Cardiac Arrest during Gamete Release in Chum Salmon Regulated by the Parasympathetic Nerve System

Abstract

Cardiac arrest caused by startling stimuli, such as visual and vibration stimuli, has been reported in some animals and could be considered as an extraordinary case of bradycardia and defined as reversible missed heart beats. Variability of the heart rate is established as a balance between an autonomic system, namely cholinergic vagus inhibition, and excitatory adrenergic stimulation of neural and hormonal action in teleost. However, the cardiac arrest and its regulating nervous mechanism remain poorly understood. We show, by using electrocardiogram (ECG) data loggers, that cardiac arrest occurs in chum salmon (Oncorhynchus keta) at the moment of gamete release for 7.39±1.61 s in females and for 5.20±0.97 s in males. The increase in heart rate during spawning behavior relative to the background rate during the resting period suggests that cardiac arrest is a characteristic physiological phenomenon of the extraordinarily high heart rate during spawning behavior. The ECG morphological analysis showed a peaked and tall T-wave adjacent to the cardiac arrest, indicating an increase in potassium permeability in cardiac muscle cells, which would function to retard the cardiac action potential. Pharmacological studies showed that the cardiac arrest was abolished by injection of atropine, a muscarinic receptor antagonist, revealing that the cardiac arrest is a reflex response of the parasympathetic nerve system, although injection of sotalol, a β-adrenergic antagonist, did not affect the cardiac arrest. We conclude that cardiac arrest during gamete release in spawning release in spawning chum salmon is a physiological reflex response controlled by the parasympathetic nervous system. This cardiac arrest represents a response to the gaping behavior that occurs at the moment of gamete release.

Physiological Responses of Free-Swimming Adult Coho Salmon to Simulated Predator and Fisheries Encounters

“…In addition, no study has concurrently measured the f H of a group of conspecifics (with or without corralling), and so the data from the present study have relevance to capture attempts on salmon aggregations, which are common during Pacific salmon migrations. Routine f H was stable and low (e.g., ∼30 beats min Ϫ1 ) relative to findings of previous studies on adult salmonids (Anderson et al 1998;Gallaugher et al 2001;Steinhausen et al 2008), particularly those engaging in prespawning behaviors Makiguchi et al 2009). …”

Sexual behaviour of a Masu salmon parr, with implications for the evolution of parr sexual behaviour in the salmonines

“…If this hypothesis is correct, then all salmonine precocious parr should display quivering and trembling gaping during milt release. The function of gaping is less clear (e.g., perhaps it is simply a neurological side effect of gamete release; Makiguchi et al 2009). Unfortunately, parr behaviour is often obscured by movements of the larger male ⁄ female partners and by the larger male's sperm cloud.…”

“…This may be because sexual behaviours such as quivering and trembling are required to stimulate the female and help coordinate partners and as such are necessary prerequisite to successful spawning. The function of gaping is less clear (e.g., perhaps it is simply a neurological side effect of gamete release; Makiguchi et al 2009). It would be interesting to ask whether parr perform these behaviours with the same intensity and frequency as migratory males and whether a female can be stimulated to spawn with the sexual feedback from only parr males.…”