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Oxygen transport and cardiovascular responses in skipjack tuna (Katsuwonus pelamis) and yellowfin tuna (Thunnus albacares) exposed to acute hypoxia

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Summary

Responses to acute hypoxia were measured in skipjack tuna (Katsuwonus pelamis) and yellowfin tuna (Thunnus albacares) (≈1–3 kg body weight). Fish were prevented from making swimming movements by a spinal injection of lidocaine and were placed in front of a seawater delivery pipe to provide ram ventilation of the gills. Fish could set their own ventilation volumes by adjusting mouth gape. Heart rate, dorsal and ventral aortic blood pressures, and cardiac output were continuously monitored during normoxia (inhalant water (PO 2>150 mmHg) and three levels of hypoxia (inhalant water PO 2≈130, 90, and 50 mmHg). Water and blood samples were taken for oxygen measurements in fluids afferent and efferent to the gills. From these data, various measures of the effectiveness of oxygen transfer, and branchial and systemic vascular resistance were calculated. Despite high ventilation volumes (4–71·min-1·kg-1), tunas extract approximately 50% of the oxygen from the inhalant water, in part because high cardiac outputs (115–132 ml·min-1·kg-1) result in ventilation/perfusion conductance ratios (0.75–1.1) close to the theoretically ideal value of 1.0. Therefore, tunas have oxygen transfer factors (ml O2·min-1·mmHg-1·kg-1) that are 10–50 times greater than those of other fishes. The efficiency of oxygen transfer from water in tunas (≈65%) matches that measured in teleosts with ventilation volumes and order of magnitude lower. The high oxygen transfer factors of tunas are made possible, in part, by a large gill surface area; however, this appears to carry a considerable osmoregulatory cost as the metabolic rate of gills may account for up 70% of the total metabolism in spinally blocked (i.e., non-swimming) fish. During hypoxia, skipjack and yellowfin tunas show a decrease in heart rate and increase in ventilation volume, as do other teleosts. However, in tunas hypoxic bradycardia is not accompanied by equivalent increases, in stroke volume, and cardiac output falls as HR decreases. In both tuna species, oxygen consumption eventually must be maintained by drawing on substantial venous oxygen reserves. This occurs at a higher inhalant water PO2 (between 130 and 90 mmHg) in skipjack tuna than in yellowfin tuna (between 90 and 50 mmHg). The need to draw on venous oxygen reserves would make it difficult to meet the oxygen demand of increasing swimming speed, which is a common response to hypoxia in both species. Because yellowfin tuna can maintain oxygen consumption at a seawater oxygen tension of 90 mmHg without drawing on venous oxygen reserves, they could probably survive for extended periods at this level of hypoxia.

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Abbreviations

BPda, BPva :

dorsal, ventral aortic blood pressure

C aO2, C vO2 :

oxygen content of arterial, venous blood

DO2 :

diffusion capacity

Eb, Ew :

effectiveness of O2 uptake by blood, and from water, respectively

Hct:

hematocrit

HR:

heart rate

PCO2 :

carbon dioxide tension

P aCO2, P vCO2 :

carbon dioxide tension of arterial and venous blood, respectively

PO2 :

oxygen tension

P aO2, P vO2, P iO2, P cO2 :

oxygen tension of arterial blood, venous blood, and inspired and expired water, respectively

pHa, pHv:

pH of arterial and venous blood, respectively

Pw—b :

effective water to blood oxygen partial pressure difference

ΔPg:

partial pressure (tension) gradient

\(\dot Q\) :

cardiac output

R:

vascular resistance

SV:

stroke volume

SEM:

standard error of mean

TO2 :

transfer factor

U:

utilization

\(\dot V\) g :

ventilation volume

\(\dot V\)O2 :

oxygen consumption

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  1. Peter G. Bushnell

    Present address: Department of Zoology, University of British Columbia, 6270 University Boulevard, V6T 2A9, Vancouver, B.C., Canada

Authors and Affiliations

  1. John A. Burns School of Medicine, Department of Physiology, University of Hawaii, 1960 East-West Road, 96822, Honolulu, HI, USA

    Peter G. Bushnell

  2. Southwest Fisheries Science Center Honolulu Laboratory, National Marine Fisheries Service, NOAA, 2570 Dole Street, 96822-2396, Honolulu, HI, USA

    Richard W. Brill

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Bushnell, P.G., Brill, R.W. Oxygen transport and cardiovascular responses in skipjack tuna (Katsuwonus pelamis) and yellowfin tuna (Thunnus albacares) exposed to acute hypoxia. J Comp Physiol B 162, 131–143 (1992). https://doi.org/10.1007/BF00398338

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