Article d’Albane Bauby (EnvIM 2019)
Over the past 25 million years, corals have evolved into one of the largest and most complex ecosystems on the planet.  Hosting more than a quarter of all marine fish species whilst covering less than 0.1% of the ocean floor, they are one of the most diverse ecosystems in the world, providing key ecosystem goods and services.  This high wealth in term of biodiversity makes them be called “the rainforest of the sea”.  It has been estimated that up to 2 million species including fish, coral, plant and other animal forms, inhabit coral. For example, the Northwest Hawaiian Island coral reef supports more than 7,000 species of fishes, invertebrates, plants, sea turtles, birds and marine mammals.  Coral reefs and its diverse inhabitants live in symbiosis, relying on each other to develop and thrive. For instance, herbivorous fishes shelter, find food, reproduce and raise their young members in the coral colony, while at the same time they play a critical role for the survival of coral reef by limiting the establishment and development of algae that hinder the prosperity of corals.  This fragile symbiosis makes corals unique and an important chain link in the biological balance of the oceans. Besides, coral reef are an incredible colourful and fascinating ecosystem and the high amount of fish varieties found within a small area make the reef a diver and snorkeler‘s paradise. As such, the largest coral reef, Australia’s Great Barrier Reef, is considered as the eighth natural wonder of the world. It began growing 20,000 years ago and today it attracts millions of tourists each year that are eager to explore and admire its colourful beauty. 
Corals reef are invertebrate animals that are part of the Cnidaria group, which also includes jelly fish and sea anemones. This type of animals are known to be particularly colourful with a large variety of shapes and sizes. They are made up by stony corals organism, named polyps, responsible for laying the foundations and building the reef structure by secreting calcium carbonate skeleton.  Each polyp corresponds to one individual coral animal. They mostly live in group of hundreds to thousands to make a colony. The anatomy of polyp is quite simple, a stomach with a single mouth opening surrounded by stinging tentacles (figure 1). 
Corals live in cooperation with microscopic algae in their tissue called zooxanthellae. These algae photosynthesize, providing 90% of the energy needed to enable corals to construct limestone skeletons. This skeleton builds the three-dimensional structure of reefs that provides habitat for million species. These algae also give their colour to coral who rely on them for their survival.
However, this valuable partnership becomes toxic for corals under certain stressful conditions such as changes in temperature, light levels, salinity and water quality.  Corals are mostly found in warm shallow-water, but can also be found in the cold, dark depths of the ocean. 
This biodiversity hotspot is particularly sensitive to changes and reflects quickly distress occurring in its environment. This is why climate change has become one of the main threats to their survival. Thus, coral reefs experience more and more bleaching events mainly due to continually increasing temperature. It corresponds to a loss of colour, turning from colourful aspect to white. This bleaching phenomenon indicates an unhealthy state of corals, that are about to die (figure 2). Therefore, this important ecosystem is one of the most endangered across the world. Its disappearance will have disastrous consequences for humans, as that rely on them for various ecosystem services. Besides, their destruction will also have devastating impacts on the marine life they host and on the whole food chain they sustain.
The Red List Index (RLI) was developed by the IUCN to show trends in overall extinction risk for species from 1980 to 2020. This provides an indicator that is used by governments to track their progress in achieving targets that reduce biodiversity loss, according to IUCN red list index website. An RLI value of 1.0 corresponds to not endangered species while a value of 0 corresponds to extinct species. The blue line shows the overall RLI with all species combined. 
As shown in the figure 3, corals species are experiencing a sharp increase in extinction risk since 1995. If this issue is not address properly, coral reefs in all 29 reef-containing World Heritage sites would cease to exist by the end of this century according to UNESCO. 
Why coral reefs are a special ecosystem?
From an economic and ecological point of view, coral reefs are one of the most important ecosystems in the world. Despite hosting more than 25% of all marine fish species, they provide numerous ecosystem services, benefits that humans receive from natural environments, corresponding to an estimated value reaching $1 Trillion globally. 
First, thanks to important biomass production in coral reef ecosystems, fishery and aquaculture can thrive and allow food security, particularly in some poor regions like Indonesia.  For instance, properly managed coral reefs can yield an average of 15 tonnes of fish and other seafood per square kilometre each year, according to the WWF website. 
Also, linked to the beauty of the scene and the presence of emblematic species, such as seahorses or sea turtles, coral reef allows an economic activity based on the recreational use of reefs in different forms such as excursions, scuba diving, boating, etc.  As such, reef tourism is estimated to be worth globally $35.8 billion per year, including direct and indirect reef tourism. 
Then, coral reefs, mangroves and seagrass absorb up to 90% of the energy in waves, leading to an effective protection of the coast. Thus, by reducing coast damages during floods and other extreme weather events, they are a source of significant savings.  Additionally, coastlines protected by them are less impacted by erosion.  For example, in French Polynesia, a good ecological state of the reefs is fundamental for 70% of the islands for coastal preservation since atolls and low islands are particularly exposed to hurricanes and tropical storms. 
Finally, coral reefs are important for medical resources since the numerous marine invertebrates (sponges, molluscs or soft corals) hosted by them represent a potential supply of new drugs for human health. Furthermore, they are used as a biological model to better understand immunity or ageing mechanisms. 
In sum, besides being a unique ecosystem that sustains diversity in marine life providing home and food for millions of species, coral reefs are also indispensable for humans in many different aspects. Around the world, over 500 million people rely on coral reef for food, income and coastal protection.  Therefore, it should be preserved and protected to make it thrives as long as possible.
Nevertheless, all these crucial services provided by coral reef for free may not last since they are particularly threatened by climate change, combined with overexploitation and pollution. According to the Global Coral Reef Monitoring Network (GCRMN), today 19% of reefs have been destroyed worldwide, 15% are seriously damaged and may disappear within the next 10 years, and 20% in the next 40 years.  A 2015 study by WWF projects that the climate-related loss of reef ecosystem services will cost $500 billion per year or more by 2100. 
Why coral reefs are particularly vulnerable to climate change?
Coral reefs are greatly influenced by the biological and physical factors of their environment. It has been demonstrated that they prosper in environments with a high degree of stability. As such, temperature, salinity and light have major impacts on where reef-building corals develop and thrive.  Climate change, with the warming of ocean, sea-level rise, change in storm patterns, change in precipitation, altered ocean current and water acidification, has a great destructive impact on them.
Coral bleaching phenomenon, which is occurring all around the globe, is a striking example of the impact of climate change on biodiversity. It is recognized to be directly due to global warming and the increasing temperature of surface water caused by the increasing concentrations of carbon dioxide in the atmosphere.  For instance, sea temperature in the tropics is estimated to increase at a rate of 1-2°C per century since 100 years. 
The first widespread mass coral bleaching documented event occurred in 1983 due to a strong El Niño, causing a temperature rise on the surface water. But it is through the second mass bleaching event in 1998-1999, during an extremely harsh El Niño followed by a strong La Niña, occurring in Indian, Pacific and Atlantic basins, that this phenomenon of bleaching corals was commonly recognized.  This bleaching event has been the worst year on record and led to a complete loss of corals in some parts of the world. 
Thus, coral bleaching appears when they are exposed with temperature exceeding the initial threshold by 0.5°C, as corals have adapted to local conditions over long periods.  At this point, there is a rupture of the symbiosis between corals and zooxanthella symbiont resulting in its expulsion from corals (figure 4). This state stays reversible during the first few days, during which they lose their ability to grow and reproduce, and it finally becomes lethal for the species a few weeks later.  The direct consequence is the loss of habitats of associated species of fish and invertebrates.
In addition to the increasing temperature of the water, carbon dioxide emissions are also causing the acidification of the ocean. Thus, oceans are well known to be carbon sinks. Since the industrial era, oceans absorb around 40% of CO2 produced by human activities, which dissolve in the water.  This dissolution of CO2 leads to an increase of hydrogen ions (H+) concentration in the water, according to the following equation. 
H2O + CO2 -> HCO3– + H+
This phenomenon is the main cause of the acidification of the ocean. Since the beginning of the last century, the pH of superficial water has decreased from 8.25 to 8.14 corresponding to an increase in the acidity of 25%. It is predicted that the pH should continue to decline by about 0.3 units until 2100. 
The issue with coral reefs is that a drop in pH leads to a loss of carbonates ions (COO2-) which is essential for their calcification to build their skeletons. The more acidic the water becomes, the more corrosive it becomes as well for calcifying organisms, changing coral reefs from growing to dissolving structures. For instance, in the Great Barrier Reef in Australia, calcification of corals has declined by 14% since 1990. 
Climate change will also lead to changes in storms patterns.  More frequent and stronger storms will exacerbate the impacts of acidification since more brittles corals will be more sensitive to extreme events damages. For example, it is estimated that tropical cyclones would increase by 10 to 20% in intensity. 
In addition, changes in precipitation with increased runoff of fresh water, sediments and land-based pollutant will lead to algal bloom and murky water. This will cause a reduction of light, directly affecting corals, already weakened by the pH and the temperature. 
Finally, altered currents will lead to changes in temperature regimes, which can affect corals as well.  For example, 16% of all tropical coral reefs were killed off by thermal stress during a single extreme El Niño–Southern Oscillation event in 1997–1998. 
In brief, corals are highly vulnerable to climate change, and particularly to thermal stress, and have a low adaptive capacity. Thus, the increase in sea surface temperature of about 1 to 3°C is projected to cause more frequent coral bleaching events with widespread mortality, according to the IPCC AR4 report. The only chance of survival for this unique ecosystem is an adaptation or acclimatization by corals. 
Is there any future for coral reefs?
With climate change and growth in human pressures, there are needs to better understand how the world is evolving and to develop new management tools to deal with changes and preserve natural processes.  Concerning coral reefs, their resilience remain in their capacity to resist or recover from degradation and maintain the provision of ecosystem goods and services. Corals have been thriving in different forms for hundreds of millions of years, and still today they have an important ability to resist and recover after destructive events like hurricanes or mass coral bleaching.
Maintaining resilience in coral reefs is a critical need for a majority of coral reefs managers worldwide to ensure their future. 
One of the main programs focusing on addressing the impact of climate change on coral reef ecosystems is the National Oceanic and Atmospheric Administration (NOAA) Coral Reef Conservation Program (CRP). This program supports resilience-based management to sustain coral reef’s resilience and human wellness.  For instance, this nationwide program funds and conducts coral reef conservation and restoration actions across the Atlantic and Pacific oceans. The CRPC activities are diverse and include monitoring and mapping, coral restoration interventions, watershed management, reduction of physical impacts to corals reef, and educational operations. 
As such, enhancing coral reefs resilience through conservation planning has become a main topic of research for managers. One example of resilience-based management is Herbivore Management Areas (HMAs) consisting of increasing herbivore biomass through the management of the spatial area. For instance, the number of herbivore fishes is increased by restricting fishing and creating protected areas. It prevents from algal overgrowth and has been demonstrated as a critical tool for maintaining ecosystem function and resilience. Thus, herbivory animals preserve space for corals settlement, which is a key process for their recovery after destructive events like bleaching. Since the HMAs is an interesting tool to increase the resilience of corals reefs, the Division of Aquatic Resources (DAR) in Hawaii decided to establish a HMAs network through the Hawaii Coral Bleaching Recovery Plan. It was identified as one of the best solutions to promote coral recovery and management effectiveness. 
Nevertheless, according to some other articles, local management such as addressing local pollution and over-exploitation is not enough to save coral reefs and ensure their future.  As stated by UNESCO, the coral reefs in all 29 reef-containing World Heritage sites would go to extinction by the end of this century if the emissions of greenhouse gases continue as a business-as-usual scenario. 
According to RCP (Representative Concentration Pathways) scenarios from the GIEC, moving from RCP8.5 to RCP4.5 scenario lead to an increase of 12 years for corals reefs lives on average. This increase of time could be enough for adaptive responses to occur. However, this is not sufficient as a long term solutions to save reefs but only an opportunity to “buy time” for adaptation and resilience. The more ambitious scenario has to be targeted. For instance, RCP2.6 and the Paris Agreement target of limiting the temperature increase to 1.5°C is the only way to durably preserve coral reef from a global decline.
This explains why there is an urgent need to stabilize greenhouse gas emissions and stop the warming of the oceans. National and international commitments have to be implemented to limit global warming to 1.5°C. Limiting greenhouse gas emissions could delay the date when a critical temperature threshold is crossed and eventually result in a stabilization of heat stress after 2100.  Besides, benefits and services that coral reefs provide for free should be included in business and finances flows. Thus, sustaining and restoring coral reefs should be seen as a long term investment.  However, there are doubts concerning the reach of the Paris Agreements target. In the case where the Paris Agreement is not reached, investments could be undertaken to support biology research such as genetic selection and heat-resistant to make corals able to bear a rising global temperature. 
In conclusion, the case of coral reefs is the perfect example of an important biodiversity hotspot highly threatened by human activities and climate change. It shows the importance of acting quickly to restrain climate change and particularly global warming. The disappearance of ecosystems like coral reefs will have disastrous consequences on human’s lives, marine biodiversity and also on the economy. More generally, this is all the endemic species that are identified as being particularly vulnerable, due to the fact that their survival relies on a very limited geographic and climatic range. Coral reefs but also wetland, freshwater habitats, alpine and artic ecosystems are at risk.  There is a possibility that some species will turn resilient to climate change, but most of them will go extinct in the next decades if nothing is done to stop efficiently greenhouse gas emissions. The importance of reaching the Paris Agreement targets is primordial but looks difficult and requires more ambitious actions with the involvement of all countries and citizens across the world.
1- Coral Guardian, what are coral reefs? Read on: https://www.coralguardian.org/en/what-are-coral-reefs/
2- Jean-Pierre Gattuso, Ove Hoegh-Guldberg, Hans-Otto Pörtner, Coral Reefs, 2014
3- UNESCO (United Nation Educational, Scientiﬁc and Cultural Organization), Impacts of Climate Change on World Heritage Coral Reefs, A First Global Scientific Assessment, 2017
4- NOAA (National Oceanic and Atmospheric Administration), Coral reef ecosystems, 2019 read on: https://www.noaa.gov/education/resource-collections/marine-life/coral-reef-ecosystems
5- IUCN (International Union for Conservation of Nature and Natural Resources), Alison L. Green and David R. Bellwood, Monitoring Functional Groups of Herbivorous Reef Fishes as Indicators of Coral Reef Resilience, 2009, read on https://www.iucn.org/sites/dev/files/import/downloads/resilience_herbivorous_monitoring.pdf
6- National Geographic, Coral Reefs 101, https://www.youtube.com/watch?v=ZiULxLLP32s
7- NOOA (National Oceanic and Atmospheric Administration), what is a coral reef made of? https://oceanservice.noaa.gov/facts/coralmadeof.html
8- ICRI (International Coral Reef Initiative), What are corals?, Coral Biology, 2020, read on: https://www.icriforum.org/about-coral-reefs/what-are-corals
9- All good: Reef-Safe Sunscreens, read on https://allgoodproducts.com/reef-friendly/
10- IUCN (International Union for Conservation of Nature and Natural Resources), Red List Index, 2020, read on https://www.iucnredlist.org/assessment/red-list-index
11- IUCN (International Union for Conservation of Nature and Natural Resources), Issues Brief, Coral reef and climate change, November 2017, read on https://www.iucn.org/sites/dev/files/coral_reefs_and_climate_change_issues_brief_final.pdf
12- IFRECO (Initiative Française pour les Récifs Coralliens), Valeur économique des services rendus par les récifs coralliens et écosystèmes associés des Outre-mer français, Rapport de synthèse, juin 2016
13- WWF (World Wildlife Fund) Fast Facts: why coral reefs are important? Financially and biologically, 2020, read on: https://wwf.panda.org/our_work/oceans/coasts/coral_reefs/coral_facts.cfm
14- Anna Woodhead, Gareth J.Williams, Christina Hicks, Coral reef ecosystem in the Anthropocene 2019
15- NOOA (National Oceanic and Atmospheric Administration), office for coastal management, fast facts coral reefs, 2020, read on: https://coast.noaa.gov/states/fast-facts/coral-reefs.html
16- Coral reef and climate change, Denis Allemand, Ocean & Climate, http://www.ocean-climate.org/wp-content/uploads/2017/03/coral-reefs-climate-change_ScientificNotes_Oct2016_BD_ppp-6.pdf
17- Ove Hoegh-Guldberg, Climate Change, coral bleaching and the future of the world’s coral reefs, School of Biological Sciences, the Coral Reef Research Institute, University of Sydney 14
18- NOOA (National Oceanic and Atmospheric Administration), what is coral bleaching? 2020, read on: https://oceanservice.noaa.gov/facts/coral_bleach.html
19- Le réveilleur, acidification des océans, 2016 https://www.youtube.com/watch?v=vtTlQ0HZZ2g&t=636s
20- NOOA (National Oceanic and Atmospheric Administration), Threats to coral reef: Climate Change, 2018, read on https://www.noaa.gov/multimedia/infographic/infographic-how-does-climate-change-affect-coral-reefs
21- WMO (World Meteorological Organization), Climate, Carbon, and Coral reefs, No. 1063, 2010
22- Intergovernmental Panel on Climate Change (WMO and UNEP), Climate Change 2007, Synthesis Report, (IPCC AR4 report), p.19
23- IUCN (International Union for Conservation of Nature and Natural Resources), Coral Reefs, Climate Change and Resilience, an Agenda for Action from the IUCN World Conservation Congress in Barcelona, 2009
24- UN environment, Jeffrey Maynard, Paul Marshall, Britt Parker, Elizabeth Mcleod, Gabby Ahmadia, Ruben van Hooidonk, Serge Planes, Gareth J Williams, Laurie Raymundo, Roger Beeden, Jerker Tamelander, A Guide to Assessing Coral Reef Resilience, 2017
25- NOOA (National Oceanic and Atmospheric Administration), The Coral Program’s Climate Change & Reef Resilience Activities, read on https://www.coris.noaa.gov/activities/projects/climate/welcome.html
26- NOAA (National Oceanic and Atmospheric Administration), Coral Reef Conservation Program, Draft Programmatic Environmental Impact Statement, 2019
27- Anne E.Chung, Lisa M.Wedding, Alison L.Green, Alan M.Friedlander, Grace Goldberg, Amber Meadows and Mark A.Hixon, Building coral reef resilience through spatial herbivore management, 2019
28- Bird Life International, Impacts of climate change on biodiversity and ecosystem services, 2020, read on https://www.birdlife.org/projects/7-impacts-climate-change-biodiversity-and-ecosystem-services