Headwinds to Understanding Stress Response Physiology: A Systematic Review Reveals Mismatch between Real and Simulated Marine Heatwaves

Laboratory experiments have long been used to guide predictions of organismal stress in response to our rapidly changing climate. However, the ability to simulate real world conditions in the laboratory can be a major barrier to prediction accuracy, creating obstacles to efforts informing ecosystem conservation and management. Capitalizing on an extensive experimental literature of coral bleaching physiology, we performed a systematic review of the literature and assembled a database to identify the methods being used to measure coral bleaching in heating experiments and assess how closely heating experiments resembled marine heatwaves (MHWs) on coral reefs. Observations of the maximum photochemical yield of Photosystem II (FV/FM), though not a direct measure of bleaching, vastly outnumbered Symbiodiniaceae density and chlorophyll (g cm-2, pg cell-1) observations in the available literature, indicating the widespread misuse of FV/FM as a proxy for coral bleaching. Laboratory studies in our database used significantly higher maximum temperatures, degree heating times ([~] 1.7 x) and heating rates ([~] 7.3 x), and significantly shorter durations ([~] 1.5 x), than MHWs on coral reefs. We then asked whether exposure differences between lab and reef altered the relationship between coral bleaching and heating metrics using the example of hormesis, the biphasic dose response wherein low to moderate doses elicit some benefit, while high doses are deleterious. We fit curves on the data both with and without ecologically relevant heating metrics and found hormetic curves in some response variables were altered with the exclusion of exposures that fell outside of the bounds of MHWs on coral reefs. Differences between lab exposures and real-world MHWs were large enough to alter the relationships, indicating a high likelihood of prediction error. We recommend laboratory-based studies of coral bleaching use ecologically relevant exposures to improve our predictions of the coral physiological response to our rapidly warming oceans.