This blog post is provided by Andrew Villeneuve and tells the #StoryBehindThePaper for the paper „Predicting organismal response to marine heatwaves using dynamic thermal tolerance landscape models”, which was recently published in the Journal of Animal Ecology. In their paper, Villeneuve and White used mechanistic thermal death time models to understand how different marine heatwave profiles might impact species with different thermal adaptations. In their simulation paper, they found short and hot heatwaves to have the same effect as long and warm heatwaves. They also found that the extent to which an organism can tolerate chronic temperatures can, in certain occasions, be more important than commonly measured acute tolerance.

Marine heatwaves: a multidimensional threat

Marine heatwaves, a niche concept twenty years ago, have since exploded into the scientific and public consciousness. Ecologists began ringing alarm bells about the dramatic ecosystem impacts of these events starting with the 1997 El Niño and expanding to dozens of major, recognised events throughout the world’s oceans. During these events, images of bone-white bleached coral and shorelines cluttered with decaying shellfish circulated broadly – indications of thermal mass mortality events. We’ve recognized that, while such heatwave or marine ‘weather’ events are transitory on a climatological scale, they have profound impacts on the ecosystem functioning during their short durations.

Extreme events are notoriously difficult to categorize when there are multiple dimensions of variability that we can measure. Marine heatwaves vary in magnitude, duration, frequency, return time, spatial extent, rate of warming and cooling. In a series of seminal papers, Hobday et al. (2016, 2018) defined a method of categorizing marine heatwave extremity on a simple scale of I-IV, Moderate to Extreme, to allow for cross-event comparisons and ease communication with governments and the public. This method relies on statistical analysis of historical conditions, where events that exceed the upper 90^th percentile of temperatures are considered a heatwave. Importantly, this categorization relies on the magnitude of the event only, and as some have pointed out, with ongoing warming we will eventually encounter years that are entirely a heatwave (Amaya et al., 2023).

While helpful, this statistical approach leaves ecologists, and anyone concerned about the impacts of marine heatwaves, out in the cold. If the primary interest is how marine heatwaves might impact marine ecosystems, should we not look to these biological impacts to determine the strength of an event, and by extension predict future impacts?

Mass mortality as tractable phenomena to categorize heatwaves

Given marine heatwaves have resulted in notable mass mortality events in marine ectotherms (Garrabou et al., 2022; Raymond et al., 2022), predicting how much mortality a heatwave will cause for a species would be one compelling approach to this categorisation problem. In our recent Journal of Animal Ecology paper, we used dynamic thermal tolerance models as an alternative approach to describing marine heatwave extremeness. Dynamic tolerance models are attractive because they leverage the fundamental logarithmic relationship between stressful temperature and empirically-measured time before death in ectotherms (so-called thermal death time models) to predict survival probability over any temperature-time series collected in the environment (Rezende et al., 2014, 2020).

Using a computational approach, we simulated 2,788 marine heatwaves of varying magnitude, duration, seasonal timing, and interannual variation and then ‘exposed’ three hypothetical organisms to each heatwave in silica. These three organisms have intersecting thermal death time curves (closely approximating some marine bivalve species) that result in differential relative performance over acute and chronic heatwave events. Using dynamic tolerance models, we extracted end survival and compared the heatmap of survival results against how a statistical definition would categorize each heatwave.

Non-linearity in physiology reveals interesting heatwave responses

As we expected, we found cases where a statistical definition of marine heatwaves failed to account for a wide range of survival scenarios within each statistical category. Indeed, the statistical method just tell us if an event is extreme compared to historical conditions, rather than if an event is extreme for the biology and ecology of a system. In one tested scenario, the extreme heatwave category (level IV) encompassed survival from ~100% to ~40% – quite a spread of results!

One important assumption of the statistical categorization method is that an event must last longer than 5 days to be considered a marine heatwave. But what does a mussel or seagrass care if an event is more or less than 5 days? From a biological perspective, what matters is if the conditions are stressful, even over short durations. We found short durations to also result in significant mortality when occurring over large magnitudes. Such acute events are common in highly variable coastal systems under the influence of tides, solar radiation, and upwelling.

We highlight two other tantalizing results. One, that there are heatwaves that look very different (e.g., short duration large magnitude versus long duration small magnitude) but theoretically result in equivalent post-event survival. These scenarios lie along survival isoclines of our survival heatmaps. It remains to be tested empirically whether this equivalency holds true in real systems.

Second, that a high acute tolerance (CT_max) does not necessarily equate with better tolerance of heatwave conditions compared to organisms with lower acute tolerance. Our intersecting thermal death time curves result in marine heatwave scenarios where one species performs better than the others. Given that cohabitating species can exhibit diverging curves (Rezende et al., 2014), we might expect different ‘winners’ and ‘losers’ depending on whether a heatwave is long or short, warm or hot. We also stress that relying on acute tolerance (e.g., CT_max)in isolation can result in misleading ranking of species tolerance. The fact that species have different time-temperature tolerance relationships is underappreciated and likely has extensive implications for heatwave tolerance.

Biological first principles to tame the chaos?

While the prospect of building thermal death time curves for every life stage and environmental history of every species is clearly untenable, ecologists can carefully select sentinel species over which to build predictive models. However, there remains much work to be done integrating other variables that affect thermal death time curves, such as acclimation or repeated events. There is also the obvious fact that a heatwave may have significant nonlethal impacts on species but result in no direct mortality. Instead, we would like to frame our research as calling for the use of biological first principles to better understand and predict the impacts of heatwaves. Altogether, mechanistic models like dynamic thermal tolerance models can account for the episodic, highly variable nature of heatwaves and are primed to enable more accurate forecasts of these events’ ecological impacts.

Further reading:

Amaya, D. J., Jacox, M. G., Fewings, M. R., Saba, V. S., Stuecker, M. F., Rykaczewski, R. R., Ross, A. C., Stock, C. A., Capotondi, A., Petrik, C. M., Bograd, S. J., Alexander, M. A., Cheng, W., Hermann, A. J., Kearney, K. A., & Powell, B. S. (2023). Marine heatwaves need clear definitions so coastal communities can adapt. Nature, 616(7955), 29–32. https://doi.org/10.1038/d41586-023-00924-2

Garrabou, J., Gómez‐Gras, D., Medrano, A., Cerrano, C., Ponti, M., Schlegel, R., Bensoussan, N., Turicchia, E., Sini, M., Gerovasileiou, V., Teixido, N., Mirasole, A., Tamburello, L., Cebrian, E., Rilov, G., Ledoux, J., Souissi, J. B., Khamassi, F., Ghanem, R., … Harmelin, J. (2022). Marine heatwaves drive recurrent mass mortalities in the Mediterranean Sea. Global Change Biology, gcb.16301. https://doi.org/10.1111/gcb.16301

Hobday, A. J., Alexander, L. V., Perkins, S. E., Smale, D. A., Straub, S. C., Oliver, E. C. J., Benthuysen, J. A., Burrows, M. T., Donat, M. G., Feng, M., Holbrook, N. J., Moore, P. J., Scannell, H. A., Sen Gupta, A., & Wernberg, T. (2016). A hierarchical approach to defining marine heatwaves. Progress in Oceanography, 141, 227–238. https://doi.org/10.1016/j.pocean.2015.12.014

Hobday, A. J., Oliver, E., Sen Gupta, A., Benthuysen, J., Burrows, M., Donat, M., Holbrook, N., Moore, P., Thomsen, M., Wernberg, T., & Smale, D. (2018). Categorizing and Naming Marine Heatwaves. Oceanography, 31(2). https://doi.org/10.5670/oceanog.2018.205

Raymond, W. W., Barber, J. S., Dethier, M. N., Hayford, H. A., Harley, C. D. G., King, T. L., Paul, B., Speck, C. A., Tobin, E. D., Raymond, A. E. T., & McDonald, P. S. (2022). Assessment of the impacts of an unprecedented heatwave on intertidal shellfish of the Salish Sea. Ecology, 103(n/a), e3798. https://doi.org/10.1002/ecy.3798

Rezende, E. L., Bozinovic, F., Szilágyi, A., & Santos, M. (2020). Predicting temperature mortality and selection in natural Drosophila populations. Science, 369(6508), 1242–1245. https://doi.org/10.1126/science.aba9287

Rezende, E. L., Castañeda, L. E., & Santos, M. (2014). Tolerance landscapes in thermal ecology. Functional Ecology, 28(4), 799–809. https://doi.org/10.1111/1365-2435.12268

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