Maximal coral thermal tolerance is found at intermediate diel temperature variability

Abstract

1. It has become critically important to identify environmental drivers of enhanced thermal tolerance in coral populations as ocean warming threatens the persistence of coral reef ecosystems globally. Variable temperature regimes that expose corals to sub-lethal heat stress have been recognized as a mechanism to increase coral thermotolerance and lessen coral bleaching; however, there is a need to better understand which thermal regimes are best for promoting coral stress hardening, and if thermal priming results in consistent benefits across species with distinct life-history strategies. 2. Standardized thermal stress assays were used to determine the relative thermal tolerance of three divergent genera of corals (Acropora, PocilloporaandPorites) originating from six reef sites fluctuating in temperature by up to 7.7°C day-1, with an annual mean diel variability of 1–3°C day-1. Bleaching severity and dark-acclimated photochemical yield (Fv/Fm) were quantified following exposure to five temperature treatments ranging from 23.0 to 36.3°C — up to 9°C above the regional maximum monthly mean. 3. The greatest thermal tolerance across all species was found at the site with intermediate mean diel temperature variability (2.2°C day-1), suggesting there is an optimal priming exposure that leads to maximal thermotolerance. Interestingly, Acropora and Pocillopora originating from the least thermally variable regimes (i.e., <1.3°C day-1) had lower thermal tolerance than corals from the most variable sites (i.e., > 2.8°C day-1), whereas the opposite was true for Porites, suggesting divergent responses to priming across taxa. 4. We highlight that fine-scale heterogeneity in temperature dynamics across habitats can increase coral thermal tolerance in diverse coral lineages, although in a non-linear manner. Remarkably, comparisons across global studies revealed that the range in coral thermotolerance uncovered in this study across a single reef system (<5 km) were as large as differences observed across vast latitudinal gradients (>300 km). This important finding indicates that local gene flow could improve thermal tolerance between habitats. However, as climate change continues, exposure to intensifying marine heatwaves is already compromising thermal priming as a mechanism to enhance coral thermal tolerance and bleaching resistance.

Thermal preconditioning modulates coral physiology and heat tolerance: A multi-species perspective

“…Despite the same mean temperatures applied in the two preconditioning treatments, the thermal tolerance of corals preconditioned with the VT treatment was increased by approximately 10 % compared to corals from the ST treatment. This is in line with the large body of literature showing that organisms from variable habitats are more stress tolerant than those from stable habitats (Bay & Palumbi, 2015;Drury et al, 2022;Oliver & Palumbi, 2011;Padilla-Gamiño et al, 2024), including specifically for corals from habitats with diel thermal variability of 2 to 3 °C (Brown et al, 2023). Moreover, temperature fluctuations have been shown to mitigate the responses to additional stressors, such as heavy metals in freshwater organisms, indicating a general improvement in stress mitigation and detoxification mechanisms (Hallman & Brooks, 2015).…”

“…Our aquarium experiments demonstrated that thermal preconditioning can be applied to stressharden corals and enhance their ability to cope with an acute heat stress pulse, contributing to the growing body of literature that has primarily reported this phenomenon from the field, including only few ex-situ studies (Ainsworth et al, 2016;Bay & Palumbi, 2015;Brown et al, 2023;Hackerott et al, 2021;Majerova et al, 2021;Martell, 2023;Wall et al, 2023). At the same time, our systematic and multi-species comparison has revealed that the receptiveness to the stress-hardening effects of thermal preconditioning strongly varied between the coral species.…”

“…The features of thermal regimes, including temperature increase, the fluctuation amplitude, temperature maxima and minima, and exposure duration, will be crucial to the success of the priming stimulus (Brown et al, 2023;Brown & Barott, 2022;Hackerott et al, 2021;Martell, 2023;Middlebrook et al, 2008). In our study, both preconditioning regimes, ST and VT, effectively induced various stress-hardening effects, including increases in stress tolerance and/or resilience, in the six coral species applying a mean temperature of 29 ˚C, i.e.…”

“…The nature of the stimulus is crucial for the priming outcome, as its effects are likely dosedependent, and excessively strong stimuli may even be detrimental to the organism (Brown et al, 2023;Hackerott et al, 2021;Martell, 2023). These intricacies are reflected by several recent studies which documented only minor or negligible positive effects (Barshis et al, 2018;Henley et al, 2022) or, in some cases, detrimental outcomes (Klepac & Barshis, 2020;Putnam & Edmunds, 2011;Schoepf et al, 2019;Thomas et al, 2018).…”

“…Further, fine-scale variations in the characteristics of a thermal priming stimulus, such as the diel temperature amplitude or the absolute temperature increase, can significantly alter the outcomes of preconditioning regimes within and across coral species (Calabrese et al, 2007;Calabrese & Mattson, 2017;Carelli & Iavicoli, 2002). For instance, the thermal tolerance of corals and the amplitude of diel temperature fluctuations followed a parabolic relationship, where the intermediate amplitudes of 2-3 °C maximized stress tolerance (Brown et al, 2023), while in other studies, larger amplitudes above 4 °C led to detrimental effects (Klepac & Barshis, 2022;Martell, 2023;Schoepf et al, 2019). Regarding stress-hardening success, of stimulus of thermal variability has generally outperformed that of a stable temperature (Drury et al, 2022).…”