Reef refugia in the aftermath of past episodes of global warming

doi:10.21203/rs.3.rs-4647970/v1

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Reef refugia in the aftermath of past episodes of global warming

https://doi.org/10.21203/rs.3.rs-4647970/v1

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In the face of rising global temperatures, coral reefs experience coral mass bleaching and mortality. Subtropical and mesophotic environments may represent refugia for reef corals under climate change, where they can survive and eventually recolonize degraded areas. Using a comprehensive database of fossil reefs, we empirically assess the efficacy of subtropical, deeper, and turbid mesophotic environments to restore coral reefs after past global warming events. We focus on tropical coral reefs over the last 275 million years and four rapid climate warming events, which coincided with global reef crises in the geological record. In the aftermath of such hyperthermal events, we observed an increase in the proportions of reefs that occur in deeper (blue) mesophotic environments. Additionally, we found a trend of reef distributions and coral shifting towards higher latitudes. The number of coral occurrences in turbid (brown mesophotic) environments also increased after hyperthermal events. Our results suggest that subtropical, blue, and brown mesophotic environments may have served as immediate refugia for shallow-water coral species escaping warming seawater. While the patterns of reef range shifts and the establishment of blue and brown mesophotic refugia following ancient hyperthermal events provide some hope for coral reefs under current climate change, full recovery took sometimes millions of years.

Ante el incremento de temperatura global, los arrecifes coralinos están experimentando eventos masivos de blanqueamiento y mortalidad. Los ambientes subtropicales y mesofóticos pueden representar refugios para los corales arrecifales, en los cuales pueden escapar de los efectos del cambio climático, sobrevivir y desde allí recolonizar áreas previamente degradadas. Mediante el uso de una exhaustiva base de datos en arrecifes coralinos, en este estudio se evaluó empíricamente la eficacia de los ambientes subtropicales y mesofóticos, tanto de aguas turbias someras (marrones) como de aguas claras profundas (azules), en la recuperación de arrecifes coralinos después de eventos hipertermales en el pasado. Nuestro enfoque se hizo en los arrecifes coralinos tropicales durante los últimos 275 millones de años y cuatro eventos de rápido calentamiento climático, los cuales coinciden con crisis globales en la ocurrencia de arrecifes en el registro fósil. Como consecuencia de dichos eventos hipertermales, observamos un aumento del número de arrecifes en ambientes mesofóticos de aguas profundas (azules). Además, encontramos una tendencia en la distribución de arrecifes y corales que se desplazan hacia latitudes más altas. También se observó un aumento en el número de corales que estuvieron presentes en ambientes de aguas turbias (marrones) después de dichos eventos hipertermales.Nuestros resultados sugieren que, en el pasado, los ambientes subtropicales, mesofóticos azules y mesofóticos marrones pudieron haber servido como refugios inmediatos para las especies de coral de aguas someras, en los cuales encuentran condiciones atenuantes ante el calentamiento oceánico. Si bien los patrones de desplazamiento de los arrecifes en el rango latitudinal y el establecimiento de refugios mesofóticos de aguas marrones y azules posteriores a eventos hipertermales brindan una luz de esperanza para el futuro de los arrecifes coralinos de cara al cambio climático actual, nuestros resultados evidencian que su total recuperación puede tomar millones de años.

mesophotic reefs (mesophotic coral ecosystems)

turbid reefs

reef refugia

scleractinian corals

fossil record

hyperthermal events

Coral reefs are one of the Earth’s most vulnerable ecosystems to climate change (Cooley et al. 2022). Their future is bleak due to the combined effects of anthropogenically induced climate change and other direct human impacts (Pandolfi et al. 2003; Hoegh-Guldberg et al. 2007, 2023; Hughes et al. 2017). We thus need to seek the potential refugia for coral reef persistence and recovery. Refugia are relatively stable and resilient habitats to which organisms can (i) retreat to get protection from environmental stressors; (ii) survive in and; (iii) expand from after the conditions are less stressful (Keppel et al. 2012; Smith et al. 2017). In this sense, reef refugia could reduce the risk of extinction and serve as a source of propagules to recolonize shallow waters for the long-term preservation of coral diversity (Baker et al. 2016; Bongaerts et al. 2017; Hughes et al. 2017; Loya et al. 2019). As thermal stress is probably the most prominent factor causing coral bleaching and ultimately reef decline (Hughes et al. 2018), reef refugia predominantly pertain to thermal refugia, which may manifest as mesophotic (Riegl and Piller 2003; Muir et al. 2018) and higher latitude habitats (Pandolfi and Kiessling 2014).

Range shift toward higher latitudes is a common response of marine organisms to rising temperatures (Lenoir et al. 2020). Reef-building corals respond the same way, given that conditions such as solar radiation, temperature, and aragonite saturation are suitable. However, irradiance may limit carbonate production and restrict coral reef growth in higher latitudes (Perry 2003; Muir et al. 2015). Mid-latitude regions, with cooler waters and reduced aragonite supersaturation, pose additional challenges for reef building (Muir et al. 2015 but see Madin et al. 2016). Despite these constraints for reef building, coral species, both today and in the geological past, have evidently expanded their ranges to higher latitudes in response to warming (Greenstein and Pandolfi 2008; Yamano et al. 2011; Kiessling et al. 2012).

Mesophotic habitats are characterized by restricted light availability and can be categorized into two distinct types: deep mesophotic habitats, also known as blue mesophotic, and turbid water environments, known as brown mesophotic (Majchrzyk et al. 2022; Fig. 1). Blue mesophotic reefs are typically described as deeper extensions of shallow reefs at intermediate depths of 30–150 m (Loya et al. 2019). Although light is a limiting factor, it is still sufficient to sustain photosymbiosis. As temperature decreases by ∼5°C per 100 m of depth in the tropics (Lesser et al. 2009), blue mesophotic environments might serve as immediate refugia for shallow water corals that cannot survive in the intolerably warm seawater (Lesser et al. 2009; Bongaerts et al. 2010; Bridge and Guinotte 2013). However, some deeper reefs today are more susceptible to bleaching than their shallow counterparts (Bongaerts et al. 2010; Diaz et al. 2023).

Despite some evidence indicating that blue mesophotic reefs host resilient coral communities (Bongaerts et al. 2010; Zweifler et al. 2021) their role as climate change refugia on a global scale remains understudied. Current studies show that the blue mesophotic habitats exhibit considerable variability as refugia, depending on coral species composition (Holstein et al. 2015; Bongaerts et al. 2017; Prasetia et al. 2017, 2022; Morais and Santos 2018) and geographic location (Bongaerts et al. 2017; Frade et al. 2018). Key uncertainties also include how well connected euphotic and mesophotic environments are (Van Oppen et al. 2011; Muir et al. 2018; Rocha et al. 2018) and if other climate-related stressors such as deoxygenation compromise the suitability of mesophotic environments as refugia (Hughes et al. 2020).

Brown mesophotic environments are characterized by the presence of abundant suspended particles in the water column. The high turbidity leads to reduced light availability, limiting photosynthesis and potentially hindering reef growth. Nonetheless, turbid environments have been observed to support thriving reef ecosystems (Rosedy et al. 2023; Travaglione et al. 2023). Furthermore, recent research indicates that turbidity plays a key role in protecting reefs from coral bleaching at local (Morgan et al. 2017; Rosedy et al. 2023; Travaglione et al. 2023) and global scales (Cacciapaglia and Van Woesik 2016; Sully and Van Woesik 2020).

The geological record provides insights into the long-term impacts of previous episodes of rapid and sustained warming on reef systems (Pandolfi and Kiessling 2014). The history of reef-building is marked by alternating periods of global reef booms and busts (Kiessling 2009). Over the past 275 million years, metazoan reefs have experienced four significant reef crises (i.e., a significant reduction in reefal calcium carbonate production per unit of time): the end-Permian (252 Ma), end-Triassic (201 Ma), Early Jurassic (180 Ma), and Paleocene-Eocene (56 Ma) (Kiessling and Simpson 2011). These major reef crises coincided with and were probably triggered by global warming events, often referred to as hyperthermal events (Kiessling et al. 2023). Hyperthermal events are brief periods of intense global warming, marked by rapid temperature rise, higher carbon levels, ocean acidification, intensified storms and flooding, and increased land erosion (Foster et al. 2018).

Mesophotic coral ecosystems are established in the fossil record (Zapalski et al. 2017; Zapalski and Berkowski 2019; Łuczyński et al. 2023), but case studies about their role during times of crisis are scarce and contradictory (Stanley and Beauvais 1994; Greenstein and Pandolfi 2008; Kiessling et al. 2009, 2012; Perrin and Bosellini 2013). Only two studies explicitly address the concept of reef refugia in the deep-time fossil record following the most profound scleractinian reef crisis at the end-Triassic mass extinction, approximately 200 million years ago (Stanley and Beauvais 1994; Kiessling et al. 2009). Other studies that tackle refugia are regional and cover younger ages (Greenstein and Pandolfi 2008; Kiessling et al. 2012), and some focus on global cooling events (Perrin and Bosellini 2013).

Here, we extend the hypothesis of reef refugia in mesophotic ecosystems (Glynn 1996) to the "DeTuMi" hypothesis, which posits that the deeper, turbid water and mid-latitudes may serve as reef refugia during hyperthermal events. To test the DeTuMi hypothesis, we focus on tropical coral reefs over the last 275 million years and asses the evidence for a poleward shift of reef-building and an increase in the proportion of blue and brown mesophotic reefs in the aftermath of climate-induced reef crises. We also tackle reef coral occurrences regardless of their occurrence in reefs or non-reef communities.

Data

Fossil coral reef occurrences and their attributes (age, type, environmental setting, bathymetry, and biotic composition), spanning the time from the Middle Permian (275 Ma) to Pleistocene (0.0117 Ma), were downloaded from the Paleo Reefs Database (PARED) (https://paleo-reefs.pal.uni-erlangen.de/) (Kiessling and Krause 2022) in September 2023. We excluded non-tropical reefs, subsurface reefs, and mud mounds. We only included reefs built by corals as either main or secondary constructors (i.e., main and secondary biota in PARED), resulting in 1125 reef sites in total (Fig. 2a). A reef site in PARED comprises any number of reefs of the same age and composition in an area of roughly 300 km² (Kiessling and Flügel 2002).

Fossil colonial coral occurrences were downloaded from the Paleobiology Database (PBDB) (https://paleobiodb.org/) in June 2023 spanning the same interval as reefs (Fig. 2b). All subsequent analyses refer to the time interval from the mid-Triassic to Pleistocene, that is, the time of scleractinian corals. We do this because the ecology of Paleozoic corals may have been significantly different from modern scleractinian corals (Scrutton 1999). Because only colonial corals are consistently reef-building, we excluded solitary corals as well as known azooxanthellate genera such as Madrepora, Lophelia, and Tubastraea from the analyses. The assignment of coloniality and symbiotic mode (i.e., zooxanthellate, azooxanthellate, and apozooxanthellate corals) was done following (Kiessling and Kocsis 2015) through the chronosphere package v0.6.1 (Kocsis and Raja 2023). Analyses were performed at the genus level because this is the most reliable level of taxonomic classification of fossil corals (Lathuilière 1996). Taxa with uncertain genus identification were excluded, as were occurrences that could not be assigned to a single geological stage. Occurrences were binned to chronostratigraphic stages (Gradstein and Ogg 2020) following the protocol in R package divDyn v0.8.2 (Kocsis et al. 2019). Unassigned occurrences were omitted from analyses. After filtering, the PBDB dataset consisted of 22,833 colonial, zooxanthellate coral occurrences of 450 scleractinian genera.

All reef sites were categorized based on: (1) bathymetry (2) turbidity, and (3) absolute paleolatitude. (1) As the absolute depth is difficult to assess in the geological record, we used an estimate for depth relative to the wave base. Wave bases can be reliably traced based on sedimentary attributes, which are connected to water energy and depth (Peters and Loss 2012). The inferred depth can thus be loosely connected with incident light. Below storm-weather wave base usually indicates a water depth of greater than 50 m in protected embayments and 100 m in open ocean settings (Peters and Loss 2012). We assume that blue mesophotic environments already start below the fair-weather wave base, which is shallower than the storm-weather wave base but not by much (Peters and Loss 2012). Accordingly, we categorized clear-water reefs that are recorded above the fair-weather wave base and in carbonate settings as shallow water reefs (i.e., euphotic), and reefs occurring below the fair-weather wave base as deeper water reefs (i.e., blue mesophotic). The coral occurrences were categorized into euphotic and blue mesophotic environments using the function categorize in divdyn R package (Kocsis et al. 2019), which classifies environments as shallow or deep based on the environmental information from the PBDB. As for reefs, coral occurrences in shallow water that also occur in turbid environments (i.e., siliciclastic or marly lithology) were excluded from the analyses.

(2) Turbidity was inferred from the environmental setting of the reef, recorded in the PARED database, where brown mesophotic reefs occur in marginal marine coastal, siliciclastically influenced shelf or platform depositional environments (i.e., subenvironment 1d in PARED; Kiessling and Flügel 2002). Colonial coral occurrences were divided into clear and brown mesophotic environments based on lithological information from the PBDB using the same approach as for the bathymetry.

(3) The absolute paleolatitudes for both reefs and corals were reconstructed with rgplates v0.3.2 package for R (Kocsis et al. 2023) and global plate models that use paleomagnetic reference frame because they report true paleolatitudes (Buffan et al. 2023). We initially used the Scotese global plate model (Scotese and Wright 2018; Kocsis and Scotese 2020, 2021). To test the robustness of the results, we additionally reconstructed paleolatitudes with the other global plate models (Torsvik and Cocks 2016; Merdith 2020; Merdith et al. 2021;). We followed the same protocol for the paleolatitudinal reconstructions of coral occurrences.

As the hyperthermal events are too brief to leave a substantial record, we assigned reefs and colonial corals respectively to (i) normal (background) times and (ii) post-hyperthermal times. The post-hyperthermal times are the succeeding stages of the onset of the hyperthermal events that caused reef crises: (i) Permian-Triassic (P/T, Induan stage, 250.9 Ma), (ii) Triassic/Jurassic (T/J, Hettangian stage, 200.4 Ma), (iii) Toarcian Oceanic Anoxic Event (TOAE, Toarcian stage, 179.5 Ma), and (iv) Paleocene-Eocene Thermal Maximum (PETM, Ypresian stage, 52 Ma) (Kiessling et al. 2023).

Statistical analyses

All analyses were performed using the R program v4.3.2 (R Core Team 2023). We calculated the proportions of the environmental settings (i.e., euphotic vs. blue mesophotic and euphotic vs. brown mesophotic) at post-hyperthermal and normal times, respectively. The standard error of difference (SE_dif) was calculated as:

$${SE}_{dif} =\sqrt{{\left(\frac{{p}_{1}*\left(1-{p}_{1}\right)}{{n}_{1}}\right)}^{2}+{\left(\frac{{p}_{2}*\left(1-{p}_{2}\right)}{{n}_{2}}\right)}^{2}}$$

where p₁ and p₂ are the sample proportions of the two groups, and n₁ and n₂ are the sample sizes of the two groups.

The limited sample size of the post-hyperthermal reefs (n = 12 for bathymetry, n = 14 for turbidity, and n = 16 for paleolatitude) limits the power of classical statistical tests. We thus applied a bootstrap approach in which we repeatedly sampled randomly (with replacement) the original dataset to create a virtual background and post-hyperthermal datasets, of the same size as our raw data. We performed 1,000,000 resampling iterations to estimate the probability that our observed increase in refugia habitats or poleward shifts are due to chance. For proportional data (e.g., occurrences in mesophotic habitats) the bootstrap p-value refers to the probability that the post-hyperthermal increase in proportions is at least as high in the random dataset as observed in the raw data. Similarly, for latitudinal shifts, the p-value refers to the probability that at least the observed poleward shift of post-hyperthermal reefs emerges due to chance.

Reefs

Reefs are generally rare in the aftermath of hyperthermal events. The scarcity of post-hyperthermal reefs is anticipated during these crises, reflecting the challenging environmental conditions that impede the normal proliferation of reefs. Thus, to increase statistical power, reefs were pooled over all four hyperthermals.

Blue mesophotic

There were 816 coral reefs at normal times and 12 post-hyperthermal reefs with inferred depth, out of which 8 occurred in euphotic and 4 in blue mesophotic habitats (Fig. 3). The proportion of reefs in blue mesophotic environments increased by 25 ± 13% following hyperthermal events compared to normal times (Fig. 4). The probability that at least this increase in blue mesophotic reefs emerges due to chance is 0.007 (bootstrap p-value).

Brown mesophotic

There were 1125 coral reefs with lithological information – 1109 at normal times and 16 at post-hyperthermal times, out of which 14 are recorded in euphotic and 2 in brown mesophotic environments. The proportion of reefs in brown mesophotic environments is statistically indistinguishable between normal and post-hyperthermal times (bootstrap p-value = 0.4) (Fig. 5).

Latitudinal distribution

There were 908 coral reefs at normal times and 16 at post-hyperthermal times. After the hyperthermal events, coral reefs shifted their ranges poleward by 8.23° (bootstrap p-value = 0.006) (Fig. 6; Scotese and Wright 2018; Kocsis and Scotese 2020, 2021). Alternative paleolatitudinal reconstructions (Torsvik and Cocks 2016; Merdith 2020; Merdith et al. 2021) yielded the same basic results. According to the Merdith model, coral reefs shifted ranges by 4.33° poleward but this shift is not significant (bootstrap p-value = 0.11) (Supplemental Fig. S1). The third global plate model (Torsvik and Cocks 2016) showed the largest poleward shift of 9.65°, which was significant (bootstrap p-value = 0.0003) (Supplemental Fig. S3).

Additionally, the association matrix shows that in the aftermath of hyperthermal events, the majority of reefs were located in the subtropical latitudes regardless of their habitat (Table 1).

Table 1

Association matrix showing the number of euphotic, brown, and blue mesophotic reefs in tropical and subtropical regions in the aftermath of hyperthermal events based on Scotese global plate model (Scotese and Wright 2018; Kocsis and Scotese 2020, 2021).
	Tropical	Subtropical
Euphotic	1	12
Brown mesophotic	1	1
Blue mesophotic	0	4

Colonial corals

The bathymetry of colonial coral occurrences changed slightly after the hyperthermal events (bootstrap p-value = 0.01) (Fig. 7). However, there is a signal in brown mesophotic habitats, which were by 8 ± 3% more occupied by corals in the aftermath of hyperthermal events (bootstrap p-value < 0.0001) (Fig. 8). Colonial corals shifted their ranges by 8.95° poleward after the global warming events based on the Scotese global plate model (Scotese and Wright 2018; Kocsis and Scotese 2020, 2021) (bootstrap p-value < 0.0001) (Fig. 9). Another model (Merdith 2020; Merdith et al. 2021) revealed the same pattern but with a slightly smaller range shift of 5.81° poleward (bootstrap p-value < 0.0001) (Supplemental Fig. S2). The third model (Torsvik and Cocks 2016) showed that corals shifted their ranges by 16.8° poleward after the hyperthermal events (bootstrap p-value < 0.0001) (Supplemental Fig. S4).

In support of the "DeTuMi" hypothesis we found that over the last 275 million years, reefs were significantly more common in blue mesophotic environments and higher latitudes in post-hyperthermal intervals than during normal times.

Although data are genuinely limited, bootstrap resampling supports our main findings that higher latitudes and blue mesophotic environments consistently served as reef refugia. The higher latitude shifts of reef corals and coral reefs may reflect the tracking of suitable environmental conditions by coral propagules. Our results underscore the importance of considering latitude as a factor influencing the survival and distribution of coral reefs during periods of environmental stress (Greenstein and Pandolfi 2008; Kiessling et al. 2012; Madin et al. 2016). The majority of euphotic, blue, and brown mesophotic reefs were established in higher latitudes in the aftermath of hyperthermal events (Table 1). The only two reefs that occurred in the tropics were, in fact, close to the tropical boundary (i.e., 22.85° and 19.8° absolute paleolatitudes). Results for post-hyperthermal latitudinal shifts vary among plate tectonic reconstructions but consistently exhibit a substantial poleward shift of reef sites and reef corals. Combined our results suggest that cooler temperatures and lower incident light may support coral persistence under climate warming.

The increase of reefs in blue mesophotic environments occurred despite widespread dysoxia and anoxia during hyperthermal events particularly in deeper waters (Zhang et al. 2023). Blue mesophotic environments can shelter corals from heat stress and thus have the capacity to contribute to shallow reef recovery. Although some modern mesophotic reefs have been reported to have a greater sensitivity to bleaching than their shallow-water counterparts (Bongaerts et al. 2010; Diaz et al. 2023), our results indicate deeper settings were beneficial for reefs in light of ancient hyperthermal events. An illustrative example of reef refugia following the most profound scleractinian reef crisis at the end-Triassic mass extinction showcases a coral-microbial reef thriving in a blue mesophotic environment and serving as an area of survival and origination for coral genera (Kiessling et al. 2009). This example indicates that blue mesophotic habitats and higher latitudes were plausible refugia early in the evolution of scleractinian corals.

Unlike reefs, coral occurrences shifted towards brown mesophotic environments post-hyperthermal events. The success of reef corals in brown mesophotic habitats is unsurprising given the richness of observations in modern (Cacciapaglia and Van Woesik 2016; Morgan et al. 2017) and fossil assemblages occurring in turbid habitats (e.g., Rosen et al. 2000; Santodomingo et al. 2016; Bosellini et al. 2022). Corals can thrive in sparse communities that do not necessarily build reefs. Our results suggest that brown mesophotic environments facilitated coral survival but limited reef growth. While turbidity may mitigate bleaching (Cacciapaglia and Van Woesik 2016; Morgan et al. 2017; Sully and Van Woesik 2020; Rosedy et al. 2023; Travaglione et al. 2023), it might also limit the light necessary for prolific reef growth. To some degree, the disparity between coral richness and reef development in brown mesophotic habitats might be related to our limited capacity to detect brown mesophotic environments in the geological record. In some highly turbid reef settings, the settlement of fine particles may be inhibited due to the high-water energy (Kleypas 1996; Larcombe and Woolfe 1999). Nevertheless, most turbid reefs, both fossil (Santodomingo et al. 2015) and recent (Perry 2005), do have siliciclastic sediments.

Potential biases

The fossil record, including the reef record, is inherently limited by preservation and sampling biases over time and space (Alroy et al. 2001; Kiessling 2005; Vilhena and Smith 2013; Close et al. 2020). Our dataset shows that the overall number of mesophotic reefs is much lower than the number of euphotic reefs. On the contrary, studies on modern reefs have shown that the number of blue mesophotic reefs might be equal to the number of shallow reefs in some regions (Harris et al. 2013). Therefore, the geological record may be biased towards euphotic reefs. This is supported by a similar bias among all marine fossil occurrences recorded in carbonates (Supplemental Figure S5). In addition, PARED refers to reef sites and reports the attributes of the largest structure in an area, which is typically in the euphotic environment. Mesophotic reefs are only reported if there is no euphotic counterpart in the same area.

Besides the limited sample size, we need to stress the coarse temporal resolution of our study. At present, coral reefs occupy less than one percent of the ocean’s surface area (Spalding et al. 2001). Therefore, it is unsurprising that reefs are also rare in the geological record (Kiessling 2009). Even at peak times of reef development, the number of coral-dominated reef sites was < 100 (i.e., Late Jurassic; Fig. 2a). Moreover, it is close to impossible to observe reefs during rapid events, such that only patterns before and after a crisis can be explored. In our study, the post-crisis fossil reefs represent newly established formations that only emerged thousands to millions of years after the onset of global warming. As such, these reefs cannot be perceived as surviving reefs in a traditional sense, but rather as the first reefs to grow after the climate stressors have vanished. However, we argue that reef recovery commenced where the stock of survivors was largest, that is, in DeTuMi refugia.

The advantage of the fossil record lies in its capacity to allow us to zoom out and observe events over larger timescales. Our study represents the first large-scale deep-time empirical assessment of the efficacy of subtropical and mesophotic reefal environments as refugia. Our study offers a broader contextualization of climate refugia for corals and coral reefs. Subtropical and blue mesophotic habitats will most likely be future reef refugia. This is particularly important considering the challenging conditions they currently confront, which are anticipated to deteriorate further in the next century (Hoegh-Guldberg et al. 2023). Although we support that climate refugia for coral reefs indeed existed in ancient hyperthermal events, full recovery could take millions of years (Flügel and Kiessling 2002) leaving us with a mixed prospect.

Competing interests

The authors declare that they have no competing interests.

Data Availability Statement

The datasets and code used in the study are available in DD’s public GitHub repository: https://github.com/DanijelaD/reef-refugia

Acknowledgments

We are grateful to A. Kocsis and S. Zahirovic for insightful discussions. We thank the editor M. S. Pratchett, topical editor, and two anonymous reviewers for their comments that improved the earlier versions of this manuscript. We also thank all contributors to the Paleobiology Database. This work was supported by the Deutsche Forschungsgemeinschaft (KI 806/17–1) and is embedded in the Research Unit TERSANE (FOR 2332: “Temperature-related Stressors as a Unifying Principle in Ancient Extinctions”). This is Paleobiology Database official publication no. TBD.

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Reef refugia in the aftermath of past episodes of global warming

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