Dead tired: evaluating the physiological status and survival of neonatal reef sharks under stress

Abstract

Marine protected areas (MPAs) can protect shark populations from targeted fisheries, but resident shark populations may remain exposed to stressors like capture as bycatch and environmental change. Populations of young sharks that rely on shallow coastal habitats, e.g. as nursery areas, may be at risk of experiencing these stressors. The purpose of this study was to characterize various components of the physiological stress response of neonatal reef sharks following exposure to an exhaustive challenge under relevant environmental conditions. To accomplish this, we monitored markers of the secondary stress response and measured oxygen uptake rates ( $\dot{M}{O}_2$ ) to compare to laboratory-derived baseline values in neonatal blacktip reef (Carcharhinus melanopterus) and sicklefin lemon sharks (Negaprion acutidens). Measurements occurred over three hours following exposure to an exhaustive challenge (gill-net capture with air exposure). Blood lactate concentrations and pH deviated from baseline values at the 3-h sample, indicating that both species were still stressed 3 h after capture. Evidence of a temperature effect on physiological status of either species was equivocal over 28-31°C. However, aspects of the physiological response were species-specific; N. acutidens exhibited a larger difference in blood pH relative to baseline values than C. melanopterus, possibly owing to higher minimum $\dot{M}{O}_2$ . Neither species experienced immediate mortality during the exhaustive challenge; although, single instances of delayed mortality were documented for each species. Energetic costs and recovery times could be extrapolated for C. melanopterus via respirometry; sharks were estimated to expend 9.9 kJ kg^-1 (15% of energy expended on daily swimming) for a single challenge and could require 8.4 h to recover. These data suggest that neonatal C. melanopterus and N. acutidens are resilient to brief gill-net capture durations, but this was under a narrow temperature range. Defining species' vulnerability to stressors is important for understanding the efficacy of shark conservation tools, including MPAs.

Keywords: Bycatch; marine protected areas; oxygen uptake rates; physiological stress response; shark nursery areas; temperature.

Figure 1:

Indicators of the stress response in juvenile blacktip reef sharks (Carcharhinus melanopterus) following an exhaustive challenge in situ. Baseline values were taken from quiescent, fasted sharks (“baseline”). Other sharks were phlebotomized immediately following exhaustive gill-net capture (“immediate”), after three hours in a recovery bag (“three-hour”) or after 3 h in a field respirometry chamber (“respirometry”). Differing letters denote statistically significant differences. Abbreviation: mean cell haemoglobin concentration (MCHC).

Figure 2:

Relationship between temperature and physiological status (blood glucose concentrations) for blacktip reef sharks (Carcharhinus melanopterus).

Figure 3:

Indicators of the stress response in juvenile sicklefin lemon sharks (Negaprion acutidens) following an exhaustive challenge in situ. Baseline values were taken from quiescent, fasted sharks (“baseline”). Other sharks were phlebotomized immediately following exhaustive gill-net capture (“immediate”) or after 3 h in a recovery bag (“three-hour”). Differing letters denote statistically significant differences. Abbreviation: mean cell haemoglobin concentration (MCHC).

Figure 4:

Relationship between temperature and physiological status (haemoglobin concentrations) for sicklefin lemon sharks (Negaprion acutidens).

Figure 5:

Representative traces of excess post-exercise oxygen consumption (EPOC). Data are presented for individual Carcharhinus melanopterus in good condition (a) and moribund (b). Oxygen uptake rates (ṀO₂) were measured for 3 h after sharks were caught in gill-nets. Recovery time was extrapolated by fitting ṀO₂ with an exponential decay function. The upper 95% confidence interval limit of minimum ṀO₂ (horizontal line) was estimated from captive C. melanopterus, and the intersection of these two lines represent an individual’s extrapolated recovery time. The data in the lower panel are not fit with a recovery curve, because this individual exhibited aerobic failure when ṀO₂ dropped below its estimated “recovered” value.