skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Role of host genetics and heat‐tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming
Abstract Identifying which factors lead to coral bleaching resistance is a priority given the global decline of coral reefs with ocean warming. During the second year of back‐to‐back bleaching events in the Florida Keys in 2014 and 2015, we characterized key environmental and biological factors associated with bleaching resilience in the threatened reef‐building coralOrbicella faveolata. Ten reefs (five inshore, five offshore, 179 corals total) were sampled during bleaching (September 2015) and recovery (May 2016). Corals were genotyped with 2bRADand profiled for algal symbiont abundance and type.O. faveolataat the inshore sites, despite higher temperatures, demonstrated significantly higher bleaching resistance and better recovery compared to offshore. The thermotolerantDurusdinium trenchii(formerlySymbiondinium trenchii) was the dominant endosymbiont type region‐wide during initial (78.0% of corals sampled) and final (77.2%) sampling; >90% of the nonbleached corals were dominated byD. trenchii. 2bRADhost genotyping found no genetic structure among reefs, but inshore sites showed a high level of clonality. While none of the measured environmental parameters were correlated with bleaching, 71% of variation in bleaching resistance and 73% of variation in the proportion ofD. trenchiiwas attributable to differences between genets, highlighting the leading role of genetics in shaping natural bleaching patterns. Notably,D. trenchiiwas rarely dominant inO. faveolatafrom the Florida Keys in previous studies, even during bleaching. The region‐wide high abundance ofD. trenchiiwas likely driven by repeated bleaching associated with the two warmest years on record for the Florida Keys (2014 and 2015). On inshore reefs in the Upper Florida Keys,O. faveolatawas most abundant, had the highest bleaching resistance, and contained the most corals dominated byD. trenchii, illustrating a causal link between heat tolerance and ecosystem resilience with global change.  more » « less
Award ID(s):
1737312
PAR ID:
10450070
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Global Change Biology
Volume:
25
Issue:
3
ISSN:
1354-1013
Page Range / eLocation ID:
p. 1016-1031
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Anthropogenic climate change compromises reef growth as a result of increasing temperatures and ocean acidification. Scleractinian corals vary in their sensitivity to these variables, suggesting species composition will influence how reef communities respond to future climate change. Because data are lacking for many species, most studies that model future reef growth rely on uniform scleractinian calcification sensitivities to temperature and ocean acidification. To address this knowledge gap, calcification of twelve common and understudied Caribbean coral species was measured for two months under crossed temperatures (27, 30.3 °C) andCO2partial pressures (pCO2) (400, 900, 1300 μatm). Mixed‐effects models of calcification for each species were then used to project community‐level scleractinian calcification using Florida Keys reef composition data andIPCC AR5 ensemble climate model data. Three of the four most abundant species,Orbicella faveolata, Montastraea cavernosa,andPorites astreoides, had negative calcification responses to both elevated temperature andpCO2. In the business‐as‐usualCO2emissions scenario, reefs with high abundances of these species had projected end‐of‐century declines in scleractinian calcification of >50% relative to present‐day rates.Siderastrea siderea, the other most common species, was insensitive to both temperature andpCO2within the levels tested here. Reefs dominated by this species had the most stable end‐of‐century growth. Under more optimistic scenarios of reducedCO2emissions, calcification rates throughout the Florida Keys declined <20% by 2100. Under the most extreme emissions scenario, projected declines were highly variable among reefs, ranging 10–100%. Without considering bleaching, reef growth will likely decline on most reefs, especially where resistant species likeS. sidereaare not already dominant. This study demonstrates how species composition influences reef community responses to climate change and how reducedCO2emissions can limit future declines in reef calcification. 
    more » « less
  2. Ocean deoxygenation is intensifying globally due to human activities – and is emerging as a grave threat to coral reef ecosystems where it can cause coral bleaching and mass mortality. However, deoxygenation is one of many threats to coral reefs, making it essential to understand how prior environmental stress may influence responses to deoxygenation. To address this question, we examined responses of the coral holobiont (i.e., the coral host, Symbiodiniaceae, and the microbiome) to deoxygenation in corals with different environmental stress backgrounds. We outplantedAcropora cervicornisfragments of known genotypes from anin situnursery to two sites in the Florida Keys spanning an inshore-offshore gradient. After four months, fragments from the outplanted corals were transferred to the laboratory, where we tested differences in survivorship, tissue loss, photosynthetic efficiency, Symbiodiniaceae cell density, and coral microbiome composition after persistent exposure to one of four oxygen treatments ranging from extreme deoxygenation (0.5 mg L-1) to normoxia (6 mg L-1). We found that, for the short duration of exposure tested in this study (four days), the entire coral holobiont was resistant to dissolved oxygen (DO) concentrations as low as 2.0 mg L-1, but that the responses of members of the holobiont decoupled at 0.5 mg L-1. In this most extreme treatment, the coral host showed decreased photosynthetic efficiency, tissue loss, and mortality, and lower Symbiodiniaceae densities in a bleaching response, but most microbial taxa remained stable. Although deoxygenation did not cause major community shifts in microbiome composition, the population abundance of some microbial taxa did respond. Site history influenced some responses of the coral host and endosymbiont, but not the coral microbiome, with corals from the more stressful inshore site showing greater susceptibility to subsequent deoxygenation. Our study reveals that coral holobiont members respond differently to deoxygenation, with greater sensitivity in the coral host and Symbiodiniaceae and greater resistance in the coral microbiome, and that prior stress exposure can decrease host tolerance to deoxygenation. 
    more » « less
  3. ABSTRACT Coral reefs are increasingly threatened by disease outbreaks, yet little is known about the genetic mechanisms underlying disease resistance. Since the 1970s, White Band Disease (WBD) has decimated the Caribbean staghorn coralAcropora cervicornis. However, 15% or more of individuals are highly disease‐resistant, and the genes controlling the production of Argonaut proteins, involved in microRNA (miRNA) post‐transcriptional gene silencing, are up‐regulated in WBD‐resistant corals. This suggests that miRNAs may be key regulators of coral immunity. In this study, we conducted an in situ disease transmission experiment with five healthy‐exposed control tanks and five WBD‐exposed tanks, each containing 50A. cervicornisgenotypes, sampled over 7 days and then sequenced miRNAs from 12 replicate genotypes, including 12 WBD‐exposed and 12 healthy‐exposed control fragments from two time points. We identified 67bona fidemiRNAs inA. cervicornis, 3 of which are differentially expressed in disease‐resistant corals. We performed a phylogenetic comparison of miRNAs across cnidarians and found greater conservation of miRNAs in more closely related taxa, including all three differentially expressed miRNAs being conserved in more than oneAcroporacoral. One of the three miRNAs has putative genomic targets involved in the cnidarian innate immunity. In addition, community detection coupled with over‐representation analysis of our miRNA–messenger RNA (mRNA) target network found two key uniqueA. cervicornismiRNAs regulating multiple important immune‐related pathways such as Toll‐like receptor pathway, endocytosis, and apoptosis. These findings highlight how multiple miRNAs may help the coral host maintain immune homeostasis in the presence of environmental stress including disease. 
    more » « less
  4. Plail, Melissa (Ed.)
    Marine heatwaves are increasing in intensity and frequency, causing worldwide coral bleaching, reductions in coral cover, and shifts in species composition. Recent studies have found, however, that inshore turbid reefs are more resistant to heat stress than offshore clear-water reefs. Inshore turbid reefs, therefore, may play a critical role as climate-change refuges for contemporary coral reefs subjected to marine heatwaves. This perspective explores the importance of inshore reefs in the past, present, and future. Paleo records show that inshore reefs were also crucial as refuges during historically warm periods. Yet, contemporary inshore reefs are especially vulnerable to pollution and land-use-change runoff, which were absent in paleo times. Therefore, inshore reefs need strategic management and protection to maintain their role as climate-change refugia as the oceans continue to warm. 
    more » « less
  5. van_der_Hooft, Justin_J J (Ed.)
    ABSTRACT Coral reefs are experiencing unprecedented loss in coral cover due to increased incidence of disease and bleaching events. Thus, understanding mechanisms of disease susceptibility and resilience, which vary by species, is important. In this regard, untargeted metabolomics serves as an important hypothesis-building tool enabling the delineation of molecular factors underlying disease susceptibility or resilience. In this study, we characterize metabolomes of four species of visually healthy stony corals, includingMeandrina meandrites,Orbicella faveolata,Colpophyllia natans, andMontastraea cavernosa, collected at least a year before stony coral tissue loss disease reached the Dry Tortugas, Florida, and demonstrate that both symbiont and host-derived biochemical pathways vary by species. Metabolomes ofMeandrina meandritesdisplayed minimal intraspecies variability and the highest biological activity against coral pathogens when compared to other species in this study. The application of advanced metabolite annotation methods enabled the delineation of several pathways underlying interspecies variability. Specifically, endosymbiont-derived vitamin E family compounds, betaine lipids, and host-derived acylcarnitines were among the top predictors of interspecies variability. Since several metabolite features that contributed to inter- and intraspecies variation are synthesized by the endosymbiotic Symbiodiniaceae, which could be a major source of these compounds in corals, our data will guide further investigations into these Symbiodiniaceae-derived pathways. IMPORTANCEPrevious research profiling gene expression, proteins, and metabolites produced during thermal stress have reported the importance of endosymbiont-derived pathways in coral bleaching resistance. However, our understanding of interspecies variation in these pathways among healthy corals and their role in diseases is limited. We surveyed the metabolomes of four species of healthy corals with differing susceptibilities to the devastating stony coral tissue loss disease and applied advanced annotation approaches in untargeted metabolomics to determine the interspecies variation in host and endosymbiont-derived pathways. Using this approach, we propose the survey of immune markers such as vitamin E family compounds, acylcarnitines, and other metabolites to infer their role in resilience to coral diseases. As time-resolved multi-omics datasets are generated for disease-impacted corals, our approach and findings will be valuable in providing insight into the mechanisms of disease resistance. 
    more » « less