Physiological effects of temperature on Greenland halibut Reinhardtius hippoglossoides shows high vulnerability of Arctic stenotherms to global warming.

Global warming affects the metabolism of ectothermic aquatic breathers forcing them to migrate and undergo high-latitudinal distribution shifts to circumvent the temperature-induced mismatch between increased metabolic demand and reduced water oxygen availability. Here the authors examined the effects of temperature on oxygen consumption rates in an Arctic stenotherm, the Greenland halibut Reinhardtius hippoglossoides, and calculated the optimal temperature for maximum aerobic scope, AS(Topt,AS ), which was found to be 2.44°C. They also investigated cardiac performance as limiting the oxygen transport chain at high temperatures by measuring maximum heart rate (fHmax ) over acute temperature increases and found various metrics related to fHmax to be at least 3.2°C higher than Topt,AS . The authors' measured Topt,AS closely reflected in situ temperature occurrences of Greenland halibut from long-term tagging studies, showing that AS of the species is adapted to its habitat temperature, and is thus a good proxy for the species' sensitivity to environmental warming. The authors did not find a close connection between fHmax and Topt,AS , suggesting that cardiac performance is not limiting for the oxygen transport chain at high temperatures in this particular Arctic stenotherm. The authors' estimate of the thermal envelope for AS of Greenland halibut was from -1.89 to 8.07°C, which is exceptionally narrow compared to most other species of fish. As ocean temperatures increase most rapidly in the Arctic in response to climate change, and species in these areas have limited possibility for further poleward-range shifts, these results suggest potential severe effects of global warming on Arctic stenotherms, such as the Greenland halibut. The considerable economic importance of the species raises concerns for future fisheries and species conservation of Arctic stenotherms in the Northern Hemisphere.

A lack of red blood cell swelling in five elasmobranch fishes following air exposure and exhaustive exercise.

In teleost fishes, catecholamine-induced increases in the activity of cation exchangers compensate for decreases in hemoglobin oxygen affinity and maximum blood oxygen carrying capacity caused by decreases in plasma pH (i.e., metabolic acidosis). The resultant red blood cell (RBC) swelling has been documented in sandbar (Carcharhinus plumbeus) and epaulette (Hemiscyllium ocellatum) sharks following capture by rod-and-reel or after a 1.5 h exposure to anoxia (respectively), although the underlying mechanisms remain unknown. To determine if RBC swelling could be documented in other elasmobranch fishes, we collected blood samples from clearnose skate (Rostroraja eglanteria), blacktip reef shark (Carcharhinus melanopterus), and sicklefin lemon shark (Negaprion acutidens) subjected to exhaustive exercise or air exposure (or both) and measured hematocrit, hemoglobin concentration, RBC count, RBC volume, and mean corpuscular hemoglobin content. We did likewise with sandbar and epaulette sharks to further explore the mechanisms driving swelling when present. We could not document RBC swelling in any species; although hematocrit increased in all species (presumably due to RBC ejection from the spleen or fluid shifts out of the vascular compartment) except epaulette shark. Our results indicate RBC swelling and associated ion shifts in elasmobranch fishes is not inducible by exercise or hypoxia, thus implying this response maybe of lesser importance for maintaining oxygen delivery during acute acidosis than in teleost fishes.

Swimming in unsteady water flows: is turning in a changing flow an energetically expensive endeavor for fish?

Unsteady, dynamic flow regimes commonly found in shallow marine ecosystems such as coral reefs pose an energetic challenge for mobile organisms that typically depend on station holding for fitness-related activities. The majority of experimental studies, however, have measured energetic costs of locomotion at steady speeds, with only a few studies measuring the effects of oscillatory flows. In this study, we used a bidirectional swimming respirometer to create six oscillatory water flow regimes consisting of three frequency and amplitude combinations for both unidirectional and bidirectional oscillatory flows. Using the goldring surgeonfish, Ctenochaetus strigosus, a pectoral-fin (labriform) swimmer, we quantified the net cost of swimming (swimming metabolic rate minus standard metabolic rate) associated with station-holding under these various conditions. We determined that the swimming costs of station-holding in the bidirectional flow regime increased by 2-fold compared with costs based on swimming over the same range velocities at steady speeds. Furthermore, as we found minimal differences in energetic costs associated with station-holding in the unidirectional, oscillating-flow compared with that predicted from steady swimming costs, we conclude that the added acceleration costs are minimal, while the act of turning is an energetically expensive endeavor for this reef fish species.

Swimming in unsteady water flows: is turning in a changing flow an energetically expensive endeavor for fish?

Unsteady, dynamic flow regimes commonly found in shallow marine ecosystems such as coral reefs pose an energetic challenge for mobile organisms that typically depend on station-holding for fitness-related activities. The majority of experimental studies, however, have measured energetic costs of locomotion at steady speeds, with only a few studies measuring the effects of oscillatory flows. In this study, we used a bidirectional swimming respirometer to create six oscillatory water flow regimes consisting of three frequency and amplitude combinations for both unidirectional and bidirectional oscillatory flows. Using the goldring surgeonfish, Ctenochaetus strigosus, a pectoral-fin (labriform) swimmer, we quantified the net cost of swimming (swimming metabolic rate minus standard metabolic rate) associated with station-holding under these various conditions. We determined that the swimming costs of station-holding in the bidirectional flow regime increased by 2-fold compared with costs based on swimming over the same range of speeds at steady velocities. Furthermore, as we found minimal differences in energetic costs associated with station-holding in the unidirectional, oscillating flow compared with that predicted from steady swimming costs, we conclude that the added acceleration costs are minimal, while the act of turning is an energetically expensive endeavor for this reef fish species.

Are all bony fishes oxygen regulators? Evidence for oxygen regulation in a putative oxygen conformer, the swamp eel Synbranchus marmoratus.

This study investigated the oxygen consumption of the putative oxygen conformer marbled swamp eel Synbranchus marmoratus during progressive hypoxia. Earlier studies have not reached an agreement on whether S. marmoratus is a conformer or a regulator. Our results support the view that S. marmoratus is an oxygen regulator, like most bony fishes.

Blood pressure in the Greenland shark as estimated from ventral aortic elasticity.

We conducted in vitro inflations of freshly excised ventral aortas of the Greenland shark, Somniosus microcephalus, and used pressure-diameter data to estimate the point of transition from high to low compliance, which has been shown to occur at the mean blood pressure in other vertebrates including fishes. We also determined the pressure at which the modulus of elasticity of the aorta reached 0.4 MPa, as occurs at the compliance transition in other species. From these analyses, we predict the average ventral aortic blood pressure in S. microcephalus to be about 2.3-2.8 kPa, much lower than reported for other sharks. Our results support the idea that this species is slow moving and has a relatively low aerobic metabolism. Histological investigation of the ventral aorta shows that elastic fibres are present in relatively low abundance and loosely connected, consistent with this aorta having high compliance at a relatively low blood pressure.

The effects of elevated potassium, acidosis, reduced oxygen levels, and temperature on the functional properties of isolated myocardium from three elasmobranch fishes: clearnose skate (Rostroraja eglanteria), smooth dogfish (Mustelus canis), and sandbar shark (Carcharhinus plumbeus).

Elevated plasma potassium levels (hyperkalemia), reduced plasma pH (acidosis), reduced blood oxygen content, and elevated temperatures are associated with species-specific rates of at-vessel and post-release mortality in elasmobranch fishes. The mechanism linking these physiological disturbances to mortality remains undetermined however, and we hypothesize that the proximate cause is reduced myocardial function. We measured changes in the functional properties of isolated ventricular myocardial strips from clearnose skate (Rostroraja eglanteria), smooth dogfish (Mustelus canis), and sandbar shark (Carcharhinus plumbeus) when subjected to the following stressors (both in isolation and in combination): hyperkalemia (7.4 mM K+), acidosis (from 7.9 to 7.1), and reduced oxygen (to 31% O2 saturation) applied at temperatures 5 °C above and below holding temperatures. We selected these species based on phylogenetic distance, diverse routine activity levels, and their tolerance to capture and transport. Stressors had a few significant species-specific detrimental impacts on myocardial function (e.g., a 33-45% decrease in net force under acidosis + low O2). Net force production of myocardial strips from clearnose skate and smooth dogfish approximately doubled following exposure to isoproterenol, demonstrating that these species possess beta-adrenergic receptors and that their stimulation could provide a mechanism for preservation of cardiac function during stress. Our results suggest that disruption of physiological homeostasis associated with capture may fatally impair cardiac function in some elasmobranch species, although research with more severe stressors is needed.

The impacts of warming and hypoxia on the performance of an obligate ram ventilator.

Climate change is causing the warming and deoxygenation of coastal habitats like Chesapeake Bay that serve as important nursery habitats for many marine fish species. As conditions continue to change, it is important to understand how these changes impact individual species' behavioral and metabolic performance. The sandbar shark (Carcharhinus plumbeus) is an obligate ram-ventilating apex predator whose juveniles use Chesapeake Bay as a nursery ground up to 10 years of age. The objective of this study was to measure juvenile sandbar shark metabolic and behavioral performance as a proxy for overall performance (i.e. fitness or success) when exposed to warm and hypoxic water. Juvenile sandbar sharks (79.5-113.5 cm total length) were collected from an estuary along the eastern shore of Virginia and returned to lab where they were fitted with an accelerometer, placed in a respirometer and exposed to varying temperatures and oxygen levels. Juvenile sandbar shark overall performance declined substantially at 32°C or when dissolved oxygen concentration was reduced below 3.5 mg l-1 (51% oxygen saturation between 24-32°C). As the extent of warm hypoxic water increases in Chesapeake Bay, we expect that the available sandbar shark nursery habitat will be reduced, which may negatively impact the population of sandbar sharks in the western Atlantic as well as the overall health of the ecosystem within Chesapeake Bay.

Combined Effects of Acute Temperature Change and Elevated pCO2 on the Metabolic Rates and Hypoxia Tolerances of Clearnose Skate (Rostaraja eglanteria), Summer Flounder (Paralichthys dentatus), and Thorny Skate (Amblyraja radiata).

Understanding how rising temperatures, ocean acidification, and hypoxia affect the performance of coastal fishes is essential to predicting species-specific responses to climate change. Although a population's habitat influences physiological performance, little work has explicitly examined the multi-stressor responses of species from habitats differing in natural variability. Here, clearnose skate (Rostaraja eglanteria) and summer flounder (Paralichthys dentatus) from mid-Atlantic estuaries, and thorny skate (Amblyraja radiata) from the Gulf of Maine, were acutely exposed to current and projected temperatures (20, 24, or 28 °C; 22 or 30 °C; and 9, 13, or 15 °C, respectively) and acidification conditions (pH 7.8 or 7.4). We tested metabolic rates and hypoxia tolerance using intermittent-flow respirometry. All three species exhibited increases in standard metabolic rate under an 8 °C temperature increase (Q10 of 1.71, 1.07, and 2.56, respectively), although this was most pronounced in the thorny skate. At the lowest test temperature and under the low pH treatment, all three species exhibited significant increases in standard metabolic rate (44-105%; p < 0.05) and decreases in hypoxia tolerance (60-84% increases in critical oxygen pressure; p < 0.05). This study demonstrates the interactive effects of increasing temperature and changing ocean carbonate chemistry are species-specific, the implications of which should be considered within the context of habitat.

Eye lens radiocarbon reveals centuries of longevity in the Greenland shark (Somniosus microcephalus).

The Greenland shark (Somniosus microcephalus), an iconic species of the Arctic Seas, grows slowly and reaches >500 centimeters (cm) in total length, suggesting a life span well beyond those of other vertebrates. Radiocarbon dating of eye lens nuclei from 28 female Greenland sharks (81 to 502 cm in total length) revealed a life span of at least 272 years. Only the smallest sharks (220 cm or less) showed signs of the radiocarbon bomb pulse, a time marker of the early 1960s. The age ranges of prebomb sharks (reported as midpoint and extent of the 95.4% probability range) revealed the age at sexual maturity to be at least 156 ± 22 years, and the largest animal (502 cm) to be 392 ± 120 years old. Our results show that the Greenland shark is the longest-lived vertebrate known, and they raise concerns about species conservation.

Fast-starting after a breath: air-breathing motions are kinematically similar to escape responses in the catfish Hoplosternum littorale.

Fast-starts are brief accelerations commonly observed in fish within the context of predator-prey interactions. In typical C-start escape responses, fish react to a threatening stimulus by bending their body into a C-shape during the first muscle contraction (i.e. stage 1) which provides a sudden acceleration away from the stimulus. Recently, similar C-starts have been recorded in fish aiming at a prey. Little is known about C-starts outside the context of predator-prey interactions, though recent work has shown that escape response can also be induced by high temperature. Here, we test the hypothesis that air-breathing fish may use C-starts in the context of gulping air at the surface. Hoplosternum littorale is an air-breathing freshwater catfish found in South America. Field video observations reveal that their air-breathing behaviour consists of air-gulping at the surface, followed by a fast turn which re-directs the fish towards the bottom. Using high-speed video in the laboratory, we compared the kinematics of the turn immediately following air-gulping performed by H. littorale in normoxia with those of mechanically-triggered C-start escape responses and with routine (i.e. spontaneous) turns. Our results show that air-breathing events overlap considerably with escape responses with a large stage 1 angle in terms of turning rates, distance covered and the relationship between these rates. Therefore, these two behaviours can be considered kinematically comparable, suggesting that air-breathing in this species is followed by escape-like C-start motions, presumably to minimise time at the surface and exposure to avian predators. These findings show that C-starts can occur in a variety of contexts in which fish may need to get away from areas of potential danger.

Blood gas, oxygen saturation, pH, and lactate values in elasmobranch blood measured with a commercially available portable clinical analyzer and standard laboratory instruments.

Blood gas, pH, and lactate data are often used to assess the physiological status and health of fish and can often be most valuable when blood samples are analyzed immediately after collection. Portable clinical analyzers allow these measurements to be made easily in the field. However, these instruments are designed for clinical use and thus process samples at 37 degrees C. A few studies have validated the use of portable clinical analyzers for assessing blood gases and acid-base profiles in teleosts, but equivalent data are not available for elasmobranchs. We therefore examined the relationship of blood gas, pH, and lactate values measured with an i-STAT portable clinical analyzer with those measured using standard laboratory blood gas (thermostatted to 25 degrees C) and lactate analyzers in samples taken from three species of carcharhiniform sharks. We found tight correlations (r2 > 0.90) between these methods for pH, pO2, pCO2, and lactate level values. We thus developed species-specific equations for converting blood values measured with an i-STAT portable clinical analyzer to those taken at 25 degrees C. Additional studies need to address a wider range of temperatures and elasmobranch species.