دورية أكاديمية
The respiratory system influences flight mechanics in soaring birds.
العنوان: | The respiratory system influences flight mechanics in soaring birds. |
---|---|
المؤلفون: | Schachner ER; Department of Physiological Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL, USA. eschachner@ufl.edu., Moore AJ; Department of Anatomical Sciences, Renaissance School of Medicine, Stony Brook University, Stony Brook, NY, USA., Martinez A; Department of Cell Biology and Anatomy, School of Medicine, Louisiana State University Health Sciences Center, New Orleans, LA, USA., Diaz RE Jr; Department of Biological Sciences, California State University Los Angeles, Los Angeles, CA, USA., Echols MS; The Medical Center for Birds, Oakley, CA, USA., Atterholt J; Department of Medical Anatomical Sciences, College of Osteopathic Medicine of the Pacific, Western University of Health Sciences, Pomona, CA, USA., W P Kissane R; Department of Musculoskeletal and Ageing Science, Institute of Life Course and Medical Sciences, University of Liverpool, Liverpool, UK., Hedrick BP; Department of Biomedical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, USA., Bates KT; Department of Musculoskeletal and Ageing Science, Institute of Life Course and Medical Sciences, University of Liverpool, Liverpool, UK. |
المصدر: | Nature [Nature] 2024 Jun; Vol. 630 (8017), pp. 671-676. Date of Electronic Publication: 2024 Jun 12. |
نوع المنشور: | Journal Article |
اللغة: | English |
بيانات الدورية: | Publisher: Nature Publishing Group Country of Publication: England NLM ID: 0410462 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1476-4687 (Electronic) Linking ISSN: 00280836 NLM ISO Abbreviation: Nature Subsets: MEDLINE |
أسماء مطبوعة: | Publication: Basingstoke : Nature Publishing Group Original Publication: London, Macmillan Journals ltd. |
مواضيع طبية MeSH: | Flight, Animal*/physiology , Hawks*/anatomy & histology , Hawks*/classification , Hawks*/physiology , Respiration* , Respiratory System*/anatomy & histology , Wings, Animal*/physiology , Wings, Animal*/anatomy & histology, Animals ; Biological Evolution ; Biomechanical Phenomena/physiology ; Lung/anatomy & histology ; Lung/physiology ; Models, Biological ; Muscle, Skeletal/anatomy & histology ; Muscle, Skeletal/physiology ; Male ; Female |
مستخلص: | The subpectoral diverticulum (SPD) is an extension of the respiratory system in birds that is located between the primary muscles responsible for flapping the wing 1,2 . Here we survey the pulmonary apparatus in 68 avian species, and show that the SPD was present in virtually all of the soaring taxa investigated but absent in non-soarers. We find that this structure evolved independently with soaring flight at least seven times, which indicates that the diverticulum might have a functional and adaptive relationship with this flight style. Using the soaring hawks Buteo jamaicensis and Buteo swainsoni as models, we show that the SPD is not integral for ventilation, that an inflated SPD can increase the moment arm of cranial parts of the pectoralis, and that pectoralis muscle fascicles are significantly shorter in soaring hawks than in non-soaring birds. This coupling of an SPD-mediated increase in pectoralis leverage with force-specialized muscle architecture produces a pneumatic system that is adapted for the isometric contractile conditions expected in soaring flight. The discovery of a mechanical role for the respiratory system in avian locomotion underscores the functional complexity and heterogeneity of this organ system, and suggests that pulmonary diverticula are likely to have other undiscovered secondary functions. These data provide a mechanistic explanation for the repeated appearance of the SPD in soaring lineages and show that the respiratory system can be co-opted to provide biomechanical solutions to the challenges of flight and thereby influence the evolution of avian volancy. (© 2024. The Author(s), under exclusive licence to Springer Nature Limited.) |
References: | Duncker, H. R. The lung air sac system of birds. A contribution to the functional anatomy of the respiratory apparatus. Ergeb. Anat. Entwicklungsgesch. 45, 1–171 (1971). King, A. S. in International Review of General and Experimental Zoology Vol. 2 (eds Felts, J. L. & Harrison, R. J.) 96 (Academic, 1966). Maina, J. N. What it takes to fly: the structural and functional respiratory refinements in birds and bats. J. Exp. Biol. 203, 3045–3064 (2000). (PMID: 1100381710.1242/jeb.203.20.3045) Lockner, F. R. & Murrish, D. E. Interclavicular air sac pressures and vocalization in mallard ducks Anas platyrhynchos. Compar. Biochem. Physiol. A 52, 183–187 (1975). (PMID: 10.1016/S0300-9629(75)80150-2) Plummer, E. M. & Goller, F. Singing with reduced air sac volume causes uniform decrease in airflow and sound amplitude in the zebra finch. J. Exp. Biol. 211, 66–78 (2008). (PMID: 1808373410.1242/jeb.011908) Akester, A. R., Pomeroy, D. E. & Purton, M. D. Subcutaneous air pourches in the Marabou stork (Leptoptilos crumeniferus). J. Zool. 170, 493–499 (1973). (PMID: 10.1111/j.1469-7998.1973.tb05063.x) Rusli, M. A brief report on the development of dorsal air sacs in hand reared Von der Decken’s hornbills (Tockus deckeni). Avian Biol. Res. 13, 87–91 (2020). (PMID: 10.1177/1758155920951685) Daoust, P.-Y., Dobbin, G. V., Ridlington Abbot, R. C. F. & Dawson, S. D. Descriptive anatomy of the subcutaneous air diverticula in the northern gannet Morus bassanus. Seabird 21, 64–76 (2008). (PMID: 10.61350/sbj.21.64) Richardson, F. Functional aspects of the pneumatic system of the California brown pelican. Condor 41, 13–17 (1939). (PMID: 10.2307/1364267) Groebbels, F. Der Vogel Vol. I (Borntraeger, 1932). Strasser, H. Ueber die Luftsäcke der Vögel. Gegenbaurs Morphol. Jahrbuch 3, 179–225 (1877). Biewener, A. A. Muscle function in avian flight: achieving power and control. Philos. Trans. R. Soc. B 366, 1496–1506 (2011). (PMID: 10.1098/rstb.2010.0353) Hamlet, M. P. & Fisher, H. I. Air sacs of respiratory origin in some procellariiform birds. Condor 69, 586–595 (1967). (PMID: 10.2307/1366430) Ulrich, F. in Wissenschaftliche Ergebnisse der deutschenTiefsee-Expedition auf dem Dampfer “Valdivia” 1898–1899 Vol. 7, 319–342 (1904). Brackenbury, J. H. Airflow dynamics in the avian lung as determined by direct and indirect methods. Respir. Physiol. 13, 319–329 (1971). (PMID: 515885010.1016/0034-5687(71)90036-3) Bretz, W. L. & Schmidt-Nielsen, K. Bird respiration: flow patterns in the duck lung. J. Exp. Biol. 54, 103–118 (1971). (PMID: 554975610.1242/jeb.54.1.103) Bruderer, B., Peter, D., Boldt, A. & Liechti, F. Wing-beat characteristics of birds recorded with tracking radar and cine camera. Ibis 152, 272–291 (2010). (PMID: 10.1111/j.1474-919X.2010.01014.x) Lovette, I. J. & Fitzpatrick, J. W. (eds) The Cornell Lab of Ornithology Handbook of Bird Biology (Wiley, 2016). Pennycuick, C. J. Modelling the Flying Bird (Elsevier, 2008). Huelsenbeck, J. P., Nielsen, R. & Bollback, J. P. Stochastic mapping of morphological characters. Syst. Biol. 52, 131–158 (2003). (PMID: 1274614410.1080/10635150390192780) Revell, L. J. Two new graphical methods for mapping trait evolution on phylogenies. Methods Ecol. Evol. 4, 754–759 (2013). (PMID: 10.1111/2041-210X.12066) Garde, B. et al. Thermal soaring in tropicbirds suggests that diverse seabirds may use this strategy to reduce flight costs. Mar. Ecol. Progr. Ser. 723, 171–183 (2023). (PMID: 10.3354/meps14410) Hedrick, T. L., Pichot, C. & de Margerie, E. Gliding for a free lunch: biomechanics of foraging flight in common swifts (Apus apus). J. Exp. Biol. 221, jeb186270 (2018). (PMID: 3045538210.1242/jeb.186270) Sapir, N., Wikelski, M., McCue, M. D., Pinshow, B. & Nathan, R. Flight modes in migrating european bee-eaters: heart rate may indicate low metabolic rate during soaring and gliding. PLoS One 5, e13956 (2010). (PMID: 21085655297871010.1371/journal.pone.0013956) Pagel, M. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of descrete characters. Proc. R. Soc. B 255, 37–45 (1994). (PMID: 10.1098/rspb.1994.0006) Felsenstein, J. A comparative method for both discrete and continuous characters using the threshold model. Am. Nat. 179, 145–156 (2012). (PMID: 2221830510.1086/663681) Charles, J., Kissane, R., Hoerhurtner, T. & Bates, K. T. From fibre to function: are we accurately representing muscle architecture and performance? Biol. Rev. 97, 1640–1676 (2022). (PMID: 3538861310.1111/brv.12856) Tobalske, B. W. Biomechanics of bird flight. J. Exp. Biol. 210, 3135–3146 (2007). (PMID: 1776629010.1242/jeb.000273) Owen, R. in The Cyclopædia of Anatomy and Physiology Vol. 1 (ed. Todd, R. B.) 265–358 (Sherwood, Gilbert and Piper, 1836). Azizi, E., Brainerd, E. L. & Roberts, T. J. Variable gearing in pennate muscles. Proc. Natl Acad. Sci. USA 105, 1745–1750 (2008). (PMID: 18230734223421510.1073/pnas.0709212105) Smith, N. P., Barclay, C. J. & Loiselle, D. S. The efficiency of muscle contraction. Prog. Biophys. Mol. Biol. 88, 1–58 (2005). (PMID: 1556130010.1016/j.pbiomolbio.2003.11.014) Casler, C. L. The air-sac systems and buoyancy of the anhinga and double-crested cormorant. Auk 90, 324–340 (1973). Boggs, D. F. Interactions between locomotion and ventilation in tetrapods. Compar. Biochem. Physiol. A 133, 269–288 (2002). (PMID: 10.1016/S1095-6433(02)00160-5) Boggs, D. F., Jenkins, F. A. Jr & Dial, K. P. The effects of the wingbeat cycle on respiration in black-billed magpies (Pica pica). J. Exp. Biol. 200, 1403–1412 (1997). (PMID: 931929710.1242/jeb.200.9.1403) Lawson, A. B., Hedrick, B. P., Echols, S. & Schachner, E. R. Anatomy, variation, and asymmetry of the bronchial tree in the African grey parrot (Psittacus erithacus). J. Anat. 282, 701–719 (2021). Schachner, E. R. et al. Perspectives on lung visualization: three-dimensional anatomical modeling of computed and micro-computed tomographic data in comparative evolutionary morphology and medicine with applications for COVID-19. Anat. Rec. https://doi.org/10.1002/ar.25300 (2023). (PMID: 10.1002/ar.25300) Lowi-Merri, T. M., Benson, R. B. J., Claramunt, S. & Evans, D. C. The relationship between sternum variation and mode of locomotion in birds. BMC Biol. 19, 165 (2021). (PMID: 34412636837787010.1186/s12915-021-01105-1) Lowi-Merri, T. M. et al. Reconstructing locomotor ecology of extinct avialans: a case study of Ichthyornis comparing sternum morphology and skeletal proportions. Proc. R. Soc. B 290, 20222020 (2023). (PMID: 36883281999306110.1098/rspb.2022.2020) Prum, R. O. et al. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526, 569–573 (2015). (PMID: 2644423710.1038/nature15697) Cooney, C. R. et al. Mega-evolutionary dynamics of the adaptive radiation of birds. Nature 542, 344–347 (2017). (PMID: 28146475532158110.1038/nature21074) Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–491 (2012). (PMID: 2312385710.1038/nature11631) Pennell, M. W. et al. geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees. Bioinformatics 30, 2216–2218 (2014). (PMID: 2472885510.1093/bioinformatics/btu181) Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 2, 217–223 (2012). (PMID: 10.1111/j.2041-210X.2011.00169.x) Maddison, W. P. & FitzJohn, R. G. The unsolved challenge to phylogenetic correlation tests for categorical characters. Syst. Biol. 64, 127–136 (2015). (PMID: 2520922210.1093/sysbio/syu070) Uyeda, J. C., Zenil-Ferguson, R. & Pennell, M. W. Rethinking phylogenetic comparative methods. Syst. Biol. 67, 1091–1109 (2018). (PMID: 2970183810.1093/sysbio/syy031) Revell, L. J. Ancestral character estimation under the threshold model from quantitative genetics. Evolution 68, 743–759 (2014). (PMID: 2415223910.1111/evo.12300) Kissane, R. W. P., Egginton, S. & Askew, G. N. Regional variation in the mechanical properties and fibre-type composition of the rat extensor digitorum longus muscle. Exp. Physiol. 103, 111–124 (2018). (PMID: 2907619210.1113/EP086483) Boggs, D. F. & Dial, K. P. Neuromuscular organization and regional EMG activity of the pectoralis in the pigeon. J. Morphol. 218, 43–57 (1993). (PMID: 2986548510.1002/jmor.1052180104) Bates, K. T. & Schachner, E. R. Disparity and convergence in bipedal archosaur locomotion. J. R. Soc. Interface 70, 1339–1353 (2012). (PMID: 10.1098/rsif.2011.0687) Dempsey, M., Maidment, S. C. R., Hedrick, B. P. & Bates, K. T. Convergent evolution of quadrupedalism in ornithischian dinosaurs was achieved through disparate forelimb muscle mechanics. Proc. R. Soc. B 290, 20222435 (2023). (PMID: 36722082989009210.1098/rspb.2022.2435) Macaulay, S. et al. Decoupling body shape and mass-distribution in birds and their dinosaurian ancestors. Nat. Commun. 14, 1575 (2023). (PMID: 369490941003351310.1038/s41467-023-37317-y) |
تواريخ الأحداث: | Date Created: 20240612 Date Completed: 20240619 Latest Revision: 20240708 |
رمز التحديث: | 20240709 |
DOI: | 10.1038/s41586-024-07485-y |
PMID: | 38867039 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1476-4687 |
---|---|
DOI: | 10.1038/s41586-024-07485-y |