Spiny dogfish, Squalus suckleyi, shows a good tolerance for hypoxia but need long recovery times

Abstract

Pacific spiny dogfish, Squalus suckleyi, move to shallow coastal waters during critical reproductive life stages and are thus at risk of encountering hypoxic events which occur more frequently in these areas. For effective conservation management, we need to fully understand the consequences of hypoxia on marine key species such as elasmobranchs. Because of their benthic life style, we hypothesized that S. suckleyi are hypoxia tolerant and able to efficiently regulate oxygen consumption, and that anaerobic metabolism is supported by a broad range of metabolites including ketones, fatty acids and amino acids. Therefore, we studied oxygen consumption rates, ventilation frequency and amplitude, blood gasses, acid-base regulation, and changes in plasma and tissue metabolites during progressive hypoxia. Our results show that critical oxygen levels (P _crit) where oxyregulation is lost were indeed low (18.1% air saturation or 28.5 Torr at 13°C). However, many dogfish behaved as oxyconformers rather than oxyregulators. Arterial blood PO₂ levels mostly decreased linearly with decreasing environmental PO₂. Blood gases and acid-base status were dependent on open versus closed respirometry but in both set-ups ventilation frequency increased. Hypoxia below P_crit resulted in an up-regulation of anaerobic glycolysis, as evidenced by increased lactate levels in all tissues except brain. Elasmobranchs typically rely on ketone bodies as oxidative substrates, and decreased concentrations of acetoacetate and β-hydroxybutyrate were observed in white muscle of hypoxic and/or recovering fish. Furthermore, reductions in isoleucine, glutamate, glutamine and other amino acids were observed. After 6 hours of normoxic recovery, changes persisted and only lactate returned to normal in most tissues. This emphasizes the importance of using suitable bioindicators adjusted to preferred metabolic pathways of the target species in conservation physiology. We conclude that Pacific spiny dogfish can tolerate severe transient hypoxic events, but recovery is slow and negative impacts can be expected when hypoxia persists.

Keywords: 1H-NMR spectroscopy; Abbreviations: PCA principal component analysis; TMAO trimethylamine oxide; amino acids; critical oxygen pressure; elasmobranch; hypoxia; ketones; metabolomics; recovery; shark.

Figure 1

Oxygen consumption rates (MO₂) of spiny dogfish, Squalus acanthias suckleyi, during progressive hypoxia in closed respirometry (dots represent MO₂ calculated over 15 min intervals, N = 10). Two individual fish with different MO₂ profiles are highlighted with triangles (with apparent critical oxygen level) and diamonds (without apparent critical oxygen level).

Figure 2

Blood parameters of spiny dogfish, Squalus acanthias suckleyi, during progressive hypoxia in closed respirometry (N = 5) or open respirometry (N = 5) where hypoxia was achieved by N₂ bubbling. Linear regressions are shown with their 95% confidence intervals and P values are indicated.

Figure 3

Plasma lactate of spiny dogfish, Squalus acanthias suckleyi, during progressive hypoxia in open respirometry (N = 5). Linear regression is shown with its 95% confidence intervals (P < 0.05).

Figure 4

Ventilation amplitude, ventilation frequency and ventilatory index of spiny dogfish, Squalus acanthias suckleyi, during progressive hypoxia in closed respirometry (N = 5) or open respirometry (N = 5) where hypoxia was reached by N₂ bubbling. P values are derived from correlation analysis, segmented linear regression provided a better fit than linear regression and is shown when significant.