Maria Grace Burton, Juan Benito, Kirsty Mellor, Emily Smith, Elizabeth Martin-Silverstone, Patrick O'Connor, Daniel J Field
{"title":"The influence of soft tissue volume on estimates of skeletal pneumaticity: implications for fossil archosaurs.","authors":"Maria Grace Burton, Juan Benito, Kirsty Mellor, Emily Smith, Elizabeth Martin-Silverstone, Patrick O'Connor, Daniel J Field","doi":"10.1098/rstb.2023.0428","DOIUrl":"10.1098/rstb.2023.0428","url":null,"abstract":"<p><p>Air space proportion (ASP), the volume fraction in bone that is occupied by air, is frequently applied as a measure for quantifying the extent of skeletal pneumaticity in extant and fossil archosaurs. Nonetheless, ASP estimates rely on a key assumption: that the soft tissue mass within pneumatic bones is negligible, an assumption that has rarely been explicitly acknowledged or tested. Here, we provide the first comparisons between estimated air space proportion (where the internal cavity of a pneumatic bone is assumed to be completely air-filled) and true air space proportion (ASPt, where soft tissues present within the internal cavities of fresh specimens are considered). Using birds as model archosaurs exhibiting postcranial skeletal pneumaticity, we find that estimates of ASPt are significantly lower than estimates of ASP, raising an important consideration that should be acknowledged in investigations of the evolution of skeletal pneumaticity and bulk skeletal density in extinct archosaurs, as well as in volume-based estimates of archosaur body mass. We advocate for the difference between ASP and ASPt to be explicitly acknowledged in studies seeking to quantify the extent of skeletal pneumaticity in extinct archosaurs, to avoid the risk of systematically overestimating the volume fraction of pneumatic bones composed of air.This article is part of the theme issue 'The biology of the avian respiratory system'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1920","pages":"20230428"},"PeriodicalIF":5.4,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11864828/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143516495","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Samuel Benjamin Gutherz, Kristin Stover, Nicholas Sze, Joseph R Groenke, Patrick M O'Connor
{"title":"Development of postcranial pneumaticity in the turkey (<i>Meleagris gallopavo</i>): insight from the forelimb skeleton.","authors":"Samuel Benjamin Gutherz, Kristin Stover, Nicholas Sze, Joseph R Groenke, Patrick M O'Connor","doi":"10.1098/rstb.2024.0357","DOIUrl":"https://doi.org/10.1098/rstb.2024.0357","url":null,"abstract":"<p><p>Postcranial skeletal pneumaticity is a phenomenon in birds in which epithelial extensions of the lung-air sac system aerate bones. Detailed development of this phenotype remains largely unknown. Here, we investigate changes in bone, soft tissue and air space volume in the developing humerus of turkeys using computed tomography and micro-computed tomography. Employing a two-phase approach, we first tracked humeral air space development <i>in vivo</i> in domesticated turkeys between week 10 (W10) and W18 post-hatch. In phase 2, we analysed air space and marrow volume change through the first 22 weeks of post-hatch development. Our results indicate that pneumatization of the humerus begins between W2 and W4 post-hatch, with air spaces expanding distally from the proximal humerus. Internal air space expands most rapidly between W7 and W9, with maximal volume reached at W15. Increased marrow growth occurs between W13 and W19, coincident with stabilization and a potential decline in relative air space volume. Our study highlights a dynamic relationship between bone, marrow and pneumatic epithelium, suggesting pneumaticity expression is likely impacted by both within-bone tissue growth dynamics and extrinsic factors related to forelimb function. This work provides the necessary gross anatomical framework for subsequent analyses of tissue-level and cellular mechanisms related to the pneumatization process.This article is part of the theme issue 'The biology of the avian respiratory system'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1920","pages":"20240357"},"PeriodicalIF":5.4,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143516385","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Aracely Martinez, Raul E Diaz, Clinton A Grand Pre, Brandon P Hedrick, Emma R Schachner
{"title":"The lungs of the finch: three-dimensional pulmonary anatomy of the zebra finch (<i>Taeniopygia castanotis</i>).","authors":"Aracely Martinez, Raul E Diaz, Clinton A Grand Pre, Brandon P Hedrick, Emma R Schachner","doi":"10.1098/rstb.2023.0420","DOIUrl":"https://doi.org/10.1098/rstb.2023.0420","url":null,"abstract":"<p><p>The avian respiratory system has been an area of biological interest for centuries, with zebra finches (<i>Taeniopygia castanotis</i>) emerging in recent decades as a primary avian model organism popularized across numerous disciplines. The pulmonary system of birds is unique in that air moves unidirectionally through the gas-exchanging lung, and previous works have suggested anatomical constraints within the bronchial network that may be coupled to the inspiratory valving mechanism in Aves. We used µCT-based segmented models to visualize and describe the morphology of the zebra finch lower respiratory system and to examine intra- and interspecific differences of the bronchial tree with the phylogenetically and ecologically different African grey parrot (<i>Psittacus erithacus</i>). Here, we show that zebra finches have highly variable lung and air sac morphology within individuals but generally do not diverge from the anatomical <i>bauplan</i> previously described for passerines. Additionally the parabronchi in the zebra finch lung are arranged into isolated segments between secondary bronchi, which has not been described and may be coupled with airflow patterns in this species. Both zebra finches and African grey parrots show constrained interostial distances and robust, caudally directed third ventrobronchi that may play an unexplored role in the unidirectional airflow patterns of birds.This article is part of the theme issue 'Biology of the avian respiratory system: development, evolutionary morphology, function and clinical considerations'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1920","pages":"20230420"},"PeriodicalIF":5.4,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143516499","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Insights into the early evolution of modern avian physiology from fossilized soft tissues from the Mesozoic.","authors":"Jingmai K O'Connor","doi":"10.1098/rstb.2023.0426","DOIUrl":"10.1098/rstb.2023.0426","url":null,"abstract":"<p><p>Modern birds (Neornithes) are the mostly highly modified group of amniotes, bearing little resemblance to other extant sauropsids. <i>Archaeopteryx</i>, with its nearly modern wings but plesiomorphic skeleton, demonstrated more than 160 years ago that soft tissue specializations preceded skeletal modifications for flight. Soft tissues are thus of great importance for understanding the early evolution of modern avian physiology. Most commonly, traces of the integumentary system are preserved; exceptional discoveries include remnants of organs. Together, these have helped to elucidate the evolution of the lungs, ovaries, plumage and beak in early diverging birds. These fossils reveal that many important adaptations for efficient digestion, high oxygen intake, reduced body mass and improved wing structure, all of which serve to improve aerial capabilities and/or meet the energetic demands of this costly form of locomotion, evolved within the first 20-30 Myr of avian evolution. Soft tissue preservation also provides important clues for understanding the ecology of early diverging birds and may even elucidate the extinction of certain groups. However, the current fossil record of Mesozoic avian soft tissues is almost entirely limited to the Early Cretaceous and thus, discoveries from the Late Cretaceous have the potential to drastically transform our interpretation of the available data.This article is part of the theme issue 'The biology of the avian respiratory system'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1920","pages":"20230426"},"PeriodicalIF":5.4,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11864835/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143516396","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Unidirectional airflow, air sacs or the horizontal septum: what does it take to make a bird lung?","authors":"Emma R Schachner, Andrew J Moore","doi":"10.1098/rstb.2023.0418","DOIUrl":"10.1098/rstb.2023.0418","url":null,"abstract":"<p><p>In this review, we evaluate the differences between the pulmonary anatomy of birds and other sauropsids, specifically those traits that make the avian respiratory system distinct: a fully decoupled and immobilized, isovolumetric gas-exchanging lung separated from compliant ventilatory air sacs by a horizontal septum. Imaging data, three-dimensional digital anatomical models and dissection images from a red-tailed hawk (<i>Buteo jamaicensis</i>), common ostrich (<i>Struthio camelus</i>), barred owl (<i>Strix varia</i>), African grey parrot (<i>Psittacus erithacus</i>) and zebra finch (<i>Taeniopygia castanotis</i>) are used to demonstrate the anatomical variation seen in the pulmonary air sacs, diverticula and the horizontal septum. We address the current state of knowledge regarding the avian respiratory system and the myriad areas that require further study, including the comparative and quantitative ecomorphology of the bronchial tree and air sacs, the non-ventilatory functions of the sacs and diverticula, the fluid dynamics and anatomical mechanisms underlying unidirectional airflow, post-cranial skeletal pneumaticity, and how all of these factors impact reconstructions of respiratory tissues in extinct archosaurs, particularly ornithodirans (i.e. pterosaurs + non-avian dinosaurs). Specifically, we argue that without evidence for the horizontal septum, a fully avian lung should not be reconstructed in non-avian ornithodirans, despite the presence of post-cranial skeletal pneumaticity.This article is part of the theme issue 'The biology of the avian respiratory system'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1920","pages":"20230418"},"PeriodicalIF":5.4,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11864838/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143516516","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The avian respiratory system: implications for anaesthesia.","authors":"John Ludders","doi":"10.1098/rstb.2023.0439","DOIUrl":"10.1098/rstb.2023.0439","url":null,"abstract":"<p><p>Anaesthesia is not a natural state for any animal, including birds. The unique anatomic and physiological attributes of the class Aves that have made it possible for birds to inhabit every continent on this planet and to live in a variety of environments, some considered challenging if not inhospitable to mammals, pose challenges to their anaesthetic management. Indeed, it is more challenging than the anaesthetic management of mammals, a reality substantiated by the fact that the risk of anaesthesia-related death of birds is up to 20 times higher than for dogs and cats. This article highlights those anatomic (respiratory system, renal-portal system), physiological (gas exchange, respiratory control mechanisms in respiratory brainstem and peripheral chemoreceptor areas, including intrapulmonary chemoreceptors) and pharmacological attributes (pharmacokinetics and pharmacodynamics) that make anaesthetic management, both inhalant and injectable anaesthesia, of birds challenging, and how those challenges are managed.This article is part of the theme issue 'The biology of the avian respiratory system'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1920","pages":"20230439"},"PeriodicalIF":5.4,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11864837/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143516492","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Iris Adam, Anja T Zai, Anna E Stepien, Homare Yamahachi, Christian M Schlepütz, Richard H R Hahnloser, Coen P H Elemans
{"title":"A synchrotron X-ray CT-based 3D atlas of the songbird syrinx with single muscle fibre resolution implies fine motor control of syringeal vocal folds.","authors":"Iris Adam, Anja T Zai, Anna E Stepien, Homare Yamahachi, Christian M Schlepütz, Richard H R Hahnloser, Coen P H Elemans","doi":"10.1098/rstb.2023.0430","DOIUrl":"10.1098/rstb.2023.0430","url":null,"abstract":"<p><p>Avian vocalizations are produced by precisely coordinated motion of the respiratory, syringeal and upper vocal tract systems. Syringeal muscles are controlled with unprecedented resolution, down to independent control of individual muscle fibres. However, we currently lack an anatomical description of syrinx muscles at single fibre resolution. Here, we combined a micron-resolution synchrotron X-ray CT scan of the zebra finch syrinx with micro-dissections of independent specimens to resolve syrinx muscle morphology at individual muscle fibre level. We define two new, previously unknown muscles and update the fibre trajectories and attachment sites of three previously described muscles. Our new insights into the fine anatomy of syrinx muscles show that not one, but both avian vocal folds can be directly controlled by contracting syrinx muscles. Thus, our data reveal novel anatomical complexity with consequences for the biomechanics and motor control of sound production.This article is part of the theme issue 'The biology of the avian respiratory system'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1920","pages":"20230430"},"PeriodicalIF":5.4,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11864832/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143516320","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sabine L Laguë, Catherine M Ivy, Julia M York, Neal J Dawson, Beverly A Chua, Luis Alza, Graham R Scott, Kevin G McCracken, William K Milsom
{"title":"Gas exchange, oxygen transport and metabolism in high-altitude waterfowl.","authors":"Sabine L Laguë, Catherine M Ivy, Julia M York, Neal J Dawson, Beverly A Chua, Luis Alza, Graham R Scott, Kevin G McCracken, William K Milsom","doi":"10.1098/rstb.2023.0424","DOIUrl":"10.1098/rstb.2023.0424","url":null,"abstract":"<p><p>High-altitude life poses physiological challenges to all animals due to decreased environmental oxygen (O<sub>2</sub>) availability (hypoxia) and cold. Supporting high metabolic rates and body temperatures with limited O<sub>2</sub> is challenging. Many birds, however, thrive at high altitudes. The O<sub>2</sub>-transport cascade describes the pathway involved in moving O<sub>2</sub> from the environment to the tissues encompassing: (i) ventilation, (ii) pulmonary O<sub>2</sub> diffusion, (iii) circulation, (iv) tissue O<sub>2</sub> diffusion, and (v) mitochondrial O<sub>2</sub> use for ATP production. Shared avian traits such as rigid lungs with cross-current gas exchange and unidirectional airflow aid in O<sub>2</sub> acquisition and transport in all birds. Many high-altitude birds, however, have evolved enhancements to some or all steps in the cascade. In this review, we summarize the current literature on gas exchange and O<sub>2</sub> transport in high-altitude birds, providing an overview of the O<sub>2</sub>-transport cascade that principally draws on the literature from high-altitude waterfowl, the most well-studied group of high-altitude birds. We close by discussing two important avenues for future research: distinguishing between the influences of plasticity and evolution and investigating whether the morphological and physiological differences discussed contribute to enhanced locomotor or thermogenic performance, a potential critical link to fitness.This article is part of the theme issue 'The biology of the avian respiratory system'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1920","pages":"20230424"},"PeriodicalIF":5.4,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11864830/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143516391","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"When the lung invades: a review of avian postcranial skeletal pneumaticity.","authors":"Andrew J Moore, Emma R Schachner","doi":"10.1098/rstb.2023.0427","DOIUrl":"https://doi.org/10.1098/rstb.2023.0427","url":null,"abstract":"<p><p>Birds are unique among extant tetrapods in exhibiting air-filled cavities that arise from the respiratory system and invade postcranial bones, a phenomenon called postcranial skeletal pneumaticity (PSP). These intraosseous cavities originate from diverticula of the ventilatory air sacs or directly from the gas-exchanging lung. Despite a long history of study, many of the basic characteristics of this system remain poorly understood. In this hybrid review, we synthesize insights from the anatomical, developmental, biomechanical and paleontological literature to review the functional and evolutionary significance of PSP. Leveraging new data, we confirm that the skeletons of pneumatic birds are not less heavy for their mass than those of apneumatic birds. Pneumatic skeletons may nonetheless be lightweight with respect to body volume, but this is a hypothesis that remains to be empirically tested. We also use micro-computed tomography scanning and deep learning-based segmentation to produce a pilot model of the pneumatized spaces in the neck of a Mallard (<i>Anas platyrhynchos</i>). This approach facilitates accurate modelling of bone architecture for quantitative comparative analysis within and between pneumatic taxa. Future work on PSP should focus on the cellular mechanisms and developmental processes that govern the onset and extent of pneumatization, which are essentially unknown.This article is part of the theme issue 'The biology of the avian respiratory system'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1920","pages":"rstb20230427"},"PeriodicalIF":5.4,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143516521","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Respiratory anatomy and physiology in diving penguins.","authors":"P J Ponganis, C L Williams, M Scadeng","doi":"10.1098/rstb.2023.0422","DOIUrl":"10.1098/rstb.2023.0422","url":null,"abstract":"<p><p>The anatomy and function of the respiratory systems of penguins are reviewed in relation to gas exchange and minimization of the risks of pulmonary barotrauma, decompression sickness and nitrogen narcosis during dives. Topics include available lung morphology and morphometry, respiratory air volumes determined with different techniques, review of possible physiological and biomechanical mechanisms of baroprotection, calculations of baroprotection limits and review of air sac and arterial partial pressure of oxygen (P<sub>O2</sub>) profiles in relation to movement of air during breathing and during dives. Limits for baroprotection to 200, 400 and 600 m in Adélie, king and emperor penguins, respectively, would require complete transfer of air sac air and reductions in the combined tracheobronchial tree-parabronchial volume of 24% in Adélie, 53% in king penguins and 76% in emperor penguins. Air sac and arterial P<sub>O2</sub> profiles at rest and during surface activity were consistent with unidirectional air flow through the lungs. During dives, P<sub>O2</sub> profiles were more complex, but were consistent with compression of air sac air into the parabronchi and air capillaries with or without additional air mixing induced by potential differential air sac pressures generated by wing movements.This article is part of the theme issue 'The biology of the avian respiratory system'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1920","pages":"20230422"},"PeriodicalIF":5.4,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11864836/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143516400","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}