The ontogeny of regulatory control of the rainbow trout (Oncorhynchus mykiss) heart and how this is influenced by chronic hypoxia exposure

Abstract

SUMMARYSalmonid embryos develop in cool waters over relatively long periods of time. Interestingly, hypoxic conditions have been found to be relatively common in some nesting sites (redds). The goals of this study were to determine the ontogeny of cardiac regulation in rainbow trout early life stages and how this is influenced by chronic hypoxia. The heart rate response to cholinergic and adrenergic receptor stimulation or inhibition was measured in individuals reared in normoxic (100% O 2 saturation) or hypoxic (30% O 2 saturation) conditions from fertilization to embryonic stages 22, 26 and 29, and larval stages 30 and 32. In normoxia, heart rate increased in response to -adrenergic receptor stimulation (isoproterenol) as early as embryonic stage 22, and decreased with the antagonist propranolol after this stage. Cholinergic stimulation (acetylcholine) was ineffective at all stages, but atropine (acetylcholine antagonist) increased heart rate at larval stage 32. This demonstrates that cardiac -adrenergic receptors are functional at early life stages, while cholinergic receptors are not responsive until after hatching. Collectively, embryos had cardioacceleration control mechanisms in place just after the heartbeat stage, while cardio-inhibitory control was not functional until after hatching. Chronic hypoxia exposure triggered bradycardia, increased the response to adrenergic stimulation in embryos and larvae, and delayed the onset of cholinergic control in larvae. In non-motile stages, therefore, survival in chronic low oxygen may depend on the ability to alter the cardiac ontogenic program to meet the physiological requirements of the developing fish.

The phylogeny and ontogeny of autonomic control of the heart and cardiorespiratory interactions in vertebrates

“…f H in larval trout, Oncorhynchus mykiss, was reduced by a β-adrenergic antagonist early in development and the adrenergic tone increased throughout development as a result of increasing levels of circulating catecholamines. In contrast, cholinergic inhibition of the heart by the addition of acetylcholine (ACh) was ineffective until after hatching (Miller et al, 2011), so that slowing of the heart upon hatching is likely to stem from the appearance of muscarinic cholinoceptors and the establishment of inhibitory nervous control of the heart via the vagus nerve, as speculated by Holeton (Holeton, 1971). If that assumption is correct, establishment of a cholinergic tonus on the heart may correspond to the onset of gill ventilation.…”

“…and E.W.T., unpublished). However, injection of atropine alone had no effect on f H of embryos until they had undergone more than 90% of development, indicating that the onset of a cardiac vagal tonus was delayed until immediately before hatching (Table 2 (Miller et al, 2011).…”

“…6). More extensive cholinergic control has been observed in some chickens but they have been subject to long periods of selective breeding (Miller et al, 2011).…”

Growth hormone transgenesis and polyploidy increase metabolic rate, alter the cardiorespiratory response and influence HSP expression to acute hypoxia in Atlantic salmon (Salmo salar) yolk-sac alevins

“…Alternatively, the absence of a cardiorespiratory response to hypoxia could be explained by a lack of chemosensory feedback at this life stage. In a recent study on the ontogeny of rainbow trout cardiac control, this hypothesis was refuted as adrenergic and cholinergic control of the heart is present shortly after hatching, and the latter can be delayed by chronic hypoxic exposure (Miller et al, 2011).…”

Fish embryos on land: terrestrial embryo deposition lowers oxygen uptake without altering growth or survival in the amphibious fishKryptolebias marmoratus

“…Hypoxia delays development in fishes (e.g. Alderdice et al, 1958;Garside, 1959Garside, , 1966Silver et al, 1963;Miller et al, 2011;Bianchini and Wright, 2013;Robertson et al, 2014). In contrast, embryos of amphibious fishes may experience relatively high oxygen availability if deposited out of water because the diffusion coefficient of oxygen in air is ∼8000 times higher than in water, and boundary layers in air are also much smaller (Dejours, 1988).…”