BIO 554/754
Ornithology

Avian Respiration


An updated version of these notes can be accessed from a new "Avian Biology' page
(http://people.eku.edu/ritchisong/avian_biology.html)
.

 

The avian respiratory system delivers oxygen from the air to the tissues and also removes carbon dioxide. In addition, the respiratory system plays an important role in thermoregulation (maintaining normal body temperature). The avian respiratory system is different from that of other vertebrates, with birds having relatively small lungs plus nine air sacs that play an important role in respiration (but are not directly involved in the exchange of gases).
 

(A). Dorsal view of the trachea (circled) and the lung of the Ostrich (Struthio camelus). The lungs are deeply entrenched into the ribs on the dorsolateral aspects (arrowhead). Filled circle, right extrapulmonary primary bronchus (EPPB). Note that the right EPPB is relatively longer, rather horizontal and relatively narrower compared with the left EPPB. Scale bar, 1 cm. (B) Close up of the dorsal aspect of the lung showing the deep costal sulci (s). Trachea, circled; filled circle, right extrapulmonary primary bronchus. Scale bar, 2 cm (Maina and Nathaniel 2001).


Used with permission of John Kimball.

The air sacs permit a unidirectional flow of air through the lungs. Unidirectional flow means that air moving through bird lungs is largely 'fresh' air & has a higher oxygen content. In contrast, air flow is 'bidirectional' in mammals, moving back & forth into & out of the lungs. As a result, air coming into a mammal's  lungs is mixed with 'old' air (air that has been in the lungs for a while) & this 'mixed air' has less oxygen. So, in bird lungs, more oxygen is available to diffuse into the blood (avian respiratory system).
 

Most birds have 9 air sacs:
  • one interclavicular sac
  • two cervical sacs
  • two anterior thoracic sacs
  • two posterior thoracic sacs
  • two abdominal sacs
Functionally, these 9 air sacs can be divided into anterior sacs (interclavicular, cervicals, & anterior thoracics) & posterior sacs (posterior thoracics & abdominals). Air sacs have very thin walls with few blood vessels. So, they do not play a direct role in gas exchange. Rather, they act as a 'bellows' to ventilate the lungs (Powell 2000). 
Source: http://numbat.murdoch.edu.au/Anatomy/avian/fig3.2.GIF


Air sacs and axial pneumatization in an extant avian. The body of bird in left lateral view, showing the cervical (C), interclavicular (I), anterior thoracic (AT), posterior thoracic (PT), and abdominal (AB) air sacs. The hatched area shows the volume change during exhalation. The cervical and anterior thoracic vertebrae are pneumatized by diverticula of the cervical air sacs. The posterior thoracic vertebrae and synsacrum are pneumatized by the abdominal air sacs in most taxa. Diverticula of the abdominal air sacs usually invade the vertebral column at several points. Diverticula often unite when they come into contact, producing a system of continuous vertebral airways extending from the third cervical vertebra to the end of the synsacrum. Modified from Duncker 1971 (Wedel 2003).


Computerized axial tomogram of an awake, spontaneously breathing goose; air is darkest. A large percentage of the bird's body is filled with the several air sacs. Upper left:  At the level of the shoulder joints (hh, humeral head) is the intraclavicular air sac (ICAS), which extends from the heart cranially to the clavicles (i.e., furcula or wishbone). S, sternum; FM, large flight muscles with enclosed air sac diverticula, arrowheads; t, trachea. Upper right: At the level of the caudal heart (H) is the paired cranial thoracic air sacs (TAS). Arrowhead points to the medial wall of the air sac (contrast enhanced with aerosolized tantalum powder). The dorsal body cavity is filled with the lungs, which are tightly attached to the dorsal and lateral body wall. V, thoracic vertebrae. Lower left: At the level of the knees (K) is the paired caudal thoracic air sacs (PTAS) and paired abdominal air sacs, with the abdominal viscera (AV) filling the ventral body cavity. The membrane separating the abdominal air sacs from one another (arrowhead) and from the caudal thoracic air sacs (arrows) can be seen. Lower right: At the level of the caudal pelvis, the abdominal air sacs, which extend to the bird's tail, can be seen. Arrow, membrane separating abdominal air sacs (Brown et al. 1997).

Birds can breathe through the mouth or the nostrils (nares). Air entering these openings (during inspiration) passes through the pharynx & then into the trachea (or windpipe). The trachea is generally as long as the neck. However, some birds, such as cranes, have an exceptionally long (up to 1.5 m) trachea that is coiled within the hollowed keel of the breastbone (shown below). This arrangement may give additional resonance to their loud calls.

The typical bird trachea is 2.7 times longer and 1.29 times wider than that of similarly-sized mammals. The net effect is that tracheal resistance to air flow is similar to that in mammals, but the tracheal dead space volume is about 4.5 times larger. Birds compensate for the larger tracheal dead space by having a relatively larger tidal volume and a lower respiratory frequency, approximately one-third that of mammals. These two factors lessen the impact of the larger tracheal dead space volume on ventilation. Thus, minute tracheal ventilation is only about 1.5 to 1.9 times that of mammals (Ludders 2001).


Examples of tracheal loops found in black swans (Cygnus atratus), whooper
                    swans (Cygnus cygnus), white spoonbills (Platalea leucorodia), helmeted curasso (Crax pauxi),
and whooping Cranes (Grus americana).
Source: http://www.ivis.org/advances/Anesthesia_Gleed/ludders2/chapter_frm.asp

The trachea bifurcates (or splits) into two primary bronchi at the syrinx. The syrinx is unique to birds & is their 'voicebox' (in mammals, sounds are produced in the larynx). The process by which the syrinx produces sounds will be covered later in the course. The primary bronchi enter the lungs & are then called mesobronchi. Branching off from the mesobronchi are smaller tubes called ventrobronchi. The ventrobrochi, in turn, lead into the still smaller parabronchi. Parabronchi can be several millimeters long and 0.5 - 2.0 mm in diameter (depending on the size of the bird) (Maina 1989) and their walls contain hundreds of tiny, branching, & anastomosing 'air capillaries' surrounded by a profuse network of blood capillaries (Welty & Baptista 1988).
 


Three-dimensional reconstruction of the gas-exchange region.
AC = air capillaries. Several air capillaries coalesce into an infundibulum (INF) (Brown et al. 1997). 

In this cross-section, note the intertwined network of blood capillaries, labeled with the presence of erythrocytes (*), and air capillaries (AC) that make up the parabronchi's mantle of gas-exchange tissue (Brown et al. 1997). 

Morphology of a chicken lung. Light microscopy (top image) and electron microscopy (bottom two images) of a chicken lung depicting the respiratory system of birds. In the bird lung, air capillaries (Ac) run along with blood capillaries forming the blood-air barrier that is typically < 0.2 µm in thickness. The barrier (shown in the bottom image) separates the lumen of the Ac (*) from the red blood cells (RBC) in the blood capillaries and consists of a mostly continuous surfactant layer (arrows), thin cytoplasmic processes of epithelial cells (Ep), a common basal membrane (Bm), and the endothelial cells of the blood capillary (En). Surfactant is a mixture of lipids and proteins that acts in the air capillaries of avian lungs both as an "antiglue" (preventing the adhesion of respiratory surfaces that may occur when the lungs collapse, e.g., during diving, swallowing of prey or on expiration) and to prevent liquid influx into the lungs (Daniels et al. 1998). Magnifications: top image - ×270; middle image - ×1,600; bottom image - ×88,000 (Image from Bernhard et al. 2001).


It's within these 'air capillaries' that the exchange of gases (oxygen and carbon dioxide) between the lungs & the blood occurs. The parabronchi then lead into larger dorsobronchi which, in turn, lead back into mesobronchi.


Source: http://wwwvet.murdoch.edu.au/Anatomy/avian/fig3.1.GIF

So, how does air flow through the avian lungs & air sacs during respiration?
 

1 - On first inhalation, air flows through the trachea & bronchi & primarily into the posterior (rear) air sacs

2 - On exhalation, air moves from the posterior air sacs & into the lungs

3 - With the second inhalation, air moves from the lungs & into the anterior (front) air sacs

4 - With the second exhalation, air moves from the anterior air sacs back into the trachea & out

Air flow is driven by changes in pressure within the respiratory system:


Changes in the position of the thoracic skeleton during breathing in a bird. The solid lines represent
thoracic position at the end of expiration while the dotted lines show the thoracic position
at the end of inspiration (Source: http://www.ivis.org/advances/Anesthesia_Gleed/ludders2/chapter_frm.asp).
 


Schematic representation of the right paleopulmonic lung and air sacs of a bird and the pathway of
       gas flow through the pulmonary system during inspiration and expiration. For purposes of clarity, the neopulmonic lung
       is not shown. The intrapulmonary bronchus is also known as the mesobronchus. A - Inspiration. B - Expiration
Source: http://www.ivis.org/advances/Anesthesia_Gleed/ludders2/chapter_frm.asp

So, it takes two respiratory cycles to move one 'packet' of air completely through the avian respiratory system (see 1, 2, 3, & 4 above). The advantage, though, is that air, high in oxygen content, always moves unidirectionally through the lungs.


Ultra-Low Oxygen Could Have Spurred Bird Breathing System -- Recent evidence suggests that oxygen levels were suppressed worldwide 175 - 275 million years ago, low enough to make breathing the air at sea level feel like respiration at high altitude. Peter Ward, a University of Washington paleontologist, theorizes that low oxygen and repeated short but substantial temperature increases because of greenhouse warming sparked two major mass-extinction events. In addition, he believes the conditions spurred the development of an unusual breathing system in Saurischian dinosaurs. Rather than having a diaphragm to force air in and out of lungs, the Saurischians had lungs attached to a series of thin-walled air sacs that appear to have functioned something like bellows to move air through the body. This breathing system, still found in today's birds, made the Saurischian dinosaurs better equipped than mammals to survive the harsh conditions in which oxygen content of air at the Earth's surface was only about half of today's 21%. "The literature always said that the reason birds had sacs was so they could breathe when they fly. But I don't know of any brontosaurus that could fly," Ward said. "However, when we considered that birds fly at altitudes where oxygen is significantly lower, we finally put it all together with the fact that the oxygen level at the surface was only 10 - 11% at the time the dinosaurs evolved. That's the same as trying to breathe at 14,000 feet. If you've ever been at 14,000 feet, you know it's not easy to breathe," he said.

Ward presented his ideas at the 2003 annual meeting of the American Geological Society  in Seattle. See: 

http://www.nature.com/nsu/031103/031103-7.html & http://www.washington.edu


Exchange of gases:

Diagram of parabronchial anatomy, gas-exchange region of the bird's lung-air-sac respiratory system. The few hundred to thousand parabronchi, one of which is fully shown here, are packed tightly into a hexagonal array. The central parabronchial lumen, through which gas flows unidirectionally during both inspiration and expiration (large arrows) is surrounded by a mantle (m) of gas-exchange tissue composed of an intertwined network of blood and air capillaries. Several air capillaries coalesce into a small manifold, i.e., the infundibulum (arrowheads), several of which in turn open into atria (*) found along the parabronchial lumen. Air moves convectively through the parabronchial lumen, while O2 diffuses radially (CO2 diffuses centrally) into the air capillary network. Blood flows centrally from the pulmonary arteries (a) located along the periphery of the parabronchi to pulmonary veins located along the parabronchial lumen, which then are drained back to the peripheral veins (v) (Modified from Duncker 1971 by Brown et al. 1997).

Top: Schematic of air flow (large arrows) and blood flow (small arrows) patterns constituting the cross-current gas-exchange mechanism operating in the avian lung. Note the serial arrangement of blood capillaries running from the periphery to the lumen of the parabronchus and the air capillaries radially departing from the parabronchial lumen. Bottom: Pressure profiles of O2 and CO2 from initial-parabronchial (PI) to end-parabronchial values (PE); and in blood capillaries from mixed venous (Pv) to arterial blood (Pa). The PO2of arterial blood is derived from a mixture of all serial air-blood capillary units and exceeds that of PE. In mammals, the PaO2 cannot exceed that of end-expiratory gas (i.e., PE) (Brown et al. 1997).

Control of Ventilation:

Ventilation and respiratory rate are regulated to meet the demands imposed by changes in metabolic activity (e.g., rest and flight) as well as other sensory inputs (e.g., heat and cold). There is likely a central respiratory control center in the avian brain, but this has not been unequivocally demonstrated. As in mammals, the central control area appears to be located in the pons and medulla oblongata with facilitation and inhibition coming from higher regions of the brain. It also appears that the chemical drive on respiratory frequency and inspiratory and expiratory duration depend on feedback from receptors in the lung as well as on extrapulmonary chemoreceptors, mechanoreceptors, and thermoreceptors (Ludders 2001).

Central chemoreceptors affect ventilation in response to changes in arterial PCO2 and hydrogen ion concentration. Peripheral extrapulmonary chemoreceptors, specifically the carotid bodies (located in the carotid arteries), are influenced by PO2 and increase their discharge rate as PO2 decreases, thus increasing ventilation; they decrease their rate of discharge as PO2 increases or PCO2 decreases. These responses are the same as those observed in mammals. Unlike mammals, birds have a unique group of peripheral receptors located in the lung called intrapulmonary chemoreceptors (IPC) that are acutely sensitive to carbon dioxide and insensitive to hypoxia. The IPC affect rate and volume of breathing on a breath-to-breath basis by acting as the afferent limb of an inspiratory-inhibitory reflex that is sensitive to the timing, rate, and extent of CO2 washout from the lung during inspiration (Ludders 2001).
 

Respiration by Avian Embryos
 

     During avian development there are three sequential stages of respiration (Tazawa 1987): prenatal (embryonic), paranatal (hatching), and postnatal (posthatching). During the prenatal stage respiratory gas exchange occurs via diffusion between the external environment and the initial gas exchanger (i.e., the area vasculosa, or the region of blood island formation and forerunner of the chorioallantoic membrane) in early embryonic life and later the vascular bed of the chorioallantois. The paranatal stage starts when the beak penetrates into the air pocket (air cell) between the inner and outer shell membranes (both internal to shell; i.e., internal pipping) this occurs during the last 2-3 days of incubation. During this stage, the lungs begin to replace the chorioallantois as the gas exchanger, yet diffusion remains the major mechanism moving gas across the shell. The postnatal stage begins when the beak penetrates the shell (i.e., external pipping) (Brown et al. 1997). 

Source: www.ece.utexas.edu/~bevans/courses/ee381k/
lectures/Tomography/milner/sld003.htm


Literature Cited:

Bernhard, W., A. Gebert, G. Vieten, G. A. Rau1, J. M. Hohlfeld, A. D. Postle, and J. Freihorst. 2001. Pulmonary surfactant in birds: coping with surface tension in a tubular lung. Am J Physiol - Regulatory Integrative and Comparative Physiology 281: R327-R337.

Brown, R.E., J. D. Brain, and N. Wang. 1997. The Avian Respiratory System: A Unique Model for Studies of Respiratory Toxicosis and for Monitoring Air Quality. Environ Health Perspectives 105:188-200.

Daniels, C.B., O. V. Lopatko, and S. Orgeig. 1998. Evolution of surface activity related functions of vertebrate pulmonary surfactant. Clin Exp Pharmacol Physiol. 25:716-721.

Duncker, H.-R. 1971. The lung air sac system of birds. Advances in Anatomy, Embryology, and Cell Biology 45: 1171.

Ludders, J.W. 2001. Inhaled Anesthesia for Birds. In:  Recent Advances in Veterinary Anesthesia and Analgesia: Companion Animals (R. D. Gleed and J. W. Ludders, eds.). International Veterinary Information Service, Ithaca, NY.  (www.ivis.org/advances/Anesthesia_Gleed/ludders2/chapter_frm.asp)

Maina, J.N. 1989. The morphometry of the avian lung. Pp. 307-368 in Form and Function in Birds (A.S. King and J. McLelland, eds.). Academic Press, London.

Maina, J. N. and C. Nathaniel. 2001. A qualitative and quantitative study of the lung of an ostrich, Struthio camelus. Journal of Experimental Biology 204: 2313-2330.

Powell, F.L. 2000. Respiration. Pp. 233-264 in Avian Physiology, fifth edition (G. Causey Whittow, ed.). Academic Press, New York, NY.

Tazawa, H. 1987. Embryonic respiration. Pp. 3 - 24 in Bird respiration, vol. 2 (T.J. Seller, ed.). CRC Press, Boca Raton, FL.

Wedel, M.J. 2003. Vertebral pneumaticity, air sacs, and the physiology of sauropod dinosaurs. Paleobiology 29: 243255.

Welty, J.C. and L. Baptista. 1988. The life of birds, fourth edition. Saunders College Publishing, New York, NY.


Useful links:

How Animals Work: Avian Respiratory Dynamics Animation

Mechanics of Respiration in Birds


More lecture notes:

Energy Balance & Thermoregulation


Back to BIO 554/754 Syllabus