Cardiac responses of the bay scallop Argopecten irradians to diel-cycling hypoxia

Bottom water oxygen concentrations in coastal environments can oscillate between fully oxygenated and hypoxic conditions on a daily basis. How benthic organisms respond to such drastic changes in oxygen availability is not well understood. Specifically, we do not know the magnitude, duration, and frequency at which diel-cycling hypoxic conditions become stressful. Here we have used non-invasive, infrared sensors to measure the cardiac activity of the Atlantic bay scallop, Argopecten irradians, in response to diel-cycling hypoxia in-situ over one-month periods as well as in controlled laboratory incubations using animals conditioned to contrasting field conditions. In the field, heartbeat rates at a well‑oxygenated site were 23.0 ± 1.8 beats minute− 1 with 12.7 ± 2.1% variance while heartbeat rates at sites with pronounced diel-cycling hypoxia were higher and more variable (site 1: 34.5 ± 3.1 beats minute− 1 with 20.8 ± 3.2% variance; site 2: 48.4 and 45.8 beats minute− 1 with 16% variance). Maximal heartbeat rates were commonly recorded around dawn when oxygen concentrations fell below 5 mg O2 L− 1 suggesting this was a threshold concentration or critical PO2 (Pc) that induced a switch to oxyconformity and onset of anaerobic metabolic pathways. In-situ cardiac activity at locations with diel-cycling hypoxia indicate that A. irradians spent nearly 40% of each day in sub-optimal conditions during which metabolic activity was reduced and/or at least partially sustained by anaerobic metabolism. During laboratory experiments, an increase in heartbeat rate in response to initial declines below 5 mg O2 L− 1 from fully oxygenated conditions suggests a regulatory response in which cardiac activity was enhanced to maintain oxygen supply. At DO below 2 mg O2 L− 1, however, heartbeat rates declined reaching a state of bradycardia and acardia during anoxia, suggesting a conformer response to severe hypoxia. Heartbeat frequency was a suitable proxy for respiration under normoxia, but heartbeat and respiration rates decoupled during severe hypoxia (< 2.0 mg O2 L− 1). A. irradians were able to survive anoxic periods between 12 and 14 h and cardiac activity rapidly returned to basal rates once full oxygen saturation was re-established. Mortality occurred after 23-32 h in anoxia regardless of prior conditioning. We speculate that repetitive exposure to periods of DO oscillations with exposure below 5 mg O2 L− 1 in the field can cause sub-lethal effects to A. irradians affecting fitness, growth, and reproductive success.