Progressive hypoxia decouples activity and aerobic performance of skate embryos.

Valentina Di Santo,Anna H Tran,Jon C Svendsen

doi:10.1093/conphys/cov067

Valentina Di Santo, Anna H Tran + Show 1 more

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https://doi.org/10.1093/conphys/cov067

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Abstract

Although fish population size is strongly affected by survival during embryonic stages, our understanding of physiological responses to environmental stressors is based primarily on studies of post-hatch fishes. Embryonic responses to acute exposure to changes in abiotic conditions, including increase in hypoxia, could be particularly important in species exhibiting long developmental time, as embryos are unable to select a different environment behaviourally. Given that oxygen is key to metabolic processes in fishes and aquatic hypoxia is becoming more severe and frequent worldwide, organisms are expected to reduce their aerobic performance. Here, we examined the metabolic and behavioural responses of embryos of a benthic elasmobranch fish, the little skate (Leucoraja erinacea), to acute progressive hypoxia, by measuring oxygen consumption and movement (tail-beat) rates inside the egg case. Oxygen consumption rates were not significantly affected by ambient oxygen levels until reaching 45% air saturation (critical oxygen saturation, S crit). Below S crit, oxygen consumption rates declined rapidly, revealing an oxygen conformity response. Surprisingly, we observed a decoupling of aerobic performance and activity, as tail-beat rates increased, rather than matching the declining metabolic rates, at air saturation levels of 55% and below. These results suggest a significantly divergent response at the physiological and behavioural levels. While skate embryos depressed their metabolic rates in response to progressive hypoxia, they increased water circulation inside the egg case, presumably to restore normoxic conditions, until activity ceased abruptly around 9.8% air saturation.

Highlights

Many marine ecosystems are expected to experience physicochemical changes associated with increasing anthropogenic greenhouse gas emissions (Intergovernmental Panel on Climate Change, 2013)
There was no gradual decrease in tail-beat frequency as a function of progressive hypoxia
Hypoxic events have increased in frequency, severity and geographical extent and it is crucial to know the response of fish performance at different levels of hypoxia (Herbert et al, 2011)

Summary

Introduction

Many marine ecosystems are expected to experience physicochemical changes associated with increasing anthropogenic greenhouse gas emissions (Intergovernmental Panel on Climate Change, 2013). As oxygen is key to sustain every aerobic activity, it is important to understand whether and how marine organisms might tune their metabolic performance to cope with more frequent and intense hypoxic events This is crucial for benthic organisms inhabiting near-coastal waters as these are expected to be much more affected by hypoxia than highly mobile, pelagic species that are likely to possess the locomotory capacity required to sustain migrations to refugia (Lauder and Di Santo, 2015). Perhaps reflecting adaptations to typically low-oxygen environments, benthic organisms are generally thought to be able to tolerate moderate-to-severe levels of hypoxia (Seibel, 2011; Heinrich et al, 2014) Despite this fact, populations of several benthic species have already declined during the last decades, and low oxygen levels are often implicated in the impairment of vital activities, including foraging and reproduction (Schurmann and Steffensen, 1997; Behrens and Steffensen, 2007; Svendsen et al, 2012)

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