86:
474:, the indentations are very small. One study in 2007 concluded that prosauropods likely had abdominal and cervical air sacs, based on the evidence for them in sister taxa (theropods and sauropods). The study concluded that it was impossible to determine whether prosauropods had a bird-like flow-through lung, but that the air sacs were almost certainly present. A further indication for the presence of air sacs and their use in lung ventilation comes from a reconstruction of the air exchange volume (the volume of air exchanged with each breath) of
234:, the primary vocalization organ of songbirds. The portion of the neural pathways which control respiration during vocalization changes air sac pressure to control vocal intensity. The pressure in the interclavicular air sac is highly correlated with the fundamental frequency of birdsong in doves. Birdsong primarily occurs in expiration and therefore syllables and fundamental frequency are highly correlated with increased interclavicular air sac pressure. Changes in air sac pressure also affect the length of the
154:. The hollow air spaces in bird bones outside of the head are connected to the air sacs in a way that a bird with a blocked windpipe and a bone broken in a manner where the inside of the bone was connected to the outside world could still breathe. These pneumatic bones are less vascularized than non-pneumatic bones and many pneumatic bones have pneumatic foramina (openings for air passage). Skeletal pneumaticity often originates developmentally as offshoots of the air sacs, especially in the
246:(the sister group to true songbirds), birds have two different sources of sound around the trachea. At high air sac pressures, the two sound sources have different frequencies, while at low pressure they have the same frequency. The generation of bird trills involves modulation of the pressure in air sacs. Since so many aspects of birdsong depend on air sac pressure, there is a trade off between trill rate and the duration of each call, though this has not been studied in depth.
193:
130:. The air sacs themselves are either poorly vascularized or entirely avascular. No gas exchange occurs within them. There are five main air sacs in birds, three of which branch from the ventrobronchi, and two of which branch from the intrapulomonary bronchus connecting the dorsobronchi and ventrobronchi. The air sacs are usually paired, except for the clavicular air sac, creating a total of 9 air sacs. However, this morphology varies among bird species. Birds such as
255:
526:
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229:
and related birds, with some studies hypothesizing that the air sac may be involved as a resonating chamber. The pressure of air in the air sac is also heavily involved in song production, as different males singing the same song have similar modulations in air sac pressure. Changes in air pressure
534:
Dinosaur respiratory systems with bird-like air sacs may have been capable of sustaining higher activity levels than mammals of similar size and build can sustain. In addition to providing a very efficient supply of oxygen, the rapid airflow would have been an effective cooling mechanism, which is
183:
In birds, some temperature control occurs in the respiratory system. Water vapor heats cool air during inhalation in the trachea, and increases its humidity. The resulting evaporative water loss varies greatly and depends on several factors including air sac pressure and the subsequent rate of air
142:
between air sacs, with higher gradients causing more air to flow over the parabronchi during inhalation and lower gradients casing more air to flow over the parabronchi during exhalation. Different air sacs alternate contraction and expansion, causing air motion, the fundamental mechanism of avian
212:
stored in the respiratory system. In penguins, air sac volumes are constricted in deep dives to protect from the effects of water pressure. Penguins have been found inflating their air sacs before dives and exhale much of the air during the deepest point of their dives to change buoyancy while
529:
The uncinate processes are the small white spurs about halfway along the ribs. The rest of this diagram shows the air sacs and other parts of a bird's respiratory system:1 cervical air sac, 2 clavicular air sac, 3 cranial thoracal air sac, 4 caudal thoracal air sac, 5 abdominal air sac (5'
593:', with multiple air sacs and a flow-through lung. Furthermore, an avian system would only need a lung volume of about 600 liters while a mammalian one would have required about 2,950 liters, which would exceed the estimated 1,700 liters of space available in a 30-ton
894:
137:
In birds, gas exchange and volume change do not occur in the same place. While gas exchange occurs in the parabronchi in the lungs, the lungs do not change volume much during respiration. Instead, voluminous expansion occurs in the air sacs. These volume changes cause
352:
fossil on which they based much of their argument was severely flattened and therefore it was impossible to tell whether the liver was the right shape to act as part of a hepatic piston mechanism. Some recent papers simply note without further comment that Ruben
584:
could not have had a reptilian respiratory system, as its tidal volume would have been less than its dead-space volume, so that stale air was not expelled but was sucked back into the lungs. Likewise, a mammalian system would only provide to the lungs about
208:, the air sacs can aid in helping birds with respiration. Movement of the muscles involved in diving can cause a pressure differential between the air sacs which would cause more air to move through the parabronchi. This would then increase the uptake of
564:
of a 30-ton specimen would be about 184 liters. This is the total volume of the mouth, trachea and air tubes. If the animal exhales less than this, stale air is not expelled and is sucked back into the lungs on the following
326:
backwards, which makes the lungs expand to inhale; when these muscles relax, the lungs return to their previous size and shape, and the animal exhales. They also presented this as a reason for doubting that
2644:
Naish D, Martill DM, Frey E (June 2004). "Ecology, systematics and biogeographical relationships of dinosaurs, including a new theropod, from the
Santana Formation (?Albian, Early Cretaceous) of Brazil".
400:") the vertebrae of the lower back and hip regions show signs of air sacs. In early sauropods only the cervical (neck) vertebrae show these features. If the developmental sequence found in bird embryos
338:
and respiratory systems would enable the reptile to achieve 50% to 70% of the oxygen flow of a mammal of similar size, and that lack of avian air sacs would not prevent the development of
604:
has argued that the evolution of the air sac system, which first appears in the very earliest dinosaurs, may have been in response to the very low (11%) atmospheric oxygen of the
112:
Avian lungs have a bronchial system in which the air flows through dorsobronchi into the parabronchi before exiting via the ventrobronchi. Gas exchange occurs at the parabronchi.
940:
480:, which when expressed as a ratio of air volume per body weight at 29 ml/kg is similar to values of geese and other birds, and much higher than typical mammalian values.
487:
dinosaurs. But this does not imply that ornithischians could not have had metabolic rates comparable to those of mammals, since mammals also do not have air sacs.
2805:
521:. If feathers retained heat, their owners would have required a means of dissipating excess heat. This idea is plausible but needs further empirical support.
2837:
Paladino FV, Spotila JR, Dodson P (1997). "A Blueprint for Giants: Modeling the
Physiology of Large Dinosaurs". In Farlow JO, Brett-Surman MK (eds.).
1477:"Boundary Conditions for Heat Transfer and Evaporative Cooling in the Trachea and Air Sac System of the Domestic Fowl: A Two-Dimensional CFD Analysis"
242:. The pressure can change midpoint of the folds of the syrinx, an action which converts the higher pressure into higher frequencies. In a species of
2725:
462:, including the group traditionally called "prosauropods", may also have had air sacs. Although possible pneumatic indentations have been found in
258:
Birds' lungs obtain fresh air during both exhalation and inhalation, because the air sacs do all the "pumping" and the lungs simply absorb oxygen.
895:"Development, structure, and function of a novel respiratory organ, the lung-air sac system of birds: to go where no other vertebrate has gone"
499:
Increase in respiratory capacity. This is probably the most common hypothesis, and fits well with the idea that many dinosaurs had fairly high
262:
From about 1870 onwards scientists have generally agreed that the post-cranial skeletons of many dinosaurs contained many air-filled cavities (
314:(1997, 1999, 2003, 2004) disputed this and suggested that dinosaurs had a "tidal" respiratory system (in and out) powered by a crocodile-like
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2815:
641:
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62:, have many air sacs in the body that are not just in bones, and they can be identified as the more primitive form of modern bird airways.
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II: an assessment of the range of motion of the limbs and vertebral column and of previous reconstructions using a digital skeletal mount"
1758:
97:. The air sacs work to produce a unidirectional flow where air enters and exits the lung at the same rate, contrasting the lungs of other
1774:
1182:
Nguyen, Quynh M.; Oza, Anand U.; Abouezzi, Joanna; Sun, Guanhua; Childress, Stephen; Frederick, Christina; Ristroph, Leif (2021-03-19).
2878:
2438:
O'Connor PM, Claessens LP (July 2005). "Basic avian pulmonary design and flow-through ventilation in non-avian theropod dinosaurs".
2134:
Ruben JA, Jones TD, Geist NR, Hillenius WJ (November 1997). "Lung structure and ventilation in theropod dinosaurs and early birds".
2354:
Hicks JW, Farmer CG (September 1999). "Gas exchange potential in reptilian lungs: implications for the dinosaur-avian connection".
85:
1012:
Bejdić, Pamela; Hadžimusić, Nejra; Šerić-Haračić, Sabina; Maksimović, Alan; Lutvikadić, Ismar; Hrković-Porobija, Amina (2021).
2272:
Hillenius WJ, Ruben JA (November–December 2004). "The evolution of endothermy in terrestrial vertebrates: Who? When? Why?".
1374:"Body Mass and Foraging Ecology Predict Evolutionary Patterns of Skeletal Pneumaticity in the Diverse "Waterbird" Clade"
790:, et al. (November 2014). "Resolving the long-standing enigmas of a giant ornithomimosaur Deinocheirus mirificus".
2804:
Reid RE (1997). "Dinosaurian
Physiology: the Case for "Intermediate" Dinosaurs". In Farlow JO, Brett-Surman MK (eds.).
2862:
601:
30:
This article is about a component of dinosaur and bird skeletal systems. For the structures in mammalian lungs, see
2691:
2219:
Ruben JA, Jones TD, Geist NR (2003). "Respiratory and reproductive paleophysiology of dinosaurs and early birds".
1475:
Sverdlova, Nina S.; Lambertz, Markus; Witzel, Ulrich; Perry, Steven F. (2012-09-20). Samakovlis, Christos (ed.).
2577:
2514:
675:
The avian respiratory system: a unique model for studies of respiratory toxicosis and for monitoring air quality
66:
are well known for the large number of air pockets in their bones (especially vertebra), although one theropod,
334:
Critics have claimed that, without avian air sacs, modest improvements in a few aspects of a modern reptile's
2866:
1249:"Robust Unidirectional Airflow through Avian Lungs: New Insights from a Piecewise Linear Mathematical Model"
561:
134:
have different air sac arrangements. The morphologies of the individual air sacs also vary among bird taxa.
535:
essential for animals that are active but too large to get rid of all the excess heat through their skins.
2662:
52:(presence of air) in their bones. Birds use air sacs for respiration as well as a number of other things.
572: – the amount of air moved into or out of the lungs in a single breath – depend on the type of
2900:
2740:
1869:"Tracheal length changes during zebra finch song and their possible role in upper vocal tract filtering"
1074:"Pulmonary pneumaticity in the postcranial skeleton of extant Aves: A case study examining Anseriformes"
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159:
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404:, air sacs actually evolved before the channels in the skeleton that accommodate them in later forms.
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the animal had: 904 liters if avian; 225 liters if mammalian; 19 liters if reptilian.
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1974:
Philosophical
Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences
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1129:"Unidirectional pulmonary airflow in vertebrates: a review of structure, function, and evolution"
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are spaces within an organism where there is the constant presence of air. Among modern animals,
719:, Martinez RN, Wilson JA, Varricchio DJ, Alcober OA, Larsson HC (September 2008). Kemp T (ed.).
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2842:
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2626:
2530:"Findarticles.com: Vertebral pneumaticity, air sacs, and the physiology of sauropod dinosaurs"
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As a cooling mechanism. It seems that air sacs and feathers evolved at about the same time in
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of the air sacs is related to the timing of all of the moving parts involved in respiration.
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346:’s claim that dinosaurs could not have had avian-style air sacs; but one points out that the
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1601:"Penguin lungs and air sacs: implications for baroprotection, oxygen stores and buoyancy"
447:, is one of the earliest dinosaurs whose fossils show evidence of channels for air sacs.
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225 − 184 = 41 liters of fresh, oxygenated air on each breath.
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Evidence of air sacs has also been found in theropods. Studies indicate that fossils of
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2010:
1969:
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514:. However this does not explain the expansion of air sacs in the quadrupedal sauropods.
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31:
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721:"Evidence for avian intrathoracic air sacs in a new predatory dinosaur from Argentina"
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Three explanations have been suggested for the development of air sacs in dinosaurs:
2684:
2585:
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2301:
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1642:
1415:
1113:
2475:
2120:
2091:
Bakker RT (1972). "Anatomical and ecological evidence of endothermy in dinosaurs".
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959:"Gross morphological features of the air sacs of the hooded crow ( Corvus cornix )"
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For a long time these cavities were regarded simply as weight-saving devices, but
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patterns are indicative of respiratory muscle activity and the airflow around the
2676:
2197:
1501:
1273:
841:
Schwarz-Wings D, Meyer CA, Frey E, Manz-Steiner HR, Schumacher R (January 2010).
745:
2705:
2061:
2036:
Döppler, Juan F.; Amador, Ana; Goller, Franz; Mindlin, Gabriel B. (2020-12-11).
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must therefore have had either a system unknown in the modern world or one like
540:
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452:
429:
397:
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342:. Very few formal rebuttals have been published in scientific journals of Ruben
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205:
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544:’ respiratory system support the evidence of bird-like air sacs in sauropods:
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283:
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116:
2001:
1946:
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1720:"Respiratory Units of Motor Production and Song Imitation in the Zebra Finch"
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1574:
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1347:
1282:
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1014:"Morphology of the Air Sacs in Crimson Rosella (Platycercus elegans) Parrots"
982:
918:
2541:"Vertebral pneumaticity, air sacs, and the physiology of sauropod dinosaurs"
2491:"Vertebral pneumaticity, air sacs, and the physiology of sauropod dinosaurs"
2421:
1799:
Beckers, Gabriël J. L.; Suthers, Roderick A.; Cate, Carel ten (2003-06-01).
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10.1002/(SICI)1097-4695(19971105)33:5<653::AID-NEU11>3.0.CO;2-A
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843:"Mechanical implications of pneumatic neck vertebrae in sauropod dinosaurs"
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This is also one of several topics featured in a post on Naish's blog,
1617:
1600:
1549:"Differential air sac pressures in diving tufted ducks Aythya fuligula"
1456:
1089:
605:
235:
163:
124:
2169:
Ruben JA, Geist NR, Hillenius WJ, Jones TD, Signore M (January 1999).
2038:"Dynamics behind rough sounds in the song of the Pitangus sulphuratus"
1884:
1825:
1816:
1735:
974:
2112:
1921:"Vocal athletics – from birdsong production mechanisms to sexy songs"
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266:), especially in the vertebrae. Pneumatization of the skull (such as
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131:
102:
1801:"Mechanisms of frequency and amplitude modulation in ring dove song"
1800:
1719:
1447:
1430:
2285:
2232:
2171:"Pulmonary function and metabolic physiology of theropod dinosaurs"
1200:
278:, but postcranial pneumatization is found only in birds, non-avian
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406:
365:
Researchers have presented evidence and arguments for air sacs in
323:
253:
84:
2871:
Out of thin air: Dinosaurs, birds, and earth's ancient atmosphere
2841:. Bloomington, Ind.: Indiana University Press. pp. 491–504.
2726:"What pneumaticity tells us about 'prosauropods', and vice versa"
1658:"Pure-tone birdsong by resonance filtering of harmonic overtones"
315:
298:
167:
41:
2559:"The Evolution of Vertebral Pneumaticity in Sauropod Dinosaurs"
538:
Calculations of the volumes of various parts of the sauropod
2810:. Bloomington: Indiana University Press. pp. 449–473.
2578:
10.1671/0272-4634(2003)023[0344:TEOVPI]2.0.CO;2
2515:
10.1666/0094-8373(2003)029<0243:VPASAT>2.0.CO;2
2604:"Origin of postcranial skeletal pneumaticity in dinosaurs"
1184:"Flow Rectification in Loopy Network Models of Bird Lungs"
2317:"Lung Ventilation and Gas Exchange in Theropod Dinosaurs"
1599:
Ponganis, P. J.; St Leger, J.; Scadeng, M. (2015-03-01).
1759:"Neural pathways for the control of birdsong production"
1656:
Beckers, G. J. L.; Suthers, R. A.; ten Cate, C. (2003).
89:
Diagram showing the general layout of air sacs in a bird
357:
argued against the presence of air sacs in dinosaurs.
506:
Improving balance and maneuvrability by lowering the
44:
possess the most air sacs (9–11), with their extinct
2433:
2431:
1547:
Boggs, D F; Butler, P J; Wallace, S E (1998-09-15).
957:
El-Sayed, Ahmed K.; Hassan, Said (15 October 2019).
530:
diverticulus into pelvic girdle), 6 lung, 7 trachea
636:. Holt-Saunders International. pp. 330–334.
483:So far no evidence of air sacs has been found in
939:: CS1 maint: DOI inactive as of February 2024 (
455:, had the most bird-like air sacs found so far.
318:mechanism – muscles attached mainly to the
1247:Harvey, Emily P.; Ben-Tal, Alona (2016-02-10).
115:Avian pulmonary air sacs are lined with simple
2873:. National Academies Press. pp. 159–198.
2708:, which Naish believes was closely related to
1968:Trevisan, M. A.; Mindlin, G. B. (2009-08-28).
673:Brown, R. E.; Brain, J. D.; Wang, N. (1997). "
552:, like dinosaurs' nearest surviving relatives
158:. Bone pneumaticity is generally found in the
2597:
2595:
2555:Detailed anatomical analyses can be found at
1970:"New perspectives on the physics of birdsong"
711:
709:
707:
8:
2799:
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72:, shows a rivalling number of air pockets.
1018:Advances in Animal and Veterinary Sciences
213:descending and ascending during the dive.
48:relatives showing a great increase in the
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2240:
2009:
1936:
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1031:10.17582/journal.aavs/2021/9.11.1959.1963
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866:
754:
744:
105:where air enters and exits the lung in a
93:Birds have a system of air sacs in their
1127:Cieri, Robert L.; Farmer, C. G. (2016).
191:
621:
27:Part of the respiratory system of birds
2031:
2029:
1914:
1912:
1910:
932:
2315:Hicks JW, Farmer CG (November 1997).
2274:Physiological and Biochemical Zoology
2221:Physiological and Biochemical Zoology
1867:Daley, Monica; Goller, Franz (2004).
1862:
1860:
1794:
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1592:
1542:
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293:proposed that they were connected to
7:
2389:Currie PJ, Chen PJ (December 2001).
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888:
886:
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305:the most efficient of all animals'.
2692:"Basal tyrant dinosaurs and my pet
1133:Journal of Comparative Physiology B
411:Comparison between the air sacs of
2566:Journal of Vertebrate Paleontology
2402:Canadian Journal of Earth Sciences
2395:from Liaoning, northeastern China"
25:
1340:10.1038/scientificamerican1271-72
963:Anatomia, Histologia, Embryologia
679:Environmental Health Perspectives
264:postcranial skeletal pneumaticity
2623:10.1111/j.1749-4877.2006.00019.x
1391:10.1111/j.1558-5646.2011.01494.x
847:Proceedings. Biological Sciences
2733:Special Papers in Palaeontology
1805:Journal of Experimental Biology
1605:Journal of Experimental Biology
1553:Journal of Experimental Biology
1372:Smith, Nathan D. (2011-11-18).
2527:Full text currently online at
1718:Franz, M.; Goller, F. (2002).
1314:Schmidt-Nielsen, Knut (1971).
1218:10.1103/PhysRevLett.126.114501
439:exhibit evidence of air sacs.
329:birds descended from dinosaurs
1:
2774:Acta Palaeontologica Polonica
2368:10.1016/S0034-5687(99)00060-2
2341:10.1126/science.278.5341.1267
2156:10.1126/science.278.5341.1267
1938:10.1016/j.anbehav.2021.04.009
1072:O'Connor, Patrick M. (2004).
612:ages of the Triassic Period.
200:, an example of a diving bird
2677:10.1080/08912960410001674200
2198:10.1126/science.283.5401.514
1919:Goller, Franz (2022-02-01).
1502:10.1371/journal.pone.0045315
1274:10.1371/journal.pcbi.1004637
746:10.1371/journal.pone.0003303
2062:10.1103/PhysRevE.102.062415
2917:
1431:"The Air Sacs of the Loon"
1253:PLOS Computational Biology
556:and birds, did not have a
238:which can also affect the
184:flow through the trachea.
29:
2739:: 207–222. Archived from
1145:10.1007/s00360-016-0983-3
911:10.1017/S1464793106007111
2867:"The Triassic Explosion"
396:In advanced sauropods ("
221:Air sacs play a role in
2422:10.1139/cjes-38-12-1705
1873:Journal of Neurobiology
1763:Journal of Neurobiology
1724:Journal of Neurobiology
1683:10.1073/pnas.1232227100
1566:10.1242/jeb.201.18.2665
1188:Physical Review Letters
913:(inactive 2024-02-27).
893:Maina, John N. (2006).
786:, Kobayashi Y, Lee HJ,
689::10.1289/ehp.97105188.
174:Other uses for air sacs
81:Air sacs in respiration
2602:Wedel MJ (June 2006).
2356:Respiration Physiology
1994:10.1098/rsta.2009.0076
859:10.1098/rspb.2009.1275
531:
416:
259:
201:
162:. Some birds, such as
90:
2839:The Complete Dinosaur
2807:The Complete Dinosaur
2787:10.4202/app.2009.0075
2393:Sinosauropteryx prima
1078:Journal of Morphology
632:, Parsons TS (1977).
528:
410:
297:like those that make
257:
240:fundamental frequency
195:
160:appendicular skeleton
88:
1757:Wild, J. M. (1998).
1429:Gier, H. T. (1952).
600:The palaeontologist
451:, a Late Cretaceous
427:, and the theropods
381:, and the theropods
170:, have solid bones.
2764:Mallison H (2010).
2659:2004HBio...16...57N
2611:Integrative Zoology
2507:2003Pbio...29..243W
2460:10.1038/nature03716
2452:2005Natur.436..253O
2414:2001CaJES..38.1705C
2333:1997Sci...278.1267R
2327:(5341): 1267–1270.
2190:1999Sci...283..514R
2148:1997Sci...278.1267R
2142:(5341): 1267–1270.
2105:1972Natur.238...81B
2054:2020PhRvE.102f2415D
1986:2009RSPTA.367.3239T
1980:(1901): 3239–3254.
1674:2003PNAS..100.7372B
1493:2012PLoSO...745315S
1332:1971SciAm.225f..72S
1320:Scientific American
1316:"How Birds Breathe"
1265:2016PLSCB..12E4637H
1210:2021PhRvL.126k4501N
812:10.1038/nature13874
804:2014Natur.515..257L
737:2008PLoSO...3.3303S
634:The Vertebrate Body
303:respiratory systems
270:) is found in both
2647:Historical Biology
1618:10.1242/jeb.113647
1090:10.1002/jmor.10190
899:Biological Reviews
574:respiratory system
532:
512:rotational inertia
417:
260:
202:
150:Birds have hollow
140:pressure gradients
128:connective tissues
95:ventilation system
91:
2848:978-0-253-21313-6
2817:978-0-253-33349-0
2557:Wedel MJ (2003).
2489:Wedel MJ (2003).
2446:(7048): 253–256.
2408:(12): 1705–1727.
2184:(5401): 514–516.
2042:Physical Review E
1885:10.1002/neu.10332
1817:10.1242/jeb.00364
1811:(11): 1833–1843.
1736:10.1002/neu.10043
1668:(12): 7372–7376.
1559:(18): 2665–2668.
975:10.1111/ahe.12504
798:(7526): 257–260.
643:978-0-03-910284-5
568:Estimates of its
562:dead-space volume
508:center of gravity
268:paranasal sinuses
143:respiration. The
107:tidal ventilation
76:Air sacs in birds
16:(Redirected from
2908:
2885:
2884:
2859:
2853:
2852:
2834:
2828:
2827:
2825:
2824:
2801:
2792:
2791:
2789:
2761:
2755:
2754:
2752:
2751:
2745:
2730:
2724:Wedel M (2007).
2721:
2715:
2699:
2688:
2670:
2641:
2635:
2634:
2608:
2599:
2590:
2589:
2563:
2554:
2552:
2546:. Archived from
2545:
2537:
2526:
2486:
2480:
2479:
2435:
2426:
2425:
2399:
2386:
2380:
2379:
2351:
2345:
2344:
2312:
2306:
2305:
2280:(6): 1019–1042.
2269:
2263:
2262:
2244:
2216:
2210:
2209:
2175:
2166:
2160:
2159:
2131:
2125:
2124:
2113:10.1038/238081a0
2088:
2082:
2081:
2033:
2024:
2023:
2013:
1965:
1959:
1958:
1940:
1925:Animal Behaviour
1916:
1905:
1904:
1864:
1855:
1854:
1828:
1796:
1787:
1786:
1754:
1748:
1747:
1715:
1706:
1705:
1695:
1685:
1653:
1647:
1646:
1620:
1596:
1587:
1586:
1568:
1544:
1533:
1532:
1522:
1504:
1472:
1461:
1460:
1450:
1426:
1420:
1419:
1393:
1384:(4): 1059–1078.
1369:
1360:
1359:
1311:
1305:
1304:
1294:
1276:
1244:
1238:
1237:
1203:
1179:
1173:
1172:
1124:
1118:
1117:
1069:
1052:
1051:
1033:
1009:
1003:
1002:
954:
945:
944:
938:
930:
890:
881:
880:
870:
838:
832:
831:
775:
769:
768:
758:
748:
713:
702:
671:
648:
647:
626:
471:Thecodontosaurus
443:, from the late
21:
2916:
2915:
2911:
2910:
2909:
2907:
2906:
2905:
2891:
2890:
2889:
2888:
2881:
2861:
2860:
2856:
2849:
2836:
2835:
2831:
2822:
2820:
2818:
2803:
2802:
2795:
2763:
2762:
2758:
2749:
2747:
2743:
2728:
2723:
2722:
2718:
2690:
2668:10.1.1.394.9219
2643:
2642:
2638:
2606:
2601:
2600:
2593:
2561:
2556:
2550:
2543:
2539:
2528:
2488:
2487:
2483:
2437:
2436:
2429:
2397:
2388:
2387:
2383:
2353:
2352:
2348:
2314:
2313:
2309:
2271:
2270:
2266:
2218:
2217:
2213:
2173:
2168:
2167:
2163:
2133:
2132:
2128:
2099:(5359): 81–85.
2090:
2089:
2085:
2035:
2034:
2027:
1967:
1966:
1962:
1918:
1917:
1908:
1866:
1865:
1858:
1798:
1797:
1790:
1756:
1755:
1751:
1717:
1716:
1709:
1655:
1654:
1650:
1598:
1597:
1590:
1546:
1545:
1536:
1474:
1473:
1464:
1448:10.2307/4081291
1428:
1427:
1423:
1371:
1370:
1363:
1313:
1312:
1308:
1259:(2): e1004637.
1246:
1245:
1241:
1181:
1180:
1176:
1126:
1125:
1121:
1071:
1070:
1055:
1011:
1010:
1006:
956:
955:
948:
931:
892:
891:
884:
853:(1678): 11–17.
840:
839:
835:
777:
776:
772:
715:
714:
705:
672:
651:
644:
628:
627:
623:
618:
580:On this basis,
501:metabolic rates
493:
460:sauropodomorphs
363:
349:Sinosauropteryx
282:dinosaurs, and
252:
223:song production
219:
217:Song production
198:emperor penguin
190:
181:
176:
152:pneumatic bones
121:secretory cells
83:
78:
35:
28:
23:
22:
15:
12:
11:
5:
2914:
2912:
2904:
2903:
2893:
2892:
2887:
2886:
2879:
2854:
2847:
2829:
2816:
2793:
2780:(3): 433–458.
2756:
2716:
2653:(2–4): 57–70.
2636:
2591:
2572:(2): 344–357.
2553:on 2015-02-15.
2501:(2): 243–255.
2481:
2427:
2381:
2362:(2–3): 73–83.
2346:
2307:
2286:10.1086/425185
2264:
2233:10.1086/375425
2227:(2): 141–164.
2211:
2161:
2126:
2083:
2025:
1960:
1906:
1879:(3): 319–330.
1856:
1788:
1769:(5): 653–670.
1749:
1730:(2): 129–141.
1707:
1648:
1611:(5): 720–730.
1588:
1534:
1462:
1421:
1361:
1306:
1239:
1194:(11): 114501.
1174:
1139:(5): 541–552.
1119:
1084:(2): 141–161.
1053:
1004:
969:(2): 159–166.
946:
905:(4): 545–579.
882:
833:
770:
703:
685:(2): 188–200.
649:
642:
620:
619:
617:
614:
578:
577:
566:
548:Assuming that
523:
522:
515:
504:
492:
489:
362:
359:
316:hepatic piston
251:
248:
218:
215:
189:
186:
180:
177:
175:
172:
82:
79:
77:
74:
50:pneumatization
32:air sac (lung)
26:
24:
14:
13:
10:
9:
6:
4:
3:
2:
2913:
2902:
2899:
2898:
2896:
2882:
2880:9780309141239
2876:
2872:
2868:
2864:
2858:
2855:
2850:
2844:
2840:
2833:
2830:
2819:
2813:
2809:
2808:
2800:
2798:
2794:
2788:
2783:
2779:
2775:
2771:
2769:
2766:"The digital
2760:
2757:
2746:on 2008-07-05
2742:
2738:
2734:
2727:
2720:
2717:
2713:
2712:
2711:Compsognathus
2707:
2703:
2697:
2695:
2686:
2682:
2678:
2674:
2669:
2664:
2660:
2656:
2652:
2648:
2640:
2637:
2632:
2628:
2624:
2620:
2616:
2612:
2605:
2598:
2596:
2592:
2587:
2583:
2579:
2575:
2571:
2567:
2560:
2549:
2542:
2535:
2531:
2524:
2520:
2516:
2512:
2508:
2504:
2500:
2496:
2492:
2485:
2482:
2477:
2473:
2469:
2465:
2461:
2457:
2453:
2449:
2445:
2441:
2434:
2432:
2428:
2423:
2419:
2415:
2411:
2407:
2403:
2396:
2394:
2385:
2382:
2377:
2373:
2369:
2365:
2361:
2357:
2350:
2347:
2342:
2338:
2334:
2330:
2326:
2322:
2318:
2311:
2308:
2303:
2299:
2295:
2291:
2287:
2283:
2279:
2275:
2268:
2265:
2260:
2256:
2252:
2248:
2243:
2238:
2234:
2230:
2226:
2222:
2215:
2212:
2207:
2203:
2199:
2195:
2191:
2187:
2183:
2179:
2172:
2165:
2162:
2157:
2153:
2149:
2145:
2141:
2137:
2130:
2127:
2122:
2118:
2114:
2110:
2106:
2102:
2098:
2094:
2087:
2084:
2079:
2075:
2071:
2067:
2063:
2059:
2055:
2051:
2048:(6): 062415.
2047:
2043:
2039:
2032:
2030:
2026:
2021:
2017:
2012:
2007:
2003:
1999:
1995:
1991:
1987:
1983:
1979:
1975:
1971:
1964:
1961:
1956:
1952:
1948:
1944:
1939:
1934:
1930:
1926:
1922:
1915:
1913:
1911:
1907:
1902:
1898:
1894:
1890:
1886:
1882:
1878:
1874:
1870:
1863:
1861:
1857:
1852:
1848:
1844:
1840:
1836:
1832:
1827:
1822:
1818:
1814:
1810:
1806:
1802:
1795:
1793:
1789:
1784:
1780:
1776:
1772:
1768:
1764:
1760:
1753:
1750:
1745:
1741:
1737:
1733:
1729:
1725:
1721:
1714:
1712:
1708:
1703:
1699:
1694:
1689:
1684:
1679:
1675:
1671:
1667:
1663:
1659:
1652:
1649:
1644:
1640:
1636:
1632:
1628:
1624:
1619:
1614:
1610:
1606:
1602:
1595:
1593:
1589:
1584:
1580:
1576:
1572:
1567:
1562:
1558:
1554:
1550:
1543:
1541:
1539:
1535:
1530:
1526:
1521:
1516:
1512:
1508:
1503:
1498:
1494:
1490:
1487:(9): e45315.
1486:
1482:
1478:
1471:
1469:
1467:
1463:
1458:
1454:
1449:
1444:
1440:
1436:
1432:
1425:
1422:
1417:
1413:
1409:
1405:
1401:
1397:
1392:
1387:
1383:
1379:
1375:
1368:
1366:
1362:
1357:
1353:
1349:
1345:
1341:
1337:
1333:
1329:
1325:
1321:
1317:
1310:
1307:
1302:
1298:
1293:
1288:
1284:
1280:
1275:
1270:
1266:
1262:
1258:
1254:
1250:
1243:
1240:
1235:
1231:
1227:
1223:
1219:
1215:
1211:
1207:
1202:
1197:
1193:
1189:
1185:
1178:
1175:
1170:
1166:
1162:
1158:
1154:
1150:
1146:
1142:
1138:
1134:
1130:
1123:
1120:
1115:
1111:
1107:
1103:
1099:
1095:
1091:
1087:
1083:
1079:
1075:
1068:
1066:
1064:
1062:
1060:
1058:
1054:
1049:
1045:
1041:
1037:
1032:
1027:
1023:
1019:
1015:
1008:
1005:
1000:
996:
992:
988:
984:
980:
976:
972:
968:
964:
960:
953:
951:
947:
942:
936:
928:
924:
920:
916:
912:
908:
904:
900:
896:
889:
887:
883:
878:
874:
869:
864:
860:
856:
852:
848:
844:
837:
834:
829:
825:
821:
817:
813:
809:
805:
801:
797:
793:
789:
785:
781:
774:
771:
766:
762:
757:
752:
747:
742:
738:
734:
730:
726:
722:
718:
712:
710:
708:
704:
700:
696:
692:
688:
684:
680:
676:
670:
668:
666:
664:
662:
660:
658:
656:
654:
650:
645:
639:
635:
631:
625:
622:
615:
613:
611:
607:
603:
598:
596:
592:
588:
583:
575:
571:
567:
563:
559:
555:
551:
547:
546:
545:
543:
542:
536:
527:
520:
516:
513:
510:and reducing
509:
505:
502:
498:
497:
496:
490:
488:
486:
485:ornithischian
481:
479:
478:
473:
472:
467:
466:
461:
456:
454:
450:
446:
442:
438:
437:
432:
431:
426:
422:
414:
413:Majungasaurus
409:
405:
403:
399:
394:
392:
391:
386:
385:
380:
376:
372:
368:
360:
358:
356:
351:
350:
345:
341:
337:
332:
330:
325:
321:
317:
313:
310:
306:
304:
300:
296:
292:
287:
285:
281:
277:
273:
269:
265:
256:
249:
247:
245:
241:
237:
233:
228:
224:
216:
214:
211:
207:
199:
194:
187:
185:
178:
173:
171:
169:
165:
161:
157:
153:
148:
146:
141:
135:
133:
129:
126:
123:supported by
122:
118:
113:
110:
108:
104:
100:
96:
87:
80:
75:
73:
71:
70:
65:
61:
60:
55:
51:
47:
43:
39:
33:
19:
2901:Lung anatomy
2870:
2857:
2838:
2832:
2821:. Retrieved
2806:
2777:
2773:
2768:Plateosaurus
2767:
2759:
2748:. Retrieved
2741:the original
2736:
2732:
2719:
2709:
2701:
2693:
2650:
2646:
2639:
2617:(2): 80–85.
2614:
2610:
2569:
2565:
2548:the original
2534:Paleobiology
2533:
2498:
2495:Paleobiology
2494:
2484:
2443:
2439:
2405:
2401:
2392:
2391:"Anatomy of
2384:
2359:
2355:
2349:
2324:
2320:
2310:
2277:
2273:
2267:
2242:10211.1/1472
2224:
2220:
2214:
2181:
2177:
2164:
2139:
2135:
2129:
2096:
2092:
2086:
2045:
2041:
1977:
1973:
1963:
1928:
1924:
1876:
1872:
1808:
1804:
1766:
1762:
1752:
1727:
1723:
1665:
1661:
1651:
1608:
1604:
1556:
1552:
1484:
1480:
1441:(1): 40–49.
1438:
1434:
1424:
1381:
1377:
1326:(6): 72–79.
1323:
1319:
1309:
1256:
1252:
1242:
1191:
1187:
1177:
1136:
1132:
1122:
1081:
1077:
1021:
1017:
1007:
966:
962:
935:cite journal
902:
898:
850:
846:
836:
795:
791:
773:
731:(9): e3303.
728:
724:
682:
678:
633:
624:
599:
594:
586:
581:
579:
570:tidal volume
554:crocodilians
549:
539:
537:
533:
519:coelurosaurs
494:
482:
477:Plateosaurus
475:
469:
465:Plateosaurus
463:
457:
453:megaraptorid
448:
440:
434:
428:
421:coelurosaurs
418:
412:
398:neosauropods
395:
388:
382:
375:coelurosaurs
371:prosauropods
364:
354:
347:
343:
333:
311:
307:
288:
261:
220:
206:diving birds
203:
182:
149:
136:
114:
111:
92:
69:Deinocheirus
67:
57:
37:
36:
2706:coelurosaur
1931:: 173–184.
788:Godefroit P
693:0091-6765.
595:Apatosaurus
587:Apatosaurus
582:Apatosaurus
565:inhalation.
550:Apatosaurus
541:Apatosaurus
491:Development
441:Coelophysis
430:Coelophysis
425:ceratosaurs
390:Coelophysis
379:ceratosaurs
336:circulatory
280:saurischian
46:dinosaurian
2823:2008-09-12
2750:2007-10-31
1826:1887/81094
1201:2103.11237
780:Barsbold R
616:References
602:Peter Ward
415:and a bird
402:is a guide
340:endothermy
309:John Ruben
284:pterosaurs
276:archosaurs
179:Water loss
145:compliance
117:epithelial
2702:Mirischia
2694:Mirischia
2663:CiteSeerX
2078:230594046
2002:1364-503X
1955:235226514
1947:0003-3472
1893:0022-3034
1835:1477-9145
1627:1477-9145
1575:1477-9145
1511:1932-6203
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