Respiratory responses to progressive hypoxia in the Amazonian oscar, Astronotus ocellatus

SUMMARYAnoxic survival requires the matching of cardiac ATP supply (i.e. maximum glycolytic potential, MGP) and demand (i.e. cardiac power output, PO). We examined the idea that the previously observed in vivo downregulation of cardiac function during exposure to severe hypoxia in tilapia (Oreochromis hybrid) represents a physiological strategy to reduce routine PO to within the heartʼs MGP. The MGP of the ectothermic vertebrate heart has previously been suggested to be ~70nmol ATPs -1 NaCN) on cardiac performance in severe hypoxia were also examined. Under normoxic conditions, cardiac performance and myocardial oxygen consumption rate were comparable to those of other teleosts. The tilapia heart maintained a routine normoxic cardiac output (Q) and PO under all hypoxic conditions, a result that contrasts with the hypoxic cardiac downregulation previously observed in vivo under less severe conditions. Thus, we conclude that the in vivo downregulation of routine cardiac performance in hypoxia is not needed in tilapia to balance cardiac energy supply and demand. Indeed, the MGP of the tilapia heart proved to be quite exceptional. Measurements of myocardial lactate efflux during severe hypoxia were used to calculate the MGP of the tilapia heart. The MGP was estimated to be 172nmol ATPs , which is only 30% lower than the PO max observed with normoxia. Even with this MGP, the additional challenge of acidosis during severe hypoxia decreased maximum ATP turnover rate and PO max by 30% compared with severe hypoxia alone, suggesting that there are probably direct effects of acidosis on cardiac contractility. We conclude that the high maximum glycolytic ATP turnover rate and levels of PO, which exceed those measured in other ectothermic vertebrate hearts, probably convey a previously unreported anoxia tolerance of the tilapia heart, but a tolerance that may be tempered in vivo by the accumulation of acidotic waste during anoxia.

Section: Perfusion Compositionsupporting

confidence: 81%

Exceptional cardiac anoxia tolerance in tilapia (Oreochromis hybrid)

Lague¹,

Speers‐Roesch

Richards

et al. 2012

“…The reduction of Na + fluxes is seen as a dual process, with an immediate effect on gill transcellular permeability, including concomitant reductions in water exchange rates, net K + loss rates, and ammonia and urea excretion rates (Wood et al, 2007;Wood et al, 2009), followed by a subsequent slower 60-65% reduction in Na + /K + -ATPase activity (Richards et al, 2007;Wood et al, 2007). These processes are not driven by oxygen limitations for the branchial MRCs because they perform well down to oxygen levels of 5 Torr (Scott et al, 2008). More likely, they fit with the occurrence of metabolic depression that these fish use when environmental oxygen levels drop below their P crit Torr in the present study, 50-70 Torr in Sloman et al (Sloman et al, 2006)], as well as into rapid changes in gill morphology, which are thought to reduce transcellular permeability (see below).…”

Section: Discussionmentioning

confidence: 99%

“…Studies on several fish species, including oscars, have identified multiple adaptive strategies to survive hypoxia and even anoxia (Almeida-Val and Hochachka, 1995;Muusze et al, 1998). Strategies involve substantial metabolic depression and increased use of anaerobic metabolic pathways (Muusze et al, 1998;Almeida-Val et al, 2000;Chippari-Gomes et al, 2005) rather than increased oxygen extraction efficiency (Scott et al, 2008), traits that scale positively with fish size (Almeida-Val et al, 2000;Sloman et al, 2006). Ventilation does increase under hypoxia (Chippari-Gomes et al, 2005; Scott et al, 2008), which puts the fish at risk of losing more ions to their extremely dilute environment due to the osmo-respiratory compromise (Randall et al, 1972;Nilsson, 2007).…”

Section: Introductionmentioning

confidence: 99%

“…Strategies involve substantial metabolic depression and increased use of anaerobic metabolic pathways (Muusze et al, 1998;Almeida-Val et al, 2000;Chippari-Gomes et al, 2005) rather than increased oxygen extraction efficiency (Scott et al, 2008), traits that scale positively with fish size (Almeida-Val et al, 2000;Sloman et al, 2006). Ventilation does increase under hypoxia (Chippari-Gomes et al, 2005; Scott et al, 2008), which puts the fish at risk of losing more ions to their extremely dilute environment due to the osmo-respiratory compromise (Randall et al, 1972;Nilsson, 2007). However, previous research has shown that under these circumstances oscars are capable of reducing their net ion losses efficiently, thereby decreasing the need for active ion uptake (Wood et al, 2007;Wood et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Interactions between hypoxia tolerance and food deprivation in Amazonian oscars, Astronotus ocellatus (Agassiz)

Boeck

Wood

Iftikar

et al. 2013

Self Cite

SUMMARYOscars are often subjected to a combination of low levels of oxygen and fasting during nest-guarding on Amazonian floodplains. We questioned whether this anorexia would aggravate the osmo-respiratory compromise. We compared fed and fasted oscars (10-14 days) in both normoxia and hypoxia (10-20 Torr, 4 h). Routine oxygen consumption rates (Ṁ O2 ) were increased by 75% in fasted fish, reflecting behavioural differences, whereas fasting improved hypoxia resistance and critical oxygen tensions (P crit ) lowered from 54 Torr in fed fish to 34 Torr when fasting. In fed fish, hypoxia reduced liver lipid stores by approximately 50% and total liver energy content by 30%. Fasted fish had a 50% lower hepatosomatic index, resulting in lower total liver protein, glycogen and lipid energy stores under normoxia. Compared with hypoxic fed fish, hypoxic fasted fish only showed reduced liver protein levels and even gained glycogen (+50%) on a per gram basis. This confirms the hypothesis that hypoxia-tolerant fish protect their glycogen stores as much as possible as a safeguard for more prolonged hypoxic events. In general, fasted fish showed lower hydroxyacylCoA dehydrogenase activities compared with fed fish, although this effect was only significant in hypoxic fasted fish. Energy stores and activities of enzymes related to energy metabolism in muscle or gills were not affected. Branchial Na + uptake rates were more than two times lower in fed fish, whereas Na + efflux was similar. Fed and fasted fish quickly reduced Na + uptake and efflux during hypoxia, with fasting fish responding more rapidly. Ammonia excretion and K + efflux were reduced under hypoxia, indicating decreased transcellular permeability. Fasted fish had more mitochondria-rich cells (MRC), with larger crypts, indicating the increased importance of the branchial uptake route when feeding is limited. Gill MRC density and surface area were greatly reduced under hypoxia, possibly to reduce ion uptake and efflux rates. Density of mucous cells of normoxic fasted fish was approximately fourfold of that in fed fish. Overall, a 10-14 day fasting period had no negative effects on hypoxia tolerance in oscars, as fasted fish were able to respond more quickly to lower oxygen levels, and reduced branchial permeability effectively.

“…Several fish species live in environments with reduced O 2 availability and can tolerate prolonged and severe hypoxia (Stecyk et al, 2004;Scott et al, 2008;Richards et al, 2009;Speers-Roesch et al, 2012;Borowiec et al, 2015). Although mitochondrial abundance and respiratory capacity are known to vary substantially between fish species (Moyes et al, 1992), we are just beginning to appreciate the relationship between mitochondrial physiology and hypoxia tolerance.…”

Section: Introductionmentioning

confidence: 99%

Mitochondrial physiology and reactive oxygen species production are altered by hypoxia acclimation in killifish (Fundulus heteroclitus)

Mahalingam

Borowiec

et al. 2016

Self Cite

Many fish encounter hypoxia in their native environment, but the role of mitochondrial physiology in hypoxia acclimation and hypoxia tolerance is poorly understood. We investigated the effects of hypoxia acclimation on mitochondrial respiration, O 2 kinetics, emission of reactive oxygen species (ROS), and antioxidant capacity in the estuarine killifish (Fundulus heteroclitus). Killifish were acclimated to normoxia, constant hypoxia (5 kPa O 2 ) or intermittent diel cycles of nocturnal hypoxia (12 h:12 h normoxia: hypoxia) for 28-33 days and mitochondria were isolated from liver. Neither pattern of hypoxia acclimation affected the respiratory capacities for oxidative phosphorylation or electron transport, leak respiration, coupling control or phosphorylation efficiency. Hypoxia acclimation also had no effect on mitochondrial O 2 kinetics, but P 50 (the O 2 tension at which hypoxia inhibits respiration by 50%) was lower in the leak state than during maximal respiration, and killifish mitochondria endured anoxia-reoxygenation without any impact on mitochondrial respiration. However, both patterns of hypoxia acclimation reduced the rate of ROS emission from mitochondria when compared at a common O 2 tension. Hypoxia acclimation also increased the levels of protein carbonyls and the activities of superoxide dismutase and catalase in liver tissue (the latter only occurred in constant hypoxia). Our results suggest that hypoxia acclimation is associated with changes in mitochondrial physiology that decrease ROS production and may help improve hypoxia tolerance.