Mechanisms and evolution of hypoxia tolerance in fish

Mandic, Milica; Todgham, Anne E.; Richards, Jeffrey G.

doi:10.1098/rspb.2008.1235

Cited by 234 publications

(256 citation statements)

References 37 publications

(57 reference statements)

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“…These two measures probably reflect different aspects of tolerance to hypoxia (Richards, 2011(Richards, , 2009Farrell and Richards, 2009) in phylogenetically corrected multispecies comparisons in fish (Dhillon et al, 2013). Instead, P crit is thought to be more closely correlated with haemoglobin P 50 for oxygen (Mandic et al, 2009;Dhillon et al, 2013). However, the whole-blood haemoglobin P 50 of killifish is approximately 0.5-0.7 kPa depending on acclimation temperature (DiMichele and Powers, 1982), whereas here we show that P crit is approximately 4.4-5.3 kPa depending on the subspecies.…”

Section: Differences Between Subspeciesmentioning

confidence: 99%

Warm acclimation improves hypoxia tolerance in Fundulus heteroclitus

McBryan

Healy

Haakons

et al. 2016

Journal of Experimental Biology

109

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Human activities are increasing both the frequency of hypoxic episodes and the mean temperature of aquatic ecosystems, but few studies have considered the possibility that acclimation to one of these stressors could improve the ability to cope with the other stressor. Here, we used Atlantic killifish, Fundulus heteroclitus, to test this hypothesis. Hypoxia tolerance was measured as time to loss of equilibrium in hypoxia (LOE hyp ) at 0.4 kPa oxygen. Time to LOE hyp declined from 73.3±6.9 min at 15°C to 2.6±3.8 min at 23°C, and at 30°C no fish could withstand this level of hypoxia. Prior acclimation to warm temperatures significantly increased time to LOE hyp . Hypoxia tolerance of the southern subspecies of killifish, F. heteroclitus heteroclitus, was greater than that of the northern subspecies, F. heteroclitus macrolepidotus, measured both as critical oxygen tension (P crit ) and as time to LOE hyp . Warm acclimation offset the negative effects of temperature on time to LOE hyp to a similar extent in the two subspecies. Warm acclimation increased total lamellar surface area of the gill in both subspecies as a result of regression of an interlamellar cell mass (ILCM). However, differences in total lamellar surface area could not explain differences in time to LOE hyp between the subspecies, suggesting that the lower time to LOE hyp of northern fish is related to their higher routine metabolic rate. These data suggest that thermal plasticity in gill morphology can improve the capacity of this species to tolerate hypoxia, and shows how existing plasticity may help organisms to cope with the complex interacting stressors that they will encounter with increasing frequency as our climate changes.

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Section: Differences Between Subspeciesmentioning

confidence: 99%

Warm acclimation improves hypoxia tolerance in Fundulus heteroclitus

McBryan

Healy

Haakons

et al. 2016

Journal of Experimental Biology

109

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“…Thus, how the swimming performance of fish is affected by variations in temperature and DO may be critical for their survival in the field (Perry et al 2005, Mandic et al 2009). Changes in temperature and levels of DO have diverse effects on oxygen availability and metabolite flux, as well as intracellular stores of ATP and PCr, and endogenous fuels stored within the white muscle, which are limiting factors of U crit , U fast and U cat , respectively.…”

Section: Introductionmentioning

confidence: 99%

Effect of temperature and dissolved oxygen on swimming performance in crucian carp

Penghan¹,

Cao²,

Fu³

2014

Aquat. Biol.

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Changing environmental conditions may affect the swimming performance of fish by affecting energy sources through changes in temperature and concentration of dissolved oxygen (DO). It has become increasingly important to investigate the effect of temperature and DO on the swimming performance of fish species as hypoxia in aquatic environments worldwide is increasing due to the effects of anthropogenic global warming. To test how different swimming modes respond to thermal and DO changes, 3 measures of swimming performance were tested: critical swimming speed (U crit ), constant acceleration speed (U cat ), and maximum speed during a fast-start (U fast ). The changes in these 3 aspects of swimming performance in juvenile crucian carp Carassius carassius were quantified at 2 different temperatures (10 and 20°C) and 3 different DO concentrations (2.5, 5, and 9 mg l −1 ). U cat was ca. 110 to 156% of U crit , whereas U fast was ca. 394 to 472% of U crit , depending on the experimental conditions. Temperature had a significant effect on all 3 measures of swimming performance, whereas DO had significant effects only on U cat and U crit (U crit but not U cat decreased in the 2.5 mg l −1 DO group). The active metabolic rate (MO 2active ) under the different experimental conditions suggested that the decrease in U crit at a lower temperature and DO level could be partially explained by a decrease in oxygen uptake capacity. These results indicate that all 3 swimming measurements should be used when addressing how temperature affects swimming performance.

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“…P crit is largely determined by the O 2 binding affinity of hemoglobin (Hb) (Mandic et al, 2009), and at Pw O2 values below P crit the ability to extract environmental O 2 to saturate Hb is constrained and thus unable to support routine metabolic rate (MR) aerobically. The animal can attempt to sustain ATP production at routine levels through an upregulation of anaerobic glycolysis, but this comes with the depletion of carbohydrate reserves and the accumulation of deleterious anaerobic end-products (Richards, 2009), ultimately limiting hypoxic survival time (Lague et al, 2012;Speers-Roesch et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Calorespirometry reveals that goldfish prioritize aerobic metabolism over metabolic rate depression in all but near-anoxic environments

Regan

Gill

Richards

2016

Journal of Experimental Biology

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Metabolic rate depression (MRD) has long been proposed as the key metabolic strategy of hypoxic survival, but surprisingly, the effects of changes in hypoxic O 2 tensions (Pw O2 ) on MRD are largely unexplored. We simultaneously measured the O 2 consumption rate (Ṁ O2 ) and metabolic heat of goldfish using calorespirometry to test the hypothesis that MRD is employed at hypoxic Pw O2 values and initiated just below P crit , the Pw O2 below which Ṁ O2 is forced to progressively decline as the fish oxyconforms to decreasing Pw O2 . Specifically, we used closed-chamber and flow-through calorespirometry together with terminal sampling experiments to examine the effects of Pw O2 and time on Ṁ O2 , metabolic heat and anaerobic metabolism (lactate and ethanol production). The closedchamber and flow-through experiments yielded slightly different results. Under closed-chamber conditions with a continually decreasing Pw O2 , goldfish showed a P crit of 3.0±0.3 kPa and metabolic heat production was only depressed at Pw O2 between 0 and 0.67 kPa. Under flow-through conditions with Pw O2 held at a variety of oxygen tensions for 1 and 4 h, goldfish also initiated MRD between 0 and 0.67 kPa but maintained Ṁ O2 to 0.67 kPa, indicating that P crit is at or below this Pw O2 . Anaerobic metabolism was strongly activated at Pw O2 ≤1.3 kPa, but only used within the first hour at 1.3 and 0.67 kPa, as anaerobic end-products did not accumulate between 1 and 4 h exposure. Taken together, it appears that goldfish reserve MRD for near-anoxia, supporting routine metabolic rate at sub-P crit Pw O2 values with the help of anaerobic glycolysis in the closed-chamber experiments, and aerobically after an initial (<1 h) activation of anaerobic metabolism in the flow-through experiments, even at 0.67 kPa Pw O2 .

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Mechanisms and evolution of hypoxia tolerance in fish

Cited by 234 publications

References 37 publications

Warm acclimation improves hypoxia tolerance in Fundulus heteroclitus

Warm acclimation improves hypoxia tolerance in Fundulus heteroclitus

Effect of temperature and dissolved oxygen on swimming performance in crucian carp

Calorespirometry reveals that goldfish prioritize aerobic metabolism over metabolic rate depression in all but near-anoxic environments

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