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Control of Breathing in Ectothermic Vertebrates

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Abstract

The sections in this article are:

1 Breathing Patterns
1.1 Rhythmic Breathing in Unimodal Aquatic Exchange
1.2 Ram Ventilation in Unimodal Aquatic Exchange
1.3 Periodic Breathing in Bimodal Exchange
1.4 Periodic Breathing in Unimodal Aerial Exchange
2 Breathing and Metabolism
3 Rhythmic Breathing: Control in Unimodal Aquatic Systems
3.1 Central Pattern Generation
3.2 Responses to Mechanoreceptor Input
3.3 Responses to Chemoreceptor Input
4 Periodic Breathing: Control in Bimodal and Unimodal Aerial Systems
4.1 Pattern Generation
4.2 Role of Peripheral Input in Pattern Generation
4.3 Responses to Chemoreceptor Input
5 Conclusion
Figure 1. Figure 1.

Relationships between partial pressures of O2 (Po2) and CO2 (Pco2) in aquatic and aerial convective systems. Dashed lines, respiratory exchange ratio (R) lines showing possible combinations of Po2 and Pco2 in unimodal air or water exchange systems working in steady state with continuous ventilation and a metabolic respiratory quotient (RQ) of 0.85. Slopes of air and water R lines differ becauseand βco2 > βo2, in water, whereas βco2 = βo2 in air [where is rate of gas uptake or output, capacitance coefficient (β) is increment of concentration per unit increment of partial pressure (β = C/P), and is flow rate of external medium]. Actual Po2 and Pco2 values in alveolar gas or opercular water depend on relationship between and . Points on air and water lines, values for mammals and trout (17°C) breathing at rest under normal conditions. Solid lines, fluctuations in alveolar gas composition during intermittent ventilation in unimodal [tortoise 71] and bimodal [clawed toad 470] animals. The Pco1 − Po2 relationships in bimodal breathers are impossible to derive theoretically. Shaded area, general range. Air exchange ratio is less than and water exchange ratio is greater than metabolic RQ in bimodal animals.

Figure 2. Figure 2.

Rhythmic breathing patterns in fish. A: movements of operculum and pressures measured in buccal and opercular cavities of roach (Leuciscus rutilus). Differential pressure between buccal and opercular cavities drives water across gill epithelium (G. Shelton and G. M. Hughes, unpublished observations). B: pressures measured in orobranchial (≡ buccal) cavity and 5th parabranchial cavity (within gill slit but outside gills) of dogfish (Scyliorhinus canicula). Differential pressure relationships are very similar to those of the teleost.

From Hughes 244
Figure 3. Figure 3.

Development of arrhythmic breathing patterns in fish. A: effect of differential levels of hypoxia on breathing movements in carp. Pio2, partial pressure of inspired O2.

From Lomholt and Johansen 351. B: effect of different swimming velocities on breathing movements in bluefish. From Roberts 441
Figure 4. Figure 4.

Breathing patterns in fish with lungs or air bladders. A: pressures measured in buccal and opercular cavities of Protopterus aethiopicus. Markers beneath opercular pressure trace indicate air‐breathing movements. Between air breaths, gill‐ventilating movements vary in frequency and amplitude. B: pressures measured in air bladder of Hoplerythrinus unitaeniatus. Note that pressure is always above atmospheric and that more than 1 buccal oscillation occurs in each ventilating cycle. C: pressures measured in air bladder of Arapaima gigas. Note that each ventilation cycle consists of a single pressure change that falls briefly below atmospheric; it is suggested that the bladder is ventilated by an aspiration pump.

A from McMahon 368; B and C from Farrell and Randall 150
Figure 5. Figure 5.

Two cycles of lung ventilation in clawed toad (Xenopus laevis). Pressures are measured in buccal cavity (BP) and the lung (LP). Flow at nares (F) is measured by blow‐hole pneumotachograph. Note that lung pressures are always above atmospheric.

From Brett and Shelton 62
Figure 6. Figure 6.

Breathing in bullfrog Rana catesbeiana Diagrams show main features of jet‐stream hypothesis and argon‐washout experiment. Gas leaves the lungs (L) via nares in coherent stream that restricts mixing with fresh air in buccal cavity (B). Nostrils then close and fresh air is pumped from buccal cavity into the lung. Washout experiment shows changes of argon concentration in gas taken continuously from sample tube (S) in rubber face mask covering top of head and nostrils. During buccal ventilations (unlabelled cycles), argon concentration of S falls as argon‐O2 mixture in experimental chamber is replaced with air (troughs of oscillations) and argon concentration in B also falls (peaks). During lung ventilations (V), the rapid rise in argon concentration followed by a more gradual decline is evidence for pocket of gas in B being bypassed by gas from L.

Adapted from Gans et al. 165. Copyright 1969 by the American Association for the Advancement of Science
Figure 7. Figure 7.

Breathing patterns in Rana pipiens are shown by pressures measured in buccal cavity and lung. Buccal oscillations, lung ventilations, and 5 sequences of lung inflation can be seen.

From West and Jones 528
Figure 8. Figure 8.

Breathing patterns in Xenopus laevis at 25°C recorded by pneumotachograph on blow hole at which animals surfaced to breathe. A and B: discrete breathing bursts followed by dives. Bursts change into more prolonged surface visits at end of B. C: taken 24 h later from same animal as B, shows breathing bout during which animal remained at surface, with its nostrils in air, ventilating its lungs at irregular intervals. D: prolonged dives interrupted by single ventilations. This behavior is seen when animal is disturbed and is caused particularly by threat at surface. (G. Shelton, unpublished observations.)

Figure 9. Figure 9.

Breathing movements in Caiman sclerops (A) and Alligator mississippiensis (B) as recorded by impedance pneumography, showing movements of thoracic wall, and body plethysmography, showing changes in total body volume. Inspiration causes upward deflection in all records. There is no change in body volume at end of inspiration even though impedance traces show inward movement of thoracic wall. A breathing cycle is a simple diphasic process.

From Naifeh et al. 384
Figure 10. Figure 10.

Variations in breathing patterns found in Atlantic loggerhead turtle [Caretta caretta (A)], Tokay lizard [Gekko gecko, (B)], and western painted turtle [Chrysemys picta (C)]. Predominantly, Caretta takes single breaths, Gekko breathe in bursts containing a few breaths, and bursts in Chrysemys contain many breaths. At different times all 3 species may exhibit arrhythmic breathing patterns (line 1) or relatively rhythmic, though periodic, patterns (line 2). Lizard and painted turtle may also show continuous breathing (line 3) when stressed. (W. K. Milsom, unpublished observations.)

Figure 11. Figure 11.

Timing of muscular activity during respiratory cycle of trout. Cycle is divided into 18 equal time intervals, and height of block within each interval indicates number of times an active electromyogram was observed. Muscles were usually active during either adduction or abduction phases. Only sternohyoideus (sternohyoid was observed to be active at all times during cycle. Add. mand., adductor mandibulae; Add. a.p.o., adductor arcus palatini et operculi; Lev. hyom., levator hyomandibulae; Pro. hyom., protractor hyoidei; Dil. oper., dilator operculi.

From Bamford 21
Figure 12. Figure 12.

Projection onto dorsal surface of location of respiratory neurons within brain stem of teleosts. Left: main sites (in black) located below paired optic lobes and in medulla below cerebellum and facial lobe. Right: main interconnections (arrows). Dashed lines (T), area defined as essential for normal rhythmic breathing by transection experiments. III m, oculomotor nucleus; t, tegmental respiratory neurons; Rf, reticular formation; V m, trigeminal motor nucleus; V d, descending trigeminal nucleus; VII m, facial motor nucleus; IX m, glossopharyngeal motor nucleus; VII i, intermediate facial nucleus; X m, vagal motor nucleus; P, muscle proprioceptive input; X, vagal sensory input.

Adapted from Ballintijn 14
Figure 13. Figure 13.

Respiratory interneurons and motoneurons in carp. Cross‐correlation and signal‐averaging techniques establish temporal relationships between medullary neuron discharge and specific components in respiratory muscle electromyograms (EMGs). Top: A and B, recordings of EMG discharges from 1, adductor mandibulae (Add. mand.); 2, levator hyomandibulae (Lev. hyom.); 3, dilator operculi (Dil. oper.); and of activity from 4, medulla showing 3 distinct respiratory neurons. High‐amplitude neuron (b) could be correlated with component occurring after 4.3‐ms delay in Add. mand. and was therefore presumed to be a motoneuron. I, averaged response in muscle, with neuron b as trigger. Low‐amplitude neuron (a) showed no such temporal correlation and was not an Add. mand. motoneuron. After 7 min, neuron b stopped firing and neuron c became active in opposite breathing phase. II and III, averaged responses showing that c was not a motoneuron of Lev. hyom. or Dil. oper. Bottom: 2 experiments. IV, good correlation with short delay (i) was found between a medullary neuron and averaged activity from Lev. hyom. After slight electrode displacement, further correlation was found with long delay (ii) between another neuron and the same muscle. First neuron was presumed to be a motoneuron and the second an interneuron. V, good correlation with averaged activity from EMG of Dil. oper., again with a long delay (iii), suggesting that trigger must be an interneuron.

Adapted from Ballintijn and Alink 15
Figure 14. Figure 14.

Relationship between gill ventilation and partial pressure of O2 of inhaled water (Pio2) in 4 teleosts: juvenile catfish Ictalurus punctatus 177, carp Cyprinus carpio 351, sturgeon Acipenser transmontanus 70, and rainbow trout Salmo gairdneri 428. Four lower panels, contribution of breathing rate (dotted lines) and stroke volume (solid lines) to change in gill ventilation. In normoxic carp, breathing is arrhythmic and large increase in rate in hypoxia is due to breathing becoming continuous 351.

Figure 15. Figure 15.

Time relationships between hypoxic stimulus and responses seen in teleost fish. A: time course in seconds of fall in Po2 in water from regions indicated (w, prebranchial water; I, buccal water; E, exhaled water) and of appearance of cardioventilatory response (R) after turning tap to admit hypoxic water.

From Eclancher 135. B: increased breathing frequency and ventilation pressures recorded in buccal cavity of trout in response to rapidly induced hypoxia. Electrode in water near animal's mouth signals first appearance of decrease in Pio2. From Bamford 21
Figure 16. Figure 16.

Relationship between water flow over gills and arterial O2 content of dorsal aortic blood in Salmo gairdneri. Horizontal and vertical bars indicate ±SEM. Number by each point, corresponding Pao2 in kPa. Arterial O2 content was changed by bubbling n2, CO2, and/or O2 into water containing fish or by making fish anemic by withdrawing red blood cells.

Adapted from Smith and Jones 479 and Randall 420
Figure 17. Figure 17.

Effects of NaCN injection on teleost chemoreceptors. Top: traces show effects of injecting 6 μg NaCN into ventral aorta of 300‐g trout on electromyogram (EMG) from an opercular muscle, integrated EMG (EMGi) and electrocardiogram (ECG). Top trace, 1‐s time marker. There was 6.2‐s latent period from start of injection, but by 10 s from start, ventilatory activity increased 3 times. Start of ventilatory response (center arrow) also corresponded with onset of hypoxic bradycardia. Bottom: comparison of effects of injecting 6 μg NaCN intravascularly into 350‐g trout (at 13°C) exposed to 3 levels of partial pressure of O2 in water (Pwo2). Stimulation of ventilatory activity (shown as EMGi in arbitrary units) is greatly reduced by simultaneous hyperoxia (Pwo2 = 210 Torr and 540 Torr). Each bar of histogram of EMGi represents 10 cycles of ventilation.

From Eclancher and Dejours 136
Figure 18. Figure 18.

Fluctuations in Pao2 and Paco2 and femoral artery Pao2 and Paco2 during intermittent breathing in unrestrained freely diving turtle Pseudemys scripta. Shaded vertical bars, brief bouts of surfacing and lung ventilation.

From Burggren and Shelton 71
Figure 19. Figure 19.

Control of breath duration and tidal volume (Vt) in turtles. Top: mean inspiratory duration (Ti) as function of inspired CO2 concentration (Fico2) in intact (open columns) and bilaterally vagotomized (shaded columns) turtles (Chrysemys picta) (W. K. Milsom, unpublished observations). Bottom: relationship between inspiratory duration and reciprocal of inspiratory flow rate (Vt · Ti−1 in ml · s−1) in intact (open circles) and vagotomized (filled circles) turtles breathing air. Regression equation describes correlation for intact animals. Slope of line equals Vt. No significant correlation exists after vagotomy.

From Milsom and Jones 375
Figure 20. Figure 20.

Effects of environmental O2 and CO2 on ventilation in 3 facultative (Erythrinus, Piabucina, and Umbra) and 1 obligate (Trichogaster) air‐breathing fish. A: relationships between aquatic Po2 and Pco2 and type of breathing shown by single specimen of Erythrinus sp. at 26°C. Suggested reasons for different breathing behaviors are: high Pco2 causes opercular flaps to close (A); low Po2 causes O2 loss to water if gills are ventilated (B); Po2 in water is inadequate to saturate blood with O2 (C); Pco2 stimulates air breathing (D); aquatic breathing is sufficient for requirements (E); gill ventilation is insufficient to saturate blood (F); and low Pco2 is insufficient to stimulate gill ventilation (G).

From Willmer 539. B: combined effects of aquatic Po2 and Pco2 on air‐breathing rate of Piabucina festae. [From Graham et al. 193.] C: relationship between air convection requirement and ventilation of suprabranchial chamber () with air in Trichogaster trichopterus at 27°C. Labeled areas, locations of data points from 5 animals in hypoxic water (Po2 = 60 Torr), hypoxic gas (Po2 = 60 Torr), and hypercapnic water (Pco2 = 21 Torr); all treatments caused significantly higher than control values (breathing air and air‐saturated water). Though total O2 consumption was not changed significantly, hypoxic and hypercapnic water increased and hypoxic gas decreased O2 uptake from suprabranchial chamber as compared with control values, thus affecting air convection requirement. [From Burggren 66.] D: effect of progressive aquatic hypoxia (25°C) on frequencies of air and water breathing in Umbra limi. Lines, averages of data drawn from 10 fish. From Gee 173


Figure 1.

Relationships between partial pressures of O2 (Po2) and CO2 (Pco2) in aquatic and aerial convective systems. Dashed lines, respiratory exchange ratio (R) lines showing possible combinations of Po2 and Pco2 in unimodal air or water exchange systems working in steady state with continuous ventilation and a metabolic respiratory quotient (RQ) of 0.85. Slopes of air and water R lines differ becauseand βco2 > βo2, in water, whereas βco2 = βo2 in air [where is rate of gas uptake or output, capacitance coefficient (β) is increment of concentration per unit increment of partial pressure (β = C/P), and is flow rate of external medium]. Actual Po2 and Pco2 values in alveolar gas or opercular water depend on relationship between and . Points on air and water lines, values for mammals and trout (17°C) breathing at rest under normal conditions. Solid lines, fluctuations in alveolar gas composition during intermittent ventilation in unimodal [tortoise 71] and bimodal [clawed toad 470] animals. The Pco1 − Po2 relationships in bimodal breathers are impossible to derive theoretically. Shaded area, general range. Air exchange ratio is less than and water exchange ratio is greater than metabolic RQ in bimodal animals.



Figure 2.

Rhythmic breathing patterns in fish. A: movements of operculum and pressures measured in buccal and opercular cavities of roach (Leuciscus rutilus). Differential pressure between buccal and opercular cavities drives water across gill epithelium (G. Shelton and G. M. Hughes, unpublished observations). B: pressures measured in orobranchial (≡ buccal) cavity and 5th parabranchial cavity (within gill slit but outside gills) of dogfish (Scyliorhinus canicula). Differential pressure relationships are very similar to those of the teleost.

From Hughes 244


Figure 3.

Development of arrhythmic breathing patterns in fish. A: effect of differential levels of hypoxia on breathing movements in carp. Pio2, partial pressure of inspired O2.

From Lomholt and Johansen 351. B: effect of different swimming velocities on breathing movements in bluefish. From Roberts 441


Figure 4.

Breathing patterns in fish with lungs or air bladders. A: pressures measured in buccal and opercular cavities of Protopterus aethiopicus. Markers beneath opercular pressure trace indicate air‐breathing movements. Between air breaths, gill‐ventilating movements vary in frequency and amplitude. B: pressures measured in air bladder of Hoplerythrinus unitaeniatus. Note that pressure is always above atmospheric and that more than 1 buccal oscillation occurs in each ventilating cycle. C: pressures measured in air bladder of Arapaima gigas. Note that each ventilation cycle consists of a single pressure change that falls briefly below atmospheric; it is suggested that the bladder is ventilated by an aspiration pump.

A from McMahon 368; B and C from Farrell and Randall 150


Figure 5.

Two cycles of lung ventilation in clawed toad (Xenopus laevis). Pressures are measured in buccal cavity (BP) and the lung (LP). Flow at nares (F) is measured by blow‐hole pneumotachograph. Note that lung pressures are always above atmospheric.

From Brett and Shelton 62


Figure 6.

Breathing in bullfrog Rana catesbeiana Diagrams show main features of jet‐stream hypothesis and argon‐washout experiment. Gas leaves the lungs (L) via nares in coherent stream that restricts mixing with fresh air in buccal cavity (B). Nostrils then close and fresh air is pumped from buccal cavity into the lung. Washout experiment shows changes of argon concentration in gas taken continuously from sample tube (S) in rubber face mask covering top of head and nostrils. During buccal ventilations (unlabelled cycles), argon concentration of S falls as argon‐O2 mixture in experimental chamber is replaced with air (troughs of oscillations) and argon concentration in B also falls (peaks). During lung ventilations (V), the rapid rise in argon concentration followed by a more gradual decline is evidence for pocket of gas in B being bypassed by gas from L.

Adapted from Gans et al. 165. Copyright 1969 by the American Association for the Advancement of Science


Figure 7.

Breathing patterns in Rana pipiens are shown by pressures measured in buccal cavity and lung. Buccal oscillations, lung ventilations, and 5 sequences of lung inflation can be seen.

From West and Jones 528


Figure 8.

Breathing patterns in Xenopus laevis at 25°C recorded by pneumotachograph on blow hole at which animals surfaced to breathe. A and B: discrete breathing bursts followed by dives. Bursts change into more prolonged surface visits at end of B. C: taken 24 h later from same animal as B, shows breathing bout during which animal remained at surface, with its nostrils in air, ventilating its lungs at irregular intervals. D: prolonged dives interrupted by single ventilations. This behavior is seen when animal is disturbed and is caused particularly by threat at surface. (G. Shelton, unpublished observations.)



Figure 9.

Breathing movements in Caiman sclerops (A) and Alligator mississippiensis (B) as recorded by impedance pneumography, showing movements of thoracic wall, and body plethysmography, showing changes in total body volume. Inspiration causes upward deflection in all records. There is no change in body volume at end of inspiration even though impedance traces show inward movement of thoracic wall. A breathing cycle is a simple diphasic process.

From Naifeh et al. 384


Figure 10.

Variations in breathing patterns found in Atlantic loggerhead turtle [Caretta caretta (A)], Tokay lizard [Gekko gecko, (B)], and western painted turtle [Chrysemys picta (C)]. Predominantly, Caretta takes single breaths, Gekko breathe in bursts containing a few breaths, and bursts in Chrysemys contain many breaths. At different times all 3 species may exhibit arrhythmic breathing patterns (line 1) or relatively rhythmic, though periodic, patterns (line 2). Lizard and painted turtle may also show continuous breathing (line 3) when stressed. (W. K. Milsom, unpublished observations.)



Figure 11.

Timing of muscular activity during respiratory cycle of trout. Cycle is divided into 18 equal time intervals, and height of block within each interval indicates number of times an active electromyogram was observed. Muscles were usually active during either adduction or abduction phases. Only sternohyoideus (sternohyoid was observed to be active at all times during cycle. Add. mand., adductor mandibulae; Add. a.p.o., adductor arcus palatini et operculi; Lev. hyom., levator hyomandibulae; Pro. hyom., protractor hyoidei; Dil. oper., dilator operculi.

From Bamford 21


Figure 12.

Projection onto dorsal surface of location of respiratory neurons within brain stem of teleosts. Left: main sites (in black) located below paired optic lobes and in medulla below cerebellum and facial lobe. Right: main interconnections (arrows). Dashed lines (T), area defined as essential for normal rhythmic breathing by transection experiments. III m, oculomotor nucleus; t, tegmental respiratory neurons; Rf, reticular formation; V m, trigeminal motor nucleus; V d, descending trigeminal nucleus; VII m, facial motor nucleus; IX m, glossopharyngeal motor nucleus; VII i, intermediate facial nucleus; X m, vagal motor nucleus; P, muscle proprioceptive input; X, vagal sensory input.

Adapted from Ballintijn 14


Figure 13.

Respiratory interneurons and motoneurons in carp. Cross‐correlation and signal‐averaging techniques establish temporal relationships between medullary neuron discharge and specific components in respiratory muscle electromyograms (EMGs). Top: A and B, recordings of EMG discharges from 1, adductor mandibulae (Add. mand.); 2, levator hyomandibulae (Lev. hyom.); 3, dilator operculi (Dil. oper.); and of activity from 4, medulla showing 3 distinct respiratory neurons. High‐amplitude neuron (b) could be correlated with component occurring after 4.3‐ms delay in Add. mand. and was therefore presumed to be a motoneuron. I, averaged response in muscle, with neuron b as trigger. Low‐amplitude neuron (a) showed no such temporal correlation and was not an Add. mand. motoneuron. After 7 min, neuron b stopped firing and neuron c became active in opposite breathing phase. II and III, averaged responses showing that c was not a motoneuron of Lev. hyom. or Dil. oper. Bottom: 2 experiments. IV, good correlation with short delay (i) was found between a medullary neuron and averaged activity from Lev. hyom. After slight electrode displacement, further correlation was found with long delay (ii) between another neuron and the same muscle. First neuron was presumed to be a motoneuron and the second an interneuron. V, good correlation with averaged activity from EMG of Dil. oper., again with a long delay (iii), suggesting that trigger must be an interneuron.

Adapted from Ballintijn and Alink 15


Figure 14.

Relationship between gill ventilation and partial pressure of O2 of inhaled water (Pio2) in 4 teleosts: juvenile catfish Ictalurus punctatus 177, carp Cyprinus carpio 351, sturgeon Acipenser transmontanus 70, and rainbow trout Salmo gairdneri 428. Four lower panels, contribution of breathing rate (dotted lines) and stroke volume (solid lines) to change in gill ventilation. In normoxic carp, breathing is arrhythmic and large increase in rate in hypoxia is due to breathing becoming continuous 351.



Figure 15.

Time relationships between hypoxic stimulus and responses seen in teleost fish. A: time course in seconds of fall in Po2 in water from regions indicated (w, prebranchial water; I, buccal water; E, exhaled water) and of appearance of cardioventilatory response (R) after turning tap to admit hypoxic water.

From Eclancher 135. B: increased breathing frequency and ventilation pressures recorded in buccal cavity of trout in response to rapidly induced hypoxia. Electrode in water near animal's mouth signals first appearance of decrease in Pio2. From Bamford 21


Figure 16.

Relationship between water flow over gills and arterial O2 content of dorsal aortic blood in Salmo gairdneri. Horizontal and vertical bars indicate ±SEM. Number by each point, corresponding Pao2 in kPa. Arterial O2 content was changed by bubbling n2, CO2, and/or O2 into water containing fish or by making fish anemic by withdrawing red blood cells.

Adapted from Smith and Jones 479 and Randall 420


Figure 17.

Effects of NaCN injection on teleost chemoreceptors. Top: traces show effects of injecting 6 μg NaCN into ventral aorta of 300‐g trout on electromyogram (EMG) from an opercular muscle, integrated EMG (EMGi) and electrocardiogram (ECG). Top trace, 1‐s time marker. There was 6.2‐s latent period from start of injection, but by 10 s from start, ventilatory activity increased 3 times. Start of ventilatory response (center arrow) also corresponded with onset of hypoxic bradycardia. Bottom: comparison of effects of injecting 6 μg NaCN intravascularly into 350‐g trout (at 13°C) exposed to 3 levels of partial pressure of O2 in water (Pwo2). Stimulation of ventilatory activity (shown as EMGi in arbitrary units) is greatly reduced by simultaneous hyperoxia (Pwo2 = 210 Torr and 540 Torr). Each bar of histogram of EMGi represents 10 cycles of ventilation.

From Eclancher and Dejours 136


Figure 18.

Fluctuations in Pao2 and Paco2 and femoral artery Pao2 and Paco2 during intermittent breathing in unrestrained freely diving turtle Pseudemys scripta. Shaded vertical bars, brief bouts of surfacing and lung ventilation.

From Burggren and Shelton 71


Figure 19.

Control of breath duration and tidal volume (Vt) in turtles. Top: mean inspiratory duration (Ti) as function of inspired CO2 concentration (Fico2) in intact (open columns) and bilaterally vagotomized (shaded columns) turtles (Chrysemys picta) (W. K. Milsom, unpublished observations). Bottom: relationship between inspiratory duration and reciprocal of inspiratory flow rate (Vt · Ti−1 in ml · s−1) in intact (open circles) and vagotomized (filled circles) turtles breathing air. Regression equation describes correlation for intact animals. Slope of line equals Vt. No significant correlation exists after vagotomy.

From Milsom and Jones 375


Figure 20.

Effects of environmental O2 and CO2 on ventilation in 3 facultative (Erythrinus, Piabucina, and Umbra) and 1 obligate (Trichogaster) air‐breathing fish. A: relationships between aquatic Po2 and Pco2 and type of breathing shown by single specimen of Erythrinus sp. at 26°C. Suggested reasons for different breathing behaviors are: high Pco2 causes opercular flaps to close (A); low Po2 causes O2 loss to water if gills are ventilated (B); Po2 in water is inadequate to saturate blood with O2 (C); Pco2 stimulates air breathing (D); aquatic breathing is sufficient for requirements (E); gill ventilation is insufficient to saturate blood (F); and low Pco2 is insufficient to stimulate gill ventilation (G).

From Willmer 539. B: combined effects of aquatic Po2 and Pco2 on air‐breathing rate of Piabucina festae. [From Graham et al. 193.] C: relationship between air convection requirement and ventilation of suprabranchial chamber () with air in Trichogaster trichopterus at 27°C. Labeled areas, locations of data points from 5 animals in hypoxic water (Po2 = 60 Torr), hypoxic gas (Po2 = 60 Torr), and hypercapnic water (Pco2 = 21 Torr); all treatments caused significantly higher than control values (breathing air and air‐saturated water). Though total O2 consumption was not changed significantly, hypoxic and hypercapnic water increased and hypoxic gas decreased O2 uptake from suprabranchial chamber as compared with control values, thus affecting air convection requirement. [From Burggren 66.] D: effect of progressive aquatic hypoxia (25°C) on frequencies of air and water breathing in Umbra limi. Lines, averages of data drawn from 10 fish. From Gee 173
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Graham Shelton, David R. Jones, William K. Milsom. Control of Breathing in Ectothermic Vertebrates. Compr Physiol 2011, Supplement 11: Handbook of Physiology, The Respiratory System, Control of Breathing: 857-909. First published in print 1986. doi: 10.1002/cphy.cp030228