Control of Breathing in Ectothermic Vertebrates

Shelton, G.; Jones, David R.; Milsom, William K.

doi:10.1002/cphy.cp030228

Cited by 72 publications

(57 citation statements)

References 442 publications

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“…Although these reflex circuits may have evolved because they allow bimodal fishes to increase air breathing and regulate their metabolic rate in aquatic hypoxia, it is conceivable that they also cause them to perform surfacing responses at irregular intervals in normoxia (Lefevre et al, 2014a). It has been proposed that the aperiodic gulping of air by animals with bimodal respiration is indeed a chemoreflex, whereby blood oxygen levels decline progressively over time after an air breath, this is monitored by oxygen-sensitive chemoreceptors in the vasculature that eventually stimulate the animal to surface and take another gulp (Milsom, 2012;Shelton et al, 1984). The overall positive relationship between SMR and ṀO 2,air could be explained by such a physiological mechanism: if the decline in blood oxygen occurs more rapidly in individuals with higher basal metabolic demands, this will stimulate more reflex air-breathing responses.…”

Section: General Patterns Of Respiratory Metabolism and Boldnessmentioning

confidence: 99%

“…Although the catfish can meet routine oxygen requirements by gill ventilation in wellaerated water, it will spontaneously gulp air at irregular intervals (Belão et al, 2011). It has been suggested that such aperiodic air gulping might be a reflex driven by peripheral oxygen chemoreceptors (Milsom, 2012;Shelton et al, 1984) and therefore could reflect individual oxygen demand. Given, however, that the catfish is a facultative air breather (Belão et al, 2011), this risky surfacing in normoxia might also be driven by individual boldness, perhaps to increase the flux of oxygen for aerobic activities such as foraging, digestion and growth.…”

Section: Introductionmentioning

confidence: 99%

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To boldly gulp: standard metabolic rate and boldness have context-dependent influences on risk-taking to breathe air in a catfish

McKenzie

Belão

Killen

et al. 2015

Journal of Experimental Biology

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The African sharptooth catfish Clarias gariepinus has bimodal respiration, it has a suprabranchial air-breathing organ alongside substantial gills. We used automated bimodal respirometry to reveal that undisturbed juvenile catfish (N=29) breathed air continuously in normoxia, with a marked diurnal cycle. Air breathing and routine metabolic rate (RMR) increased in darkness when, in the wild, this nocturnal predator forages. Aquatic hypoxia (20% air saturation) greatly increased overall reliance on air breathing. We investigated whether two measures of risk taking to breathe air, namely absolute rates of aerial O 2 uptake (Ṁ O2,air ) and the percentage of RMR obtained from air (%Ṁ O2,air ), were influenced by individual standard metabolic rate (SMR) and boldness. In particular, whether any influence varied with resource availability (normoxia versus hypoxia) or relative fear of predation (day versus night). Individual SMR, derived from respirometry, had an overall positive influence on Ṁ O2,air across all contexts but a positive influence on %Ṁ O2,air only in hypoxia. Thus, a pervasive effect of SMR on air breathing became most acute in hypoxia, when individuals with higher O 2 demand took proportionally more risks. Boldness was estimated as time required to resume air breathing after a fearful stimulus in daylight normoxia (T res ). Although T res had no overall influence on Ṁ O2,air or %Ṁ O2,air , there was a negative relationship between T res and %Ṁ O2,air in daylight, in normoxia and hypoxia. There were two T res response groups, 'bold' phenotypes with T res below 75 min (N=13) which, in daylight, breathed proportionally more air than 'shy' phenotypes with T res above 115 min (N=16). Therefore, individual boldness influenced air breathing when fear of predation was high. Thus, individual energy demand and personality did not have parallel influences on the emergent tendency to take risks to obtain a resource; their influences varied in strength with context.

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Section: General Patterns Of Respiratory Metabolism and Boldnessmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

To boldly gulp: standard metabolic rate and boldness have context-dependent influences on risk-taking to breathe air in a catfish

McKenzie

Belão

Killen

et al. 2015

Journal of Experimental Biology

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“…In air breathers, arterial pH regulation is achieved by ventilator-y control of PCO,. In water breathers, control is independent of ventilation, and blood acid-base status in the face of temperature change is maintained through changes in blood bicarbonate concentration (Shelton et al 1986). …”

Section: Bloodmentioning

confidence: 98%

Cardiovascular and respiratory physiology of tuna: adaptations for support of exceptionally high metabolic rates

Bushnell

Jones

1994

Environ Biol Fish

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Both physical and physiological modifications to the oxygen transport system promote high metabolic performance of tuna . The large surface area of the gills and thin blood-water barrier means that 02 utilization is high (30-50%) even when ram ventilation approaches 101 min-'kg-' . The heart is extremely large and generates peak blood pressures in the range of 70-100 mmHg at frequencies of 1-5 Hz . The blood 02 capacity approaches 16 ml dl-'and a large Bohr coefficient (-0 .83 to -1 .17) ensures adequate loading and unloading of 02 from the well buffered blood (20.9 slykes) . Tuna muscles have aerobic oxidation rates that are 3-5 times higher than in other teleosts and extremely high glycolytic capacity (150 µmot g' lactate generated) due to enhanced concentration of glycolytic enzymes . Gill resistance in tuna is high and may be more than 50% of total peripheral resistance so that dorsal aortic pressure is similar to that in other active fishes such as salmon or trout . An 0, delivery/demand model predicts the maximum sustained swimming speed of small yellowfin and skipjack tuna is 5 .6 BL s' and 3 .5 BL sec', respectively. The surplus 0, delivery capacity at lower swimming speeds allows tuna to repay large oxygen debts while swimming at 2-2 .5 BL s -' . Maximum oxygen consumption (7-9 x above the standard metabolic rate) at maximum exercise is provided by approximately 2 x increases in each of heart rate, stroke volume, and arterial-venous 02 content difference .

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“…Typically, most species that have been examined exhibit hyperventilation that is mediated by increases in breathing frequency and/or ventilatory stroke volume (Dejours, 1973;Janssen and Randall, 1975;Randall et al, 1976;Smatresk and Cameron, 1982;Perry and Gilmour, 1996;Crocker et al, 2000;Perry et al, 2009b) (for reviews, see Shelton et al, 1986;Perry and Wood, 1989;Milsom, 1995;Gilmour, 2001;Perry and Gilmour, 2002;Gilmour and Perry, 2007;Perry et al, 2009a;Perry and Abdallah, 2012). The cardiovascular responses to hypercapnia have received less attention but in those few species that have been examined, a conserved response appears to be bradycardia Sundin et al, 2000;Reid et al, 2000;Perry and McKendry, 2001;Gilmour et al, 2005) which may, or may not, be associated with an increase in arterial blood pressure (reviewed by Gilmour and Perry, 2007).…”

Section: Introductionmentioning

confidence: 99%

Cardiac responses to hypercapnia in larval zebrafish (Danio rerio): The links between CO2 chemoreception, catecholamines and carbonic anhydrase

Miller

Pollack

Bradshaw

et al. 2014

Journal of Experimental Biology

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The ontogeny of carbon dioxide (CO 2 ) sensing in zebrafish (Danio rerio) has not been examined. In this study, CO 2 -mediated increases in heart rate were used to gauge the capacity of zebrafish larvae to sense CO 2 . CO 2 is thought to be detected via neuroepithelial cells (NECs), which are homologous to mammalian carotid body glomus cells. Larvae at 5 days post-fertilization (d.p.f.) exhibited tachycardia when exposed for 30 min to 0.75% CO 2 (~5.63 mmHg); at 7 d.p.f., tachycardia was elicited by 0.5% CO 2 (~3.75 mmHg). Based on pharmacological evidence using β-adrenergic receptor (β-AR) antagonists, and confirmed by β 1 -AR translational gene knockdown using morpholinos, the reflex tachycardia accompanying hypercapnia was probably mediated by the interaction of catecholamines with cardiac β 1 receptors. Because the cardiac response to hypercapnia was abolished by the ganglionic blocker hexamethonium, it is probable that the reflex cardio-acceleration was mediated by catecholamines derived from sympathetic adrenergic neurons. Owing to its likely role in facilitating intracellular acidification during exposure to hypercapnia, it was hypothesized that carbonic anhydrase (CA) is involved in CO 2 sensing, and that inhibition of CA activity would blunt the downstream responses. Indeed, the cardiac response to hypercapnia (0.75% CO 2 ) was reduced in fish at 5 d.p.f. exposed to acetazolamide, a CA inhibitor, and in fish experiencing zCAc (CA2-like a) knockdown. Successful knockdown of zCAc was confirmed by CA activity measurements, western blotting and immunocytochemistry. Co-injection of embryos with zCAc morpholino and mRNA modified at the morpholino binding site restored normal levels of CA activity and protein levels, and restored (rescued) the usual cardiac responses to hypercapnia. These data, combined with the finding that zCAc is expressed in NECs located on the skin, suggest that the afferent limb of the CO 2 -induced cardiac reflex in zebrafish larvae is initiated by coetaneous CO 2 -sensing neuroepithelial cells.

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Control of Breathing in Ectothermic Vertebrates

Cited by 72 publications

References 442 publications

To boldly gulp: standard metabolic rate and boldness have context-dependent influences on risk-taking to breathe air in a catfish

To boldly gulp: standard metabolic rate and boldness have context-dependent influences on risk-taking to breathe air in a catfish

Cardiovascular and respiratory physiology of tuna: adaptations for support of exceptionally high metabolic rates

Cardiac responses to hypercapnia in larval zebrafish (Danio rerio): The links between CO2 chemoreception, catecholamines and carbonic anhydrase

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