral view of isosurface of the intact head. (b) Voxel reconstruction of intact head to simulate a lateral radiograph. (c) skull isosurface. Scale bars = 5cm. 66 2.2. Phylogenetic relationships of taxa and clades referred to in this study. Topology based on Hassanin & Douzery (2003). 69 2.3. (a) Right medial view of Amira-generated isosurface of AMNH 202492. (b) Stereopairs of specimen in (a). Scale bars = 5cm. 71 2.4. Drawings of selected computerized tomographic (CT) images of the face of AMNH 202492 showing narial structures in successive transverse sections (a-i). (j) Skull in left lateral view to show the rostrocaudal levels of sections depicted in (a-i). Scale bars = 5cm. 73 2.5. (a) Left lateral view of Amira-generated isosurface of skull of AMNH 202492. (b) Stereopairs of specimen in (a). Scale bars = 5cm. 77 2.6. (a) Right medial view of Amira-generated isosurface of skull of AMNH 202492. (b) Stereopairs of specmen in (a). Scale bars = 5cm. 82 3.1. Skulls (left) and reconstructions (right) of extinct, putative, proboscis- bearing taxa. (a) Diprotodon, a marsupial. (b) Moeritherium, a basal proboscidean. (c) Glyptodon, a xenarthran. (d) Astrapotherium, an astrapothere. (e) Homalodotherium, a notoungulate. (f) Pyrotherium, a pyrothere. (g) Theosodon, a liptoptern. Skulls in (a), (b), and (g) from Carroll (1988). Skull and reconstruction in (c) from Gillette and Ray (1981). Skulls in (d) and (e) from Riggs (1935, 1937). Skull in (f) from Colbert et al. (2001). Reconstructions in (a), (b), (d), (e), (f), and (g) from Dixon et al. (1993). 95 3.2. Cladogram of proboscis-bearing mammals. * indicates taxa for which there is description of narial anatomy. Overall topology from Novacek (1993). Topology for Phocidae from Bininda-Emonds, Gittleman, & Purvis (1999). Topology for Ruminantia from Hassanin & Douzery (2003). 97 3.3. Skulls (left) and facial anatomy (right) of extant proboscis-bearing taxa. (a) Sus scrofa (from Dyce, Sack, & Wensing, 1987). (b) Tapirus terrestris (from Witmer et al., 1999). (c) Alces alces (from Clifford & Witmer, in review). (d) Cystophora cristata (original drawing by Ryan Ridgely, Ohio University). (e) Saiga tatarica and (f) Madoqua guentheri (from Frey & Hofmann, 1997). 99 11 3.4. Exaptation of maxillolabial musculature (mmax) in perissodactyls. Horses (a) and tapirs (b) have separated the origins of maxillolabial musculature, whereas these muscles primitively share a common origin. Modified from Boas & Paulli (1908a). 102 3.5. Nasal cartilages in a generalized phocid (a) and a hooded seal (b) showing elaboration of mobile lateral accessory cartilages. Modified from Brønsted (1932). 103 3.6. Nasal cavity of moose (a), tapir (b), elephant (c), and saiga (d) to illustrate rotation of the maxilloturbinate (mt) out of the main airflow through the nasal cavity resulting from vestibular enlargement.
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