Breathing and locomotion in birds. A thesis submitted to the University of Manchester for the degree of Doctor of Philosophy in the Faculty of Life Sciences. 2010 Peter George Tickle Contents Abstract 4 Declaration 5 Copyright Statement 6 Author Information 7 Acknowledgements 9 Organisation of this PhD thesis 10 Chapter 1 General Introduction 13 1. Introduction 14 1.1 The Avian Respiratory System 14 1.1.1 Structure of the lung and air sacs 16 1.1.2 Airflow in the avian respiratory system 21 1.1.3 The avian aspiration pump 25 1.2 The uncinate processes in birds 29 1.2.1 Uncinate process morphology and biomechanics 32 1.3 Constraints on breathing in birds 33 1.3.1 Development 33 1.3.2 Locomotion 35 1.3.2.1 The appendicular skeleton 35 1.3.2.2 Overcoming the trade-off between breathing 36 and locomotion 1.3.2.3 Energetics of locomotion in birds 38 1.4 Evolution of the ventilatory pump in birds 41 1.5 Overview and Thesis Aims 42 2 Chapter 2 Functional significance of the uncinate processes in birds. 44 Chapter 3 Ontogenetic development of the uncinate processes in the 45 domestic turkey (Meleagris gallopavo). Chapter 4 Uncinate process length in birds scales with resting metabolic rate. 46 Chapter 5 Load carrying during locomotion in the barnacle goose (Branta 47 leucopsis): The effect of load placement and size. Chapter 6 A continuum in ventilatory mechanics from early theropods to 48 extant birds. Chapter 7 General Discussion 49 References 64 3 Abstract of a thesis by Peter George Tickle submitted to the University of Manchester for the degree of PhD in the Faculty of Life Sciences and entitled ‘Breathing and Locomotion in Birds’. September 2010 Birds are a diverse group of vertebrates, with over 10,000 extant species. Diversification into volant, aquatic and terrestrial environmental niches has precipitated a remarkable morphological diversity between species. Birds have a unique respiratory system consisting of a rigid lung connected to an air sac system. Air is pumped into the respiratory system via movements of the ribcage and sternum. Previous research identified the uncinate processes, ossified projections extending from the vertebral ribs, as critical respiratory and locomotor structures. Uncinate processes facilitate inspiration and expiration through associated muscles that displace the ribs and therefore sternum. External intercostal muscles project from the processes and function during locomotion to stabilise body roll. Therefore uncinate processes provide a link between breathing and locomotion in birds. The objective of my PhD is to extend beyond this basic research on uncinate processes to investigate how diversity in avian body morphology relates to the fundamental functions of breathing and locomotion. While the function of uncinate processes in respiration has been identified, the mechanism whereby ventilatory movements are elicited is not known. Therefore I present a model that demonstrates how respiratory movements of the skeleton are facilitated by the lever action of uncinate processes. Furthermore, variation in process and sternal morphology is driven by adaptation to different forms of locomotion. Therefore fundamental differences in breathing mechanics may be associated with specialisation to locomotor behaviour. Detailed developmental studies of the uncinate processes in birds are almost nonexistent. I provide the first detailed description of developmental changes in the uncinate processes in the turkey. Ossification of the uncinate processes begins around the time of hatch. However, the base is cartilaginous upon hatching and so the lever action of the processes may be compromised in the chick. I provide further evidence for a functional link between process length and respiratory physiology, since elongated processes support an elevated resting metabolic rate in birds. This link was further explored in physiological experiments where the energetic cost of walking in the barnacle goose was manipulated by load carrying. Carrying extra mass on the sternum is more energetically costly than an equivalent back load indicating that the cost of breathing increased. A directly proportional relationship exists between increasing mass of back load and metabolic rate, while sternal loads were approximately twice as expensive to carry during locomotion. Leg loads incurred the greatest increase in metabolism. Finally, I demonstrate how uncinate processes functioned as respiratory structures in basal avian species and a theropod ancestor of modern birds. Development of the uncinate processes may have been an important step in the evolution of the avian lung - air sac system. The principal findings of the five first author research articles presented in this PhD thesis shed important new light on the ventilatory mechanics in birds and highlight interactions between breathing and locomotion. Diversity in avian body morphology driven by adaptation to various locomotor behaviours has resulted in modification of the respiratory system. 4 Declaration No portion of the work referred to in this thesis has been submitted in support of an application for another degree or qualification of this or any other university or other institute of learning. Signed: Date: 5 Copyright Statement 1) The author of this thesis (including any appendices and/or schedules to this thesis) owns certain copyright or related rights in it (the “Copyright”) and he has given The University of Manchester certain rights to use such Copyright, including for administrative purposes. 2) Copies of the thesis, either in full or in extracts and whether in hard or electronic copy, may be made only in accordance with the Copyright, Designs and Patents Act 1988 (as amended) and regulations issued under it or, where appropriate, in accordance with licensing agreements which the University has from time to time. This page must form part of any such copies made. 3) The ownership of certain Copyright, patents, designs, trade marks and other intellectual property (the “Intellectual Property”) and any reproductions of copyright works in this thesis, for example graphs and tables (“Reproductions”), which may be described in this thesis, may be owned by the author and may be owned by third parties. Such Intellectual Property and Reproductions cannot and must not be made available for use without prior written permission of the owner(s) of the relevant Intellectual Property and/or Reproductions. 4) Further information on the conditions under which disclosure, publication and commercialisation of this thesis, the Copyright and any intellectual Property and/or Reproductions described in it may take place is available in the University IP Policy (see http://www.campus.manchester.ac.uk/medialibrary/policies/intellectual- property.pdf), in any relevant Thesis restriction declarations deposited in the University Library, University Library’s regulations (see http://www.manchester.ac.uk/library/aboutus/regulations) and in The University’s policy on presentation of Theses. Signed: Date: 6 Author Information Name: Peter George Tickle Date of Birth: 13th September 1983 Nationality: British Address: 50 Norris Road, Sale, Cheshire, M33 3QR, UK Curriculum Vitae 1989-1996 Brooklands Primary School, Sale, Cheshire, UK 1996-2002 Sale Grammar School, Sale, Cheshire, UK 2002-2005 B.Sc. (Hons), School of Biological Sciences, University of Manchester, UK 2005-2006 Research technician, Faculty of Life Sciences, University of Manchester, UK 2006-2010 PhD, Faculty of Life Sciences, University of Manchester, Manchester, UK. Supervisor: Dr J. R. Codd. Publications (1) Tickle, P. G., Ennos, A. R., Lennox, L. E., Perry, S. F. and Codd, J. R. (2007) Functional significance of uncinate processes in birds. J. Exp. Biol. 210, 3955- 3961. (2) Tickle, P. G. and Codd, J. R. (2009) Ontogenetic development of the uncinate processes in the domestic turkey (Meleagris gallopavo). Poultry Sci. 88, 179-184. 7 (3) Tickle, P. G., Nudds, R. L. and Codd, J. R. (2009) Uncinate process length in birds scales with resting metabolic rate. PLoS ONE 4(5), e5667. (4) Nudds, R.L., Gardiner, J.D., Tickle, P.G. Codd, J.R. (2010) Energetics and kinematics of walking in the barnacle goose (Branta leucopsis). Comp. Biochem. Physiol. A . 156, 318-324. (5) Tickle, P. G., Richardson, M. F. and Codd, J.R. (2010) Load carrying during locomotion in the barnacle goose (Branta leucopsis): the effect of load placement and size. Comp. Biochem. Physiol. A 156, 309-317. (6) Codd, J. R., Heuer, C. and Tickle, P. G. (2010) Uncinate processes in birds and other tetrapods. ZFMK Bonner Zool. Beitr. In press. (7) Waring, K., Tickle, P.G., Stokkan, K. A.., Codd, J.R. and Sellers, W.I. The musculoskeletal anatomy of the reindeer (Rangifer tarandus): fore and hind limb. Polar Biol. In press. (8) Nudds, R., Folkow, L., Lees, J. Tickle, P. Stokkan, K-A and Codd. J. Cost of terrestrial transport in Svalbard rock ptarmigan (Lagopus muta hyperborea): first evidence for energy savings from aerial running in a bird. Proc. R. Soc. B. In review. (9) Tickle, P. G., Norell, M. A., Nudds, R. L. and Codd, J. R. A continuum in breathing mechanics from early theropods to living birds. Proc. R. Soc. Lond. B. In review. (10) Tickle P.G., Lean, S., Rose, K. and Codd, J.R. How increasing speed and load carriage affects the energetics and kinematics of locomotion in the tufted duck (Aythya fuligula). In preparation. (11) Tickle, P.G., Nudds, R.L. & Codd, J.R. Scaling of uncinate process length, flight muscle mass and breathing frequency in birds. In preparation. Conference Presentations (1) Tickle, P. G. and Codd, J. R. (2007) Accessory breathing structures in birds with different locomotor modes. Society for Experimental Biology, Glasgow, UK, 31st March – 4th April, 2007. (2) Tickle, P. G., Manning, P. L. and Codd, J. R. (2008) Uncinate processes in extant birds and extinct dinosaurs. Invited Presentation: Progressive Palaeontology, Manchester, UK, 29th May, 2008. (3) Tickle, P. G. (2009) The energetics of load bearing in the barnacle goose (Branta leucopsis). Invited Presentation: International Congress of Respiratory Science, Bonn, Germany, 9th-13th August 2009.