Rates of hypoxia induction alter mechanisms of O2 uptake and the critical O2 tension of goldfish

Abstract

The rate of hypoxia induction (RHI) is an important but overlooked dimension of environmental hypoxia that may affect an organism's survival. We hypothesized that, compared with rapid RHI, gradual RHI will afford an organism more time to alter plastic phenotypes associated with O₂ uptake and subsequently reduce the critical O₂ tension (<i>P</i>_crit) of the rate of O₂ uptake (<i>Ṁ</i>_O₂ ). We investigated this by determining <i>P</i>_crit values for goldfish exposed to short (∼24 min), typical (∼84 min) and long (∼480 min) duration <i>P</i>_crit trials to represent different RHIs. Consistent with our predictions, long duration <i>P</i>_crit trials yielded significantly lower <i>P</i>_crit values (1.0-1.4 kPa) than short and typical duration trials, which did not differ (2.6±0.3 and 2.5±0.2 kPa, respectively). Parallel experiments revealed these time-related shifts in <i>P</i>_crit were associated with changes to aspects of the O₂ transport cascade that took place over the hypoxia exposures: gill surface areas and haemoglobin-O₂ binding affinities were significantly higher in fish exposed to gradual RHIs over 480 min than fish exposed to rapid RHIs over 60 min. Our results also revealed that the choice of respirometric technique (i.e. closed versus intermittent) does not affect <i>P</i>_crit or routine <i>Ṁ</i>_O₂ , despite the significantly reduced water pH and elevated CO₂ and ammonia levels measured following closed-circuit <i>P</i>_crit trials of ∼90 min. Together, our results demonstrate that gradual RHIs result in alterations to physiological parameters that enhance O₂ uptake in hypoxic environments. An organism's innate <i>P</i>_crit is therefore most accurately determined using rapid RHIs (<90 min) so as to avoid the confounding effects of hypoxic acclimation.