Thermoregulatory response in juvenile Hippocampus erectus: Effect of magnitude and rate of thermal increase on metabolism and antioxidative defence

Abstract

Behavioural, physiological and biochemical mechanisms constitute the adaptive capacities that allow marine ectotherms to explore the environment beyond their thermal optimal. Limitations to the efficiency of these mechanisms define the transition from moderate to severe thermal stress, and serve to characterise the thermoregulatory response in the zone of thermal tolerance. We selected a tropical population of Hippocampus erectus to describe the timing of the physiological and biochemical mechanisms in response to the following increments in water temperature: (i) 4°C abrupt (26-30°C in <5 min); (ii) 7°C abrupt (26-33°C); (iii) 4°C gradual (1°C every 3 h) and (iv) 7°C gradual (1.5°C every 3 h). The routine metabolic rate (Rrout) of juvenile H. erectus was measured immediately before and after 0.5, 12 and 28 h of being exposed to each thermal treatment. Samples of muscle and abdominal organs were taken to quantify indicators of aerobic and anaerobic metabolism and antioxidant enzymes and oxidative stress at each moment throughout exposure. Results showed a full thermoregulatory response within 0.5 h: Rrout increased in direct correspondence with both the magnitude and rate of thermal increase; peroxidised lipids rapidly accumulated before the antioxidant defence was activated and early lactate concentrations suggested an immediate, yet temporary, reduction in aerobic scope. After 12 h, Rrout had decreased in sea horses exposed to 30°C, but not to 33°C, where Rrout continued high until the end of trials. Within 28 h of thermal exposure, all metabolite and antioxidant defence indicators had been restored to control levels (26°C). These findings testify to the outstanding thermal plasticity of H. erectus and explain their adjustment to rapid fluctuations in ambient temperature. Such features, however, do not protect this tropical population from the deleterious effects of chronic exposure to temperatures that have been predicted for the future.

Keywords: antioxidative defence; ocean warming; routine metabolism; sea horses; thermal biology; thermal tolerance.

FIGURE 1

Oxygen consumption (mean values ± standard deviation) of juvenile Hippocampus erectus prior to thermal change and after 0.5, 12 and 28 h of exposure to (a) abrupt increments from 26 to 30°C (Ab 30) and 26 to 33°C (Ab 33); (b) abrupt (Ab 30) and gradual increments from 26 to 30°C (Gr 30) and (c) abrupt (Ab 33) and gradual increments from 26 to 33°C (Gr 33).

FIGURE 2

Principal coordinate ordination on metabolites (Lact, Gluco, Prot, Chol, Acyl) of juvenile Hippocampus erectus measured after 0.5, 12 and 28 h of exposure to abrupt and gradual increments from 26 to 30°C (4°C, Ab 30 and Gr 30) and 26 to 33°C (7°C, Ab 33 and Gr 33 respectively) and in a control group kept constant a 26°C (Control). Data were log‐transformed and normalised prior to obtaining a resemblance matric of Euclidean distances between samples.

FIGURE 3

Principal Coordinate ordination on antioxidant enzymes and oxidative stress indicators (GSH, SOD, CAT, GST, LPO, PO) of juvenile Hippocampus erectus measured after 0.5, 12 and 28 h of exposure to abrupt and gradual increments from 26 to 30°C (4°C, Ab 30 and Gr 30) and 26 to 33°C (7°C, Ab 33 and Gr 33 respectively) and in a control group kept constant a 26°C (Control). Data were log‐transformed and normalised prior to obtaining a resemblance matric of Euclidean distances between samples.

FIGURE 4

Principal Coordinate ordination on esterase activity (AChE, CbE) of juvenile Hippocampus erectus measured after 0.5, 12 and 28 h of exposure to abrupt and gradual increments from 26 to 30°C (4°C, Ab 30 and Gr 30) and 26 to 33°C (7°C, Ab 33 and Gr 33 respectively) and in a control group kept constant a 26°C (Control). Data were log‐transformed and normalised prior to obtaining a resemblance matric of Euclidean distances between samples.