The power struggle: assessing interacting global change stressors via experimental studies on sharks

Abstract

Ocean warming and acidification act concurrently on marine ectotherms with the potential for detrimental, synergistic effects; yet, effects of these stressors remain understudied in large predatory fishes, including sharks. We tested for behavioural and physiological responses of blacktip reef shark (Carcharhinus melanopterus) neonates to climate change relevant changes in temperature (28 and 31 °C) and carbon dioxide partial pressures (pCO₂; 650 and 1050 µatm) using a fully factorial design. Behavioural assays (lateralisation, activity level) were conducted upon 7-13 days of acclimation, and physiological assays (hypoxia tolerance, oxygen uptake rates, acid-base and haematological status) were conducted upon 14-17 days of acclimation. Haematocrit was higher in sharks acclimated to 31 °C than to 28 °C. Significant treatment effects were also detected for blood lactate and minimum oxygen uptake rate; although, these observations were not supported by adequate statistical power. Inter-individual variability was considerable for all measured traits, except for haematocrit. Moving forward, studies on similarly 'hard-to-study' species may account for large inter-individual variability by increasing replication, testing larger, yet ecologically relevant, differences in temperature and pCO₂, and reducing measurement error. Robust experimental studies on elasmobranchs are critical to meaningfully assess the threat of global change stressors in these data-deficient species.

Figure 1

Behaviour of blacktip reef shark (Carcharhinus melanopterus) neonates measured under various temperatures and partial pressures of carbon dioxide (pCO₂). Relative (L_R; a) and absolute (L_A; b) lateralisation indices, and activity levels (overall dynamic body acceleration, ODBA; c) were quantified for sharks acclimated to ambient (28 °C and 650 µatm pCO₂), high pCO₂ (28 °C and 1050 µatm pCO₂), high temperature (31 °C and 650 µatm pCO₂), and high temperature and high pCO₂ (31 °C and 1050 µatm pCO₂) conditions for 7–13 days. Dots represent individual observations.

Figure 2

Hypoxia tolerance of blacktip reef shark (Carcharhinus melanopterus) neonates measured under various temperatures and partial pressures of carbon dioxide (pCO₂). Hypoxia tolerance was quantified as the percent air saturation at which sharks exhibited the onset of muscle spasms (OS). Sharks were acclimated to ambient (28 °C and 650 µatm pCO₂), high pCO₂ (28 °C and 1050 µatm pCO₂), high temperature (31 °C and 650 µatm pCO₂), and high temperature and pCO₂ (31 °C and 1050 µatm pCO₂) conditions for 14 days. Dots represent individual observations.

Figure 3

Oxygen uptake rates (ṀO₂) of blacktip reef shark (Carcharhinus melanopterus) neonates measured under various temperatures and partial pressures of carbon dioxide (pCO₂). Minimum (ṀO_2Min; a) and maximum (ṀO_2Max; b) oxygen uptake rates, absolute (AAS; c) and factorial aerobic scope (FAS; d), excess post-exercise oxygen consumption (EPOC; e), and time to recover ṀO₂ post-exercise (f) were quantified for sharks acclimated to ambient (28 °C and 650 µatm pCO₂), high pCO₂ (28 °C and 1050 µatm pCO₂), high temperature (31 °C and 650 µatm pCO₂), and high temperature and high pCO₂ (31 °C and 1050 µatm pCO₂) conditions for 16 days. Dots represent individual observations.

Figure 4

Acid-base and haematological status of blacktip reef shark (Carcharhinus melanopterus) neonates measured under various temperatures and partial pressures of carbon dioxide (pCO₂). Blood pH (a) and lactate (b), haematocrit (Hct; c), haemoglobin concentration ([Hb]; d), and mean corpuscular haemoglobin concentration (MCHC; e) were quantified for sharks acclimated to ambient (28 °C and 650 µatm pCO₂), high pCO₂ (28 °C and 1050 µatm pCO₂), high temperature (31 °C and 650 µatm pCO₂), and high temperature and pCO₂ (31 °C and 1050 µatm pCO₂) conditions for 17 days. Dots represent individual observations.