Uncinate Process Length in Birds Scales with Resting Metabolic Rate Peter Tickle, Robert Nudds, Jonathan Codd* Faculty of Life Sciences, University of Manchester, Manchester, United Kingdom Abstract A fundamental function of the respiratory system is the supply of oxygen to meet metabolic demand. Morphological constraints on the supply of oxygen, such as the structure of the lung, have previously been studied in birds. Recent research has shown that uncinate processes (UP) are important respiratory structures in birds, facilitating inspiratory and expiratory movements of the ribs and sternum. Uncinate process length (UPL) is important for determining the mechanical advantage for these respiratory movements. Here we report on the relationship between UPL, body size, metabolic demand and locomotor specialisation in birds. UPL was found to scale isometrically with body mass. Process length is greatest in specialist diving birds, shortest in walking birds and intermediate length in all others relative to body size. Examination of the interaction between the length of the UP and metabolic demand indicated that, relative to body size, species with high metabolic rates have corresponding elongated UP. We propose that elongated UP confer an advantage on the supply of oxygen, perhaps by improving the mechanical advantage and reducing the energetic cost of movements of the ribs and sternum. Citation: Tickle P, Nudds R, Codd J (2009) Uncinate Process Length in Birds Scales with Resting Metabolic Rate. PLoS ONE 4(5): e5667. doi:10.1371/ journal.pone.0005667 Editor: Alejandro Lucia, Universidad Europea de Madrid, Spain Received February 23, 2009; Accepted April 20, 2009; Published May 27, 2009 Copyright: 2009 Tickle et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This research was funded by the BBSRC (G011338/1) and The Leverhulme Trust (F/00 120/BH). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: jonathan.codd@manchester.ac.uk Introduction The avian respiratory system consists of a relatively rigid lung coupled with a series (in most birds) of nine compliant air-sacs [1]. The anatomical arrangement of these air-sacs facilitates the bellows-like movement of inspired air unidirectionally across the parenchymal tissue [2,3]. Like all tetrapods birds face a possible mechanical constraint during simultaneous locomotion and ventilation [4,5]. However, almost all extant birds and some non-avian maniraptoran dinosaurs exhibit osteological characters known as uncinate processes (UP). These bony projections on the vertebral ribs (oriented in the caudo-dorsal direction) play a key role in enabling simultaneous ventilation and locomotion. The function of the UP was thought to be linked with stiffening the rib cage [6,7] or as a site for attachment of flight muscles [8]. However, their role as accessory breathing structures, first suggested by Zimmer [9], was confirmed in recent research [10]. The Mm. appendicocostales projects from the proximal edge of the uncinate process, and inserts onto the following vertebral rib [11]. Activity of the Mm. appendicocostales is associated with craniad movement of the ribs and a ventral displacement of the sternum during inspiration [10]. UP also provide a site for the attachment of projections from the M. externus obliquus abdominus, which pull the sternum dorsally during expiration [10]. Geometric modelling of the avian rib cage indicated that UP act as levers that improve the mechanical advantage for forward rotation of the dorsal ribs and therefore ventral movement of the sternum during inspiration [12]. Morphological variations in UP have been demonstrated to correspond to adaptations to different forms of locomotion [12]. Birds adapted to diving have the longest processes, flying and swimming birds have UP of intermediate length whilst the shortest UP occur in walking species [12]. Given the important respiratory function of the UP, variation in morphology suggests that differences in ventilatory mechanics may be driven by adaptation to locomotion. The presence of these processes in some non-avian maniraptoran dinosaurs has also been linked to avian-like breathing mechanics in these theropod ancestors of modern birds [13]. Respiration powers locomotion by providing metabolic energy. Resting metabolic rate (RMR) is often used to investigate the relationship between metabolism and body weight [14]. Lasiewski and Dawson [15] provided a review and re-analysis of published values of bird RMR. Using data from a range of species, RMR was reported to scale to the two-thirds power of body mass (RMR/Mb2/3), i.e. in proportion to body surface area [15,16]. However, by re-analysing the scaling relationship in separate passerine and non-passerine groups, Lasiewski and Dawson [15] calculated that RMR scales as Mb0.72. The projected 0.72 scaling coefficient found by Lasiewski and Dawson [15] is very similar to the O [17] or L [16,18] scaling component often used to describe the relationship between basal metabolic rate and body size for mammals. A common relationship between metabolism and body weight may therefore exist amongst endothermic vertebrates. Avian RMR has been reported to vary according to phylogeny, circadian rhythms and ecological variables [15,19–23]. Further- more, passerines have an elevated metabolic rate when compared to non-passerine species [15], while RMR is greater for birds during their period of normal activity [19,20]. However, some controversy exists on the scaling relationship between passerine and non-passerine birds with studies either reporting [24] or not PLoS ONE | www.plosone.org 1 May 2009 | Volume 4 | Issue 5 | e5667