Regulated bradycardia in the pulmonate limpet Siphonaria (Gastropoda: Mollusca) during pollutant exposure: implication for biomarker studies

Abstract

Although the cardiac activity of invertebrates is now widely used as a biomarker of marine pollution, few studies consider the intrinsic factors causing the variability of heart rate (HR), including the physiological states associated with metabolic depression and behavioural isolation. We examined the cardiac responses to copper exposure of a pulmonate limpet ( Siphonaria capensis Quoy and Gaimard), known to adaptively depress heart rate (and metabolic rate) under naturally stressful conditions (hyposalinity). Analysis of variance was used to assess the effects of copper concentration (0–1000 μg/L), exposure time (0–2 h), and individual difference (eight limpets per concentration) on heart rate parameters. Minute by minute heart rate (HR) and heart rate variability (HRV), and bradycardia (≤10 beats/min) were determined from continuous recording traces. Most of the HR variance was attributable to the interaction of concentration and individuals (35.8%). Considerably lower mean HRs for the higher range of copper concentrations (250 to 1000 μg/L), compared to the lower range (0 to 50 μg/L), were attributable to the virtually exclusive induction of bradycardia in the higher concentration treatments. With increasing concentration, bradycardia was induced sooner and became less interspersed with near normal heart rates (i.e., less episodic). This regulated bradycardial response is apparently associated with isolation (avoidance) behaviour rather than with copper uptake. These findings have implications for biomarker exercises which use heart rate, in cases where invertebrates depress metabolism.