Relationships between the peak hypoxic ventilatory response and critical O2 tension in larval and adult zebrafish (Danio rerio)

Abstract

Fish increase ventilation during hypoxia, a reflex termed the hypoxic ventilatory response (HVR). The HVR is an effective mechanism to increase O 2 uptake, but at a high metabolic cost. Therefore, when hypoxia becomes severe enough, ventilation declines, as its benefit is diminished. The water oxygen partial pressure (Pw O2) at which this decline occurs is expected to be near the critical Pw O2 (P crit), the Pw O2 at which O 2 consumption begins to decline. Our results indicate that in zebrafish (Danio rerio), the relationship between peak HVR and P crit is dependent on developmental stage. Peak ventilation occurred at Pw O2 values higher than P crit in larvae, but at a Pw O2 significantly lower than P crit in adults. Larval zebrafish use cutaneous respiration to a greater extent than branchial respiration and the cost of sustaining the HVR may outweigh the benefit, whereas adult zebrafish, which rely on branchial respiration, may benefit from using HVR at Pw O2 below P crit .

Oxygen supply capacity breathes new life into critical oxygen partial pressure (Pcrit)

“…The oxygen supply capacity, whether directly determined or extracted from a P crit value, defines the α-line that describes the oxygen limit for every MR from SMR to MMR. This definition of P crit is consistent with current physiological theory and the α-method provides a simple, repeatable and precise Behrens and Steffensen, 2007;Birk et al, 2018;Birk et al, 2019;Brill et al, 2015;Burggren et al, 2019a,b;Caposella 2012;Childress, 1975;Childress and Seibel, 1998;Christensen and Colacino 2000;Claireaux and Chabot 2016;Collins et al, 2013;Cowles and Chidress, 1995;Crear and Forteath, 2000;Dall 1986;Ern et al, 2016;Fu et al, 2011;Lefevre et al, 2015;Mandic et al, 2020;Negrete and Esbaugh, 2019;Nillson and Ostlund-Nilsson, 2004;Onthank et al, 2021;Paschke et al, 2010;Reemeyer and Rees, 2019;Rutherford and Thuesen, 2005;Schurmann and Steffenson, 1997;Seibel and Childress, 2000;Slesinger et al, 2019;Snyder et al, 2016;Speers-Roesch, 2012;Staples et al, 2000;Stoffels 2015;Thuy et al, 2010;Tuong et ). SMR (filled symbols) are also shown for some species.…”

“…However, the α-method resulted in higher values on average (mean difference=4.4%), which reflects its dependence on the highest α 0 values, rather than a regression through all values as in other P crit methods. In the species analyzed here, α ranged from 0.09 µmol O 2 g −1 h −1 kPa −1 for the deep-sea anglerfish, Melanocetus johnsoni, at 5°C (Cowles and Childress, 1995), to 4.11 µmol O 2 g −1 h −1 kPa −1 at 28°C for larval zebrafish, Danio rerio (Mandic et al, 2020; Table S1). These values are within the range previously reported for a similar diversity of species and are correlated with the MR at which they were determined (α=0.195×SMR+0.317; Pearson's r=0.98, P<0.001; Fig.…”

Hif‐1α is not required for the development of cardiac adrenergic control in zebrafish (Danio rerio)

“…Because exposure to hypoxia during early development has been shown to increase sympathetic nerve innervation in mammals and birds (Rook et al, 2014; Rouwet et al, 2002), for our studies of sympathetic nerve innervation (immunohistochemistry), some larvae were raised from 0 to 7 days postfertilisation (dpf) in flow through mesh‐bottomed containers that were flushed with pre‐equilibrated normoxic (O 2 partial pressure [PO 2 ]: 153 mmHg; 20.4 kPa) or hypoxic (PO2: 45 mmHg; 6.0 kPa) system water at 28.5°C. This level of hypoxia (45 mmHg) was selected as it induces a peak hypoxic ventilatory response in zebrafish larvae (Mandic et al, 2020) but is above the P crit (oxygen partial pressure at which aerobic metabolism begins to decline) in both genotypes (wild‐type and hif‐1α −/− ), (Mandic et al, 2020) meaning that they would presumably not need to resort to anaerobic metabolism. These fish were then raised to adulthood (3.5 months postfertilisation) under standard (normoxic) rearing conditions.…”

Breathing new life into the critical oxygen partial pressure (Pcrit): a new definition, interpretation and method of determination

“…For comparative purposes, the rates and PO2 values are converted to common units in Table 1 and in the text. In the species analyzed here, a ranged from 0.09 µmol O2 g -1 h -1 kPa -1 for the deep-sea anglerfish, Melanocetus johnsoni, at 5°C (Cowles and Childress, 1995), to 16.65 µmol O2 g -1 h -1 kPa -1 at 28°C for larval zebrafish, Danio rerio (Mandic et al 2020; Table 1). These values are within the previously reported range and are correlated with metabolic rate (Deutsch et al, 2020;Seibel and Deutsch, 2020;Kielland et al, 2019).…”