Low O2 acclimation shifts the hypoxia avoidance behaviour of snapper (Pagrus auratus) with only subtle changes in aerobic and anaerobic function

Abstract

SUMMARYIt was hypothesised that chronic hypoxia acclimation (preconditioning) would alter the behavioural low-O 2 avoidance strategy of fish as a result of both aerobic and anaerobic physiological adaptations. Avoidance and physiological responses of juvenile snapper (Pagrus auratus) were therefore investigated following a 6week period of moderate hypoxia exposure (10.2-12.1kPa P O2 , 21±1°C) and compared with those of normoxic controls (P O2 =20-21kPa, 21±1°C). The critical oxygen pressure (P crit ) limit of both groups was unchanged at ~7kPa, as were standard, routine and maximum metabolic rates. However, hypoxia-acclimated fish showed increased tolerances to hypoxia in behavioural choice chambers by avoiding lower P O2 levels (3.3±0.7 vs 5.3±1.1kPa) without displaying greater perturbations of lactate or glucose. This behavioural change was associated with unexpected physiological adjustments. For example, a decrease in blood O 2 carrying capacity was observed after hypoxia acclimation. Also unexpected was an increase in whole-blood P 50 following acclimation to low O 2 , perhaps facilitating Hb-O 2 off-loading to tissues. In addition, cardiac mitochondria measured in situ using permeabilised fibres showed improved O 2 uptake efficiencies. The proportion of the anaerobic enzyme lactate dehydrogenase, at least relative to the aerobic marker enzyme citrate synthase, also increased in heart and skeletal red muscle, indicating enhanced anaerobic potential, or in situ lactate metabolism, in these tissues. Overall, these data suggest that a prioritization of O 2 delivery and O 2 utilisation over O 2 uptake during long-term hypoxia may convey a significant survival benefit to snapper in terms of behavioural low-O 2 tolerance.

Aquatic surface respiration and swimming behaviour in adult and developing zebrafish exposed to hypoxia

“…Yet another possibility is that severe hypoxia may be perceived by fish as a noxious or painful stimulus. Some authors have identified an aversive behaviour that may lead fish away from regions of severe hypoxia and toward the surface (Petersen and Petersen, 1990;Weltzien et al, 1999;Poulsen et al, 2011;Cook et al, 2013). In the present study, ASR behaviour in zebrafish was punctuated with brief trips to the bottom of the chamber before returning rapidly to the surface.…”

Hypoxia delays hematopoiesis: retention of embryonic hemoglobin and erythrocytes in larval rainbow trout,Oncorhynchus mykiss, during chronic hypoxia exposure

“…One explanation for this discrepancy is that a developmentally appropriate P 50 value may be guarded in early life stages regardless of environmental O 2 levels to ensure adequate unloading at the tissues, as seen in some adult teleosts (e.g. Cook et al, 2013). Although hypoxic larvae are developmentally delayed and smaller than their normoxic counterparts, they still experience an eightfold increase in mass between Stages 27 and 35, and their mass is only 7 and 29% less than stage-matched normoxic Stage 33 and 35 larvae, respectively.…”

Mitochondrial energetics of benthic and pelagic Antarctic teleosts

“…Interestingly, a recent study by Urschel and O'Brien (2009) Leak respiration rates observed when both complexes I and II were activated at temperatures below ABT only constitute about 10% of state III rates obtained at the same temperature (Figure 2). This value is small compared to about 50% of state III with only complex I activated in snapper mitochondria (Cook et al 2013), and slightly lower than 15% of state III found in permeabilized heart ventricle fibers of triplefin blennies at 15°C (Hilton et al 2010). However, similar values have been obtained for the notothenioid L. nudifrons (10.2% at 0°C), which suggest a low proton leakiness of the inner mitochondrial membrane in notothenioids (Hardewig et al 1999b).…”

“…More recent studies utilized titrations including PM to activate complex I, PMS to activate both complexes I and II and others have used rotenone as a complex I inhibitor in the presence of S to activate solely complex II (Weinstein and Somero 1998;Hardewig et al 1999a;Lannig et al 2005). The addition of glutamate and the overall combination of PMGS in a single run has been utilized in snappers recently (Cook et al 2013), and our study constitutes the first attempt in notothenioids. Recent studies on human muscle mitochondria showed additive effects of those substrates, mainly due to the convergent nature of the ETS (Gnaiger 2009).…”

“…Recent advances in mitochondrial physiology have provided insights into the use of substrate combinations for maximally engaging electron carriers and substrate transporters for measurements of OXPHOS capacity in mammals (Gnaiger 2010a;Gnaiger 2010b). The activation of both mitochondrial complexes I and II in fish mitochondria by the simultaneous addition of millimolar levels of pyruvate, glutamate, malate and succinate have been proven useful in activating mitochondrial respiration in fishes (Cook et al 2013). …”