Hypoxia tolerance in Atlantic cod

Oxygen saturation levels that killed 50 and 5% of cod Gadus morhua over 96 h averaged 21·2 and 27·7%, respectively. No fish survived at 10% saturation and only a few survived at 16% saturation, whereas no mortality occurred at 34 and 40% oxygen saturation. Since metabolic rate and oxygen consumption increase with increasing temperature, we hypothesized that cod would be less tolerant to hypoxic conditions at 6 than at 2° C. However, temperature (2 and 6° C) had no measurable impact on cod survival. Small (mean & S.D.; 45·2 ± 4·2 cm) and large (57·5 ± 3·8 cm) cod had the same tolerance to hypoxia. At the end of the experiments, hypoxia had a significant effect on blood haematocrit, mean cellular haemoglobin content, liver lactate, plasma glucose and plasma lactate, but accounted for only a small fraction (< 10%) of the variation, except for plasma lactate which exhibited a strong response with concentrations increasing progressively with decreasing levels of oxygen saturation. Temperature had a significant effect on most variates in normoxia and hypoxia. Variates also affected by oxygen level showed significant interactions between oxygen and size or temperature effects. However, these interactions accounted for only a small proportion of the variation. Physiological parameters indicated that extending the duration of our tests beyond 96 h would not have changed our estimates of the lethal thresholds. Hypoxic conditions are a permanent feature of the deep waters of the Gulf of St Lawrence. This study shows that a significant portion of the benthic habitats in the Gulf are uninhabitable for cod which would be expected to avoid waters below 28% oxygen saturation.     

Metabolic and cardiorespiratory responses of summer flounder Paralichthys dentatus to hypoxia at two temperatures

To quantify the tolerance of summer flounder Paralichthys dentatus to episodic hypoxia, resting metabolic rate, oxygen extraction, gill ventilation and heart rate were measured during acute progressive hypoxia at the fish's acclimation temperature (22° C) and after an acute temperature increase (to 30° C). Mean ±s.e. critical oxygen levels (i.e. the oxygen levels below which fish could not maintain aerobic metabolism) increased significantly from 27 ± 2% saturation (2·0 ± 0·1 mg O(2) l(-1) ) at 22° C to 39 ± 2% saturation (2·4 ± 0·1 mg O(2) l(-1) ) at 30° C. Gill ventilation and oxygen extraction changed immediately with the onset of hypoxia at both temperatures. The fractional increase in gill ventilation (from normoxia to the lowest oxygen level tested) was much larger at 22° C (6·4-fold) than at 30° C (2·7-fold). In contrast, the fractional decrease in oxygen extraction (from normoxia to the lowest oxygen levels tested) was similar at 22° C (1·7-fold) and 30° C (1·5-fold), and clearly smaller than the fractional changes in gill ventilation. In contrast to the almost immediate effects of hypoxia on respiration, bradycardia was not observed until 20 and 30% oxygen saturation at 22 and 30° C, respectively. Bradycardia was, therefore, not observed until below critical oxygen levels. The critical oxygen levels at both temperatures were near or immediately below the accepted 2·3 mg O(2) l(-1) hypoxia threshold for survival, but the increase in the critical oxygen level at 30° C suggests a lower tolerance to hypoxia after an acute increase in temperature.     

Ocean warming and hypoxia affect embryonic growth,fitness and survival of small-spotted catsharks,Scyliorhinus canicula

Elasmobranchs are key to a healthy marine ecosystem but are under threat from human activities, such as destructive fisheries and shark finning. Embryos of oviparous elasmobranchs may be further challenged during development by rising temperatures and falling dissolved oxygen concentrations in their intertidal environment. However, the impact of climate change on survival and growth of oviparous elasmobranchs is still poorly understood. Here, we investigate the effects of temperature and hypoxia on the growth and survival of small-spotted catshark (Scyliorhinus canicula) embryos by incubating eggs in normoxia 15°C, normoxia 20°C, hypoxia 15°C, or hypoxia 20°C. Incubation under the elevated temperature increased the embryonic growth rate, yolk consumption rate and Fulton's condition factor at hatching, whilst decreasing the total length and body mass of newly hatched sharks. Under low oxygen conditions (50% air saturation) the survival rate of S. canicula embryos dropped significantly and the temperature-induced increase in Fulton's condition factor was reversed. Together, these data demonstrate both the individual and compound effects of elevated temperature and hypoxia on the survival and growth during early ontogeny of a ubiquitous, coastal elasmobranch, S. canicula.     

Respiration and low oxygen tolerance of two fish species from the Arabian Sea, Cubiceps whiteleggi and Coryphaena hippurus

During the 1987 cruise of F.S. Meteor in the Arabian Sea, respiration rates and effects of low oxygen saturation on behaviour and respiration have been investigated in two fish species. Cubiceps whiteleggi is an inhabitant of the partly oxygen-depleted epipelagic zone. It is more tolerant to oxygen shortage than the second species, Coryphaena hippurus. At naturally occuring temperatures, first response to low oxygen was noted at values slightly below air saturation in C. hippurus and at 20–30% oxygen saturation in C. whiteleggi. After exposure to low oxygen saturation, the reaction patterns were completely different for the two species, reflecting the particular requirements of their living space. In C. hippurus lethal oxygen saturations seemed to be reached just below 60% oxygen saturation. In C. whiteleggi first mortality occurred at 10% oxygen saturation.     

Influence of temperature and ambient oxygen on the swimming energetics of cyprinid larvae and juveniles

Synopsis The relationship between respiration and swimming speed of larvae and juveniles (2–100 mg fresh mass) of Danube bleak, Chalcalburnus chalcoides (Cyprinidae), was measured at 15° and 20° C under hypoxic (50% air saturation), normoxic, and hyperoxic (140% air saturation) conditions. In a flow-tunnel equipped with a flow-through respirometer the animals swam at speeds of up to 8 lengths · s^-1; speeds were sustained for at least two minutes. The mass specific standard, routine, and active respiration rates declined with increasing body mass at both temperatures. Metabolic intensity increased with temperature, but also the critical swimming speed (at which oxygen uptake reached its maximum) was higher at 20° than at 15° C by about 30%. Nevertheless, the oxygen debt incurred by the fish at the highest speeds was about 40%, and the net cost of swimming about 32%, lower at 20° than at 15°C. The standard metabolic rate was more strongly dependent on temperature (Q₁₀ around 2.5) than the maximum active rate (Q₁₀ below 2). Whereas standard and routine respiration rates were well regulated over the pO₂-range investigated (8.5–25.8 kPa), the active rates showed a conformer-like pattern, resulting in factorial scopes for activity between 2 and 4. Under hypoxia, the critical swimming speed was lower than under normoxia by about 1.51 · s^-1, but the net cost of swimming was also lower by about 30%. On the other hand, hyperoxia neither increased the swimming performance nor did it lead to a further increase of the metabolic cost of swimming. The hypoxia experiments suggest that in response to lowered tensions of ambient oxygen maintenance functions of metabolism not directly related to swimming may be temporarily reduced, leading to increased apparent swimming efficiency under these conditions. The responses of the larvae of Danube bleak to low temperature and low ambient oxygen are discussed in terms of the metabolic strategies by which energy-limited animals meet the challenge of environmental deterioration.     

Behaviour of rainbow trout Oncorhynchus mykiss presented with a choice of normoxia and stepwise progressive hypoxia

The objective of this study was to identify behavioural adjustments leading to avoidance of hypoxia. Using the oxygen-sensitive species rainbow trout Oncorhynchus mykiss as a model, individual fish were recorded while moving freely between two sides of a test arena: one with normoxia and one with stepwise progressive hypoxia [80-30% dissolved oxygen (DO) air saturation]. The results demonstrated a gradual decrease in the total time spent in hypoxia starting at 80% DO air saturation. At this DO level, the avoidance of hypoxia could not be attributed to changes in spontaneous swimming speed, neither in normoxia nor in hypoxia. Reducing the DO level to 60% air saturation resulted in decreased spontaneous swimming speed in normoxia, yet the number of trips to the hypoxic side of the test arena remained unchanged. Moreover, data revealed increased average residence time per trip in normoxia at DO levels ≤60% air saturation and decreased average residence time per trip in hypoxia at DO levels ≤50% air saturation. Finally, the spontaneous swimming speed in hypoxia increased at DO levels ≤40% air saturation and the number of trips to hypoxia decreased at the 30% DO air saturation level. Thus, avoidance of the deepest hypoxia was connected with a reduced number of trips to hypoxia as well as decreased and increased spontaneous swimming speed in normoxia and hypoxia, respectively. Collectively, the data support the conclusions that the mechanistic basis for avoidance of hypoxia may (1) not involve changes in swimming speed during mild hypoxia and (2) depend on the severity of hypoxia.     

Effects of temperature and dissolved oxygen on heart rate,ventilation rate and oxygen consumption of spangled perch,Leiopotherapon unicolor (Günther 1859), (Percoidei,Teraponidae)

Summary Heart, ventilation and oxygen consumption rates ofLeiopotherapon unicolor were studied at temperatures ranging from 5 to 35°C, and during progressive hypoxia from 100% to 5% oxygen saturation. Biopotentials recorded from the water surrounding the fish corresponded to ventilation movements, and are thought to originate from the ventilatory musculature. Cardio-respiratory responses to temperature and dissolved oxygen follow the typical teleost pattern, with bradycardia, increased ventilation rate and reduced oxygen consumption occurring during hypoxia. However, ventilation rate did not increase at 15°C and below. Ventilation rate showed a slower response to increasing temperature (normoxic Q₁₀=1.39) than heart rate and oxygen consumption (normoxic Q₁₀=2.85 and 2.38).L. unicolor is unable to survive prolonged hypoxia by utilising anaerobic metabolism, but has a large gill surface area which presumably facilitates oxygen uptake in hypoxic environments. Periodic ventilation during normoxia in restingL. unicolor may improve ventilation efficiency by increasing the oxygen diffusion gradient across the gills.Abbreviations EBG electrobranchiogram - ECG electrocardiogram     

A comparison of carbon dioxide production and oxygen uptake in sediment cores from four south Swedish lakes

Carbon dioxide production and oxygen uptake were measured in undisturbed sediment cores taken during winter from four lakes of different trophic state. Respiration was measured at 5, 10, 15 and 20°C at high oxygen saturation (75–100%). The respiratory quotient, calculated from the mean values of carbon dioxide production and oxygen uptake at each temperature for each lake, was 0.83–0.96 with a mean value for the four lakes of 0.90. At very low oxygen saturations (<10%) carbon dioxide production was 21–42% of the production at 20°C and high oxygen saturations. The results indicate that under aerobic conditions, oxygen uptake and carbon dioxide production are closely-coupled processes in these lake sediments.     

The effect of progressive hypoxia on swimming activity and schooling in Atlantic herring

Schools of herring exposed to progressive hypoxia show a peak in velocity during severe hypoxia, at 15–34% oxygen saturation, followed by a decrease in swimming speed until school disruption occurred. The observed increase in swimming speed during severe hypoxia reveals a graded response, since the lower the fish's swimming speed prior to severe hypoxia ( U ₉₅₋₅₀, the speed at oxygen saturations between 95 and 50%), the greater the relative increase in swimming speed. The oxygen saturations at which both peak velocity and school disruption occurred were lower for fish with lowest U ₉₅₋₅₀, suggesting that the fish with the slowest speed U ₉₅₋₅₀ reach their critical P_O2 (at which there is respiratory distress) last, i.e. at lower oxygen saturation. At a functional level, it is suggested that herring encountering hypoxia increase their speed in order to find more favourable conditions, and the magnitude of this increase is modulated by their respiratory distress. It is also hypothesised that the observed increase in speed may be related to an increase in the rate of position shifting within the school. Since the oxygen saturation at which the response to hypoxia occurs and the magnitude of the response are related to the fish's preferred speed prior to severe hypoxia, it is suggested that such a preferred speed should be measured in experiments testing the effect of hypoxia on fish behaviour.     

Differential survival of juvenile sockeye and coho salmon exposed to low dissolved oxygen during winter

Juvenile sockeye salmon (43–78 mm) survived 100% for 24 h in cages in ice–covered Black Lake, Alaska at oxygen saturations >65% (9 mg l^–1), but only 45% at 24% saturation (3·0–3·3 mg l^–1) and none at <17% saturation (2·3 mg l^–1). All juvenile coho (50–120 mm) survived 100% for 24 h down to 21% oxygen saturation (3·1 mg l^–1), and all 50 coho survived 4–5 days at 23–24% saturation (3·2–3·3 mg l^–1).     

Hypoxia, low salinity and lowered temperature reduce embryo survival and hatch rates in black bream Acanthopagrus butcheri (Munro, 1949)

Embryo survival and hatch rates were measured in black bream Acanthopagrus butcheri exposed to different treatments of dissolved oxygen: hypoxic and normoxic, three salinities: 15, 23 and 35 and two temperatures: 16 and 20° C. Hypoxic conditions (50% saturation) reduced 1 day embryo survival by up to 15% ( P < 0·05) compared to embryos held in normoxic (>80% saturation) conditions. Temperature had no effect on the survival of embryos in these treatments, however, lowered salinity significantly reduced embryo survival at 20° C, but not at 16° C. Mean hatch rates were reduced by 10–28% in hypoxic treatments ( P < 0·05) and lowered salinity treatments ( P < 0·05). Hatching was delayed by up to 24 h at 16° C and very low (or zero) hatching occurred in hypoxic treatments at salinities of 15 and 23. These results confirm that environmental conditions in estuaries are important factors in determining spawning success of black bream and are discussed in relation to global warming and climate change that are likely to alter the physical conditions in southern Australian estuaries.     

Tolerance of parr of Arctic charr, Salvelinus alpinus, to reduced dissolved oxygen concentrations

One year old pan Item Windermere (north west England) tolerated lower incipient lethal levels of oxygen [18 20 mg 1 ¹: 15 17% air saturation value (ASV)] at lower (5, 10°C) than at higher (15, 20°C) an elimation temperatures (2·2 2·4 mg 1 ¹ 22 25% ASV). Values were not significantly different for two races of charr in the lake and are amongst the lowest recorded for salmenid species.     

Tolerance, behaviour and oxygen consumption in the sand goby, Pomatoschistus minutus (Pallas), exposed to hypoxia

Behavioural and metabolic reactions of Pomatoschistus minutus (Pallas) exposed to various degrees of hypoxia were studied. At 15°C and 20‰ mortality was 50% at 15.2% oxygen saturation. Avoidance and oxygen saturation showed a linear inverse relationship. At levels lower than 60% saturation increased activity occurred; avoidance was significant at 30% saturation. Active, routine and standard MO₂ correlated linearly with weight at 6 and 15°C (salinity = 19‰). During hypoxia at 15°C routine MO₂ rose significantly at 60–50% and 40–30% saturation expressed either as MO₂ during longer periods at night or MO₂ at shorter intervals during the day. Standard MO₂ was unaffected by hypoxia at 15°C. Haemoglobin concentration was significantly increased when P. minutus was acclimatized to 35% saturation.     

The effect of progressive hypoxia on school structure and dynamics in Atlantic herring Clupea harengus

The effect of progressive hypoxia on the structure and dynamics of herring (Clupea harengus) schools in laboratory conditions was investigated. The length, width and depth of schools of about 20 individuals were measured from video recordings to test the hypothesis that during hypoxia fish schools change their shape and volume. School shape (calculated as the ratios of length/depth, width/depth and length/width) did not change significantly during hypoxia. School length, width, depth, area and volume were all significantly increased at 20% oxygen saturation. Volume, area and width were more sensitive to hypoxia; volume and width were also increased at 25% and area at 30% oxygen saturation. The degree of position changing (shuffling) of individuals within the school was also analysed. Shuffling in normoxia was observed to occur largely through 'O-turn' manoeuvres, a 360( degrees )turn executed laterally to the school that allowed fishes in the front to move to the back. O-turn frequency during normoxia was 0.69 O-turns fish(-1) min(-1) but significantly decreased with hypoxia to 0.37 O-turns fish(-1) min(-1) at 30% oxygen saturation. Shuffling was also investigated by measuring the persistence time of individual herring in leading positions (i.e. the first half of the school). No significant changes occurred during hypoxia, indicating that the decrease in O-turn frequency does not affect shuffling rate during hypoxia, and that position shuffling in hypoxic conditions is mainly due to overtaking or falling back by individual fishes. School integrity and positional dynamics are the outcome of trade-offs among a number of biotic factors, such as food, predator defence, mating behaviour and various physical factors that may impose certain limits. Among these, our results indicate that oxygen level modulates schooling behaviour. Oxygen alters whole-school parameters at oxygen saturation values that can be encountered by herring in the field, indicating that oxygen availability is an important factor in the trade-offs that determine school volume. An increase in school volume in the wild may increase the oxygen available to each individual. However, shuffling rate is not affected by hypoxia, indicating that the internal dynamics of positioning is the result of the balance of other factors, for example related to the nutritional state of each individual fish as suggested by previous studies.     

The functional morphology of erythrocytes of the black scorpion fish <Emphasis Type="Italic">Scorpaena porcus</Emphasis> (Linnaeus, 1758) (scorpaeniformes: scorpaenidae) during hypoxia

The influence of hypoxia on the morphological characteristics of circulating erythrocytes of the scorpion fish Scorpaena porcus (Linnaeus, 1758) has been investigated in an in vivo experiment. Under a 4-h adaptation of the fish to the conditions of ranked hypoxia their erythrocytes demonstrated a number of consecutive reactions. The volume and the surface area of the red blood cells was reduced by 4–5% (p < 0.001) at an oxygen concentration of 2.6 mg/L (30% saturation of water with oxygen) and increased by 4% (p < 0.001) at a concentration of 1.3 mg/L (15% saturation), relative to the control values (normoxia: 7–8 mg/L). The observed reaction of erythrocytes coincided quantitatively and qualitatively (the order of events) with the results of the experiments we performed previously in vitro. Our study has shown that the physiology of the black scorpion fish is tolerant to hypoxia and allows autonomous functioning of red blood cells under conditions of oxygen deficit.     

Saturation dependency of the Bohr effect: interactions among H-+, CO2, and DPG.

The Bohr effect was measured in normal whole blood and in blood with low DPG concentration as a function of oxygen saturation. pH was changed by varying CO2 concentration (CO2 Bohr effect) or by addition of isotonic NaOH or HC1 at constant PCO2 (fixed acid Bohr effect). At nornal DPG concentration CO2 Bohr effect was -0.52 at 50% blood oxygen saturation, increasing in magnitude at lower saturation and decreasing in magnitude at higher saturation. In DPG depleted blood with base excess (BE) similar to 0 meq/1, there was similar dependence of CO2 Bohr effect on oxygen saturation. At BE similar to -10 meq/1, influence of saturation was comparable, but the magnitude of the Bohr effect was markedly increased at all saturations. Fixed acid Bohr effect at normal DPG concentration was -0.45 at saturations of 50-90% but decreased at lower saturations. In DPG-depleted blood fixed acid Bohr effect averaged about -0.33 with minimal variation with saturation. Influence of DPG on oxygen affinity was greater at intermediate saturations and less at saturations below 20% and above 80%. Effect of CO2, independent of pH, was many fold greater at lower oxygen saturations than at higher saturations. These results support the suggestion that the alpha chain of hemoglobin is the site of the initial oxygenation reaction. Physiologically they indicate that the relative contribution of CO2 and fixed acid, as well as the level of oxygen saturation and DPG concentration, may be important in determining PO2 of capillary blood and resulting oxygen delivery.     

Comparative effects of long-term hypoxia on growth, feeding and oxygen consumption in juvenile turbot and European sea bass

When juvenile turbot Scophthalmus maximus and sea bass Dicentrarchus labrax were fed to satiation, growth and food intake were depressed under hypoxia (3·2±0·3 and 4·5±0·2 mg O₂ l^-1). However, no significant difference in growth was observed between fishes maintained in hypoxia and fed to satiation and fishes reared in normoxia (7·4±0·3 mg O₂ l^-1) and fed restricted rations (same food intake of fishes at 3·2 mg O₂ l^-1). Routine oxygen consumption of fishes fed to satiation was higher in normoxia than in hypoxia due to the decrease in food intake in the latter. Of the physiological parameters measured, no significant changes were observed in the two species maintained in hypoxia. This study confirms the significant interaction between environmental oxygen concentrations, feeding and growth in fishes. Decrease in food intake could be an indirect mechanism by which prolonged hypoxia reduces growth in turbot and sea bass, and may be a way to reduce energy and thus oxygen demand.     

The effect of hypoxia on locomotor performance and behaviour during escape in Liza aurata

Escape performance was investigated in the golden grey mullet Liza aurata exposed to various levels of oxygen: >85 ( i.e. normoxia), 50, 20 and 10 % air saturation. Since the golden grey mullet performed aquatic surface respiration when air saturation approached 15–10 %, escape performance was tested at 10 % air saturation with and without access to the surface (10 % S and 10 % C, respectively). Various locomotor and behavioural variables were measured, such as cumulative distance, maximum swimming speed, acceleration, responsiveness (per cent of responding fish), response latency and directionality. Golden grey mullet showed a decrease in responsiveness when the oxygen level was reduced to 10 % air saturation, whether the surface access was obstructed or not. Hypoxia did not have any effect on the response latency. Cumulative distance and maximum swimming speed over a fixed time were significantly different between normoxic conditions and 10 % C, while no differences were found in maximum acceleration. While the fish's 'C‐bend' was mainly directed away from the stimulus in normoxia, the proportion of away and towards 'C‐bend' was random when the oxygen was ≤20 % air saturation. This suggested an impairment of the left‐right discrimination at the initiation of the fast start. Hypoxia affected golden grey mullet escape performance mainly through an impairment of responsiveness and directionality, while locomotor performance was affected only in severe hypoxia when the surface was obstructed. The study showed that, in addition to forcing the fish to the surface as shown by previous studies, hypoxia may also reduce fish elusiveness facing a predator by directly impairing its escape performance.     

The metabolic and biochemical responses of tropical whitespotted bamboo shark Chiloscyllium plagiosum to alterations in environmental temperature

The capacity of tropical whitespotted bamboo sharks Chiloscyllium plagiosum to metabolically compensate, at both the whole‐animal and biochemical levels, to prolonged exposure to temperatures higher (30° C) and lower (20 and 15° C) than their native temperature (24·5° C) was examined. As expected, whitespotted bamboo shark oxygen consumption increased upon exposure to 30° C and decreased at 20 and 15° C. Initial changes in oxygen consumption were maintained even after months at the experimental temperature, indicating that whitespotted bamboo sharks did not compensate metabolically to the experimental temperatures. Maximal activities and thermal sensitivity of citrate synthase and lactate dehydrogenase from whitespotted bamboo shark white locomotor muscle were similar between control animals maintained at 24·5° C and those maintained at 15° C, indicating that cold‐exposed animals did not compensate at the biochemical level. Similarly, lactate dehydrogenase activity did not change following prolonged exposure to 30° C. White muscle from whitespotted bamboo sharks maintained at 30° C had significantly lower citrate synthase activity than did control animals. This result was surprising given the lack of metabolic compensation at the whole‐animal level. Overall, whole‐animal oxygen consumption measurements supported the hypothesis that animals from thermally stable environments lacked the capacity to metabolically compensate to altered temperatures. Enzymatic results, however, suggested that the metabolic potential of muscle could change following temperature acclimation even in the absence of metabolic compensation at the whole‐animal level.     

Respiratory responses to short term hypoxia in the snapping turtle, Chelydra serpentina

Among vertebrates, turtles are able to tolerate exceptionally low oxygen tensions. We have investigated the compensatory mechanisms that regulate respiration and blood oxygen transport in snapping turtles during short exposure to hypoxia. Snapping turtles started to hyperventilate when oxygen levels dropped below 10% O(2). Total ventilation increased 1.75-fold, essentially related to an increase in respiration frequency. During normoxia, respiration occurred in bouts of four to five breaths, whereas at 5% O(2), the ventilation pattern was more regular with breathing bouts consisting of a single breath. The increase in the heart rate between breaths during hypoxia suggests that a high pulmonary blood flow may be maintained during non-ventilatory periods to improve arterial blood oxygenation. After 4 days of hypoxia at 5% O(2), hematocrit, hemoglobin concentration and multiplicity and intraerythrocytic organic phosphate concentration remained unaltered. Accordingly, oxygen binding curves at constant P(CO(2)) showed no changes in oxygen affinity and cooperativity. However, blood pH increased significantly from 7.50+/-0.05 under normoxia to 7.72+/-0.03 under hypoxia. The respiratory alkalosis will produce a pronounced in vivo left-shift of the blood oxygen dissociation curve due to the large Bohr effect and this is shown to be critical for arterial oxygen saturation.