{"title":"Respiratory contributions to birdsong-evolutionary considerations and open questions.","authors":"Franz Goller","doi":"10.1098/rstb.2023.0431","DOIUrl":"10.1098/rstb.2023.0431","url":null,"abstract":"<p><p>Respiration plays a central role in avian vocal behaviour by providing the airstream that induces vibration of vocal folds. In this role, respiratory movements dictate the coarse temporal pattern of song, while simultaneously fulfilling its vital functions. Whereas these aspects have been investigated in oscines, little information exists in other taxa. Broad taxonomic information is, however, necessary for addressing questions regarding evolutionary specializations of the respiratory system. Acoustic recordings of unstudied taxa suggest that rapid action by respiratory muscles is a basal trait within birds. In addition to controlling the timing of vocalization, respiratory activity also influences acoustic features such as sound amplitude and frequency. The latter is more strongly influenced by respiratory driving pressure in non-vocal learners. Singing, as a highly dynamic respiratory activity presents an opportunity for studying detailed ventilation patterns and thus could give insight into the basic control of airflow in the avian lung-air sac system. Although we have learned many details of how respiratory control is tied into cortical song control, many open questions remain. Control of respiratory pacemaker circuitry by upstream vocal control centres, respiratory input in initiation of vocalization and the use of online feedback from the respiratory system are all incompletely understood.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":"20230431"},"PeriodicalIF":5.4,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11864833/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143516427","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}
Srinivasa Reddy Kunchala, Albert van Dijk, Edwin J A Veldhuizen, Henk P Haagsman, Sandra Orgeig
{"title":"Adaptation and conservation of CL-10/11 in avian lungs: implications for their role in pulmonary innate immune protection.","authors":"Srinivasa Reddy Kunchala, Albert van Dijk, Edwin J A Veldhuizen, Henk P Haagsman, Sandra Orgeig","doi":"10.1098/rstb.2023.0425","DOIUrl":"https://doi.org/10.1098/rstb.2023.0425","url":null,"abstract":"<p><p>The common avian origin of many zoonotic infections and epidemics warrants investigation into the mechanism of respiratory surface protection in reservoir species such as birds. Our recent molecular investigations on the evolution and pulmonary expression of an ancient family of proteins, the C-type lectins, have revealed unique molecular adaptations in the surfactant proteins avian SP-A1 (aSP-A1), aSP-A2 and aSP-C coupled with the loss of surfactant protein-D (SP-D) in the avian lineage. As surfactant proteins are members of the collectin family, a subgroup of the C-type lectins, an <i>in silico</i> search for related non-surfactant collectin proteins (Collectin-10 (CL-10) and Collectin-11 (CL-11)) in the NCBI genome database was conducted to understand their evolution in the avian lineage. In addition, both CL-10 and CL-11 gene expression in the lungs and other organs of zebra finches and turkeys was confirmed by PCR. These PCR-confirmed zebra finch and turkey CL-10 and CL-11 sequences were compared with sequenced and <i>in silico</i>-predicted vertebrate homologues to develop a phylogenetic tree. Compared with avian surfactant proteins, CL-10 and CL-11 are highly conserved among vertebrates, suggesting a critical role in development and innate immune protection. The conservation of CL-11 EPN and collagen domain motifs may compensate to some extent for the loss of SP-D in the avian lineage.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":"20230425"},"PeriodicalIF":5.4,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143516323","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":"Biology of the avian respiratory system: development, evolutionary morphology, function and clinical considerations.","authors":"John N Maina, Emma R Schachner","doi":"10.1098/rstb.2023.0419","DOIUrl":"10.1098/rstb.2023.0419","url":null,"abstract":"<p><p>The respiratory biology of birds has been of interest to researchers for centuries, particularly owing to its dramatically heterogeneous structure, unusual ability for non-ventilatory structures to invade nearly all parts of the body (including the skeleton) in many taxa, and its exceptional efficiency under high-altitude hypoxia. Advances in imaging, experimental and developmental techniques, as well as recent palaeontological specimens have facilitated new discoveries, analyses and progress in the field. Comprehensively, this theme issue shows the origin of the modern avian respiratory system, current controversies and how the evolution of respiratory structures in birds has impacted their biology from the molecular, to the cellular, to the phylogenetic level. This collection of articles addresses progress the field has made, gaps in our knowledge and where the field needs to go, with a primary focus on adult and embryonic form and function but also touching on vocalization and clinical aspects of avian respiratory biology.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":"20230419"},"PeriodicalIF":5.4,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11864829/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143516383","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":"Structure and function of the avian respiratory system.","authors":"J N Maina","doi":"10.1098/rstb.2023.0435","DOIUrl":"10.1098/rstb.2023.0435","url":null,"abstract":"<p><p>Among the extant air-breathing vertebrates, the avian respiratory system is the most efficient gas exchanger. Novel morphological and physiological adaptations and specializations largely explain its exceptional functional superiority. Anatomically, the avian respiratory system is separated into lungs that serve as gas exchangers and air sacs that operate as ventilators. Utterly rigid, the avian lungs are deeply fixed to the ribs and the vertebrae. A thin blood-gas barrier (BGB), vast respiratory surface area and large pulmonary capillary blood volume generate high total pulmonary morphometric diffusing capacity of O<sub>2</sub>. The weak allometric scaling of the thickness of the BGB indicates optimization for gas exchange; the negative scaling and strong correlation between the surface density of the respiratory surface area and body mass show the extreme subdivision of the gas exchange tissue; and the respiratory surface area, the pulmonary capillary blood volume and the total pulmonary morphometric diffusing capacity of O<sub>2</sub> correlate strongly and positively with body mass. The arrangement of the structural components of the exchange tissue form crosscurrent-, countercurrent-like- and multicapillary serial arterialization gas exchange designs. By synchronized actions of the air sacs, the palaeopulmonic part of the of the avian lung is efficiently ventilated continuously and unidirectionally in a caudocranial direction.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":"20230435"},"PeriodicalIF":5.4,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11864839/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143516435","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}
Warren Burggren, Edward Dzialowski, Barbara Tzschentke
{"title":"The avian embryo as a time-honoured animal model in developmental, biomedical and agricultural research.","authors":"Warren Burggren, Edward Dzialowski, Barbara Tzschentke","doi":"10.1098/rstb.2023.0438","DOIUrl":"10.1098/rstb.2023.0438","url":null,"abstract":"<p><p>Avian embryos have been at the core of embryological, morphological, physiological and biochemical/molecular research, especially involving research in three primary areas: developmental, biomedical and agricultural research. As developmental models, the avian embryo-especially that of the chicken-has been the single most used embryo model, perhaps in part from the combination of large size, ease of access and prior knowledge base. Developmental research with avian embryos has included organ system studies of the heart, vasculature, lungs, kidneys, nervous system, etc., as well as integrated physiological processes including gas-exchange, acid-base and ion/water regulation. In terms of translational research, avian embryos have modelled vascular development, based on the easily accessible chorioallantoic membrane under the eggshell. This same respiratory organ has enabled toxicological studies of how pollutants affect vertebrate development. Investigation of the transition to pulmonary breathing and the associated emergence of respiratory control has also relied heavily upon the avian embryo. In addition to developmental and biomedical investigations, the avian embryo has been studied intensively due to the huge importance of domesticated birds as a food source. Consequently, the effects of environment (including temperature, humidity, noise levels and photoperiod) during incubation on subsequent post-hatch phenotype are being actively investigated.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":"20230438"},"PeriodicalIF":5.4,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11864840/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143516491","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}
Wilfried Klein, Vinícius Pereira Ribeiro, Ray Brasil Bueno de Souza
{"title":"Avian air sacs and neopulmo: their evolution, form and function.","authors":"Wilfried Klein, Vinícius Pereira Ribeiro, Ray Brasil Bueno de Souza","doi":"10.1098/rstb.2023.0421","DOIUrl":"10.1098/rstb.2023.0421","url":null,"abstract":"<p><p>The avian respiratory system is composed of an exchange structure (parabronchi) and a pump (air sacs) to perform gas exchange. While there are many studies dealing with the morphology and function of the palaeopulmonic parabronchi, the air sacs and the neopulmo have been somewhat neglected from a comparative and functional point of view, not always receiving a closer examination that they deserve. While a decent amount of data are available regarding air sac and neopulmo morphology on a family level or for domestic species, several orders of birds have yet to be investigated. Owing to the lack of detailed specific data, we did not perform a comparative phylogenetic analysis but compiled data regarding air sac and neopulmo morphology and analysed them from the viewpoint of current phylogenetic relations while also discussing aspects of these structures regarding avian physiology.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":"20230421"},"PeriodicalIF":5.4,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11864834/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143516326","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}
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}
{"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}
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}