Adrenergic and adenosinergic regulation of the cardiovascular system in an Antarctic icefish: Insight into central and peripheral determinants of cardiac output

Joyce, William; Egginton, Stuart; Farrell, Anthony P.; Axelsson, Michael

doi:10.1016/j.cbpa.2018.12.012

Cited by 9 publications

(7 citation statements)

References 75 publications

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“…The fish were killed with a sharp blow to the head followed by the destruction of the brain. The spleen was dissected and placed in physiological saline [composed of (in mM): NaCl (250), KCl (2.5), MgCl2 (0.9), CaCl2 (2.5), TES acid (3.1), TES sodium salt (6.1), glucose (5.6), pH 7.95–8.00 at 1°C] (Joyce et al ., 2019). Spleen strips were dissected and studied as described previously (Nilsson et al ., 1996).…”

Section: Methodsmentioning

confidence: 99%

“…The white‐blooded icefish (16 species in the family Channichthyidae) have forsaken haemoglobin altogether (Ruud, 1954), and red blood cells (RBCs) are vestigial and rare (Barber et al ., 1981), reducing Ht ( i.e ., packed cell volume) to <1%. Since the loss of haemoglobin expression, this lineage has diversified over the past 7.8–4.8 millions of years (Coppe et al ., 2013; Near et al ., 2012) and to support sufficient oxygen transport, icefishes rely on increased blood volume and enlarged hearts to pump a greater cardiac output (Egginton et al ., 2019; Hemmingsen et al ., 1972; Hemmingsen & Douglas, 1970; Holeton, 1970; Joyce et al ., 2018a; Joyce et al ., 2019). By contrast, many red‐blooded species are masters of regulating Ht, such that during periods of rest, it is low (< 15%), but can be increased two‐ to three‐fold during exercise, digestion or warming (Axelsson, 2005; Brijs et al ., 2019; Davison et al ., 1994; Egginton et al ., 1991; Franklin et al ., 1993; Joyce et al ., 2018b; Wells et al ., 1984).…”

Section: Introductionmentioning

confidence: 99%

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Regulation of splenic contraction persists as a vestigial trait in white‐blooded Antarctic fishes

Joyce

Axelsson

2020

Journal of Fish Biology

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In fishes, the spleen can function as an important reservoir for red blood cells (RBCs), which, following splenic contraction, may be released into the circulation to increase haematocrit during energy‐demanding activities. This trait is particularly pronounced in red‐blooded Antarctic fishes in which the spleen can sequester a large proportion of RBCs during rest, thereby reducing blood viscosity, which may serve as an adaptation to life in cold environments. In one species, Pagothenia borchgrevinki, it has previously been shown that splenic contraction primarily depends on cholinergic stimulation. The aim of the present study was to investigate the regulation of splenic contraction in five other Antarctic fish species, three red‐blooded notothenioids (Dissostichus mawsoni Norman, 1937, Gobionotothen gibberifrons Lönnberg, 1905, Notothenia coriiceps Richardson 1844) and two white‐blooded “icefish” (Chaenocephalus aceratus Lönnberg, 1906 and Champsocephalus gunnari Lönnberg, 1905), which lack haemoglobin and RBCs, but nevertheless possess a large spleen. In all species, splenic strips constricted in response to both cholinergic (carbachol) and adrenergic (adrenaline) agonists. Surprisingly, in the two species of icefish, the spleen responded with similar sensitivity to red‐blooded species, despite contraction being of little obvious benefit for releasing RBCs into the circulation. Although the icefish lineage lost functional haemoglobin before diversifying over the past 7.8–4.8 millions of years, they retain the capacity to contract the spleen, likely as a vestige inherited from their red‐blooded ancestors.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Regulation of splenic contraction persists as a vestigial trait in white‐blooded Antarctic fishes

Joyce

Axelsson

2020

Journal of Fish Biology

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“…In fact, a unique evolutionary development of the notothenioids is the complete loss of functional erythrocytes in adult members of the family Channichthyidae (icefish), while in red-blooded notothenioids, the number of circulating erythrocyte cells at rest is approximately half that found in temperate teleost species (Axelsson, 2005;Graham and Fletcher, 1985;Hemmingsen, 1991). While the complete loss or decrease of erythrocytes in notothenioids is associated with a substantial reduction in blood viscosity, it also coincides with similar reductions in blood oxygen carrying capacity, which has inevitably led to the development of a range of other cardiovascular modifications (Axelsson, 2005;Axelsson et al, 1992;Hemmingsen, 1991;Joyce et al, 2018Joyce et al, , 2019. In the icefish group, these adjustments consist of larger blood volume, an enlarged heart and significantly reduced vascular resistance, whereas in the red-blooded notothenioids, the level of circulatory adjustments is believed to differ depending on the ecology of the various species (Axelsson, 2005;Axelsson et al, 1992;Buckley et al, 2014;Joyce et al, 2018Joyce et al, , 2019.…”

Section: Introductionmentioning

confidence: 99%

“…While the complete loss or decrease of erythrocytes in notothenioids is associated with a substantial reduction in blood viscosity, it also coincides with similar reductions in blood oxygen carrying capacity, which has inevitably led to the development of a range of other cardiovascular modifications (Axelsson, 2005;Axelsson et al, 1992;Hemmingsen, 1991;Joyce et al, 2018Joyce et al, , 2019. In the icefish group, these adjustments consist of larger blood volume, an enlarged heart and significantly reduced vascular resistance, whereas in the red-blooded notothenioids, the level of circulatory adjustments is believed to differ depending on the ecology of the various species (Axelsson, 2005;Axelsson et al, 1992;Buckley et al, 2014;Joyce et al, 2018Joyce et al, , 2019. It has been proposed that the next step in the evolutionary sequence for nototheniod fishes was an increase in their capacity for systemic oxygen delivery (i.e.…”

Section: Introductionmentioning

confidence: 99%

Extreme blood boosting capacity of an Antarctic fish represents an adaptation to life in a sub-zero environment

Brijs

Axelsson

Rosengren

et al. 2019

Journal of Experimental Biology

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Blood doping, the practice of boosting the oxygen carrying capacity of blood, is an illegal strategy used by human athletes to enhance aerobic capacity and athletic performance. Interestingly, the practice of boosting blood oxygen carrying capacity is also naturally prevalent in the animal kingdom via the splenic release of stored erythrocytes. Here, we demonstrate that an Antarctic notothenioid fish, the bald notothen (Pagothenia borchgrevinki), is a master of this practice. Because of the sub-zero environment these fish inhabit, they sequester a large proportion of erythrocytes in the spleen during times of inactivity to reduce the energetic and physiological costs associated with continuously pumping highly viscous blood around the body. However, in response to metabolically demanding situations (i.e. exercise and feeding), these fish contract the spleen to eject stored erythrocytes into circulation, which boosts blood oxygen carrying capacity by up to 207% (cf. exercise-induced increases of ∼40-60% in a range of other vertebrates and ∼5-25% in blood-doping athletes). By evaluating cardiorespiratory differences between splenectomized (unable to release erythrocytes from the spleen) and sham-operated individuals, we demonstrate the metabolic benefits (i.e. aerobic scope increase of 103%) and the cardiovascular trade-offs (i.e. ventral aortic blood pressure and cardiac workload increase of 12% and 30%, respectively) associated with the splenic blood-boosting strategy. In conclusion, this strategy provides bald notothens with an extraordinary facultative aerobic scope that enables an active lifestyle in the extreme Antarctic marine environment, while minimizing the energetic and physiological costs of transporting highly viscous blood during times of reduced energetic demand.

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“…The control of peripheral vascular tone (see Glossary) is paramount for the regulation of cardiac output by virtue of altering vascular resistance or conductance (see Glossary) to match blood flow to metabolic demands (Bada et al, 2012;González-Alonso et al, 2008;Guyton, 1968;Joyce et al, 2019). Conductance (blood flow/ Δ pressure) is the reciprocal of resistance (Δ pressure/blood flow), and these two indices are widely assumed to be interchangeable.…”

Section: Introductionmentioning

confidence: 99%

Weighing the evidence for using vascular conductance, not resistance, in comparative cardiovascular physiology

Joyce

White

Raven

et al. 2019

Journal of Experimental Biology

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Vascular resistance and conductance are reciprocal indices of vascular tone that are often assumed to be interchangeable. However, in most animals in vivo, blood flow (i.e. cardiac output) typically varies much more than arterial blood pressure. When blood flow changes at a constant pressure, the relationship between conductance and blood flow is linear, whereas the relationship between resistance and blood flow is non-linear. Thus, for a given change in blood flow, the change in resistance depends on the starting point, whereas the attendant change in conductance is proportional to the change in blood flow regardless of the starting conditions. By comparing the effects of physical activity at different temperatures or between speciesconcepts at the heart of comparative cardiovascular physiologywe demonstrate that the difference between choosing resistance or conductance can be marked. We also explain here how the ratio of conductance in the pulmonary and systemic circulations provides a more intuitive description of cardiac shunt patterns in the reptilian cardiovascular system than the more commonly used ratio of resistance. Finally, we posit that, although the decision to use conductance or resistance should be made on a case-by-case basis, in most circumstances, conductance is a more faithful portrayal of cardiovascular regulation in vertebrates.

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Adrenergic and adenosinergic regulation of the cardiovascular system in an Antarctic icefish: Insight into central and peripheral determinants of cardiac output

Abstract: This is a repository copy of Adrenergic and adenosinergic regulation of the cardiovascular system in an Antarctic icefish: Insight into central and peripheral determinants of cardiac output..

Cited by 9 publications

References 75 publications

Regulation of splenic contraction persists as a vestigial trait in white‐blooded Antarctic fishes

Regulation of splenic contraction persists as a vestigial trait in white‐blooded Antarctic fishes

Extreme blood boosting capacity of an Antarctic fish represents an adaptation to life in a sub-zero environment

Weighing the evidence for using vascular conductance, not resistance, in comparative cardiovascular physiology

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