Research on sablefish (Anoplopoma fimbria) suggests that limited capacity to increase heart function leaves hypoxic fish susceptible to heat waves

Abstract

Studies of heart function and metabolism have been used to predict the impact of global warming on fish survival and distribution, and their susceptibility to acute and chronic temperature increases. Yet, despite the fact that hypoxia and high temperatures often co-occur, only one study has examined the effects of hypoxia on fish thermal tolerance, and the consequences of hypoxia for fish cardiac responses to acute warming have not been investigated. We report that sablefish (Anoplopoma fimbria) did not increase heart rate or cardiac output when warmed while hypoxic, and that this response was associated with reductions in maximum O₂ consumption and thermal tolerance (CT_max) of 66% and approximately 3°C, respectively. Further, acclimation to hypoxia for four to six months did not substantially alter the sablefish's temperature-dependent physiological responses or improve its CT_max. These results provide novel, and compelling, evidence that hypoxia can impair the cardiac and metabolic response to increased temperatures in fish, and suggest that some coastal species may be more vulnerable to climate change-related heat waves than previously thought. Further, they support research showing that cross-tolerance and physiological plasticity in fish following hypoxia acclimation are limited.

Keywords: cardiac function; climate change; haematology; hypoxia; temperature; thermal tolerance.

Figure 1.

Cardiorespiratory responses of normoxia- and hypoxia-acclimated sablefish exposed to hypoxic or normoxic warming. Shown are (a,b) heart rate (ƒ_H), (c,d) cardiac output (Q̇$\dot{Q}$), (e,f) stroke volume (V_S), (g,h) O₂ consumption (Ṁ$\dot{M}$O₂) and (i,j) O₂ extraction (Ṁ$\dot{M}$O₂/Q̇$\dot{Q}$). Hypoxic warming, left panels; normoxic warming, right panels. Symbols without a letter in common are significantly different across the sampling points/temperatures (p < 0.05). In the case of a significant acclimation effect and/or acclimation × sampling interaction, lower and uppercase letters indicate differences within the normoxia- and hypoxia-acclimated groups, respectively. Asterisks indicate significant differences between acclimation groups at a particular sampling point (*p < 0.05; **p < 0.01; ***p < 0.001). Values are means ± s.e.m. with n = 14–15 per group for the initial experiment (except at 22°C where n = 9–10 per group, because 4–6 fish had already reached their CT_max), and with n = 9 for the additional experiment (except at 24°C where n = 8, because one fish had already reached its CT_max).

Figure 2.

The capacity of normoxia- and hypoxia-acclimated sablefish to increase cardiorespiratory function (i.e. heart function and oxygen consumption/extraction by the tissues) when exposed to hypoxic and normoxic warming, and parameters related to thermal tolerance. Values for scope were calculated as maximum—resting values for (a) cardiac output (Q̇), (b) O₂ consumption (Ṁ$\dot{M}$O₂) and (c) O₂ extraction (Ṁ$\dot{M}$O₂/Q̇). (d) Parameters for thermal tolerance are the onset temperature of cardiac arrhythmias (T_arrhythmia) and the critical thermal maximum (CT_max). The normoxia-acclimated fish tested under hypoxia are compared to the other two groups (n.s. = p > 0.05; *p < 0.05; **p < 0.01; ***p < 0.001). Values are means ± s.e.m. with n = 14–15 and n = 9 per group for hypoxic and normoxic warming, respectively. (Online version in colour.)

Figure 3.

The relationship between Ṁ$\dot{M}$O₂ and Q̇ in normoxia- and hypoxia-acclimated sablefish exposed to hypoxic and normoxic warming. No significant linear regression could be fitted to the data for the normoxia and hypoxia acclimation groups tested under hypoxia (p = 0.064 and p = 0.884, respectively), whereas a significant linear regression was fitted to the data for the fish tested under normoxia (p < 0.001, r² = 0.918, y = 8.6x–112.0). The symbols for the latter group are labelled with grey numbers, which indicate the following conditions: 1, 12°C; 2, 14°C; 3, 16°C; 4, 18°C; 5, 20°C; 6, 22°C; 7, 24°C at normoxia. Values are means ± s.e.m. with n = 14–15 per group for the hypoxic warming experiment (except at 22°C where n = 9–10 per group, because 4–6 fish had already reached their CT_max), and with n = 9 for the normoxic warming experiment (except at 24°C where n =8, because one fish had already reached its CT_max).

Figure 4.

Haematological changes in normoxia- and hypoxia-acclimated sablefish when exposed to hypoxic warming. Shown are blood/plasma levels of (a) haematocrit (Hct), (b) haemoglobin (Hb), (c) mean cellular haemoglobin concentration (MCHC), (d) lactate, (e) glucose, (f) cortisol, (g) adrenaline and (h) noradrenaline. CT_max, critical thermal maximum. Symbols without a letter in common are significantly different across the sampling points/temperatures (p < 0.05). In the case of a significant acclimation effect and/or acclimation × sampling interaction, lower and uppercase letters indicate differences within the normoxia- and hypoxia-acclimated groups, respectively. Asterisks indicate significant differences between acclimation groups at a particular sampling point (**p < 0.01; ***p < 0.001). Values are means ± s.e.m. with n = 9–10 per group.