Jonathan A. W. Stecyk

Trophic Structure and Community Stability in an Overfished Ecosystem

Gobbled by Gobies A common feature of overfished marine ecosystems is a tendency for biomass to become dominated by jellyfish and microbes, and for the habitat to become anoxic or hypoxic as large fish species are removed. The Benguela ecosystem off the coast of Namibia is a case in point. Utne-Palm et al. (p. 333) describe how the loss of overfished sardines from the Benguela fishery has provided an opportunity for an endemic fish species, the bearded goby, to exploit jellyfish and microbial biomass and to increase in number. These small fish have in turn become the predominant prey species for the larger fish, birds, and mammals in the region. The significance of the goby lies in its ability to forage on resources traditionally regarded as “dead-ends.” The bearded goby has thus become a key stabilizing component to the turnover of energy in the Benguela ecosystem. An endemic goby exploits jellyfish and microbial biomass, partially restoring the food chain in the Benguela ecosystem. Since the collapse of the pelagic fisheries off southwest Africa in the late 1960s, jellyfish biomass has increased and the structure of the Benguelan fish community has shifted, making the bearded goby (Sufflogobius bibarbatus) the new predominant prey species. Despite increased predation pressure and a harsh environment, the gobies are thriving. Here we show that physiological adaptations and antipredator and foraging behaviors underpin the success of these fish. In particular, body-tissue isotope signatures reveal that gobies consume jellyfish and sulphidic diatomaceous mud, transferring “dead-end” resources back into the food chain.

α-Adrenergic regulation of systemic peripheral resistance and blood flow distribution in the turtle Trachemys scripta during anoxic submergence at 5°C and 21°C

SUMMARY Anoxic exposure in the anoxia-tolerant freshwater turtle is attended by substantial decreases in heart rate and blood flows, but systemic blood pressure (Psys) only decreases marginally due to an increase in systemic peripheral resistance (Rsys). Here, we investigate the role of the α-adrenergic system in modulating Rsys during anoxia at 5°C and 21°C in the turtle Trachemys scripta, and also describe how anoxia affects relative systemic blood flow distribution (%Q̇sys) and absolute tissue blood flows. Turtles were instrumented with an arterial cannula for measurement of Psys and ultrasonic flow probes on major systemic blood vessels for determination of systemic cardiac output (Q̇sys). α-Adrenergic tone was assessed from vascular injections of α-adrenergic agonists and antagonists (phenylephrine and phentolamine, respectively) during normoxia and following either 6 h (21°C) or 12 days (5°C) of anoxic submergence. Coloured microspheres, injected through a left atrial cannula during normoxia and anoxia, as well as after α-adrenergic stimulation and blockade during anoxia at both temperatures, were used to determine relative and absolute tissue blood flows. Anoxia was associated with an increased Rsys and functional α-adrenergic vasoactivity at both acclimation temperatures. However, while anoxia at 21°C was associated with a high systemicα -adrenergic tone, the progressive increase of Rsys at 5°C was not mediated by α-adrenergic control. A redistribution of blood flow away from ancillary vascular beds towards more vital circulations occurred with anoxia at both acclimation temperatures. %Q̇sys and absolute blood flow were reduced to the digestive and urogenital tissues (approximately 2- to 15-fold), while %Q̇sys and absolute blood flows to the heart and brain were maintained at normoxic levels. The importance of liver and muscle glycogen stores in fueling anaerobic metabolism were indicated by increases in %Q̇sys to the muscle at 21°C (1.3-fold) and liver at 5°C (1.7-fold). As well, the crucial importance of the turtle shell as a buffer reserve during anoxic submergence was indicated by 40-50% of Q̇sys being directed towards the shell during anoxia at both 5°C and 21°C. α-Adrenergic stimulation and blockade during anoxia caused few changes in %Q̇sys and absolute tissue blood flow. However, there was evidence of α-adrenergic vasoactivity contributing to blood flow regulation to the liver and shell during anoxic submergence at 5°C.

New insights into the plasticity of gill structure

The ability of some fishes to reversibly remodel their gill morphology has become a focus of research after the discovery of extreme morphological gill plasticity in crucian carp and goldfish-both members of the cyprinid genus Carassius. Their lamellae are largely embedded in an interlamellar cell mass (ILCM) during normoxic conditions in cold water. The ILCM regresses in hypoxia, warm water, and during exercise, whereby the respiratory surface area and the capacity for oxygen uptake are greatly increased. There may be several reasons for covering the lamellae when oxygen needs are low. Reducing osmoregulatory costs have been suggested as an advantage of gill remodeling, but this has been difficult to show, putting the importance of the osmo-respiratory compromise into question. Other reasons could be to limit uptake of toxic substances and to reduce the risks for infections. In support for the latter, we present evidence showing that crucian carp infected by gill flukes maintain their ILCM when exposed to hypoxia. So far, gill remodeling in response to oxygen needs has been seen in several cyprinids, killifish and eel. In response to other environmental factors it may also occur in salmonids and anabantoids, revealing a phylogenetically widespread occurrence among teleosts.

Differential regulation of AMP-activated kinase and AKT kinase in response to oxygen availability in crucian carp (Carassius carassius)

We investigated whether two kinases critical for survival during periods of energy deficiency in anoxia-intolerant mammalian species, AMP-activated kinase (AMPK), and protein kinase B (AKT), are equally important for hypoxic/anoxic survival in the extremely anoxia-tolerant crucian carp (Carassius carassius). We report that phosphorylation of AMPK and AKT in heart and brain showed small changes after 10 days of severe hypoxia (0.3 mg O2/l at 9 degrees C). In contrast, anoxia exposure (0.01 mg O2/l at 8 degrees C) substantially increased AMPK phosphorylation but decreased AKT phosphorylation in carp heart and brain, indicating activation of AMPK and deactivation of AKT. In agreement, blocking the activity of AMPK in anoxic fish in vivo with 20 mg/kg Compound C resulted in an elevated metabolic rate (as indicated by increased ethanol production) and tended to reduce energy charge. This is the first in vivo experiment with Compound C in a nonmammalian vertebrate, and it appears that AMPK plays a role in mediating anoxic metabolic depression in crucian carp. Real-time RT-PCR analysis of the investigated AMPK subunit revealed that the most likely composition of subunits in the carp heart is alpha2, beta1B, gamma2a, whereas a more even expression of subunits was found in the brain. In the heart, expression of the regulatory gamma2-subunit increased in the heart during anoxia. In the brain, expression of the alpha1-, alpha2-, and gamma1-subunits decreased with anoxia exposure, but expression of the gamma2-subunit remained constant. Combined, our findings suggest that AMPK and AKT may play important, but opposing roles for hypoxic/anoxic survival in the anoxia-tolerant crucian carp.

Regulation of the Cardiorespiratory System of Common Carp (Cyprinus carpio) during Severe Hypoxia at Three Seasonal Acclimation Temperatures

Little is known of the cardiorespiratory control mechanisms utilized by hypoxia‐tolerant teleost fish to tolerate prolonged periods (h) of near anoxic exposure. Here, we report on the cardiorespiratory control mechanisms of the common carp Cyprinus carpio L. during normoxia and prolonged, severe hypoxic (<0.3 mg O2 L−1) exposure at acclimation temperatures of 5°C, 10°C, and 15°C. Through serial intra‐arterial injections of α‐ and β‐adrenergic, cholinergic, and purinergic antagonists while measuring cardiac output (Q), heart rate (fH), ventral aortic blood pressure, and respiration rate, we established that autonomic cardiovascular and respiratory control was preserved during severe hypoxia at all three acclimation temperatures and contributed to downregulation of cardiorespiratory activity. Specifically, inhibitory cholinergic tone mediated up to 76% reductions in fH and Q during hypoxia, whereas the accompanying arterial hypotension was attenuated by an upregulation of an α‐adrenergically mediated peripheral vasoconstriction. Despite the overall cardiac downregulation, a large, stimulatory cardiac β‐adrenergic tone was present during prolonged, severe hypoxia, possibly to protect the heart from attendant acidotic conditions. Purinergic blockade, following α‐adrenergic and cholinergic antagonists, showed that the hypoxic ventilatory depression, which reversed the 2.3‐ to 7.7‐fold increases in respiration rate that occurred with the onset of hypoxia, was a result of purinergic inhibition at all three acclimation temperatures. In contrast, purinergic inhibition of cardiac activity during hypoxia might be important only at 5°C. Finally, given that cardiac power output was reduced 72%–87% during prolonged, severe hypoxia and that glycolysis yields approximately 94% less ATP per mole glucose than oxidative phosphorylation, it seems unlikely that the common carp sufficiently reduces its cardiac energy demand to a level to preclude activation of a partial Pasteur effect. This means that glycogen stores will be used and waste products will accumulate at faster rates, a finding that may help explain why the common carp cannot tolerate such extended periods of severe hypoxia (weeks to months) at cold acclimation temperatures as the freshwater turtle, which is able to reduce its cardiac energy demand to a level that does not require a Pasteur effect and also blunts autonomic cardiovascular control.

Species-specific effects of near-future CO2 on the respiratory performance of two tropical prey fish and their predator

Ocean surface CO2 levels are increasing in line with rising atmospheric CO2 and could exceed 900μatm by year 2100, with extremes above 2000μatm in some coastal habitats. The imminent increase in ocean pCO2 is predicted to have negative consequences for marine fishes, including reduced aerobic performance, but variability among species could be expected. Understanding interspecific responses to ocean acidification is important for predicting the consequences of ocean acidification on communities and ecosystems. In the present study, the effects of exposure to near-future seawater CO2 (860μatm) on resting (M˙ O2rest) and maximum (M˙O2max) oxygen consumption rates were determined for three tropical coral reef fish species interlinked through predator-prey relationships: juvenile Pomacentrus moluccensis and Pomacentrus amboinensis, and one of their predators: adult Pseudochromis fuscus. Contrary to predictions, one of the prey species, P. amboinensis, displayed a 28-39% increase in M˙O2max after both an acute and four-day exposure to near-future CO2 seawater, while maintaining M˙O2rest. By contrast, the same treatment had no significant effects on M˙O2rest or M˙O2max of the other two species. However, acute exposure of P. amboinensis to 1400 and 2400μatm CO2 resulted in M˙O2max returning to control values. Overall, the findings suggest that: (1) the metabolic costs of living in a near-future CO2 seawater environment were insignificant for the species examined at rest; (2) the M˙O2max response of tropical reef species to near-future CO2 seawater can be dependent on the severity of external hypercapnia; and (3) near-future ocean pCO2 may not be detrimental to aerobic scope of all fish species and it may even augment aerobic scope of some species. The present results also highlight that close phylogenetic relatedness and living in the same environment, does not necessarily imply similar physiological responses to near-future CO2.

Elevated CO2 enhances aerobic scope of a coral reef fish

The oceans are absorbing excess atmospheric CO2, and this is causing ocean acidification. Surprisingly, one coral reef damselfish exhibits enhanced aerobic performance after living at projected future ocean CO2 levels for 17 days. Identifying both the winners and losers under climate change scenarios is vital to conserving marine biodiversity.

Effects of temperature and anoxia upon the performance of in situ perfused trout hearts

SUMMARY Rainbow trout (Oncorhynchus mykiss) are likely to experience acute changes in both temperature and oxygen availability and, like many other organisms, exhibit behavioural selection of low temperatures during hypoxia that acts to reduce metabolism and alleviate the demands on the heart. To investigate whether low temperature protects cardiac performance during anoxia, we studied the effects of an acute temperature change, from 10°C to either 5°C, 15°C or 18°C, upon the performance of in situ perfused trout hearts before, during and after exposure to 20 min of anoxia. Routine cardiac workload mimicked in vivo conditions at the given temperatures, and the effects of anoxia were evaluated as maximal cardiac performance before and after 20 min of anoxic perfusion. Functional data were related to maximal activities of glycolytic enzymes and energetic status of the heart at the termination of the experiment. At high oxygenation, maximum cardiac output and power output increased with temperature (Q10 values of 1.8 and 2.1, respectively) as a result of increased heart rate. Hypoxia tolerance was inversely related to temperature. At 5°C, the hearts maintained routine cardiac output throughout the 20 min period of anoxia, and maximal cardiac performance was fully restored following reoxygenation. By contrast, cardiac function failed sooner during anoxia as temperature was increased and maximal performance after reoxygenation was reduced by 25%, 35% and 55% at 10°C, 15°C and 18°C, respectively. Increased functional impairment following anoxic exposure at elevated temperature occurred even though both cardiac glycolytic enzyme activity and the rate of lactate production were increased proportionally with cardiac work. Nonetheless, there was no indication of myocardial necrosis, as biochemical and energetic parameters were generally unaffected by anoxia.

Cardiac survival in anoxia-tolerant vertebrates: An electrophysiological perspective

Certain vertebrates, such as freshwater turtles of the genus Chrysemys and Trachemys and crucian carp (Carassius carassius), have anoxia-tolerant hearts that continue to function throughout prolonged periods of anoxia (up to many months) due to successful balancing of cellular ATP supply and demand. In the present review, we summarize the current and limited understanding of the cellular mechanisms underlying this cardiac anoxia tolerance. What emerges is that cold temperature substantially modifies cardiac electrophysiology to precondition the heart for winter anoxia. Intrinsic heart rate is slowed and density of sarcolemmal ion currents substantially modified to alter cardiac action potential (AP) characteristics. These changes depress cardiac activity and reduce the energetic costs associated with ion pumping. In contrast, anoxia per se results in limited changes to cardiac AP shape or ion current densities in turtle and crucian carp, suggesting that anoxic modifications of cardiac electrophysiology to reduce ATP demand are not extensive. Additionally, as knowledge of cellular physiology in non-mammalian vertebrates is still in its infancy, we briefly discuss the cellular defense mechanisms towards the acidosis that accompanies anoxia as well as mammalian cardiac models of hypoxia/ischemia tolerance. By examining if fundamental cellular mechanisms have been conserved during the evolution of anoxia tolerance we hope to have provided a framework for the design of future experiments investigating cardiac cellular mechanisms of anoxia survival.

Correlation of cardiac performance with cellular energetic components in the oxygen-deprived turtle heart.

The relationship between cardiac energy metabolism and the depression of myocardial performance during oxygen deprivation has remained enigmatic. Here, we combine in vivo (31)P-NMR spectroscopy and MRI to provide the first temporal profile of in vivo cardiac energetics and cardiac performance of an anoxia-tolerant vertebrate, the freshwater turtle (Trachemys scripta) during long-term anoxia exposure (approximately 3 h at 21 degrees C and 11 days at 5 degrees C). During anoxia, phosphocreatine (PCr), unbound levels of inorganic phosphate (effective P(i)(2-)), intracellular pH (pH(i)), and free energy of ATP hydrolysis (dG/dxi) exhibited asymptotic patterns of change, indicating that turtle myocardial high-energy phosphate metabolism and energetic state are reset to new, reduced steady states during long-term anoxia exposure. At 21 degrees C, anoxia caused a reduction in pH(i) from 7.40 to 7.01, a 69% decrease in PCr and a doubling of effective P(i)(2-). ATP content remained unchanged, but the free energy of ATP hydrolysis (dG/dxi) decreased from -59.6 to -52.5 kJ/mol. Even so, none of these cellular changes correlated with the anoxic depression of cardiac performance, suggesting that autonomic cardiac regulation may override putative cellular feedback mechanisms. In contrast, during anoxia at 5 degrees C, when autonomic cardiac control is severely blunted, the decrease of pH(i) from 7.66 to 7.12, 1.9-fold increase of effective P(i)(2-), and 6.4 kJ/mol decrease of dG/dxi from -53.8 to -47.4 kJ/mol were significantly correlated to the anoxic depression of cardiac performance. Our results provide the first evidence for a close, long-term coordination of functional cardiac changes with cellular energy status in a vertebrate, with a potential for autonomic control to override these immediate relationships.