Basic Avian Pulmonary Design and Flow-Through

SUPPLEMENTARY INFORMATION

Basic Avian Pulmonary Design and Flow-Through

Ventilation in Nonavian Theropod Dinosaurs

O’Connor and Claessens, 2005

I. Included specimens and rationale for sample choice.Data for region-specific pneumaticity in birds were obtained from 234 air-sac injected and 204 skeletal preparations, including representatives of 18 avian Orders (see Supplementary Table 1). Specimens were chosen not only to provide wide taxonomic coverage, but to examine pneumaticity in species that span a large body size range and represent the diverse ecomorphs (e.g., soaring, diving, obligate terrestriality, etc.) present in Avialae.

Nonavian theropods examined include representatives of all major neotheropod clades (e.g., coelophysoid [Dilophosaurus wetherilli UCMP 77270/37302], spinosauroid [Baryonyx walkeri BMNH R.9951],allosauroid [Allosaurus fragilis CM 11844/USNM 8367, Neovenator salerii BMNH R.10001], tyrannosauroid [Tyrannosaurus rex FMNH PR 2081], maniraptoriform[Ornithomimidae indet NMNM 4736]); however, a recently recovered, exquisitely-preserved specimen of the abelisauroid theropod Majungatholus atopus (Figs. 3, 4; UA 8678), consisting of a complete precaudal vertebral column, is one of the best-preserved basal neotheropods yet recovered, and forms a case-study for many of the inferences discussed herein.

Museum locations and abbreviations used throughout text and Supplementary Information: The Natural History Museum, London (BMNH); Carnegie Museum of Natural History, Pittsburgh (CM); Field Museum of Natural History, Chicago (FMNH PR); Museum für Naturkunde der Humboldt-Universität, Berlin (MB); Musee National du Niger, Niamey (MNN); National Museum of Natural History, Washington D.C. (NMNH);Stony Brook University, New York (SBU);Université d’Antananarivo, Madagascar (UA); University of CaliforniaMuseum of Paleontology, Berkeley (UCMP).

II. Methodology used to characterize pulmonary anatomy and ventilatory kinematics in extant birds.

Pulmonary injection protocol – Extant birds used in this study were either prepared in the Department of Anatomical Sciences (StonyBrookUniv.) or the Department of Biomedical Sciences (OhioUniv.), or were studied in the Duncker Collection (Univ. Giessen, Germany). Salvage specimens were prepared by infilling the pulmonary apparatus with either latex or polyester resin (Batson’s No. 17 Anatomical Corrosion Kit) via a negative-pressure injection chamber4.After soft-tissue maceration, this technique provides a detailed cast of the pulmonary system (e.g., Fig. 1b) and allows a direct association between region-specific skeletal pneumaticity and different components of the pulmonary air sac system.

Cineradiographic analysis of skeletal kinematics during lung ventilation – Movements of the trunk skeleton in birds (Dromaius novaehollandiae, Numida meleagris, and Nothoprocta perdicaria) were filmed using high-speed cineradiography (x-ray filming). Cineradiography was undertaken with a Siemens system employing 16 mm Kodak Eastman Plus-X reversal film and Mini Digital Video. Still images were recorded on Kodak Industrex M-2 film. Kinematic data were recorded at 220 mA, 38 kV, 100 frames per second (fps) using a Photosonics series 2000 high speed cine camera. Digital video was recorded with a Sony DCR VX 1000 camera at 60 fps and 1/250 shutter speed at 220 mA and 50-90 kV. Skeletal movements were recorded in lateral and dorsoventral projection, and were analyzed using Adobe Premiere, Photoshop, NIH Image, and Macromedia Flash. All animal experiments were conducted in accordance with State and Institutional guidelines.In vivo movements were correlated with joint anatomy and structure in extinct archosaurs.

III. Supplementary Table 1. Pneumaticity profiles for taxa examined in study.

SUPPLEMENTARY TABLE 1. Postcranial Axial Pneumaticity Profiles for Nonavian and Avian Theropods
NONAVIAN THEROPOD TAXA
Taxon / CRC / MC / CAC / CRT / CAT / SS / CA / VR / SR / ST
COELOPHYSOIDEA
Dilophosaurus wetherillia / + / + / + / + / ? / ? / 0 / 0 / --- / ---
Liliensternus liliensternib / + / + / + / + / ? / ? / 0 / --- / --- / ---
NEOTHEROPODA
Ceratosaurus nasicornisc / + / + / + / + / + / ?/+ / 0 / --- / --- / ---
Spinostropheus gautierid / + / + / + / + / ?/+ / --- / --- / --- / --- / ---
ABELISAUROIDEA
Majungatholus atopuse / + / + / + / + / + / + / 0 / 0 / --- / ---
Masiakasaurus knopflerif / + / + / + / + / + / + / 0 / --- / --- / ---
SPINOSAUROIDEA
Baryonyx walkerig / + / + / + / + / + / + / + / 0 / --- / ---
ALLOSAUROIDEA
Allosaurus fragilish / + / + / + / + / + / + / 0 / ? / --- / ---
Neovenator saleriii / + / + / + / + / + / + / 0 / 0 / --- / ---
TYRANNOSAUROIDEA
Tyrannosaurus rexj / + / + / + / + / + / + / 0 / 0 / --- / ---
ORNITHOMIMOSAURIA
Ornithomimidae indet.k / --- / --- / --- / --- / --- / + / ? / --- / --- / ---
aUCMP 77270, bMB R.2175, cNMNH 4735, dMNN TIG6, eUA 8678, fFMNH PR 2142, gBMNH R.9951,
hCM 11844/NMNH 8367, iBMNH R.10001, jFMNH PR 2081, kNMNH 4736
AVIAN TAXA
Taxon / CRC / MC / CAC / CRT / CAT / SS / CA / VR / SR / ST
STRUTHIONIFORMES
Struthio camelus / + / + / + / + / + / + / + / + / + / +
RHEIFORMES
Rhea americana / + / + / + / + / + / + / + / + / + / +
CASUARIIFORMES
Casuarius casuarius / + / + / + / + / + / + / + / + / + / +
Dromaius novaehollandiae / + / + / + / + / + / + / + / + / + / +
GALLIFORMES
Chrysolophus pictus / + / + / + / + / + / + / 0 / + / + / +
Gallus gallus / + / + / + / + / + / + / 0 / + / + / +
Meleagris gallopavo / + / + / + / + / + / + / 0 / + / 0 / +
Perdix perdix / 0 / 0 / 0 / + / + / 0 / 0 / 0 / + / +
ANSERIFORMES
Chauna chavaria / + / + / + / + / + / + / + / + / + / +
Anser anser / + / + / + / + / + / + / 0 / + / + / +
Anser albifrons / + / + / + / + / + / + / 0 / 0 / + / +
Cygnus atratus / + / + / + / + / + / + / 0 / 0 / + / +
Cygnus columbianus / + / + / + / + / + / + / 0 / 0 / + / +
Cygnus olor / + / + / + / + / + / + / 0 / 0 / + / +
Tadorna tadorna / + / + / + / + / + / + / 0 / 0 / + / +
Aix galericulata / 0 / + / + / + / + / + / 0 / 0 / + / +
Aix sponsa / + / + / + / + / + / 0 / 0 / 0 / + / +
Cairina moschata / + / + / + / + / + / + / 0 / 0 / + / +
Anas platyrhynchos / + / + / + / + / + / + / 0 / 0 / 0 / +
Anas crecca / + / + / + / + / + / + / 0 / 0 / 0 / +
SUPPLEMENTARY TABLE 1. Continued
Taxon / CRC / MC / CAC / CRT / CAT / SS / CA / VR / SR / ST
ANSERIFORMES continued
Aythya ferina / 0 / 0 / + / + / 0 / 0 / 0 / 0 / 0 / 0
Aythya fuligula / 0 / 0 / + / + / 0 / 0 / 0 / 0 / 0 / 0
Mergellus albellus / 0 / 0 / 0 / + / 0 / 0 / 0 / 0 / 0 / 0
Mergus merganser / 0 / + / + / + / + / 0 / 0 / 0 / 0 / +
GAVIIFORMES
Gavia arctica / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0
PODICIPEDIFORMES
Podiceps cristatus / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0
Podiceps ruficollis / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0
PROCELLARIIFORMES
Fulmaris glacialis / 0 / 0 / + / 0 / 0 / 0 / 0 / 0 / 0 / 0
Puffinus puffinus / 0 / 0 / + / 0 / 0 / 0 / 0 / 0 / 0 / 0
PELECANIFORMES
Pelecanus erythrorhynchus / + / + / + / + / + / + / + / + / + / +
Phalacrocorax aristotelis / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0
Sula bassana / + / + / + / + / + / + / + / 0 / + / +
Sula dactylatra / + / + / + / + / + / + / + / 0 / + / +
SPHENISCIFORMES
Spheniscus demeris / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0
Aptenodytes patagonicus / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0
Eudyptes cristatus / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0
CICONIIFORMES
Ciconia ciconia / + / + / + / + / + / + / + / + / + / +
Nycticorax nycticorax / + / + / + / + / + / + / 0 / + / + / +
Ardea cinerea / + / + / + / + / + / + / 0 / + / ? / +
Phoenicoparrus ruber / 0 / 0 / + / + / + / + / 0 / + / + / +
FALCONIFORMES
Accipiter nissus / + / + / + / + / + / + / 0 / + / + / +
Buteo buteo / + / + / + / + / + / + / 0 / + / + / +
Buteo jamaicensis / + / + / + / + / + / + / 0 / + / + / +
Circus aeruginosus / + / + / + / + / + / + / 0 / + / + / +
Circus cyaneus / + / + / + / + / + / + / 0 / + / + / +
Falco tinnunculus / + / + / + / + / + / + / 0 / + / + / +
STRIGIFORMES
Athene noctua / ? / + / + / + / + / 0 / 0 / 0 / 0 / 0
Asio otus / + / + / + / + / + / + / 0 / + / + / +
Bubo virginianus / + / + / + / + / + / + / 0 / + / + / +
Strix aluco / + / + / + / + / + / + / 0 / + / + / +
GRUIFORMES
Balearica pavonina / + / + / + / + / + / + / + / + / + / +
Anthropoides virgo / 0 / + / + / + / + / + / 0 / + / + / +
Fulica atra / 0 / + / + / + / + / 0 / 0 / ? / ? / 0
Rallus aquaticus / 0 / 0 / + / 0 / 0 / 0 / 0 / 0 / 0 / 0
Porphyrula alleni / + / + / + / + / + / + / 0 / + / 0 / 0
Gallinula chloropus / 0 / 0 / 0 / 0 / + / + / 0 / 0 / 0 / 0
SUPPLEMENTARY TABLE 1. Continued
Taxon / CRC / MC / CAC / CRT / CAT / SS / CA / VR / SR / ST
PSITTACIFORMES
Psittacus erithacus / + / + / + / + / + / + / 0 / + / + / +
Nymphicus hallandicus / + / + / + / + / + / + / 0 / + / + / +
Psephotus haematonotus / ?/+ / + / + / + / + / + / 0 / + / + / +
CHARADRIIFOMRES
Alca torda / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0
Fratercula arctica / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0
Uria aalge / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0 / 0
Larus argentatus / + / + / + / + / + / + / 0 / 0 / 0 / 0
Larus marinus / + / + / + / + / + / 0 / 0 / 0 / 0 / 0
Larus canus / + / + / + / + / + / 0 / 0 / 0 / 0 / 0
Larus ridibundus / + / + / + / + / 0 / 0 / 0 / 0 / 0 / 0
Sterna hirundo / + / + / + / 0 / 0 / 0 / 0 / 0 / 0 / 0
COLUMBIFORMES
Streptopelis decaocta / + / + / + / + / + / + / 0 / + / + / +
Columba livia / + / + / + / + / + / + / 0 / + / + / +
PICIFORMES
Ramphastos swainsonii / + / + / + / + / + / + / 0 / + / + / +
Dendrocpus major / ? / + / + / + / + / + / 0 / + / + / +
PASSERIFORMES
Corvus monedula / + / + / + / + / + / + / 0 / + / + / +
Corvus corone / + / + / + / + / + / + / 0 / + / + / +
Pica pica / + / + / + / + / + / + / 0 / + / + / +
Nucifraga caryocatactes / + / + / + / + / + / + / 0 / + / + / +
Garrulus glandarius / + / + / + / + / + / + / 0 / + / + / +
Boxed area indicates those regions of the vertebral column pneumatized by abdominal air sac diverticula in extant birds
+, indicates pneumatic bone; 0, indicates apneumatic bone; ?, indicates ambiguous pneumatic state; ---, indicates element not available for analysis
CA, caudal vertebrae; CAC, caudal cervical vertebrae; CAT, caudal thoracic vertebrae; CRC, cranial cervical vertebrae; CRT, cranial thoracic vertebrae; MC, middle cervical vertebrae; SR, sternal ribs; SS, synsacral vertebrae; ST, sternum; VR, vertebral ribs

IV. Supplementary Table 2. Kinematic data table for sternal movement in ventilating birds.

Bird
(weight) / Ventral Excursion of Sternum (mm) / Increase in ventral displacement of the caudal sternal margin (%) / Sample Size (n)
Cranial Margin / Caudal Margin
Mean / Range / SD / Mean / Range / SD
Guinea Fowl 1 (2.10 kg) / 0.68 / 0.50 – 0.82 / 0.11 / 2.32 / 1.70 – 2.88 / 0.40 / 243 / 11
Guinea Fowl 2 (2.80 kg) / 0.79 / 0.68 – 0.90 / 0.08 / 2.68 / 2.29 – 3.05 / 0.30 / 242 / 6
Tinamu 1 (0.48 kg) / 0.97 / 0.85 – 1.19 / 0.11 / 2.38 / 2.12 – 2.50 / 0.16 / 147 / 11
Tinamu 2 (0.49 kg) / 0.93 / 0.78 – 1.15 / 0.11 / 2.75 / 2.30 – 3.37 / 0.31 / 196 / 11
Emu 1 (2.36 kg) / 8.31 / 5.0 - 11.1 / 1.90 / 9.12 / 5.4 – 12.2 / 2.03 / 10 / 11

Sternal displacement during ventilation in guinea fowl (Numida meleagris), tinamu (Nothoprocta perdicaria), and emu (Dromaius novaehollandiae), showing the greater ventral excursion of the caudal margin of the sternum. The more modest increase in displacement of the caudal margin of the emu sternum in part reflects the short length of the sternum in this group.

V. Supplementary Video 1.Cineradiographic (X-ray film) clip of a 0.48 kg Tinamou (Nothoprocta perdicaria), demonstrating the greater excursion of the caudal margin of the sternum and posterior ventral body wall upon inspiration. Experimental subject in lateral projection at 70 kV and 220mA, X-ray positive (head is to the left side of image). (see appended Quicktime file).

O’Connor and Claessens Supplementary Information—1