POSTCRANIAL SKELETAL PNEUMATICITY, BONE STUCTURE, AND FORAGING STYLE IN TWO CLADES OF NEOGNATH BIRDS _______________________________ A thesis Presented to The Honors Tutorial College Ohio University _______________________________ In Partial Fulfillment of the Requirements for Graduation from the Honors Tutorial College with the degree of Bachelors of Science in Biological Sciences _______________________________ by Sarah C. Gutzwiller June 2010 This thesis has been approved by The Honors Tutorial College and the Department of Biological Sciences ______________________________ Dr. Patrick O’Connor Associate Professor, Biomedical Sciences Thesis Advisor ______________________________ Dr. Soichi Tanda Honors Tutorial College, Director of Studies Biological Sciences ______________________________ Jeremy Webster Dean, Honors Tutorial College Acknowledgements I would like to thank the Ohio University Honors Tutorial College for providing countless opportunities and gracious support throughout my undergraduate career. A special thanks to my Director of Studies, Dr. Tanda, and my Thesis Advisor, Dr. O’Connor, for their direction and guidance. Thank you to the Carnegie Museum of Natural History, the Ohio University Vertebrate Collections, the Ohio University microCT, and the Ohio University Office of the Vice Provost for Research for providing specimens, equipment, and funding. I also wish to thank Ryan Ridgely, Anne Su, and other colleagues and friends for helping me throughout my project. TABLE OF CONTENTS List of Figures ii List of Tables iii List of Abbreviations iii Abstract 1 Introduction 2 Rationale of the Current Study 11 Goals of the Current Study 23 Materials and Methods 24 Hypotheses and Predictions 29 Results 30 Discussion 44 Conclusions 50 Literature Cited 52 Appendices 57 Gutzwiller Senior Thesis—i LIST OF FIGURES Fig. 1 Phylogenetic hypothesis of extant birds 3 Fig. 2 Pulmonary latex injection detailing the avian air sac system. 6 Fig. 3 Pulmonary injection of the Blackheaded gull (Larus 7 ridibundus). Fig. 4 Pneumatic bones from Marabou stork (CM 118743). A, 8 cervical vertebra; B, humerus; PF, pneumatic foramen. Fig. 5 Example of anatomical distribution of pneumaticity in extant 10 birds. Fig. 6 The Common Murre (Uria aalge). 16 Fig. 7 The Western Gull (Larus occidentalis). 17 Fig. 8 The Great Skua (Catharacta skua). 18 Fig. 9 The Double-crested Cormorant (Phalacrocorax auritus). 21 Fig. 10 The Anhinga (Anhinga anhinga). 22 Fig. 11 The Brown Pelican (Pelecanus occidentalis). 23 Fig. 12 MicroCT scanner housed at Ohio University. 26 Fig. 13 Cross-sectional μCT slice of a middle cervical vertebra from 27 a Great Skua (Catharacta skua). Fig. 14 Average Pneumaticity Index (PI) values for two dedicated 31 diving specialists (murre and puffin) and two non-diving specialists (gull and skua). Fig. 15 The log transformed average species body mass regressed 33 upon the arcsine transformed average Pneumaticity Index for each charadriiform species. Fig. 16 Phylogenetic hypothesis of Charadriiformes with relative 35 pneumaticity Fig. 17 Box and whisker plots of cervical trabecular bone volume 37 fractions for each charadriiform species. Fig. 18 Box and whisker plots of thoracic trabecular bone volume 38 fractions for each charadriiform species. Fig. 19 Box and whisker plots of cortical bone thickness for each 39 charadriiform species. Fig. 20 Average Pneumaticity Index (PI) values for two dedicated 40 diving specialists (anhinga and cormorant) and non-diving specialist (pelican). Fig. 21 Box and whisker plots of cervical trabecular bone volume 41 fractions for each pelecaniform species. Fig. 22 Box and whisker plots of thoracic trabecular bone volume 42 fractions for each pelecaniform species. Fig. 23 Box and whisker plots of cortical bone thickness for each 43 pelecaniform species. Gutzwiller Senior Thesis—ii LIST OF TABLES Table 1 Focal species 24 LIST OF ABBREVIATIONS ABD abdominal air sac AU anatomical unit AXD axillary diverticulum BV/TV trabecular bone volume fraction CA caudal vertebrae CAC caudal cervical vertebrae CAT caudal thoracic vertebrae CAUDTH caudal thoracic air sac Cb.T cortical bone thickness CERV cervical air sac CL clavicular air sac CoV coefficient of variance CRC cranial cervical vertebrae CRT cranial thoracic vertebrae CRTH cranial thoracic air sac IMDIV intermuscular diverticula MC middle cervical vertebrae PF pneumatic foramen PI pneumaticity index SS synsacral vertebrae TR trachea μCT micro-computed tomography VOI volume of interest Gutzwiller Senior Thesis—iii ABSTRACT Extant birds represent the only living sauropsid group in which pulmonary air sacs aerate the postcranial skeleton. The degree of variability in birds is notable, ranging from taxa that are completely apneumatic to those characterized by air within most of the postcranial skeleton. Although numerous factors (e.g., body size) have been linked with ‘relative’ pneumaticity, comparative studies examining this system remain limited. This project sought to (1) examine whole-body patterns of pneumaticity in select charadriiform and pelecaniform birds, (2) evaluate relationships among relative pneumaticity, body size and locomotor specializations (e.g. diving, soaring) and (3) examine if/how bone structure is altered in pneumatic versus apneuamtic vertebrae. Species-specific pneumaticity profiles were used to examine relative pneumaticity. Results suggest that the largest flying birds exhibit a higher degree of pneumaticity relative to smaller birds (e.g. larids). In contrast, skeletal pneumaticity has been independently lost in multiple lineages of diving specialists. Such reductions in skeletal pneumaticity likely result in decreased buoyancy in birds specialized for dive foraging. Conversely, aerating the postcranial skeleton offers a mechanism that allows volumetric increases in bone without concomitant increases in body mass. Thus, the potential to differentially pneumatize the postcranial skeleton may have played a role in relaxing constraints on body size evolution and/or habitat exploitation during the course of avian evolution. Patterns of pneumaticity and bone structure within charadriiforms and pelecaniforms are also discussed. Gutzwiller Senior Thesis—1 INTRODUCTION Living birds include a vast diversity of approximately 10,000 species that occupy 22 orders (Fig. 1; Perrins, 2009). They have exploited an array of niches from the terrestrial seed-eating finches of the Galapagos to the aquatic fish-eating penguins of the Antarctic. They utilize a variety of social systems, breeding behaviors, and locomotor styles (Perrins, 2009; Simons, 2010). Paralleling this diversity in lifestyle, birds are diverse in morphology. They can range greatly in size and body mass (Dunning, 1993). For example, the Vervain Hummingbird (Mellisuga minima) weighs an average of 2.4 grams, whereas the ostrich (Struthio camelus) averages 83,500 grams. Whether in size or in shape, the morphology often reflects the function (Perrins, 2009). For example, the shape of a bird’s beak may reflect its diet. A Hawfinch has a stout, thick beak optimal for cracking open hard-shelled seeds, while a Sword-billed hummingbird has a long, thin beak ideal for collecting nectar from passionflowers. Thus a distinct relationship exists between form (morphology) and function (lifestyle). Gutzwiller Senior Thesis—2 Figure 1. Phylogenetic hypothesis of extant birds. Taken from O’Connor (2009) Form and Function When studying the relationship between form and function, birds make an excellent study group. Such diversity in lifestyle and morphology allows researchers to examine form-function relationships and to be able to apply these insights to the study of the ecology, conservation, and evolution of birds. Researchers can use the understanding of form-function relationships in three important ways: (1) they can apply the knowledge of the anatomy and physiology of one species to another species that is less understood; (2) they may be able to examine the morphology of an extinct species and hypothesize the function and Gutzwiller Senior Thesis—3 lifestyle of that animal; (3) they can examine mechanisms of evolution that have resulted in the vast diversity of living animals around us today. Foraging Specializations and Evolutionary Adaptation An aspect of lifestyle that varies among neognath birds is foraging mode or style. Foraging style is a significant aspect of an organism’s ecology. Not only does it determine how and what an organism consumes, it represents a trade-off in organismal energetics (Maurer, 1996). For optimal pay-off, the energy gained through foraging must be greater than the energy used to forage. Due to the impact of this energetic balance on the survival and fitness of the organism, foraging style is highly susceptible to natural selection. Adaptive foraging styles can reflect the environmental pressures and evolutionary constraints that are acting upon the organism. Understanding foraging style can reveal what factors have led to the diversification of birds. Some birds are specialized dive foragers, whereas others are nondiving forms, specialized in other means of foraging, such as in-flight capture and/or shoreline feeding. Specialization in a certain foraging strategy can be reflected in the morphology of the bird. For example, foot-propelled diving specialists have elongated and more posteriorly-positioned hind limbs (Raikow, 1970; Johnsgard, 1987; McCracken, et al. 1999). This adaptation aids in the pursuit of prey under water. Likewise, birds specialized