Thermal tolerance and hypoxia tolerance are associated in blacktip reef shark (Carcharhinus melanopterus) neonates

Abstract

Thermal dependence of growth and metabolism can influence thermal preference and tolerance in marine ectotherms, including threatened and data-deficient species. Here, we quantified the thermal dependence of physiological performance in neonates of a tropical shark species (blacktip reef shark, Carcharhinus melanopterus) from shallow, nearshore habitats. We measured minimum and maximum oxygen uptake rates (ṀO2), calculated aerobic scope, excess post-exercise oxygen consumption and recovery from exercise, and measured critical thermal maxima (CTmax), thermal safety margins, hypoxia tolerance, specific growth rates, body condition and food conversion efficiencies at two ecologically relevant acclimation temperatures (28 and 31°C). Owing to high post-exercise mortality, a third acclimation temperature (33°C) was not investigated further. Acclimation temperature did not affect ṀO2 or growth, but CTmax and hypoxia tolerance were greatest at 31°C and positively associated. We also quantified in vitro temperature (25, 30 and 35°C) and pH effects on haemoglobin–oxygen (Hb–O2) affinity of wild-caught, non-acclimated sharks. As expected, Hb–O2 affinity decreased with increasing temperatures, but pH effects observed at 30°C were absent at 25 and 35°C. Finally, we logged body temperatures of free-ranging sharks and determined that C. melanopterus neonates avoided 31°C in situ. We conclude that C. melanopterus neonates demonstrate minimal thermal dependence of whole-organism physiological performance across a seasonal temperature range and may use behaviour to avoid unfavourable environmental temperatures. The association between thermal tolerance and hypoxia tolerance suggests a common mechanism warranting further investigation. Future research should explore the consequences of ocean warming, especially in nearshore, tropical species.

Elasmobranch Responses to Experimental Warming, Acidification, and Oxygen Loss—A Meta-Analysis

“…Moreover, the effects of EA and EWA have not been addressed and should be considered in future studies. On the other hand, no significant effects of either treatment were observed over hypoxia tolerance (Figure 6B; Supplementary Table 3), despite previous indication that these two responses may be intertwined (Butler and Taylor, 1975;Ely et al, 2014;Bouyoucos et al, 2020a). Likewise, cell stress levels, particularly oxidative damage, appear not to be affected by EA (Figure 6C; Supplementary Table 3), with elasmobranchs relying on non-enzymatic ROS-scavengers in addition to enzymatic antioxidants, which may be a potential explanation for their resilience (Lopes et al, 2018;Pegado et al, 2020a).…”

“…In addition to increasing oxygen demands, oxygen affinity typically decreases with temperature (Nikinmaa et al, 2019), and several elasmobranch species have been shown to adjust their hematological profile in response to environmental challenges, namely temperature (Butler and Taylor, 1975;Neale et al, 1977;Bouyoucos et al, 2020a;Pegado et al, 2020b). However, no significant overall effect was detected for EW or EA for the endpoints analyzed here, with insufficient data to conduct the analysis for EWA (Figure 5E; Supplementary Table 3).…”

“…Thermal tolerance showed an overall positive response to EW (Figure 6A; Supplementary Table 3). It is nonetheless worth noting that, while thermal tolerance does seem to increase, thermal safety margins are likely to decline (Bouyoucos et al, 2020a), which is particularly important in the context of gradual OW and simultaneously more pervasive MHWs. In this context, while animals may cope with OW and mild MHWs, their capacity to withstand severe or extreme MHWs may be undercut.…”

Future thermal regimes for epaulette sharks (Hemiscyllium ocellatum): growth and metabolic performance cease to be optimal

“…The initial slope of oxygen uptake was used to calculate Ṁ O 2Max , and then neonates remained in the chamber until oxygen uptake rates returned to Ṁ O 2Rest levels measured for the individuals during their respective previous trial at 30 days post-hatch. A scaling exponent of 0.89 was used to correct the mass of each individual for the allometric relationship of mass and metabolic rate 47 , 48 . Finally, aerobic scope (AS) was calculated as Ṁ O 2Max − Ṁ O 2Rest 31 .…”

Diel Rhythm and Thermal Independence of Metabolic Rate in a Benthic Shark

“…Each chamber consisted of a flush pump (small chambers: 1200 L h -1 ; large chamber: 2400 L h -1 ) that pumped water from the water bath and one recirculating pump (small chambers: 1200 L h -1 ; large chamber: 2400 L h -1 ) that circulated water through an external loop for proper homogeneous mixing within the chamber. Oxygen levels were measured every 2 sec using an OXROB3 fiber optic probe inserted approximately 5 cm into the chamber proper via the overflow outlet (Bouyoucos et al, 2020a) connected to a Firesting Optical Oxygen Meter (Pyroscience GmbH, Aachen, Germany).…”