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Cardiovascular Adjustments to Diving in Mammals and Birds

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Historical Landmarks
2 The Basic Problem for Diving Animals
3 Decreased Sensitivity to Asphyxia
4 Oxygen Stores and Principles of Their Utilization
5 Cardiovascular Adjustments During and After Diving
5.1 General Aspects
5.2 Cardiac Output
5.3 Regional Circulation During Diving and on Emersion
6 Morphological Specializations in Vascular Beds of Diving Animals
6.1 Arteries
6.2 Shunts
6.3 Veins
7 Metabolic Consequences
8 Central Integration of Cardiovascular Responses
8.1 Medullary Reflex Mechanisms
8.2 Suprabulbar Influences
8.3 Other Reflex Influences
9 Diving Responses in Humans and Some Clinical Applications
9.1 Responses in Humans
9.2 Clinical Applications
Figure 1. Figure 1.

Basic problem facing air‐breathing animal when submerged: constantly decreasing arterial content of oxygen (upper graph) and constantly increasing arterial content of carbon dioxide (lower graph). Abscissa: duration of dive (min).

Prom Scholander
Figure 2. Figure 2.

Total estimated oxygen stores of humans, harbor seal, ribbon seal, fur seal, sea lion, and sea otter.

From Hill . Data for marine mammals from Lenfant et al.
Figure 3. Figure 3.

Experiment showing variation in arterial lactate (LA) in a seal before, during, and after 15‐min dive. Also shown are concomitant variations in arterial content of oxygen and carbon dioxide. Two upper curves indicate respiratory activity.

From Scholander
Figure 4. Figure 4.

Blood pressure record from femoral artery of a harbor seal during an 8‐min dive, obtained with Harvard rubber membrane manometer.

From Irving et al.
Figure 5. Figure 5.

Changes in cardiac output before, during, and after 90‐s dive in the duck. Included are data on heart rate and stroke volume. Note 20‐fold decrease in cardiac output during submersion and 50‐fold increase in cardiac output on emersion.

From Folkow et al.
Figure 6. Figure 6.

Heart rate responses of a harbor seal during a trained (unrestrained) pool dive (A) compared with response of same seal during (restrained) forced dive (B). Note immediate drop in heart rate in both cases and extreme bradycardia in the latter.

From Eisner
Figure 7. Figure 7.

Percent change in organ blood flow (ml min−1 g−1) during diving in the Weddell seal. Asterisks, probability (P <0.05) dive value differs from predive control.

From Zapol et al.
Figure 8. Figure 8.

Tissue blood flow at 4 levels of harbor seal brain at 2, 5, and 10 min of submersion, as well as after 40 s of recovery after 10‐min dive, in percent of predive (control) values determined by use of radioactively labeled microspheres. Above columns are number of samples. (From A. S. Blix, R. Eisner, and J. Kjekshus, unpublished observations.)

Figure 9. Figure 9.

Mean blood flow and instantaneous blood velocity in left circumflex coronary artery in the harbor seal during a 5‐min dive. Note that flow abruptly diminishes immediately after beginning of dive and is transiently restored at 30‐ to 45‐s intervals. Response suggests rhythmic neurogenic spasmlike coronary vasoconstrictions modulated by myocardial metabolic demand. (From R. Eisner, A. S. Blix, R. Millard, F. Kjekshus, and D. Franklin, unpublished observations.)

Figure 10. Figure 10.

Blood flow in abdominal aorta and renal artery of the harbor seal at beginning and end of an 8‐min dive (arrows). Note virtual cessation of flow during submersion. Time marks in seconds.

From Eisner et al. . Copyright 1966 by the American Association for the Advancement of Science
Figure 11. Figure 11.

Blood flow in kidney and skeletal muscle of the diving coypu compared with that in the cat in response to increasing rates of direct sympathetic vasoconstrictor fiber stimulation. Note extreme vasoconstriction in diver, even at low discharge rates.

Adapted from Folkow et al.
Figure 12. Figure 12.

A: angiograms of peripheral (abdominal) arteries of a harbor seal. During breathing in air at surface position, well‐filled arteries of flanks (thin arrow) and hind flippers (arrowhead) are seen. B: during diving same arteries in same animal are profoundly constricted and consequently poorly filled with contrast medium. Also shown is bladder (marked B).

From Bron et al. . Copyright 1966 by the American Association for the Advancement of Science
Figure 13. Figure 13.

Plastic cast of venous system of the harp seal, head (not shown) to the right, prone position, heart marked H. Arrows indicate direction of venous blood flow while breathing in air (top) and during diving (bottom). Note shift in flow direction in extradural intravertebral vein in response to diving.

From Ronald et al. , with permission from Functional Anatomy of Marine Mammals, edited by R. J. Harrison. Copyright by Academic Press, Inc. (London) Ltd
Figure 14. Figure 14.

Changes in arterial lactate concentration (arterial) together with concomitant changes in coronary arteriovenous difference (A‐CS) for lactate during and after 16‐min dives (indicated by waveform line) in the harbor seal. Note progressively increasing release of lactate from heart during dive and shift to myocardial uptake of lactate immediately after emergence (recovery).

From Kjekshus, Blix, et al.
Figure 15. Figure 15.

Initial cardiovascular responses to diving in the restrained duck. A: muscle blood flow and heart rate in normal predive (C), dive (D), and recovery (R) situations, left, and same parameters before (C), during (D), and after (R) a dive of similar duration but without chemoreceptor activation, as a result of maintained oxygenation of blood throughout dive, right. B: blood pressure record of a duck in normal (asphyxial) dive situation (upper graph) and in nonasphyxic dive (lower graph). Chemoreceptors in latter are not stimulated due to maintained oxygenation of blood, and initial, immediate response is not further accentuated.

A from Blix et al. ; B from Blix
Figure 16. Figure 16.

Effects of excitation of carotid body chemoreceptors alone (CB, filled blocks) and during electrical stimulation of central cut end of superior laryngeal nerve (SLN + CB, cross‐hatched blocks) on pulse interval and respiratory minute volume in the harbor seal. Open blocks (SLN), stimulation of the superior laryngeal nerve alone; filled circles (C), control values.

From Eisner et al.
Figure 17. Figure 17.

Effect of diving on heart rate in the duck. Left, original oscilloscope record; right, plot of the heart rate. Dive commenced at 0 time. A: control; intact duck. B: record obtained 1 h after surgical denervation of arterial chemoreceptors. C: record obtained 6 days later.

From Jones and Purves
Figure 18. Figure 18.

Effect of predive Stimulation of chemoreceptors on development of diving responses in the duck. A: normal blood pressure record obtained at sea level. B: blood pressure response obtained in dive commenced at simulated altitude of 6,000 m, resulting in predive arterial partial pressure of O2 of 33 mmHg (4.4 kPa) without an increase in arterial partial pressure of CO2. Note nearly immediate development of intense bradycardia response when chemoreceptors are stimulated prior to dive (B) as compared with normal dive situation (A).

From Blix and Berg
Figure 19. Figure 19.

Maternal and fetal heart rates in the Weddell seal during 20‐min simulated dives and recovery.

From Liggins et al.
Figure 20. Figure 20.

Predive anticipatory bradycardia and presurfacing anticipatory tachycardia in the harp seal, demonstrating powerful suprabulbar influences on development and maintenance of diving responses.

From Casson and Ronald . Reprinted with permission from Pergamon Press, Ltd
Figure 21. Figure 21.

Diagram illustrating integration of reflexes involved in initiation and development of diving responses in mammals and birds. Responses are evoked by stimulation of telereceptors and/or trigeminal and glossopharyngeal receptors. In some cases (notably in very short dives) initial cardiovascular responses can be occluded by corticohypothalamic influences. Normally, however, they are stimulated, albeit to a different extent in different species, immediately on cessation of breathing. In seals initial responses are usually profound, whereas in ducks they are more modest. In prolonged dives arterial chemoreceptors are activated and initiate secondary reinforcement of initial responses. In ducks chemoreceptors are required for full development of responses, whereas in seals they merely ensure that initial responses are maintained. Thus the cardiovascular system of diving animals is converted by intense peripheral vasoconstriction so that the huge blood oxygen store is delivered only to heart, brain, adrenals, and pregnant uterus. In this situation other tissues have to rely on local stores of oxygen and/or anaerobic metabolism. This dramatic redistribution of blood takes place at a largely maintained arterial blood pressure due to a well‐balanced reduction of cardiac output. Arterial baroreceptors together with cardiac volume receptors are instrumental in execution of this balance.



Figure 1.

Basic problem facing air‐breathing animal when submerged: constantly decreasing arterial content of oxygen (upper graph) and constantly increasing arterial content of carbon dioxide (lower graph). Abscissa: duration of dive (min).

Prom Scholander


Figure 2.

Total estimated oxygen stores of humans, harbor seal, ribbon seal, fur seal, sea lion, and sea otter.

From Hill . Data for marine mammals from Lenfant et al.


Figure 3.

Experiment showing variation in arterial lactate (LA) in a seal before, during, and after 15‐min dive. Also shown are concomitant variations in arterial content of oxygen and carbon dioxide. Two upper curves indicate respiratory activity.

From Scholander


Figure 4.

Blood pressure record from femoral artery of a harbor seal during an 8‐min dive, obtained with Harvard rubber membrane manometer.

From Irving et al.


Figure 5.

Changes in cardiac output before, during, and after 90‐s dive in the duck. Included are data on heart rate and stroke volume. Note 20‐fold decrease in cardiac output during submersion and 50‐fold increase in cardiac output on emersion.

From Folkow et al.


Figure 6.

Heart rate responses of a harbor seal during a trained (unrestrained) pool dive (A) compared with response of same seal during (restrained) forced dive (B). Note immediate drop in heart rate in both cases and extreme bradycardia in the latter.

From Eisner


Figure 7.

Percent change in organ blood flow (ml min−1 g−1) during diving in the Weddell seal. Asterisks, probability (P <0.05) dive value differs from predive control.

From Zapol et al.


Figure 8.

Tissue blood flow at 4 levels of harbor seal brain at 2, 5, and 10 min of submersion, as well as after 40 s of recovery after 10‐min dive, in percent of predive (control) values determined by use of radioactively labeled microspheres. Above columns are number of samples. (From A. S. Blix, R. Eisner, and J. Kjekshus, unpublished observations.)



Figure 9.

Mean blood flow and instantaneous blood velocity in left circumflex coronary artery in the harbor seal during a 5‐min dive. Note that flow abruptly diminishes immediately after beginning of dive and is transiently restored at 30‐ to 45‐s intervals. Response suggests rhythmic neurogenic spasmlike coronary vasoconstrictions modulated by myocardial metabolic demand. (From R. Eisner, A. S. Blix, R. Millard, F. Kjekshus, and D. Franklin, unpublished observations.)



Figure 10.

Blood flow in abdominal aorta and renal artery of the harbor seal at beginning and end of an 8‐min dive (arrows). Note virtual cessation of flow during submersion. Time marks in seconds.

From Eisner et al. . Copyright 1966 by the American Association for the Advancement of Science


Figure 11.

Blood flow in kidney and skeletal muscle of the diving coypu compared with that in the cat in response to increasing rates of direct sympathetic vasoconstrictor fiber stimulation. Note extreme vasoconstriction in diver, even at low discharge rates.

Adapted from Folkow et al.


Figure 12.

A: angiograms of peripheral (abdominal) arteries of a harbor seal. During breathing in air at surface position, well‐filled arteries of flanks (thin arrow) and hind flippers (arrowhead) are seen. B: during diving same arteries in same animal are profoundly constricted and consequently poorly filled with contrast medium. Also shown is bladder (marked B).

From Bron et al. . Copyright 1966 by the American Association for the Advancement of Science


Figure 13.

Plastic cast of venous system of the harp seal, head (not shown) to the right, prone position, heart marked H. Arrows indicate direction of venous blood flow while breathing in air (top) and during diving (bottom). Note shift in flow direction in extradural intravertebral vein in response to diving.

From Ronald et al. , with permission from Functional Anatomy of Marine Mammals, edited by R. J. Harrison. Copyright by Academic Press, Inc. (London) Ltd


Figure 14.

Changes in arterial lactate concentration (arterial) together with concomitant changes in coronary arteriovenous difference (A‐CS) for lactate during and after 16‐min dives (indicated by waveform line) in the harbor seal. Note progressively increasing release of lactate from heart during dive and shift to myocardial uptake of lactate immediately after emergence (recovery).

From Kjekshus, Blix, et al.


Figure 15.

Initial cardiovascular responses to diving in the restrained duck. A: muscle blood flow and heart rate in normal predive (C), dive (D), and recovery (R) situations, left, and same parameters before (C), during (D), and after (R) a dive of similar duration but without chemoreceptor activation, as a result of maintained oxygenation of blood throughout dive, right. B: blood pressure record of a duck in normal (asphyxial) dive situation (upper graph) and in nonasphyxic dive (lower graph). Chemoreceptors in latter are not stimulated due to maintained oxygenation of blood, and initial, immediate response is not further accentuated.

A from Blix et al. ; B from Blix


Figure 16.

Effects of excitation of carotid body chemoreceptors alone (CB, filled blocks) and during electrical stimulation of central cut end of superior laryngeal nerve (SLN + CB, cross‐hatched blocks) on pulse interval and respiratory minute volume in the harbor seal. Open blocks (SLN), stimulation of the superior laryngeal nerve alone; filled circles (C), control values.

From Eisner et al.


Figure 17.

Effect of diving on heart rate in the duck. Left, original oscilloscope record; right, plot of the heart rate. Dive commenced at 0 time. A: control; intact duck. B: record obtained 1 h after surgical denervation of arterial chemoreceptors. C: record obtained 6 days later.

From Jones and Purves


Figure 18.

Effect of predive Stimulation of chemoreceptors on development of diving responses in the duck. A: normal blood pressure record obtained at sea level. B: blood pressure response obtained in dive commenced at simulated altitude of 6,000 m, resulting in predive arterial partial pressure of O2 of 33 mmHg (4.4 kPa) without an increase in arterial partial pressure of CO2. Note nearly immediate development of intense bradycardia response when chemoreceptors are stimulated prior to dive (B) as compared with normal dive situation (A).

From Blix and Berg


Figure 19.

Maternal and fetal heart rates in the Weddell seal during 20‐min simulated dives and recovery.

From Liggins et al.


Figure 20.

Predive anticipatory bradycardia and presurfacing anticipatory tachycardia in the harp seal, demonstrating powerful suprabulbar influences on development and maintenance of diving responses.

From Casson and Ronald . Reprinted with permission from Pergamon Press, Ltd


Figure 21.

Diagram illustrating integration of reflexes involved in initiation and development of diving responses in mammals and birds. Responses are evoked by stimulation of telereceptors and/or trigeminal and glossopharyngeal receptors. In some cases (notably in very short dives) initial cardiovascular responses can be occluded by corticohypothalamic influences. Normally, however, they are stimulated, albeit to a different extent in different species, immediately on cessation of breathing. In seals initial responses are usually profound, whereas in ducks they are more modest. In prolonged dives arterial chemoreceptors are activated and initiate secondary reinforcement of initial responses. In ducks chemoreceptors are required for full development of responses, whereas in seals they merely ensure that initial responses are maintained. Thus the cardiovascular system of diving animals is converted by intense peripheral vasoconstriction so that the huge blood oxygen store is delivered only to heart, brain, adrenals, and pregnant uterus. In this situation other tissues have to rely on local stores of oxygen and/or anaerobic metabolism. This dramatic redistribution of blood takes place at a largely maintained arterial blood pressure due to a well‐balanced reduction of cardiac output. Arterial baroreceptors together with cardiac volume receptors are instrumental in execution of this balance.

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Arnoldus Schytte Blix, Björn Folkow. Cardiovascular Adjustments to Diving in Mammals and Birds. Compr Physiol 2011, Supplement 8: Handbook of Physiology, The Cardiovascular System, Peripheral Circulation and Organ Blood Flow: 917-945. First published in print 1983. doi: 10.1002/cphy.cp020325