Ecological energetics of climate change for tropical sharks

Ian Bouyoucos investigated mechanisms of vulnerability to climate change in newborn reef shark populations. He found that blacktip reef sharks (Carcharhinus melanopterus) and sicklefin lemon sharks (Negaprion acutidens) exhibit unique physiological and behavioural responses to climate change conditions. Tropical shark populations could become adversely affected by ocean warming and acidification

Digestive rates of old and new leaves of Sarracenia purpurea without the assistance of Diptera inquilines.

Natural History & EvolutionPrevious research of the purple pitcher plant (Sarracenia purpurea) characterizes the effects of aging on its pitcher leaves, though to date there are no studies that characterize changes in plant-produced digestive enzymes in relation to age. This study looked at the digestive rates in 20 old and new pitchers with and without their Dipteran inquilines, in Mud Lake Bog, MI. Digestion of flies did not differ significantly between pitchers with and without the Diptera in both old and new leaves (P>0.5). During the course of the study the Diptera reoccurred in all but three pitchers, though digestion between old and new pitchers still did not differ significantly (P>0.5). These data suggest that there is no relative difference in digestive rate due to age, though this study could not fully account for purely plant-based digestion.http://deepblue.lib.umich.edu/bitstream/2027.42/89054/1/Bouyoucos_Winfield_2011.pd

Aerobic and anaerobic activity metabolism of an elasmobranch

Animals have finite energy stores and rates at which organisms acquire and use energy can have consequences for fitness. Furthermore, net rates of energy gain or loss can be affected in unknown or unpredictable ways in response to anthropogenic or environmental stressors. Elasmobranchs, in particular, represent some of the most exploited vertebrate taxa on the planet, and many species are data deficient with regard to a basic understanding of energetics or how stressors alter patterns of energy use and allocation. Therefore, the focus of this research was to define relationships between the behavior and energy use for a species of shark both undisturbed in the wild and subjected to the stress of fishing capture. To accomplish this goal, two complimentary series of experiments were conducted to define the frequency and energetic costs of different swimming behaviors in wild, free-swimming sharks (chapter one), and to define the effect of simulated commercial longline fishing capture on the swimming behavior and energy use of a shark (chapter two). The study presented in chapter one offered new insight into the energetics and behavioral partitioning of wild sharks, thereby providing a baseline from which to assess behavioral and, therefore, energetic responses of sharks to stressors. The study presented in chapter two offered an enhanced understanding of the energetics and behavioral responses of sharks to commercial longline capture, with implications for mitigating sub-lethal outcomes of fisheries capture for incidentally caught and released sharks. Together, these studies offer insight into why sharks behave the way they do, stressed or unstressed, and the energetic consequences of their actions, with application to elasmobranch conservation.

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

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 (⁠ṀO2⁠) 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 ṀO2⁠. 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

Same species, different prerequisites: investigating body condition and foraging success in young reef sharks between an atoll and an island system

Acquiring and storing energy is vital to sharks of all age-classes. Viviparous shark embryos receive endogenous maternal energy reserves to sustain the first weeks after birth. Then, in order to maintain body condition, sharks must start foraging. Our goal was to understand whether maternal energy investments vary between blacktip reef sharks (Carcharhinus melanopterus) from two populations and to what extent body condition and the initiation of foraging might be affected by presumably variable maternal investments. A total of 546 young sharks were captured at St. Joseph atoll (Seychelles) and Moorea (French Polynesia) between 2014 and 2018, and indices of body condition and percentage of stomachs containing prey were measured. Maternal investment was found to be site-specific, with significantly larger, heavier, and better conditioned individuals in Moorea. Despite these advantages, as time progressed, Moorea sharks exhibited significant decreases in body condition and were slower to initiate foraging. We suggest that the young sharks’ foraging success is independent of the quality of maternal energy resources, and that other factors, such as prey availability, prey quality, and/or anthropogenic stressors are likely responsible for the observed differences across sites. Insights into intraspecific variations in early life-stages may further support site-specific management strategies for young sharks from nearshore habitats

Analysing tropical elasmobranch blood samples in the field: blood stability during storage and validation of the HemoCue (R) haemoglobin analyser

Blood samples collected from wild-caught fishes can provide important information regarding the effects of capture (and thus post-release survival) as well as other stressors. Unfortunately, blood samples often cannot be analysed immediately upon sampling, and blood parameters (e.g. blood oxygen levels and acid-base parameters) are known to change with storage duration due to the metabolic activity of the red blood cells. We obtained blood samples from both untreated and stressed individuals of both blacktip reef shark (Carcharhinus melanopterus) and sicklefin lemon shark (Negaprion acutidens) to determine the effects of storage duration on blood pH, haematocrit and haemoglobin concentration ([Hb]). We found no significant effects after storage on ice for up to 180 minutes. Moreover, to validate the usability of a HemoCue haemoglobin analyser (a point-of-care device), we compared data from this device to [Hb] determined using the cyanomethaemoglobin method with blood samples from 10 individuals from each of the aforementioned species as well as epaulette shark (Hemiscyllium ocellatum). Values from the HemoCue consistently overestimated [Hb], and we therefore developed the necessary correction equations. The correction equations were not statistically different among the three elasmobranch species within the biologically relevant range but did differ from published corrections developed using blood from temperate teleost fishes. Although the HemoCue is useful in field situations, development of species-specific calibration equations may be necessary to ensure the reliability of inter-species comparisons of blood [Hb]. Together, these data should increase confidence in haematological stress indicators in elasmobranch fishes, measurements of which are critical for understanding the impact of anthropogenic stressors on these ecologically important species

Validation of a portable, waterproof blood pH analyser for elasmobranchs

Quantifying changes in blood chemistry in elasmobranchs can provide insights into the physiological insults caused by anthropogenic stress, and can ultimately inform conservation and management strategies. Current methods for analysing elasmobranch blood chemistry in the field are often costly and logistically challenging. We compared blood pH values measured using a portable, waterproof pH meter (Hanna Instruments HI 99161) with blood pH values measured by an i- STAT system (CG4+ cartridges), which was previously validated for teleost and elasmobranch fishes, to gauge the accuracy of the pH meter in determining whole blood pH for the Cuban dogfish (Squalus cubensis) and lemon shark (Negaprion brevirostris). There was a significant linear relationship between values derived via the pH meter and the i- STAT for both species across a wide range of pH values and temperatures (Cuban dogfish: 6.8-7.1 pH 24-30 degrees C; lemon sharks: 7.0-7.45 pH 25-31 degrees C). The relative error in the pH meter's measurements was similar to +/- 2.7%. Using this device with appropriate correction factors and consideration of calibration temperatures can result in both a rapid and accurate assessment of whole blood pH, at least for the two elasmobranch species examined here. Additional species should be examined in the future across a wide range of temperatures to determine whether correction factors are universal

Simulated heatwave and fishing stressors alter corticosteroid and energy balance in neonate blacktip reef sharks, Carcharhinus melanopterus

The increasing frequency and duration of marine heatwaves attributed to climate change threatens coastal elasmobranchs and may exacerbate existing anthropogenic stressors. While the elasmobranch stress response has been well studied, the role of the unique corticosteroid-1α-hydroxycorticosterone (1α-OHB)-in energy balance is not understood. Therefore, 1α-OHB's utility as a stress biomarker in elasmobranch conservation physiology is equivocal. Here, we analyse the roles of corticosteroids, 1α-OHB and corticosterone, and metabolites, glucose and 3-hydroxybutyrate (3-HB), in response to stress in a protected tropical shark species, the blacktip reef shark (Carcharhinus melanopterus). Wild-caught neonates were exposed to ambient (27°C) or heatwave conditions (29°C) and subsequently a simulated fishing stressor (1 min air exposure). Blood samples were taken prior to temperature exposure, prior to air exposure, and 30 min, 1 h, 24 h, and 48 h post-Air exposure at treatment temperatures. Plasma 1α-OHB was elevated for 48 h in 27°C-exposed sharks but declined over time in 29°C-exposed sharks. Plasma 1α-OHB was not correlated with either metabolite. Plasma glucose was higher and plasma 3-HB was lower in 29°C-exposed sharks. In a separate experiment, blood samples were collected from both neonate and adult sharks immediately following capture and again 5 min later, and analysed for corticosteroids and metabolites. Plasma 1α-OHB increased in neonates within 5 min, but neonates displayed lower plasma 1α-OHB and higher glucose concentrations than adults. We conclude that 1α-OHB does not serve as a classic glucocorticoid role in C. melanopterus under these stressors. Furthermore, we show for the first time, ontogenetic differences in plasma 1α-OHB. Ultimately, our findings provide insights into hormonal control of energy mobilization during stress in C. melanopterus, particularly during simulated heatwave conditions, which seem to alter both endocrine and energy mobilization. Further work is needed to determine the utility of 1α-OHB as a biomarker for the mobilization of energy during a stress event in elasmobranchs

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

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

Tolerance to Hypercarbia Is Repeatable and Related to a Component of the Metabolic Phenotype in a Freshwater Fish

Freshwater fish may be exposed to high levels of carbon dioxide (CO2) because of several actions, including anesthesia and high levels of aquatic respiration and potentially as the result of using high-CO2 plumes as a barrier to the movements of invasive fishes. Metabolic phenotype can potentially drive how freshwater fish respond to high CO2. We therefore quantified how tolerance (measured using time to equilibrium loss [ELT]) was driven by metabolic phenotype in a cosmopolitan freshwater fish species, Micropterus salmoides. ELT was repeatable, with 60% of the variance across trials attributable to individual differences. For each fish, standard metabolic rate and maximum metabolic rate were measured using respirometers and time to exhaustion after a chase test was recorded. Fish with high anaerobic performance were less tolerant to elevated CO2, potentially as a result of preexisting metabolic acidosis. Standard metabolic rate and aerobic scope did not predict ELT. Our findings define which fish may be more vulnerable to high CO2, a potential mechanism for this tolerance, and show that tolerance to high CO2 may be acted on by natural selection. Should freshwater ecosystems become elevated in CO2, by either natural means or anthropogenic means, it is possible that there is potential for heritable selection of CO2 tolerance, evidenced by the fact that ELT was found to be repeatable."The study was supported by Illinois Department of Natural Resources (CAFWS-93) and the US Geological Survey, through funds provided to C.D.S. by the Great Lakes Restoration Initiative (G14AC00119)."https://www.journals.uchicago.edu/doi/abs/10.1086/69337