American Society of Naturalists

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“Timing metabolic depression: predicting thermal stress in extreme intertidal environments”

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Tin Yan Hui, Yun-wei Dong, Guo-dong Han, Sarah L. Y. Lau, Martin C. F. Cheng, Chayanid Meepoka, Monthon Ganmanee, and Gray A. Williams (Oct 2020)

Anticipatory metabolic depression aligns with temporal structure of rock temperature in a tropical intertidal oyster

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Metabolic depression as a convergent strategy in intertidal ectotherms to survive in thermally extreme but energy-poor environments?

The high shore rock oyster, <i>Isognomon nucleus</i>, forms dense beds in the upper littoral fringe in central Thailand where the rock temperature exceeds 50&nbsp;°C regularly during the hot season.<br />(Credit: Gray A. Williams)
The high shore rock oyster, Isognomon nucleus, forms dense beds in the upper littoral fringe in central Thailand where the rock temperature exceeds 50 °C regularly during the hot season.
(Credit: Gray A. Williams)

Surviving on the highest tidal levels of tropical shores is extremely challenging given the long periods of extremely hot desiccating conditions when the tide is out. This is especially true if you are a sessile organism and yet the oyster, Isognomon nucleus, dominates this habitat on shores in central Thailand. Researchers from the Swire Institute of Marine Science, The University of Hong Kong and collaborators combined laboratory assays and field measurements to determine how this species manages to form dense beds at this extreme tidal level, where rock temperatures can reach 60 °C, exceeding the oysters lethal limits, and rare tidal submergence restrains feeding opportunities.

By measuring the heart rates of these animals over a thermal ramp Hui and colleagues found that the oyster undergoes extraordinary (by >50% and sometimes to flatline) metabolic depression when temperatures increase during low tides. The temperatures at which this depression occurs are related to the rock temperatures and Hui and colleagues demonstrated a strong coupling between physiology and predictability of the thermal environment. They hypothesized that temporal predictability in rock temperature can be exploited by the oyster as an early warning signal to initiate metabolic depression and prepare for severe thermal stress. This ‘early warning’ system allows preparative shifts in physiology to be achieved in a timely fashion following these cues in the environment and allows individual performance to be buffered against survival costs during unfavorable conditions, such as the high energetic costs required to maintain metabolism during severe thermal stress.

Hui and colleagues argue this coupling between organismal physiology and temporal predictability of the environment plays a key role in determining species performance and survival in extreme thermal environments and, importantly, that the prevalence of metabolic depression in distantly-related high shore ectotherms suggests convergent evolution of this strategy as an underlying, key mechanism to survive in thermally extreme but energy-poor environments.


Abstract

Anticipatory changes in organismal responses, triggered by reliable environmental cues for future conditions, are key to species’ persistence in temporally variable environments. Such responses were tested by measuring the physiological performance of a tropical, high shore oyster in tandem with the temporal predictability of environmental temperature. Heart rate of the oyster increased with environmental temperatures until body temperature reached ~37 °C, when a substantial depression occurred (~60%) before recovery between ~42–47 °C, after which cardiac function collapsed. The sequential increase, depression and recovery in cardiac performance aligned with temporal patterns in rock surface temperatures, where the risk to reach temperatures close to the oysters’ lethal limit accelerates if the rock heats up beyond ~37 °C, coinciding closely with the body temperature at which the oysters initiate metabolic depression. The increase in body temperature over a critical threshold serves as an early-warning cue to initiate anticipatory shifts in physiology and energy conservation before severe thermal stress occurs on the shore. Cross-correlating the onset of physiological mechanisms and temporal structures in environmental temperatures, therefore, reveals the potential role of reliable, real-time environmental cues for future conditions in driving the evolution of anticipatory responses.