Abstract
The subpectoral diverticulum (SPD) is an extension of the respiratory system in birds that is located between the primary muscles responsible for flapping the wing1,2. 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.
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Data availability
All high-resolution images of the axial and transverse µCT slices, code from the character correlation analysis and MDA models have been uploaded to Data Dryad and are available here: https://doi.org/10.5061/dryad.0k6djhb64.
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Acknowledgements
We thank the Tracy Aviary for allowing us to use retrospective imaging data of birds that had been scanned for clinical purposes unrelated to this study; J. Stevens for her time aggregating and processing the DICOM data for this project; R. Wilhite and P. Laporte for assisting with specimens; J. Ziermann and W. Klein for assistance with German translations; T. Skorka for assistance with imaging; and E. Stanley for intubating and inflating one of the hawks. Funding for this study was provided by the Louisiana State University Health Sciences Center Research Enhancement Program Fund to E.R.S. and B.P.H. and the University of Florida Gatorade Award Allocation to E.R.S.
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E.R.S. conceptualized the study. E.R.S., A.J.M. and K.T.B. designed the study. E.R.S. did the anatomical dissections. E.R.S., R.E.D., M.S.E., B.P.H. and J.A. acquired the CT and µCT data. E.R.S., A.J.M. and A.M. segmented the 3D anatomical models. E.R.S and A.J.M analysed and scored the CT and µCT data for phylogenetic analysis. A.J.M. completed the character correlation analysis. K.T.B. completed the biomechanical models, with anatomical input from E.R.S. R.K performed the muscle fascicle analysis. E.R.S., A.J.M., K.T.B., R.K. and B.P.H. wrote the original draft. All authors critically reviewed and contributed to the final draft of the manuscript. All authors approved the final version of the manuscript.
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Extended data figures and tables
Extended Data Fig. 1 Details of intubation and anatomy of the subpectoral diverticula in the red-tailed hawk (Buteo jamaicensis).
a, Adult male specimen (Ptolemy) in ventral view. b, View of the tracheotomy with a medium sized polyethylene tube sutured into the cut trachea with silk Ethicon suture, and pectoralis muscle (p) exposed by dissection. c, Magnified view of b with the pectoralis reflected cranially on the left side; arrow indicates the inflated SPD. d, Right inflated SPD (indicated by the arrow) is exposed as the pectoralis is reflected cranially with forceps. Scale bars, 1 cm.
Extended Data Fig. 2 Segmented surface models of the SPD in cranial and right lateral views.
a–u, The right (turquoise) and left (blue) subpectoral diverticulum, pectoral girdle and humeri of the red-tailed hawk (B. jamaicensis) (a–e,h–l,o–s) and Swainson’s hawk (B. swainsoni) (f,g,m,n,t,u) in ventral (a–g), left lateral (h–n) and cranial (o-u) views in various states of inflation. a,h,o, Ptolemy: male, deceased, and artificially inflated via a tracheotomy. b,i,p, Lysimachus: male, deceased, and deflated (imaged at natural end tidal volume). c,j,q, Seleucus: male, deceased, and artificially inflated via a tracheotomy. d,k,r, Seleucus: male, deceased, imaged deflated. e,l,s, Roxana: female, live, sedated, natural apnoea. f,m,t, Polyperchon: male, deceased, and artificially inflated a tracheotomy. g,n,u, Eurydice: female, live, sedated, natural apnoea with vascular contrast selectively removed from the model.
Extended Data Fig. 3 Methods for selecting homologous axial (transverse) slices across Aves.
a–c, Volume rendered models of a red-tailed hawk (B. jamaicensis; Ptolemy) in ventral view with a pink line showing where the axial/transverse slice is taken on the surface of the bird (a), a keel-billed toucan (Ramphostos sulfuratus) in dorsal view demonstrating the location of the sagittal slice (b) and a Brandt’s cormorant (Phalacrocorax penicillatus) showing the location of the coronal slice aligned to the thoracic vertebrae (c). d–f, In all birds, the axial–transverse images are selected using the multiplanar reconstruction (MPR) viewer in the DICOM viewers OsiriX MD or Horos. The windows are aligned so that the axial slice lines up with where the coracoid processes articulate with the sternal plate, and the coronal and sagittal slices are aligned with the thoracic vertebrae. The axial/transverse slice (e) is then enlarged and exported as a TIFF for analysis. Abbreviations: ax, axial/transverse; cor, coronal; sag, sagittal.
Extended Data Fig. 4 Axial µCT images of the SPD in B. jamaicensis and B. swainsoni, showing variation and capacity for differential and asymmetric inflation and collapse of the structure.
Each axial slice was selected in the multiplanar reconstruction (MPR) viewer in Horos or OsiriX MD with the window aligned perpendicular to the thoracic (dorsal) vertebrae and sternal keel, and the axial slice was selected at the location where the coracoids articulate with the sternal plate. a, Ptolemy (B. jamaicensis): adult male, deceased, artificially inflated to maximum inspiratory capacity. b, Lysimachus (B. jamaicensis): adult male, deceased, natural end tidal volume. c, Alexander (B. jamaicensis): sub-adult female, deceased, artificially inflated to near-maximum inspiratory capacity. d, Seleucus (B. jamaicensis): adult male, deceased, artificially inflated to near/at maximum inspiratory capacity. e, Roxana (B. jamaicensis): adult female, live and sedated, natural apnoea. f, Olympias (B. jamaicensis): adult female, live and sedated, natural apnoea; note the total collapse of her SPD. g, Polyperchon (B. swainsoni): adult male, deceased, artificially inflated to near/at maximum inspiratory capacity, wings extended. h, Eurydice (B. swainsoni): adult female, live and sedated, natural apnoea.
Extended Data Fig. 5 Axial CT and µCT images of the SPD across Aves (part 1).
Each axial slice was selected using the MPR as in Extended Data Fig. 3. Purple text and arrows indicate presence of the SPD. a, Southern cassowary (Casuarius casuarius). b, Emu (Dromaius novaehollandiae). c, Common ostrich (Struthio camelus). d, Elegant crested tinamou (Eudromia elegans). e, Falcated duck (Anas falcata). f, Northern pintail (Anas acuta). g, Redhead (Aythya americana). h, Spectacled eider (Somateria fischeri). i, Steller’s eider (Polysticta stelleri). j, Canada goose (Branta canadensis). k, Trumpeter swan (Cygnus buccinator). l, Tundra swan (Cygnus columbianus). m, Helmeted curassow (Pauxi pauxi). n, Chicken (Gallus gallus). o, Crested partridge (Rollulus roulroul). p, Anna’s hummingbird (Calypte anna). q, Tawny frogmouth (Podargus strigoides). r, Violet turaco (Musophaga violacea). s, Nicobar pigeon (Caloenas nicobarica). t, Black crowned crane (Balearica pavonina). u, Western grebe (Aechmophorus occidentalis). v, Chilean flamingo (Phoenicopterus chilensis). w, Black-necked stilt (Himantopus mexicanus). x, Common murre (Uria aalge). y, Western gull (Larus occidentalis). z, Pacific loon (Gavia pacifica). aa, Common loon (Gavia immer). bb, Yellow-billed loon (Gavia adamsii). cc, Sooty shearwater (Puffinus griseus). dd, Brandt’s cormorant (Phalacrocorax penicillatus). ee, Scarlet ibis (Eudocimus ruber).
Extended Data Fig. 6 Axial CT and µCT images of the SPD across Aves (part 2).
Each axial slice was selected using the MPR as in Extended Data Fig. 3. Purple text and arrows indicate presence of the SPD. a, White pelican (Pelecanus erythrorhynchos). b, Brown pelican (Pelecanus occidentalis). c, Black crowned night heron (Nycticorax nycticorax). d, Turkey vulture (Cathartes aura). e, Andean condor (Vultur gryphus). f, Common buzzard (Buteo buteo). g, Bald eagle (Haliaeetus leucocephalus). h, Golden eagle (Aquila chrysaetos). i, Bateleur (Terathopius ecaudatus). j, Spectacled owl (Pulsatrix perspicillata). k, Great horned owl (Bubo virginianus). l, Southern ground hornbill (Bucorvus leadbeateri). m, Green woodhoopoe (Phoeniculus purpureus). n, Curl-crested aracari (Pteroglossus beauharnaesii). o, Keel-billed toucan (Ramphastos sulfuratus). p, Gyr/saker falcon hybrid (Falco rusticolus/cherrug). q, Peregrine falcon (Falco peregrinus). r, Sulphur-crested cockatoo (Cacatua galerita). s, Blue-and-yellow macaw (Ara ararauna). t, African grey parrot (Psittacus erithacus). u, Moluccan eclectus parrot (Eclectus roratus). v, Australian zebra finch (Taeniopygia castanotis). w, Common raven (Corvus corax). x, Blue-faced honeyeater (Entomyzon cyanotis).
Extended Data Fig. 7 Ancestral-state reconstruction and statistical tests of a correlation between soaring flight and the SPD.
a, The inferred evolutionary histories of soaring flight (left) and the SPD (right), with pie charts illustrating the posterior probability (PP) of a character-state transition for branches with probabilities >0.1. b, AIC values associated with Pagel’s18 test of discrete character correlation under four competing models. The best-fit model is one in which the evolution of the SPD depends on the presence of soaring flight and character transition rates are asymmetrical (ARD_dep); in order of decreasing fit, the remaining models include: dependent character evolution with symmetrical transition rates (SYM_dep); independent character evolution with symmetrical transition rates (SYM_dep); and independent character evolution with asymmetrical transition rates (ARD_indep). c, Posterior distribution of the value of the correlation coefficient (r) for Felsenstein’s19 implementation of the threshold model. The 95% highest posterior density (marked by red dashed lines) is well-removed from zero.
Extended Data Fig. 8 Additional data on the architecture of the pectoralis muscle in the red-tailed hawk and in non-soaring birds.
a, Three specimens of soaring birds (B. jamaicensis) do not differ significantly from each other in their mean pectoralis fascicle lengths (n = 80 fascicles per muscle), but each have significantly shorter fascicle lengths than all four non-soaring species measured here. b, Functional morphospace (normalized mean fascicle length versus normalized PCSA) plots of the pectoralis muscle in soaring and non-soaring birds illustrating their similar PCSAs, but shorter fascicle lengths in soaring birds. This suggests a more force-based architectural specialization in soaring muscles versus a more power/displacement specialization in non-soaring species. c,d, The strong cranial-to-caudal variation in fascicle length noted at the whole-muscle level (see Fig. 3c in main text), with significant increases in fascicle length in caudal regions, is present in both the superficial (c) and the deep (d) (whiskers denote min and maximum data range, n = 40 per bird, n = 10 per region) layers of the pectoralis (although note that the overall fascicle lengths are consistently longer in superficial than in deep parts of the muscle). Open circles indicate non-soaring birds, whereas filled circles indicate the red-tailed hawks in c,d. Two-way factorial ANOVA test statistics are presented in c,d, with statistical significance described as *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001.
Extended Data Fig. 9 Muscle moment arm data from the nine modelled strands from the deep part of the pectoralis muscle in five hawks.
a–i, Comparisons of real muscle paths (orange bars) that are guided across the interface between the deepest part of the pectoralis, the SPD and hypothetical straight-line paths (blue bars) that deliberately ignore the contribution of the SPD to pectoralis geometry. Eurydice (a), Lysimachus with the shoulder joint axis defined as described in the main text (b), Lysimachus with alternative shoulder joint axis of rotation (c), Polyperchon with the shoulder joint axis defined as described in the main text (d), Polyperchon with alternative shoulder joint axis of rotation (e), Ptolemy with the shoulder joint axis defined as described in the main text (f), Ptolemy with alternative shoulder joint axis of rotation (g), Roxana based on the right side (h) and Roxana based on the left side (i). Comparison of moment arms in Lysimachus (b,c), Polyperchon (d,e) and Ptolemy (f,g) calculated about different joint axis angles illustrates that the qualitative comparisons and conclusions presented here are not sensitive to the precise angle of shoulder rotation prescribed in the models. j, Comparison of pectoralis moment arms in Seleucus in the nine deep muscle strands wrapping across the surface of the SPD when the SPD is inflated versus deflated.
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Schachner, E.R., Moore, A.J., Martinez, A. et al. The respiratory system influences flight mechanics in soaring birds. Nature 630, 671–676 (2024). https://doi.org/10.1038/s41586-024-07485-y
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DOI: https://doi.org/10.1038/s41586-024-07485-y
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