Cardiac responses to anoxia in the Pacific hagfish, Eptatretus stoutii.


In the absence of any previous study of the cardiac status of hagfishes during prolonged anoxia and because of their propensity for oxygen-depleted environments, the present study tested the hypothesis that the Pacific hagfish Eptatretus stoutii maintains cardiac performance during prolonged anoxia. Heart rate was halved from the routine value of 10.4±1.3 beats min⁻¹ by the sixth hour of an anoxic period and then remained stable for a further 30 h. Cardiac stroke volume increased from routine (1.3±0.1 ml kg⁻¹) to partially compensate the anoxic bradycardia, such that cardiac output decreased by only 33% from the routine value of 12.3±0.9 ml min⁻¹ kg⁻¹. Cardiac power output decreased by only 25% from the routine value of 0.26±0.02 mW g⁻¹. During recovery from prolonged anoxia, cardiac output and heart rate increased to peak values within 1.5 h. Thus, the Pacific hagfish should be acknowledged as hypoxic tolerant in terms of its ability to maintain around 70% of their normoxic cardiac performance during prolonged anoxia. This is only the second fish species to be so classified.

Journal of Experimental Biology 213: 3692-3698

Only a few of the more than 25,000 species of fishes are known to be tolerant of severe hypoxia, and even anoxia. Even so, there are representatives among cyclostomes, elasmobranchs and teleosts. Among teleosts, the carp family has several hypoxia-tolerant species, e.g. the common carp, Cyprinus carpio (Stecyk and Farrell, 2002; Stecyk et al., 2004) and the tilapia, Oreochromis hybrid sp. (Speers-Roesch et al., 2010), but the crucian carp, Carassius carassius, stands out as being tolerant of anoxia for days to weeks at temperatures of 5–8°C (Hyvärinen et al., 1985; Nilsson, 1990; Nilsson, 2001; Shoubridge and Hochachka, 1980; Stecyk et al., 2004; Vornanen and Tuomennoro, 1999). The most hypoxia-tolerant elasmobranch appears to be the epaulette shark, Hemiscyllium ocellatum, which can withstand hours of severe hypoxia at 25°C (Nilsson and Renshaw, 2004; Stenslokken et al., 2004; Wise et al., 1998). Among cyclostomes, hagfishes routinely inhabit oxygen-depleted environments, such as hypoxic sediments. In addition, their feeding strategy of burrowing into the coelomic cavities of dead or moribund animals exposes them to short periods of severe hypoxia or anoxia (Axelsson et al., 1990; Forster et al., 1992; Perry et al., 1993; Perry et al., 2009). However, whether or not hagfishes are anoxia tolerant is unclear, although there are certainly suggestions that the heart can function under anoxic conditions (Forster, 1991; Hansen and Sidell, 1983).

Given the possibility that hagfishes might be anoxia tolerant, the objective of the present study was to characterize the cardiac responses in the Pacific hagfish, Eptatretus stoutii (Lockington 1878), to prolonged anoxia because most vertebrate hearts do not tolerate even severe hypoxia. It has been suggested that the ability to maintain cardiac function without sufficient oxygen requires a low routine cardiac power output and ATP demand, a high cardiac glycolytic potential and a means of dealing with anaerobic wastes (Farrell, 1991b; Farrell and Stecyk, 2007). In this regard, hagfishes are recognized as having the lowest cardiac power output among all fishes (Farrell, 2007a), an in vitro or in situ cardiac glycolytic potential that can serve these needs (Forster, 1991; Hansen and Sidell, 1983) and a blood volume larger than any vertebrate (Forster et al., 2001).

Although the cardiovascular features of hagfish suggest that they could maintain cardiac performance during prolonged periods of anoxia, the requisite measurements of cardiac power output, the product of ventral aortic blood flow and pressure, are lacking. Instead, such measurements have been limited to severely hypoxic hagfishes for a period of 30 min or less. Under these conditions, cardiac output was maintained or slightly increased in the Atlantic hagfish, Myxine glutinosa, and the New Zealand hagfish, Eptatretus cirrhatus (Axelsson et al., 1990; Forster et al., 1992). Furthermore, Hansen and Sidell (Hansen and Sidell, 1983) had earlier shown that the gross mechanical activity (frequency and force of heart beat) of an in situ heart was maintained in anaesthetized M. glutinosa for 3 h after cardiac poisoning with either cyanide or azide to stop mitochondrial respiration, as well as during severe hypoxia (gills perfused with nitrogen-equilibrated water). However, given that the majority of hypoxia-tolerant vertebrates reduce cardiac power output by 50–95% during severe hypoxia, the only exception being crucian carp (Stecyk et al., 2004), there is the possibility that hagfish, extant representatives of fish with the most primitive chambered heart, also depress cardiac power output during prolonged anoxia. Thus, the purpose of this study was to test the hypothesis that the Pacific hagfish, like the crucian carp, maintain cardiac performance during prolonged anoxia.