Arapaima gigas maintains gas exchange separation in severe aquatic hypoxia but does not suffer branchial oxygen loss

TY - JOUR

T1 - Arapaima gigas maintains gas exchange separation in severe aquatic hypoxia but does not suffer branchial oxygen loss

AU - Aaskov, Magnus L.

AU - Jensen, Rasmus J.

AU - Skov, Peter Vilhelm

AU - Wood, Chris M.

AU - Wang, Tobias

AU - Malte, Hans

AU - Bayley, Mark

N1 - Publisher Copyright: © 2022. Published by The Company of Biologists Ltd.

PY - 2022/3

Y1 - 2022/3

N2 - One of the most air-reliant obligate air-breathing fish is the South American Arapaima gigas, with substantially reduced gills impeding gas diffusion, thought to be a result of recurring aquatic hypoxia in its habitat. In normoxic water, A. gigas is reported to satisfy 70–80% of its O 2 requirement from the air while excreting 60–90% of its CO 2 to the water. If this pattern of gas exchange were to continue in severely hypoxic water, O 2 loss at the gills would be expected. We hypothesized therefore that partitioning of CO 2 would shift to the air phase in severe aquatic hypoxia, eliminating the risk of branchial O 2 loss. By adapting a respirometer designed to measure aquatic M ̇ O2/M ̇ CO2, we were able to run intermittent closed respirometry on both water and air phase for both of these gasses as well as sample water for N-waste measurements (ammonia-N, urea-N) so as to calculate metabolic fuel utilization. In contrast to our prediction, we found that partitioning of CO 2 excretion changed little between normoxia and severe hypoxia (83% versus 77% aquatic excretion, respectively) and at the same time there was no evidence of branchial O 2 loss in hypoxia. This indicates that A. gigas can utilize distinct transfer pathways for O 2 and CO 2. Routine and standard M ̇ O2, N-waste excretion and metabolic fuel utilization did not change with water oxygenation. Metabolism was fuelled mostly by protein oxidation (53%), while carbohydrates and lipids accounted for 27% and 20%, respectively.

AB - One of the most air-reliant obligate air-breathing fish is the South American Arapaima gigas, with substantially reduced gills impeding gas diffusion, thought to be a result of recurring aquatic hypoxia in its habitat. In normoxic water, A. gigas is reported to satisfy 70–80% of its O 2 requirement from the air while excreting 60–90% of its CO 2 to the water. If this pattern of gas exchange were to continue in severely hypoxic water, O 2 loss at the gills would be expected. We hypothesized therefore that partitioning of CO 2 would shift to the air phase in severe aquatic hypoxia, eliminating the risk of branchial O 2 loss. By adapting a respirometer designed to measure aquatic M ̇ O2/M ̇ CO2, we were able to run intermittent closed respirometry on both water and air phase for both of these gasses as well as sample water for N-waste measurements (ammonia-N, urea-N) so as to calculate metabolic fuel utilization. In contrast to our prediction, we found that partitioning of CO 2 excretion changed little between normoxia and severe hypoxia (83% versus 77% aquatic excretion, respectively) and at the same time there was no evidence of branchial O 2 loss in hypoxia. This indicates that A. gigas can utilize distinct transfer pathways for O 2 and CO 2. Routine and standard M ̇ O2, N-waste excretion and metabolic fuel utilization did not change with water oxygenation. Metabolism was fuelled mostly by protein oxidation (53%), while carbohydrates and lipids accounted for 27% and 20%, respectively.

KW - Air-breathing fish

KW - Anoxia

KW - Fuel use

KW - Gas exchange

KW - Respirometry

KW - Teleost

UR - http://www.scopus.com/inward/record.url?scp=85126925039&partnerID=8YFLogxK

U2 - 10.1242/jeb.243672

DO - 10.1242/jeb.243672

M3 - Journal article

C2 - 35132994

AN - SCOPUS:85126925039

SN - 0022-0949

VL - 225

JO - Journal of Experimental Biology

JF - Journal of Experimental Biology

IS - 6

M1 - jeb243672

ER -