Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia

Abstract

SummaryHypoxia survival in fish requires a well-coordinated response to either secure more O 2 from the hypoxic environment or to limit the metabolic consequences of an O 2 restriction at the mitochondria. Although there is a considerable amount of information available on the physiological, behavioral, biochemical and molecular responses of fish to hypoxia, very little research has attempted to determine the adaptive value of these responses. This article will review current attempts to use the phylogenetically corrected comparative method to define physiological and behavioral adaptations to hypoxia in intertidal fish and further identify putatively adaptive biochemical traits that should be investigated in the future. In a group of marine fishes known as sculpins, from the family Cottidae, variation in hypoxia tolerance, measured as a critical O 2 tension (P crit ), is primarily explained by variation in mass-specific gill surface area, red blood cell hemoglobin-O 2 binding affinity, and to a lesser extent variation in routine O 2 consumption rate (M O2 ). The most hypoxia-tolerant sculpins consistently show aquatic surface respiration (ASR) and aerial emergence behavior during hypoxia exposure, but no phylogenetically independent relationship has been found between the thresholds for initiating these behaviors and P crit . At O 2 levels below P crit , hypoxia survival requires a rapid reorganization of cellular metabolism to suppress ATP consumption to match the limited capacity for O 2 -independent ATP production. Thus, it is reasonable to speculate that the degree of metabolic rate suppression and the quantity of stored fermentable fuel is strongly selected for in hypoxia-tolerant fishes; however, these assertions have not been tested in a phylogenetic comparative model.

Effect of temperature on the metabolism, behaviour and oxygen requirements of Sparus aurata

“…In line with previous observations, we found that the increase in RMR with temperature led to an elevation of the LOS (Schurmann & Steffensen 1997, Claireaux & Lagardère 1999, Valverde et al 2006, Barnes et al 2011, Richards 2011, Svendsen et al 2012, Mamun et al 2013, Remen et al 2013). This confirms that temperature is an important factor to consider when determining oxygen thresholds.…”

“…Anaerobic ATP production is far less efficient than aerobic ATP production, and the duration of survival becomes dependent on the availability of substrates for anaerobiosis (Richards 2009(Richards , 2011. Further, a drop in O 2 to levels below the LOS can be expected to induce stress (increased plasma levels of corticosteroids and catecholamines) and lactic acidosis (Van Raaij et al 1996, Vianen et al 2001, Petersen & Gamperl 2011, Remen et al 2012, 2013.…”

“…One of the main factors influencing metabolic rate is temperature (Fry 1947(Fry , 1971, which is closely correlated with LOS and S crit (e.g. Schurmann & Steffensen 1997, Claireaux & Lagardère 1999, Barnes et al 2011, Richards 2011, Mamun et al 2013, Remen et al 2013. In order to develop an applicable oxygen threshold for the S. aurata industry, it is therefore necessary to investigate the relationship between temperature and LOS for this species.…”

The real limits to marine life: a further critique of the Respiration Index

“…The P crit is defined as the oxygen partial pressure below which metabolism cannot be regulated independently of P O 2 and may be indicated by either a reduction in oxygen consumption or an accumulation of anaerobic metabolites (e.g., lactate). Broad comparative studies have revealed that, below a "saturation threshold" (∼ 5 kPa; Seibel, 2011), the P crit closely matches the oxygen level to which a species is exposed in its natural range (Childress and Seibel, 1998;Seibel, 2011;Richards, 2011). This means that existing oxygen levels are the effective limit for marine life.…”

Effects of hypoxia in the gills of the Manila clam Ruditapes philippinarum using NMR-based metabolomics

“…Exposed to hypoxia, marine organisms may develop multiple physiological defects in respiration, metabolism, growth, and reproduction. The low levels of dissolved oxygen in seawater are associated with a decline in zooplankton (Elliott et al, 2012) and remarkable undesirable changes in the growth rates, mortality, reproduction, and predator-avoidance behavior of nektons (Gotanda et al, 2011;Richards, 2011;Rouhi et al, 2010). The adverse effects of marine hypoxia, in synergy with other factors such as abnormal temperature and overfishing, cause not only irreversible damage to the native ecosystem, but impose severe limitations on the productivity of local fisheries (Jackson, 2008).…”