Distinct physiological strategies are used to cope with constant hypoxia and intermittent hypoxia in killifish (Fundulus heteroclitus)

Abstract

Many fish encounter hypoxia on a daily cycle, but the physiological effects of intermittent hypoxia are poorly understood. We investigated whether acclimation to constant (sustained) hypoxia or to intermittent diel cycles of nocturnal hypoxia (12 h normoxia:12 h hypoxia) had distinct effects on hypoxia tolerance or on several determinants of O 2 transport and O 2 utilization in estuarine killifish. Adult killifish were acclimated to normoxia, constant hypoxia, or intermittent hypoxia for 7 or 28 days in brackish water (4 ppt). Acclimation to both hypoxia patterns led to comparable reductions in critical O 2 tension and resting O 2 consumption rate, but only constant hypoxia reduced the O 2 tension at loss of equilibrium. Constant (but not intermittent) hypoxia decreased filament length and the proportion of seawatertype mitochondrion-rich cells in the gills (which may reduce ion loss and the associated costs of active ion uptake), increased blood haemoglobin content, and reduced the abundance of oxidative fibres in the swimming muscle. In contrast, only intermittent hypoxia augmented the oxidative and gluconeogenic enzyme activities in the liver and increased the capillarity of glycolytic muscle, each of which should facilitate recovery between hypoxia bouts. Neither exposure pattern affected muscle myoglobin content or the activities of metabolic enzymes in the brain or heart, but intermittent hypoxia increased brain mass. We conclude that the pattern of hypoxia exposure has an important influence on the mechanisms of acclimation, and that the optimal strategies used to cope with intermittent hypoxia may be distinct from those for coping with constant hypoxia.

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“…LDH is one of the enzymes of glycolytic pathway responsible for the anaerobic conversion of pyruvate to lactate, and it is ubiquitously present in most tissues. During the anaerobic metabolic shift, caused by hypoxia, there may be an up-regulation of LDH activities in different tissues (Borowiec, Darcy, Gillette, & Scott, 2015). The present study revealed an increase in LDH activity in both liver and muscle tissues after 72h of hypoxia exposure.…”

“…The present study revealed an increase in LDH activity in both liver and muscle tissues after 72h of hypoxia exposure. However, muscle LDH remained unchanged after exposure to hypoxia in killifish Fundulus heteroclitus (Greaney, Place, Cashon, Smith, & Powers, 1980), However, there was an increase in activities of liver LDH in the above fish, Fundulus heteroclitus during hypoxic conditions (Borowiec et al, 2015). This may be due to an increase in lactate level during hypoxia, as lactate is the substrate for gluconeogenesis in liver.…”

Warm acclimation improves hypoxia tolerance in Fundulus heteroclitus

“…Remodelling of gill morphology has primarily been investigated in the context of acclimation to hypoxia (e.g. Crispo and Chapman, 2010), and this has been shown to occur via changes in the ILCM in a variety of fish species (Sollid et al, 2003(Sollid et al, , 2005aNilsson, 2007;Ong et al, 2007;Matey et al, 2008;Turko et al, 2012;Dhillon et al, 2013;Johannsson et al, 2014;Anttila et al, 2015) including killifish (Borowiec et al, 2015). Less is known about the effects of thermal acclimation on gill morphology, but decreases in the ILCM at warmer temperatures have been observed in crucian carp, goldfish (Sollid et al, 2005b;Mitrovic and Perry, 2009) and killifish (Barnes et al, 2014).…”

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

“…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.…”

“…Hypoxia acclimation has often been shown to improve hypoxia tolerance (Fu et al, 2011;Dan et al, 2014;Borowiec et al, 2015) but the importance of changes in mitochondrial physiology to this process has not been well examined in fish, particularly in hypoxiatolerant species. Acclimation of mammals to moderate hypoxia (such as at high altitudes) reduces or has no effect on mitochondrial respiratory capacity (Costa et al, 1997;Nouette-Gaulain et al, 2005;Horscroft and Murray, 2014).…”