Increasingly frequent marine heatwaves are devastating coral reefs. Corals that survive these extreme events must rapidly recover if they are to withstand subsequent events, and long-term survival in the face of rising ocean temperatures may hinge on recovery capacity and acclimatory gains in heat tolerance over an individual’s lifespan. To better understand coral recovery trajectories in the face of successive marine heatwaves, we monitored the responses of bleaching-susceptible and bleaching-resistant individuals of two dominant coral species in Hawai’i,
Marine heatwaves are occurring more frequently as climate change intensifies, resulting in global mass coral bleaching events several times per decade. Despite the time between marine heatwaves decreasing, there is evidence that reef-building corals can develop increased bleaching resistance across repetitive marine heatwaves. This phenomenon of acclimatization via environmental memory may be an important strategy to ensure coral persistence; however, we still understand very little about the apparent acclimatization or, conversely, sensitization (i.e., stress accumulation or weakening) of reef-building corals to consecutive heatwaves and its implications for the trajectory and resilience of coral reefs. Here, we highlight that not only will some corals become stress hardened via marine heatwaves, but many other individuals will suffer sensitization during repeat heatwaves that further exacerbates their stress response during repeat events and depresses fitness. Under current and predicted climate change, it is necessary to gain a better understanding of the acclimatization vs. sensitization trajectories of different species and individuals on the reef, as well as identify whether changes in bleaching susceptibility relates to physiological acclimatization, trade-offs with other biological processes, and ultimately coral persistence in the Anthropocene.
more » « less- Award ID(s):
- 1923743
- NSF-PAR ID:
- 10388566
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Integrative And Comparative Biology
- Volume:
- 62
- Issue:
- 6
- ISSN:
- 1540-7063
- Page Range / eLocation ID:
- p. 1748-1755
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Montipora capitata andPorites compressa , over a decade that included three marine heatwaves. Bleaching-susceptible colonies ofP. compressa exhibited beneficial acclimatization to heat stress (i.e., less bleaching) following repeat heatwaves, becoming indistinguishable from bleaching-resistant conspecifics during the third heatwave. In contrast, bleaching-susceptibleM. capitata repeatedly bleached during all successive heatwaves and exhibited seasonal bleaching and substantial mortality for up to 3 y following the third heatwave. Encouragingly, bleaching-resistant individuals of both species remained pigmented across the entire time series; however, pigmentation did not necessarily indicate physiological resilience. Specifically,M. capitata displayed incremental yet only partial recovery of symbiont density and tissue biomass across both bleaching phenotypes up to 35 mo following the third heatwave as well as considerable partial mortality. Conversely,P. compressa appeared to recover across most physiological metrics within 2 y and experienced little to no mortality. Ultimately, these results indicate that even some visually robust, bleaching-resistant corals can carry the cost of recurring heatwaves over multiple years, leading to divergent recovery trajectories that may erode coral reef resilience in the Anthropocene. -
more » « less
Abstract Global climate change is altering coral reef ecosystems. Notably, marine heatwaves are producing widespread coral bleaching events that are increasing in frequency, with projections for annual bleaching events on reefs worldwide by mid‐century.
Responses of corals to elevated seawater temperatures are modulated by abiotic factors (e.g. environmental regimes) and dominant Symbiodiniaceae endosymbionts that can shift coral traits and contribute to physiological legacy effects on future response trajectories. It is critical, therefore, to characterize shifting physiological and cellular states driven by these factors and evaluate their influence on in situ bleaching (and recovery) events. We use back‐to‐back bleaching events (2014, 2015) in Hawai'i to characterize the cellular and organismal phenotypes of
Montipora capitata corals dominated by heat‐sensitiveCladocopium or heat‐tolerantDurusdinium Symbiodiniaceae at two reef sites.Despite fewer degree heating weeks in the first‐bleaching event relative to the second (7 vs. 10),
M. capitata bleaching severity was greater [bleached cover: ~70% (2014) vs. 50% (2015)] and environmental history (site effects) on coral phenotypes were more pronounced. Symbiodiniaceae affected bleaching responses, but immunity and antioxidant activity was similar in all corals, despite differences in bleaching phenotypes.We demonstrate that repeat bleaching triggers cellular responses that shift holobiont multivariate phenotypes. These perturbed multivariate phenotypes constitute physiological legacies, which set corals on trajectories (positive and/or negative) that influence future coral performance. Collectively, our data support the need for greater tracking of stress response in a multivariate context to better understand the biology and ecology of corals in the Anthropocene.
A free
Plain Language Summary can be found within the Supporting Information of this article. -
more » « less
Abstract Ocean warming is causing global coral bleaching events to increase in frequency, resulting in widespread coral mortality and disrupting the function of coral reef ecosystems. However, even during mass bleaching events, many corals resist bleaching despite exposure to abnormally high temperatures. While the physiological effects of bleaching have been well documented, the consequences of heat stress for bleaching‐resistant individuals are not well understood. In addition, much remains to be learned about how heat stress affects cellular‐level processes that may be overlooked at the organismal level, yet are crucial for coral performance in the short term and ecological success over the long term. Here we compared the physiological and cellular responses of bleaching‐resistant and bleaching‐susceptible corals throughout the 2019 marine heatwave in Hawai'i, a repeat bleaching event that occurred 4 years after the previous regional event. Relative bleaching susceptibility within species was consistent between the two bleaching events, yet corals of both resistant and susceptible phenotypes exhibited pronounced metabolic depression during the heatwave. At the cellular level, bleaching‐susceptible corals had lower intracellular pH than bleaching‐resistant corals at the peak of bleaching for both symbiont‐hosting and symbiont‐free cells, indicating greater disruption of acid–base homeostasis in bleaching‐susceptible individuals. Notably, cells from both phenotypes were unable to compensate for experimentally induced cellular acidosis, indicating that acid–base regulation was significantly impaired at the cellular level even in bleaching‐resistant corals and in cells containing symbionts. Thermal disturbances may thus have substantial ecological consequences, as even small reallocations in energy budgets to maintain homeostasis during stress can negatively affect fitness. These results suggest concern is warranted for corals coping with ocean acidification alongside ocean warming, as the feedback between temperature stress and acid–base regulation may further exacerbate the physiological effects of climate change.
-
Increasing ocean temperatures threaten coral reefs globally, but corals residing in habitats that experience high thermal variability are thought to be better adapted to survive climate-induced heat stress. Here, we used long-term ecological observations and in situ temperature data from Heron Island, southern Great Barrier Reef to investigate how temperature dynamics within various thermally variable vs. thermally stable reef habitats change during a marine heatwave and the resulting consequences for coral community survival. During the heatwave, thermally variable habitats experienced larger surges in daily mean and maxima temperatures compared to stable sites, including extreme hourly incursions up to 36.5 °C. The disproportionate increase in heat stress in variable habitats corresponded with greater subsequent declines in hard coral cover, including a three-times greater decline within the thermally variable Reef Flat (70%) and Deep Lagoon (83%) than within thermally stable habitats along sheltered and exposed areas of the reef slope (0.3–19%). Interestingly, the thermally variable Reef Crest experienced comparatively small declines (26%), avoiding the most severe tidal ponding and resultant heat stress likely due to proximity to the open ocean equating to lower seawater residence times, greater mixing, and/or increased flow. These results highlight that variable thermal regimes, and any acclimatization or adaptation to elevated temperatures that may lead to, do not necessarily equate to protection against bleaching and mortality during marine heatwaves. Instead, thermally stable habitats that have greater seawater exchange with the open ocean may offer the most protection to corals during the severe marine heatwaves that accompany a changing climate.more » « less
-
more » « less
Abstract Microbiomes are essential features of holobionts, providing their hosts with key metabolic and functional traits like resistance to environmental disturbances and diseases. In scleractinian corals, questions remain about the microbiome's role in resistance and resilience to factors contributing to the ongoing global coral decline and whether microbes serve as a form of holobiont ecological memory. To test if and how coral microbiomes affect host health outcomes during repeated disturbances, we conducted a large‐scale (32 exclosures, 200 colonies, and 3 coral species sampled) and long‐term (28 months, 2018–2020) manipulative experiment on the forereef of Mo'orea, French Polynesia. In 2019 and 2020, this reef experienced the two most severe marine heatwaves on record for the site. Our experiment and these events afforded us the opportunity to test microbiome dynamics and roles in the context of coral bleaching and mortality resulting from these successive and severe heatwaves. We report unique microbiome responses to repeated heatwaves in
Acropora retusa ,Porites lobata , andPocillopora spp., which included: microbiome acclimatization inA. retusa , and both microbiome resilience to the first marine heatwave and microbiome resistance to the second marine heatwave inPocillopora spp. Moreover, observed microbiome dynamics significantly correlated with coral species‐specific phenotypes. For example, bleaching and mortality inA. retusa both significantly increased with greater microbiome beta dispersion and greater Shannon Diversity, whileP. lobata colonies had different microbiomes across mortality prevalence. Compositional microbiome changes, such as changes to proportions of differentially abundant putatively beneficial to putatively detrimental taxa to coral health outcomes during repeated heat stress, also correlated with host mortality, with higher proportions of detrimental taxa yielding higher mortality inA. retusa . This study reveals evidence for coral species‐specific microbial responses to repeated heatwaves and, importantly, suggests that host‐dependent microbiome dynamics may provide a form of holobiont ecological memory to repeated heat stress.
