Understanding the exceptional heat tolerance of reef corals from the Persian/Arabian Gulf

Lead Research Organisation: University of Southampton
Department Name: School of Ocean and Earth Science

Abstract

Shallow water coral reefs are on decline at a global scale and are expected to be lost within this century. The increasing frequency and intensity of heat stress episodes have been identified as the major threat to reefs survival. The impact of high temperature on corals can be exacerbated by regional factors such as pollution of coastal seawater. In the Persian/Arabian Gulf (hereafter: "the Gulf") corals are exposed to elevated salinity levels and unusual nutrient concentrations. At the same time, they endure extreme temperature maxima that would kill corals elsewhere on the planet. Despite the crucial role of the lipid composition of zooxanthellae in defining the susceptibility of reef corals to heat stress, the specific lipid signature characterising the symbionts of Gulf corals is as yet completely unexplored. The proposed study will address this knowledge gap by applying a mass spectrometric (MS) approach to compare the lipid profiles of zooxanthellae from Gulf corals flourishing in an extreme temperature habitat (Abu Dhabi, UAE) with those of conspecifics that experience typical tropical conditions in the Indo/South Pacific (Hoga Island, Fiji). We will analyse samples from the two field sites collected at different seasons over a year. In parallel, we will monitor changes in the physicochemical environment over the same period. This strategy will identify key differences in the quantitative / qualitative lipid composition of zooxanthellae associated with coral survival at high temperature and with the dynamic response to changes in environmental conditions. We will use our established laboratory strains of Porites lobata originating from the Gulf and the Pacific to examine how altered temperature, nutrient concentrations and salinity individually affect the lipid complement of zooxanthellae. The experiments under controlled conditions will allow us to test our hypothesis that the unique physicochemical environment of the Gulf promotes thermotolerance of corals by altering the lipid composition of zooxanthellae. The comparative approach of this project will be enabled by the highly complementary expertise of the participating scientists (coral physiology/molecular biology/biochemistry; lipid biology/mass spectrometry & biogeochemistry). The project will benefit from excellent project partners (Burt, Voolstra, Suggett, Smith) that provide substantial in-kind contributions and from the support of a large international consortium of stakeholders from academia, industry, governmental and non-governmental organizations concerned with the coral ecosystems of the Gulf.

Planned Impact

The outcomes of the proposed research will facilitate the prediction of the adaptability of reef corals to global warming and is of global significance for governmental policy makers and various non-governmental organisations involved in reef conservation. In particular, the results of the study will underline the importance of the Persian / Arabian Gulf coral communities as unique examples of stress resilient corals, making a strong case in support of their rigorous conservation. Increased efforts are indeed required to protect these corals ecosystems for the future and save them for a sustainable exploitation by the local population, as a reservoir of exceptional genetic material and as a natural laboratory for a broad scientific community. The key activity to increase the impact of the proposed study is the establishment of a "Mideast Coral Reef Society" with the aim to improve the knowledge exchange between representatives of academia, industry / private sector, governmental and non-governmental organisations. The impact activity will create a web-based framework that promotes the constituting activities and knowledge exchange during the early phase of the association. Furthermore, the support will help the development into a self sustained organisation, either as independent group or integrated into an existing organisation such as the International Society of Coral Reef Studies (ISRS).
The initiative for the Mideast Coral Reef Society was jointly presented by the PI and Prof. John Burt from the New York University Abu Dhabi as part of the pilot work undertaken for this project and received strong support from local and international stakeholders from the above-mentioned sectors. At present, over 50 representatives from Saudi Arabia, Kuwait, Bahrain, Iran, Jordan, Egypt, Oman, Abu Dhabi, Qatar, Dubai, Australia, USA, Canada, Germany, Russia, UK, India and Taiwan expressed their support for the initiative (see attached letter of support).
Climate change, especially the warming of the oceans, is a pressing problem for human societies. The loss of coral reefs and their biodiversity is predicted to occur within the next 100 years and will have major social, economic and political consequences for reef dependent populations. Coral reefs have an iconic status among the general public, who are increasingly aware of their key status among the biologically most diverse ecosystems and their importance for humanity. The concern about the potential loss of the reefs is correspondingly high.
We will address these concerns and engage the general public by a series of outreach activities and inform about the concept of our work, the progress and the results via oral presentations, internet publications, and print media.

Publications

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Ferrier-Pagès C (2016) Phosphorus metabolism of reef organisms with algal symbionts in Ecological Monographs

 
Description Over the past decades, mass bleaching events caused primarily by elevated seawater temperatures have become more frequent and contribute significantly to the observed degradation of coral reefs. In the Persian/Arabian Gulf ("the Gulf") corals are exposed to elevated salinity levels and unusual nutrient concentrations. At the same time, they endure extreme temperature maxima that would kill corals elsewhere on the planet. Hence, they represent ideal models to study the basis of heat stress tolerance and contribute essential information required to forecast the fate of coral reefs in the warmer oceans of the future.
In this project, we explore the physiological basis for the stress resilience of the Gulf corals. The outcomes of our research facilitates the prediction of the adaptability of reef corals to global warming. In particular, the results of the study underline the importance of the Persian/Arabian Gulf coral communities as unique examples of stress resilient corals, making a strong case in support of their rigorous conservation.
The results of our research have been published in scientific journals and communicated to the public in diverse events and engagement activities. Summary of key findings:

Key Findings 1 (published):
In light of the bleak predictions for coral reefs, drastic measures such as the intentional translocation of individuals has been proposed to rescue threatened species and ecosystems (Hoegh-Guldberg et al. 2008, Science 321, 345-346, 397 citations). Since the oceanographic conditions in the Gulf are believed to prevent a natural dispersal of Gulf corals to adjacent seas (Sheppard et al. 1992), their "assisted migration" has been proposed to help the restoration of reefs devastated by rising sea surface temperature in the Indo-Pacific (Riegl et al. 2011; Coles 2003).
We found that, despite the dominant opposing surface current, gene flow exists from the Gulf into the adjacent Gulf of Oman, potentially facilitating a natural pre-adaptation of Indian Ocean populations to the projected warming seas.
Furthermore, we demonstrate experimentally that the superior fitness of Gulf corals at high temperatures is associated with local adaptations to the high salinity of the Gulf and would be lost if they were transferred directly to other reef environments. Indeed, our study of the ancestry of three Porites species along >1000 km of coastline in the Arabian Gulf and the Gulf of Oman through the molecular identification of their symbiotic algae, reveals a restricted distribution of Gulf corals within the adjacent seas. Hence, coral reef management cannot rely on assisted migration as a "quick fix" solution for reefs devastated by global warming, but should rather concentrate on alternative actions to strengthen the resilience of reef ecosystems.

Key Findings 2 (published)
By analysing nuclear ribosomal DNA, we have recently shown that Symbiodinium clade C3 is the prevalent symbiont in coral species in Abu Dhabi, UAE whereas clade D zooxanthellae, proposed candidates for thermotolerant symbioses, were not encountered. This finding was puzzling since clade C3 symbionts have not usually been found to be exceptionally thermotolerant, but have rather been defined as a cosmopolitan, generalist clade. In this paper, we have answered two important questions to establish the significance of clade C3 zooxanthellae for the functioning of the coral-alga symbiosis in extreme temperature environments: (1) Is the prevalence of these C3 zooxanthellae in the Southern / Southeastern Gulf a temporal phenomenon that might be reverted seasonally or permanently to a dominance of clade D symbionts? (2) Does the C3 zooxanthellae lineage from the Gulf represent a cryptic species that cannot been identified by the resolution of "classical" ITS2 sequence phylotyping?
We addressed these questions by monitoring the seasonal dominance of zooxanthellae types in individual colonies of six coral species over three years and by analysing an alternative phylogenetic marker (psbAncr) of C3-type zooxanthellae along >400 km of coastline in the Persian/Arabian Gulf. We found that the predominant symbionts from Gulf corals represent a new species that we named Symbiodinium thermophilus. Despite some species-specific variability in seasonal composition of the zooxanthellae complement, S. thermophilus remains the prevalent symbiont of corals from the Gulf, the world's hottest sea.
Our results demonstrate that the molecular method that is currently most often used to classify coral symbionts might obscure significant taxonomic features and has insufficient capacity to identify heat tolerant symbionts. Hence, the insights provided by our paper allow us to link the molecular taxonomy of alga symbionts with their stress tolerance, an important advance in predicting the resilience of coral under the pressure of climate change.

Key Findings 3 (published)
One key to coral survival in the world's warmest reefs are symbioses with a newly discovered alga, Symbiodinium thermophilum. Currently, it is unknown whether this symbiont originated elsewhere or emerged from unexpectedly fast evolution catalysed by the extreme environment. Through the analysis of genetic diversity of symbiotic algae across >5,000 km of the Persian Arabian Gulf (PAG), the Gulf of Oman and the Red Sea coastline, we show that S. thermophilum is a member of a highly diverse, ancient group of symbionts cryptically distributed outside the PAG. We argue that the adjustment to temperature extremes by PAG corals was facilitated by the positive selection of preadapted symbionts. Our findings suggest that maintaining the largest possible pool of potentially stress tolerant genotypes by protecting existing biodiversity is crucial to promote rapid adaptation to present-day climate change, not only for coral reefs but for ecosystems in general.

Key Findings 4 (published)
We have transferred our findings from experiments in laboratory conditions to the natural environment in the Persian/Arabian gulf, using a combination of remote sensing analyses and nutrient data from monitoring programs provided by the Environmental Ministries of Abu Dhabi and Kuwait and have demonstrated a link between algal blooms in the proximity of urban hot spots, subsequent depletion of nutrients in the water column and heat-stress induced coral bleaching. Moreover, we found that the combination of remote-sensing approaches using satellite imagery together with ground-based nutrient measurements is required to generate meaningful data sets with the spatial and temporal resolution required to identify coral bleaching-causing environmental conditions for coastal management and policy development.

Key Findings 5 (published)
We have found that a depletion of the water from nutrients, particularly from phosphate, renders corals more susceptible to bleaching. These conditions can be induced through nitrogen enrichment of coral reef waters or through a disturbance of the natural nutrient balance by phytoplankton blooms. In collaboration with the Environmental Agency Abu Dhabi, we used data from remote sensing and in-situ measurements to pinpoint the environmental conditions accompanying the 2012 coral bleaching event in the Southern Arabian Gulf, comparing them to the non-bleaching years 2013-2015. We have found that the coral bleaching event in 2012 was promoted by unfavourable nutrient levels in the water column in the region.

Key Finding 6 (Published)
As part of the research under this grant, we found that the exceptional heat tolerance is associated with the adaptions to live at unusually high salinity levels prevailing in the Southern Arabian Gulf. In collaboration with researchers from the King Abdullah University of Science and Technology (KAUST, Saudi Arabia), we could establish that the symbiotic algae from Gulf corals express high levels of the osmolyte Floridoside. This compound does not only protect cells from osmotic stress but it functions also as antioxidant and has therefore the potential to mitigate the impact of heat stress in high salinity environments.
Exploitation Route The key activity to increase the impact of the proposed study is the establishment of the Mideast Coral Reef Society with the aim to improve the knowledge exchange between representatives of academia, industry/private sector, governmental and non-governmental organisations. The webpage is live (http://mideastcrs.org) and the official launch has taken place during the Coral Reefs of Arabia conference in Abu Dhabi, February 2015. Newsletters, featuring a summary of the latest research news in the specific area are publish periodically.
The Mideast Coral Reef Society (MCRS) was founded as platform to communicate scientific findings to academics, governmental organisations, NGOs and private sector companies. Funding was provided through "Pathways to Impact" of a NERC Standard Grant. The society has currently 200 subscribing members. Six newsletters were produced since 2013 to communicate with the members.
A collaboration with the Environmental Agency Abu Dhabi established during the proposal has given us access to environmental monitoring data. We interpreted the data and communicated our findings as part of a senior management workshop funded by Policy/Southampton (Wiedenmann & D'Angelo 2017). Further data access was granted and new opportunities for change monitoring practise was proposed. Recently, we have been approached by the International Society for Reef Studies (ISRS), the principal learned society to which reef scientists and managers from across the world belong. The ISRS offered the MCRS the opportunity to become a regional chapter under the umbrella of the ISRS. This move could be completed relatively quickly and a testimonial from the ISRS president should be available.
We have educated the general public about the importance of protecting coral reefs through communicating the value of reefs as source of tools for biomedical research, using the aesthetically pleasing phenomenon of coral fluorescence as vector to for our message. This approach was applied at different levels:
Coral fluorescence themed exhibitions at the Southampton Boatshow 2015, the Southampton Science and Engineering Festival and the Royal Society Summer Science Exhibition 2017. This latter exhibit was seen by an estimated 20k visitors. A dedicated outreach brochure has been produced for this event which has be also distributed for teaching purposes, at the 2017 Royal Soc Summer Science Exhibition and at trade fairs through our industry collaborator., [D'Angelo, C., & Wiedenmann, J. (2015). See the Light - The science of fluorescence. Outreach brochure, University of Southampton].
We have collaborated with a leading UK Ornamental Trader Tropical Marine Centre (TMC) London on the function and regulation of fluorescent coral pigments. A novel type of LED Aquarium lighting was developed by the industry collaborators on the back of our research and the research of two GSNOCS CASE students that were funded the industry partner. This organisation has also sponsored the outreach aquarium at NOCS with its fluorescence function in the NOCS reception since its set-up.
A broad public audience has been reached through successful media work that resulted in prominent exposure including articles in the major print media (eg. The Economist, New York Times, National Geographic, Science, Nature), radio (e.g. BBC Radio 4, Inside Science, Naked Scientist) and TV (eg. ABC News Australia; BBC One Show, BBC World News etc.).
The research features in the "Creating a Sea Change" campaign of the University with the aim to inspire current and prospective students and is outlined on a webpage Webpage / "Our Impact" (http://www.southampton.ac.uk/news/2016/07/coral-bleaching.page) and as banner on the outside of Building 32 at the University of Southmpton.
The research is communicated Twitter account @theCoralReefLab in 2015 by regular high content tweets. Among the rapidly growing number of followers (>800) are influential coral researcher such as Terry Hughes, Ruth Gates, Mark Eakin and institutions (NOOA, AIMS, SeaSIMS).
A video on the research is available on Youtube #GlowingCorals https://www.youtube.com/watch?v=z0j4ehL0Meg which attracted >1400 views.
Sectors Agriculture, Food and Drink,Education,Environment,Leisure Activities, including Sports, Recreation and Tourism,Government, Democracy and Justice,Other

URL http://noc.ac.uk/corals
 
Description We have formed a collaboration with the Environmental Agency Abu Dhabi, UAE that has given us access to environmental monitoring data. We have interpreted the data and communicated our findings as part of a Senior Management Workshop (Abud-Dhabi 25. October 2017) funded by Policy/Southampton (Wiedenmann & D'Angelo 2017). The workshop concentrated on the proposal, based on our research, of new opportunities to change monitoring practises in the region.
First Year Of Impact 2017
Sector Environment,Other
Impact Types Policy & public services

 
Description Workshop for managers and policy makers
Geographic Reach Asia 
Policy Influence Type Influenced training of practitioners or researchers
Impact Discussed with governmental representatives the optimisation of environmental monitoring programs in the Persian/Arabian Gulf to render them more efficient to predict and pinpoint water conditions that endanger coral reefs in the region.
 
Description Collaborating with governmental organisations to improve environmental monitoring practice in the Middle East
Amount £5,000 (GBP)
Organisation University of Southampton 
Sector Academic/University
Country United Kingdom
Start 11/2016 
End 11/2017
 
Description Collaborating with governmental organisations to improve environmental monitoring practice in the Middle East 
Organisation Environmental Agency
PI Contribution We have had access and interpreted the confidential environmental data provided by the Environmentla Agency Abu-Dhabi. We have communicated our findings as part of a senior management workshop funded by Policy/Southampton.
Collaborator Contribution The Environmental Agency Abu Dhabi gives me and the team access to confidential environmental monitoring data in the region. This data is key to ground our remote sensing data analysis and has been fundamental in our impact activities (policy report). Further data access was granted and new opportunities for change monitoring practise was proposed.
Impact Wiedenmann, J. and D'Angelo C. (2017) "Water Quality and Resilience of Coral Reefs in the Arabian Gulf". Policy Report, presented to governmental representatives of the middle east within Workshop for Managers and Policy Makers, 25.10.2017, Abu-Dhabi, UAE.
Start Year 2015
 
Description Coral reefs: life in the balance 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Newspaper article in "The Guardian / The Observer" that details the devastating consequences of coral bleaching, explained in detail for a wider audience. (http://www.theguardian.com/environment/2014/mar/09/coral-reefs-bleaching-life-in-the-balance)

I was approached by BBC several times to give live interviews for BBC World News and BBC News.
Year(s) Of Engagement Activity 2014
URL http://www.theguardian.com/environment/2014/mar/09/coral-reefs-bleaching-life-in-the-balance
 
Description Dec. 2017 Organiser, Session "Nutrient Physiology and Ecology of Coral Reefs". European Coral Reef Symposium, Oxford, UK including Opening Presentation 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Dec. 2017 Organiser, Session "Nutrient Physiology and Ecology of Coral Reefs". European Coral Reef Symposium, Oxford, UK including Opening Presentation
Year(s) Of Engagement Activity 2017
 
Description Glowing Corals - YouTube Video 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Video that showcase the main research at the Coral Reef Laboratory in Southampton.
Year(s) Of Engagement Activity 2017,2018
URL https://www.youtube.com/watch?v=z0j4ehL0Meg
 
Description Mideast Coral Reef Society Initiative (MCRS) 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact The Mideast Coral Reef Society (MCRS) is an association of researchers and members of governmental, non-governmental, academic, industry and private sector organisations with an interest in a broad range of aspects of Middle Eastern reefs (ROPME Sea Area (RSA; Persian/Arabian Gulf), Sea of Oman, Gulf of Aden, and the Red Sea). The organisation promotes collaboration among researchers and knowledge exchange with stakeholders outside academia with the aim to generate a deep understanding of the functioning of these unique ecosystems and to promote their conservation and sustainable use. Read more about the mission of the MCRS Initiative.
Year(s) Of Engagement Activity 2014,2015,2016,2017
URL http://www.mideastcrs.org/
 
Description Mideast Coral Reef Society Newsletter 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Newsletter was distribute to the ~300 subscribers
Year(s) Of Engagement Activity 2018
 
Description Newsletters MidEast Coral Reef Society (MCRS) Initiative 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact The newsletters presents contributions [references of publications in the interest areas of the MCRS Initiative, descriptions of research projects, job advertisements, etc.] that are particularly focussed / of special interest to the coral reefs of the Persian/Arabian Gulf.
Year(s) Of Engagement Activity 2015,2016,2017
URL http://www.mideastcrs.org/newsletter
 
Description Press Release: Surviving harsh environments becomes a death-trap for specialists corals 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact The press article was prepared by the PI of the grant and released through the media hub of the University of Southampton, resulting in a high media interest on the published findings.
Year(s) Of Engagement Activity 2015
 
Description Press release: Coral reefs highlight the key role of existing biodiversity for climate change adaptation 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Press release associated with Hume et al. 2016. Received global news coverage
• Altmetric Score: 144
• Coverage in The Economist (~11 million readers) and Nature Middle East
• PNAS featured image (http://www.pnas.org/site/media/Featured_Image_red.xhtml)
Year(s) Of Engagement Activity 2016
URL https://www.eurekalert.org/pub_releases/2016-04/uos-crh040116.php
 
Description Royal Society Summer Science Exhibition 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact I presented together with my team the "Glowing Corals" exhibit over the week-long Royal Society Summer Science Exhibition in London, UK. The exhibition is made up of 22 exhibits, selected in a competitive process, featuring cutting-edge science and research being done right now across the UK. "Glowing Corals" was focussed on the application of fluorescence properties of corals and sea anemones, both in medicine and ecological research. The exhibition attracted 13,611 visitors and "Glowing Corals" was voted "Best exhibit on show 2017", news coverage reached in >24 countries: 279.8 million viewers.
Year(s) Of Engagement Activity 2017
URL https://royalsociety.org/science-events-and-lectures/2017/summer-science-exhibition/exhibits/glowing...
 
Description Southampton Science and Engineering Festival 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact I presented together with my team a "Glowing Sea Anemones" exhibit that examined the fluorescent properties of british sea anemones, and the use of fluorescence in biomedical research and monitoring practices.
Year(s) Of Engagement Activity 2017
URL https://www.southampton.ac.uk/per/university/festival/index.page
 
Description Workshop for Managers and Policy Makers 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Policymakers/politicians
Results and Impact One day workshop with representatives of key governmental and scientific organisations from Kuwait, UAE and Dubai, to discuss new opportunities to optimise environmental monitoring programs in the Persian/Arabian Gulf, and them more efficient to predict and pinpoint water conditions that endanger coral reefs in the region.
Year(s) Of Engagement Activity 2006,2012,2017