Nigel H. West

Changing respiratory importance of gills, lungs and skin during metamorphosis in the bullfrog Rana catesbeiana.

Oxygen uptake (MO2) and carbon dioxide excretion (MCO2) by the skin, lungs and gills (if present) of Rana catesbeiana have been measured at 20 degrees C during 4 developmental stages - strictly water breathing tadpoles, air breathing tadpoles, post-metamorphic bullfrogs and 4-year-old adult bullfrogs. In aquatic tadpoles, branchial performance is comparable to that of teleost fishes, but a large skin area to body mass ratio, particularly for the tail, plus a thin and highly vascularized skin, presumably facilitates a large (60% of total MO2) cutaneous O2 uptake. As development proceeds, MO2 by the gills decreases and the lungs assume importance in O2 uptake, but the skin remains the major organ of O2 uptake until metamorphosis is nearly complete. Immediately after metamorphosis, O2 uptake by the lung is elevated to 80% of total MO2. Carbon dioxide excretion in both aquatic and air breathing tadpoles was also achieved mostly by the skin (60% of total MCO2, R = 0.9). The lungs of air breathing tadpoles excreted less than 2% of total MCO2, rising to a maximum of only 20% (R = 0.2) even in adult bullfrogs. The considerable importance of the skin to CO2 excretion thus rises even further with the degeneration of the gills at metamorphosis, with R for the skin rising from 0.8 before metamorphosis to 7.5 in adults. Thus, large adjustments in skin and lung gas exchange occur as the larval gills slowly degenerate, and lung ventilation is initiated and increased. Aquatic O2 uptake is rapidly superseded by the uptake of O2 from the air, while CO2 excretion largely remains a function of the aquatic respiratory surfaces throughout the life cycle of the bullfrog.

Hypoxemic threshold for lung ventilation in the toad

The relationship between the activity of the buccal force pump, expressed as the time integral of positive buccal pressure, and PaO2 was investigated in conscious toads, Bufo marinus, unidirectionally ventilated at a high flow rate (240-260 ml/min). The high ventilatory flow rate meant that PaO2 was largely independent of the animals ventilatory activity so that the relationship between pulmonary ventilation and PaO2 was effectively open-loop. The hypoxemic threshold (PaO2) for lung ventilation was 54.2 mm Hg in hypocapnia (PaCO2 = 4.7 +/- 0.3 mm Hg), 82.6 mm Hg in normocapnia (PaCO2 = 11.6 +/- 0.2 mm Hg), and 137.9 mm Hg in hypercapnia (PaCO2 = 20.1 +/- 0.1 mm Hg). Unidirectional ventilation with 20% O2 in N2, a condition in which the toads were normoxic but hypocapnic, stopped pulmonary ventilation cycles. Taken with existing evidence that hyperoxia stops pulmonary ventilation even under conditions in which PaCO2 is elevated this suggests that hypoxic and hypercapnic stimuli summate to drive lung ventilation in the toad. Bilateral denervation of the carotid labyrinths decreased pulmonary ventilation in absolute terms, but did not reduce the proportionate increase in pulmonary ventilation in response to normocapnic hypoxia, suggesting that chemoreceptors within the carotid labyrinth may contribute to, but are not solely responsible for, the hypoxemic ventilatory drive.

Functional characteristics of arterial chemoreceptors in an amphibian (Bufo marinus).

In order to further describe the functional characteristics of arterial chemoreceptors of anuran amphibians, multi-unit chemoreceptor discharge frequency (MCDF) was recorded from the carotid (N = 23) or aortic nerve (N = 2) of pithed, unidirectionally ventilated toads (Bufo marinus). MCDF increased with decreasing PaO2: typically, the threshold PaO2 lay between 40 and 60 mmHg. The MCDF-PaO2 relationship was right-shifted along the PaO2 axis by increasing PaCO2 (N = 5). In three toads, the MCDF-PaO2 relationship was unaffected when CaO2 was reduced 35-89% by hemorrhage. MCDF was also unaffected by occlusion of the outflow from the heart, though it increased upon release of the occlusion. MCDF was stimulated by epinephrine, and inhibited by dopamine. Our results demonstrate that the MCDF responds to the range of PaO2 and PaCO2 values encountered in vivo, suggesting that arterial chemoreceptors may participate in ventilatory control in toads. The receptors do not respond to the rate of oxygen delivery per se, and may be influenced by catecholamines known to exist in the carotid labyrinth.

Impact of long-term captivity on basal metabolism in birds

Abstract 1. 1. Merlins ( Faico columbarius ) held in captivity for periods ranging from 7 months to 3 years had significantly higher basal metabolic rates and body temperatures than freshly caught birds. 2. 2. When developing energetic models for free-living birds based on laboratory-derived values for basal metabolic rate and activity costs, it may be necessary to use freshly caught birds to avoid captivity-related changes in these values.

Pulmonary vagal modulation of ventilation in toads (Bufo marinus)

This study examined the role of pulmonary vagal feedback on hypercapnic chemosensitivity and breathing pattern formation in cane toads (Bufo marinus). Decerebrate, paralysed toads were uni-directionally ventilated with air, 2.5% CO(2) or 5.0% CO(2) with the lungs inflated or deflated, before and after pulmonary vagotomy. Motor output from the mandibular branch of the trigeminal nerve served as an index of fictive breathing. As respiratory drive was increased, breathing frequency increased and breaths were clustered into discrete episodes separated by periods of apnea. Lung deflation tended to enhance episodic breathing while inflation biased the system towards apnea at low levels of respiratory drive and a pattern of continuous, small breaths at higher levels of respiratory drive. Following bilateral pulmonary vagotomy there was no increase in ventilation during hypercapnia and lung inflation/deflation had no effect on breathing pattern. In isolated brainstem-spinal cord preparations from the same animals, all variables associated with fictive breathing were unaffected by changes in superfusate pH from 8.0 to 7.6. The breathing pattern from the in vitro preparations was highly variable. This study demonstrates a crucial role for vagal feedback in modulating respiration and the respiratory responses to hypercapnia in B. marinus.

Phylogenetic Trends in the Baroreceptor Control of Arterial Blood Pressure

This article attempts to draw out current themes in the comparative physiology of baroreceptors in order to point out potential areas of future research. The first theme concerns the distribution of baroreceptive zones in the central cardiovascular system. Baroreceptor populations are widely distributed among jawed vertebrates. Multiple baroreceptive zones commonly occur within segments of the central cardiovascular system derived from the embryonic visceral arch arteries and are innervated by the corresponding visceral arch nerves. Aortic (fourth arch) and pulmonary (sixth arch), but not carotid, baroreceptors are the most conspicuous populations, at least in terms of the consistency with which they have been functionally identified. A second theme that links baroreceptor structure to function has emerged recently. Unmyelinated baroreceptors have been identiied in amphibians, reptiles, and mammals. Such receptors have thresholds ranging from near to well above normal arterial pressures and act predominantly to mediate reflex responses to increases in arterial blood pressure above the normal range. In contrast, myelinated baroreceptors with thresholds well below normal arterial pressures have so far only been positively identiied in mammals. Quantitative data suggest that the reflex regulation of arterial pressure in nonmammalian vertebrates is of physiological importance. In the toad, open-loop analysis of the pulmocutaneous baroreflex suggests that the peak capacity of this reflex to regulate arterial blood pressure is of the same order of magnitude as that of the carotid sinus baroreflex in the dog. However, as only unmyelinated baroreceptors are present in the toad, expression of this reflex is largely restricted to arterial pressures well above the normal range. Finally, it is appealing to speculate that differences in the structure and function of baroreceptors between vertebrate classes are linked to corresponding differences in vascular anatomy and metabolic rate. Unmyelinated baroreceptors may be widely distributed in vertebrates, which would reflect a widespread need to protect the circulation from damaging increases in arterial pressure. In vertebrates with incompletely divided hearts, baroreflexes may be of particular importance in protecting the circulation of the gas exchanger from excessive pressures. Low-threshold myelinated baroreceptors may represent a relatively specialized addition topressure-regulating systems in endothermic vertebrates that have poor tolerance to even transient hypotension.

Factors terminating nonventilatory periods in the turtle, Chelydra serpentina

PaO2, PaCO2 and pHa were measured via an extracorporeal loop in conscious snapping turtles (Chelydra serpentina) breathing air or hypoxic (10, 15% O2), hyperoxic (30% O2), or hypercapnic (2% CO2) gases. Turtles breathed into an inverted funnel ventilated with the test gas. Breathing was recorded with a differential pressure transducer. In all turtles, nonventilatory periods were interrupted by breathing episodes containing multiple breaths. In normoxia, PaO2 at the end of nonventilatory periods ranged from 22-128 mm Hg, although PaCO2 showed a less than 5 mm Hg variation about the mean. There was a positive correlation between PaCO2 at the end of the nonventilatory period and the number of breaths in the succeeding period of ventilation. PaCO2 at the end of nonventilatory periods did not change significantly in hyperoxia, although mean PaO2 was significantly increased. In hypoxia, on the other hand, mean PaO2 was significantly reduced and PaCO2 at the end of the nonventilatory period was slightly, but significantly lower. Nonventilatory periods were shorter when turtles breathed 15% O2 (9.3 +/- 1.2 min) or 10% O2 (5.5 +/- 0.3 min) than when they breathed air (17.6 +/- 3.4 min). The results indicate that, in undisturbed turtles, the most important stimulus triggering a breathing episode is the rise in PaCO2 to a critical value during the preceding nonventilatory period. An increase in hypoxic drive shortens the nonventilatory period. However, in normoxia, PaO2 at the end of many nonventilatory periods probably does not fall sufficiently to stimulate O2-sensitive chemoreceptors.

Cardiovascular responses to neurohormones in conscious chickens and ducks

Cardiovascular responses (cardiac frequency, fH; mean arterial pressure, Pa; ischiatic arterial blood flow; Qi; ischiatic vascular resistance, Ri) to 1-norepinephrine (NE), acetylcholine (ACH), [Asp1, Val5]-angiotensin II (ANG II), and arginine vasotocin (AVT) were studied in conscious chickens (Gallus gallus) and Pekin ducks (Anas platyrhynchos). Age-dependent changes, in the cardiovascular variables and the responses to the native avian neurohormones, were also studied in ducks. NE injection caused larger increases in Pa and Ri, and a greater associated fall in fH, in ducks than in chickens. The pressor effect of ANG II was more persistent and developed at a slower rate than the response to NE in both species, although the pressor effect was greater in ducks. Interestingly, ANG II injection caused a tachycardia in these baroreceptor-intact birds. ACH and AVT produced similar rapid falls in Pa and a corresponding tachycardia in both species, although the fH response was greater in ducks. ANG II rapidly increased NE concentration in the arterial plasma of adult ducks, while AVT increased epinephrine (E) concentration. Resting Pa and hematocrit were lower, and fH was higher, in immature ducks. Immature ducks also were less responsive than adults to the cardiovascular actions of NE, ACH, AVT, and ANG II. The results demonstrate differences in the cardiovascular responses to neurohormones in chickens and ducks consistent with a higher level of cardioinhibitory nervous tone and a greater sensitivity to sympathetic stimuli in the aquatic species, which increase during maturation.

Relative distribution of blood flow in rats during surface and submerged swimming.

The relative distribution of blood flow was investigated in conscious rats with a radiological imaging technique that utilizes technetium-99m ethyl cysteinate dimer (99mTc-ECD). The objective of the study was to determine the effects of locomotory activity on the distribution of blood flow during a dive response. We compared the relative distribution of systemic flow in rats at rest, surface swimming and during periods of voluntarily initiated underwater swimming. The pattern of blood flow differed considerably between the three groups of rats. In resting controls, blood flow was widely distributed throughout the whole body with the thoraco-abdominal region receiving the largest fraction of cardiac output. During surface swimming blood shifted towards the exercising limbs, while during underwater swimming systemic blood flow was largely restricted to the head and thorax. However, the active front and hind limbs were not rendered totally ischemic. This suggests that the demands of exercising skeletal muscle partially over-ride the peripheral vasoconstriction during asphyxic diving in conscious rats. Furthermore, relative blood flow to the head increased during underwater swimming, which supports the view that there is a preferential maintenance of blood flow to the brain.

Response characteristics of pulmocutaneous arterial baroreceptors in the toad, Bufo marinus.

1. Response characteristics of baroreceptors with receptive fields in the pulmocutaneous artery (p.c.a.) were determined in pithed toads by applying pressure steps, ramps, sine waves, and volume infusions into the vascularly isolated and perfused p.c.a. 2. The baroreceptors exhibited phasic and tonic discharge thresholds (30.3 +/‐ 2.3 and 36.2 +/‐ 2.8 mmHg respectively) which were above mean arterial pressure values reported for conscious undisturbed toads. They are comparable, in this respect, to non‐myelinated mammalian arterial baroreceptors. 3. The maximum‐phasic and minimum‐adapted discharge frequencies of the p.c.a. baroreceptors were low (30 and 2‐3 spikes s‐1, respectively), but resembled those reported for mammalian non‐myelinated baroreceptors when an adjustment was made for the difference in the temperature of mammalian and amphibian preparations. 4. The sensitivity of the baroreceptor discharge frequency to pressure (delta F/delta P) was estimated from pressure‐step and pressure‐ramp stimuli. Both estimates were greater than those reported for mammalian systemic arterial baroreceptors after the values were normalized to the maximum discharge frequency of the receptors. delta F/delta P and saturation discharge frequency values estimated from ramp stimuli increased with the dP/dt of pressure ramps. 5. The diameter of the p.c.a. was measured by sonomicrometry in toads anaesthetized with urethane. The diameter pulsation was 7.7 +/‐ 0.3% of the mean diameter (3.5 +/‐ 0.1 mm) at a mean pulse pressure of 22 +/‐ 1 mmHg, and Petersons pressure‐strain modulus was calculated to be 4.0 X 10(5) +/‐ 0.3 X 10(5) dyn cm‐2, which suggests that the p.c.a. is highly compliant, and in this respect is comparable to the pulmonary artery, but not to systemic arteries, in mammals. Baroreceptor discharge began near the point of peak dynamic compliance (dV/dP) and continued as dV/dP decreased. Increasing the rate of infusion reduced the peak dV/dP, but increased the baroreceptor discharge frequency. 6. The response to sinusoidal oscillating pressure stimuli was distorted by rectification. Increasing the frequency of sinusoidal stimulation over the range 0.05‐1.0 cycles s‐1 reduced the number of spikes per cycle, but increased the mean discharge frequency.