Cardiorespiratory physiology and swimming capacity of Atlantic salmon (Salmo salar) at cold temperatures

Abstract

We investigated how acclimation to 8, 4 and 1°C, and acute cooling from 8 to 1°C, affected the Atlantic salmon's aerobic and anaerobic metabolism, and cardiac function, during a critical swim speed (Ucrit) test. This study revealed several interesting temperature-dependent effects. First, while differences in resting heart rate (fH) between groups were predictable based on previous research (range ∼28-65 beats min-1), with values for 1°C-acclimated fish slightly higher than those of acutely exposed conspecifics, the resting cardiac output () of 1°C-acclimated fish was much lower and compensated for by a higher resting blood oxygen extraction (ṀO2/). In contrast, the acutely exposed fish had a ∼2-fold greater resting stroke volume (VS) compared with that of the other groups. Second, increases in fH (1.2- to 1.4-fold) contributed little to during the Ucrit test, and the contributions of (VS) versus ṀO2/ to aerobic scope (AS) were very different in the two groups tested at 1°C (1°C-acclimated and 8-1°C fish). Finally, Ucrit was 2.08 and 1.69 body lengths (BL) s-1 in the 8 and 4°C-acclimated groups, but only 1.27 and 1.44 BL s-1 in the 1°C-acclimated and 8-1°C fish, respectively - this lower value in 1°C versus 8-1°C fish despite higher values for maximum metabolic rate and AS. These data: support recent studies which suggest that the capacity to increase fH is constrained at low temperatures; show that cardiorespiratory function at cold temperatures, and its response to increased demands, depends on exposure duration; and suggest that AS does not constrain swimming capacity in salmon when chronically exposed to temperatures approaching their lower limit.

Keywords: Acclimation; Cardiac function; Cold; Heart; Oxygen extraction; Swimming; Temperature.

Fig. 1.

Schematic diagram of the experimental design used to determine the critical swim speed (U_crit) of Atlantic salmon exposed to cold temperatures and its effect on their cardiorespiratory and stress physiology. Three groups of fish were acclimated to 8, 4 or 1°C and tested at their respective acclimation temperature, and a fourth group was acclimated to 8°C and tested at 1°C (acute cold exposure). The total time at each swim speed was 15 min and was composed of: a 5 min open (O) period; a 3–10 min closed (C) period to allow the drop in the partial pressure of oxygen (P_O2) to be recorded; and a final open (O) period to allow for percentage saturation to return to >85%. Cardiorespiratory parameters [heart rate (f_H), stroke volume (V_S), cardiac output () and oxygen consumption (Ṁ_O2)] were recorded at rest, at each increase in swim speed, immediately after exhaustion, and 1 h post-exhaustion. Blood samples for various haematological parameters were taken as indicated by ‘X’ (i.e. at rest, immediately after exhaustion and 1 h post-exhaustion).

Fig. 2.

The cardiorespiratory responses of Atlantic salmon acclimated to 8, 4 and 1°C or acutely cooled from 8 to 1°C and then subjected to a U_crit test. (A) f_H, (B) , (C) Ṁ_O2, (D) V_S and (E) oxygen extraction (Ṁ_O2/) at each step during the U_crit test, starting at an initial (resting) speed of 0.25 BL s⁻¹. Dotted lines indicated the speed when the number of fish (n) was reduced, and numbers above particular points indicate the remaining number of fish that made it to that swim speed within a specific group. Values are means±1 s.e.m. with n=7–9 per group, unless otherwise indicated.

Fig. 3.

The haematological responses of Atlantic salmon acclimated to 8, 4 and 1°C or acutely cooled from 8 to 1°C and then subjected to a U_crit test. Data were obtained prior to (at rest), at the end of (exhaustion) and 1 h after (1 h recovery) the U_crit test. Box plots show median (horizontal line), upper and lower quartiles (box) and the 1.5× interquartile range (whiskers). (A) Haematocrit (Hct), (B) haemoglobin concentration ([Hb]) and (C) mean cellular Hb concentration (MCHC). Values without a letter in common are significantly different (P<0.05) between groups at a particular sampling point (lowercase letters) and between sampling points within a group (uppercase letters). Values are means±1 s.e.m. with n=6–8 per group.

Fig. 4.

Changes in plasma lactate and cortisol levels in Atlantic salmon acclimated to 8, 4 and 1°C or acutely cooled from 8 to 1°C and then subjected to a U_crit test. Data were obtained prior to (at rest), at the end of (exhaustion) and 1 h after (1 h recovery) the U_crit test. (A) Plasma lactate. (B) Plasma cortisol. Values without a letter in common are significantly different (P<0.05) between groups at a particular sampling point (lowercase letters) and between sampling points within a group (uppercase letters). The data point in A that is circled represents an outlier and was removed from statistical analysis. Values are means±1 s.e.m. with n=5–8 per group.