skip to main content


Title: Transcriptomic resilience, symbiont shuffling, and vulnerability to recurrent bleaching in reef‐building corals
Abstract

As climate change progresses and extreme temperature events increase in frequency, rates of disturbance may soon outpace the capacity of certain species of reef‐building coral to recover from bleaching. This may lead to dramatic shifts in community composition and ecosystem function. Understanding variation in rates of bleaching recovery among species and how that translates to resilience to recurrent bleaching is fundamental to predicting the impacts of increasing disturbances on coral reefs globally. We tracked the response of two heat sensitive species in the genusAcroporato repeated bleaching events during the austral summers of 2015 and 2017. Despite a similar bleaching response, the speciesAcropora gemmiferarecovered faster based on transcriptome‐wide gene expression patterns and had a more dynamic algal symbiont community thanAcropora hyacinthusgrowing on the same reef. Moreover,A. gemmiferahad higher survival to repeated heat extremes, with six‐fold lower mortality thanA. hyacinthus. These patterns suggest that speed of recovery from a first round of bleaching, based on multiple mechanisms, contributes strongly to sensitivity to a second round of bleaching. Furthermore, our data uncovered intragenus variation in a group of corals thought generally to be heat‐sensitive and therefore paint a more nuanced view of the future health of coral reef ecosystems against a backdrop of increasing thermal disturbances.

 
more » « less
NSF-PAR ID:
10460727
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Molecular Ecology
Volume:
28
Issue:
14
ISSN:
0962-1083
Page Range / eLocation ID:
p. 3371-3382
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Mass thermal bleaching events are a primary threat to coral reefs, yet the sublethal impacts, particularly on energetics and reproduction, are poorly characterized. Given that the persistence of coral populations is contingent upon the reproduction of individuals that survive disturbances, there is an urgent need to understand the sublethal effects of bleaching on reproductive output to accurately predict coral recovery rates. In 2019, the French Polynesian island of Mo’orea experienced a severe mass bleaching event accompanied by widespread coral mortality. At the most heavily impacted sites, we observedAcropora hyacinthusindividuals that were resistant to bleaching, alongside colonies that bleached but showed signs of symbiont recovery shortly after the bleaching event. We collected fragments fromA. hyacinthuscolonies five months post-bleaching and, using energetic assays and histological measurements, examined the physiological and reproductive consequences of these two distinct heat stress responses. Despite healthy appearances in both resistant and recovered corals, we found that recovered colonies had significantly reduced energy reserves compared to resistant colonies. In addition, we detected compound effects of stress on reproduction: recovered colonies displayed both a lower probability of containing gametes and lower fecundity per polyp. Our results indicate that bleaching inflicts an energetic constraint on the concurrent re-accumulation of energy reserves and development of reproductive material, with decreased reproductive potential of survivors possibly hampering overall reef resilience. These findings highlight the presence of intraspecific responses to bleaching and the importance of considering multiple trajectories for individual species when predicting population recovery following disturbance.

     
    more » « less
  2. Voolstra, Christian R. (Ed.)

    Widespread mapping of coral thermal resilience is essential for developing effective management strategies and requires replicable and rapid multi-location assays of heat resistance and recovery. One- or two-day short-term heat stress experiments have been previously employed to assess heat resistance, followed by single assays of bleaching condition. We tested the reliability of short-term heat stress resistance, and linked resistance and recovery assays, by monitoring the phenotypic response of fragments from 101Acropora hyacinthuscolonies located in Palau (Micronesia) to short-term heat stress. Following short-term heat stress, bleaching and mortality were recorded after 16 hours, daily for seven days, and after one and two months of recovery. To follow corals over time, we utilized a qualitative, non-destructive visual bleaching score metric that correlated with standard symbiont retention assays. The bleaching state of coral fragments 16 hours post-heat stress was highly indicative of their state over the next 7 days, suggesting that symbiont population sizes within corals may quickly stabilize post-heat stress. Bleaching 16 hours post-heat stress predicted likelihood of mortality over the subsequent 3–5 days, after which there was little additional mortality. Together, bleaching and mortality suggested that rapid assays of the phenotypic response following short-term heat stress were good metrics of the total heat treatment effect. Additionally, our data confirm geographic patterns of intraspecific variation in Palau and show that bleaching severity among colonies was highly correlated with mortality over the first week post-stress. We found high survival (98%) and visible recovery (100%) two months after heat stress among coral fragments that survived the first week post-stress. These findings help simplify rapid, widespread surveys of heat sensitivity inAcropora hyacinthusby showing that standardized short-term experiments can be confidently assayed after 16 hours, and that bleaching sensitivity may be linked to subsequent survival using experimental assessments.

     
    more » « less
  3. Abstract

    The prevalence of global coral bleaching has focused much attention on the possibility of interventions to increase heat resistance. However, if high heat resistance is linked to fitness tradeoffs that may disadvantage corals in other areas, then a more holistic view of heat resilience may be beneficial. In particular, overall resilience of a species to heat stress is likely to be the product of both resistance to heat and recovery from heat stress. Here, we investigate heat resistance and recovery among individualAcropora hyacinthuscolonies in Palau. We divided corals into low, moderate, and high heat resistance categories based on the number of days (4–9) needed to reach significant pigmentation loss due to experimental heat stress. Afterward, we deployed corals back onto a reef in a common garden 6‐month recovery experiment that monitored chlorophylla, mortality, and skeletal growth. Heat resistance was negatively correlated with mortality during early recovery (0–1 month) but not late recovery (4–6 months), and chlorophyllaconcentration recovered in heat‐stressed corals by 1‐month postbleaching. However, moderate‐resistance corals had significantly greater skeletal growth than high‐resistance corals by 4 months of recovery. High‐ and low‐resistance corals on average did not exhibit skeletal growth within the observed recovery period. These data suggest complex tradeoffs may exist between coral heat resistance and recovery and highlight the importance of incorporating multiple aspects of resilience into future reef management programs.

     
    more » « less
  4. 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 inAcropora retusa,Porites lobata, andPocilloporaspp., which included: microbiome acclimatization inA. retusa, and both microbiome resilience to the first marine heatwave and microbiome resistance to the second marine heatwave inPocilloporaspp. Moreover, observed microbiome dynamics significantly correlated with coral species‐specific phenotypes. For example, bleaching and mortality inA. retusaboth significantly increased with greater microbiome beta dispersion and greater Shannon Diversity, whileP. lobatacolonies 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.

     
    more » « less
  5. Abstract

    Marine heatwaves are increasing in frequency and duration, threatening tropical reef ecosystems through intensified coral bleaching events. We examined a strikingly variable spatial pattern of bleaching in Moorea, French Polynesia following a heatwave that lasted from November 2018 to July 2019. In July 2019, four months after the onset of bleaching, we surveyed > 5000 individual colonies of the two dominant coral genera,PocilloporaandAcropora, at 10 m and 17 m water depths, at six forereef sites around the island where temperature was measured. We found severe bleaching increased with colony size for both coral genera, butAcroporableached more severely thanPocilloporaoverall. Acroporableached more at 10 m than 17 m, likely due to higher light availability at 10 m compared to 17 m, or greater daily temperature fluctuation at depth. Bleaching inPocilloporacorals did not differ with depth but instead varied with the interaction of colony size and Accumulated Heat Stress (AHS), in that larger colonies (> 30 cm) were more sensitive to AHS than mid-size (10–29 cm) or small colonies (5–9 cm). Our findings provide insight into complex interactions among coral taxa, colony size, and water depth that produce high spatial variation in bleaching and related coral mortality.

     
    more » « less