Symbiosis, the interdependence of different organisms for the benefit of one or both participants, is prevalent in the oceans as it is on land. Within the spectrum of marine symbioses, zooxanthellae clearly have a special, and exceptionally long-standing, relationship with numerous partners.
Scleractinian corals and zooxanthellae originated and diversified together, between 140–200 mya. Zooxanthellae are not just found in Scleractinia, however, and also occur in other cnidarians (soft corals, anemones and their allies) as well as in an assortment of other animals encompassing single-celled ciliated protists, sponges, flatworms and molluscs (including giant clams). Once thought to be a single dinoflagellate species, Symbiodinium microadriaticum, zooxanthellae have been found to be genetically diverse (consisting of many genetic types or 'clades'), and new Symbiodinium species are described regularly, although they all look similar.
Detailed morphological and genetic analyses have recently revealed a wealth of different zooxanthellae species, and the divergent Symbiodinium clades have recently been partitioned into multiple genera, including Breviolum, Cladocopium, Durusdinium and Gerakladium, better reflecting their long evolutionary history (LaJeunesse, Parkinson, Gabrielson et al., 2018).
They can all live independently, although not in such concentrated numbers nor with such long-term security as they can in the tissues of hosts. In corals (but not clams) they live inside the cells of the host organisms — in the innermost (gastrodermal) layer of the two cell layer body wall. All zooxanthellae are tiny, (approximately one hundredth of a millimetre in diameter), and only one to four occur within each coral cell.
Zooxanthellae photosynthesise as do other plants, with up to 95% of the nutrients they produce being leaked directly to the host organism. Nevertheless corals are voracious feeders, capturing zooplankton using the stinging batteries of nematocysts housed on their tentacles. Most species feed only at night, when the zooxanthellae are not photosynthesizing. Therefore corals have two very different food sources, termed autotrophy and heterotrophy respectively. The contributions to nutrition from each source vary in relation to ambient conditions. However, many if not most corals that are kept in darkness (so that their zooxanthellae cannot photosynthesise) will start to die after a few months irrespective of how much food they have from elsewhere.
The main points about coral - algal symbiosis are (and see, for example, the general reference van Oppen and Lough, 2018):
Coral tissue that has turned white or pale is described as 'bleached'. This phenomenon has a very broad spectrum of effects in its appearance and impact on corals. Minor bleaching can occur in small patches on a few individual colonies on otherwise unaffected reefs. Moderate bleaching can occur on some or all parts of some colonies of the more susceptible coral species while others remain unaffected. Major, or mass, bleaching can affect virtually all corals on whole tracts of reefs, particularly their shallower slopes. From the air, entire reef tracts can appear a ghostly white colour, as corals expel their zooxanthellae en masse. During this phase, corals can initially appear 'fluorescent', as they pale progressively to stark white. Within weeks, corals that have died are coated with algae, and the reef becomes a graveyard of dull brown coral skeletons trailing strands of algae waving in the current.
Bleaching is a symptom of stress in the coral and/or the coral's zooxanthellae. Much of the natural patchy bleaching occasionally seen in otherwise healthy corals is unimportant as it causes little or no long-term problems for a colony. Such patches may be due to a temporary loss of photosynthetic pigment from the zooxanthellae, predators of many sorts, or attacks from neighbouring colonies in the battle for growing space. Colony-wide bleaching is clearly of more concern as this can result in the death of the coral. Such bleaching has a number of causes including disease, lowered salinity, high temperature or increased light (usually as a result of very calm sea conditions and/or turbidity decrease). In each case, severe bleaching indicates that the coral's tissue integrity has been compromised. Although any of these causes can result in widespread mortality, by far the most common and most conspicuous cause is a combination of high light and elevated temperature. Where this occurs across whole reef tracts it is known as 'mass bleaching' which often leads to mass death of corals.
Such temperature/light-induced bleaching usually begins with excessively elevated levels of photosynthesis which leads zooxanthellae to produce toxic levels of oxygen. This occurs most commonly in shallow reef waters where corals are exposed to a combination of high sea-water temperatures and high levels of sunlight, for corals can regulate the quantity of zooxanthellae in their tissues, but not the rate at which these produce oxygen. Under conditions of high temperature and excess light, zooxanthellae become poisonous, actually deactivating the sunscreens corals produce to protect themselves. After studying this process in detail, coral physiologists have discovered it to be a general phenomenon also found in terrestrial plants as a mechanism for protecting leaf tissue from excess oxygen through over-exposure to sunlight.
In corals exposed to extreme levels of solar radiation in general and ultra-violet light in particular, together with high water temperatures (usually associated with shallow ponded water), zooxanthellae produce oxygen 4-8 times faster than the coral host can take it up. When this happens, some oxygen ceases to play a normal role in photosynthesis and becomes chemically active as oxygen radicals causing cellular distress. As oxygen radicals become toxic, the zooxanthellae that produce them are expelled by the corals even though this action too puts the corals at risk. Expulsion most commonly takes place by sloughing-off the gastrodermal cells in which the algae live, but there are also other mechanisms like resorption and tissue death. Such discoveries explain why bleaching is light - as well as temperature-dependent. They also explain a host of experimental variations correlated with environment, colony characteristics (shape and species) and the place and depth where experimental corals were originally collected. Additionally they help to explain why some corals die after they bleach: even when other nutrients are present and there is plenty of food in the form of zooplankton they may simply not have enough gastrodermal cells to function.
The temperature/light conditions which cause corals to expel their zooxanthellae are normally not localised and commonly affect a significant portion of the reef experiencing the temperature pulse. This can result in widespread mass bleaching of coral colonies, particularly at shallow depth.
Mass bleaching was first recorded in early 1980 in the Caribbean and surrounding seas (notably in Jamaica and the Bahamas), the far eastern Pacific (Panama and the Galápagos Islands) and in isolated instances in the Pacific (notably French Polynesia and Thailand), and on the Great Barrier Reef.
There have been seven major bleaching events on the Great Barrier Reef, the three spanning the summer seasons of 1981/82, 1997/98 and 2001/02 being the most widespread, at least prior to the recent 2016 and 2017 years. However, it was the 1981/82 mass bleaching event that really drew attention to the association between ocean temperature and bleaching.
The 1997/98 mass bleaching event was extraordinarily widespread. It affected reefs in over 50 countries throughout the Pacific and Indian Oceans, the Red Sea and the Caribbean, and even affected corals in high latitudes including those of the Red Sea and Arabian Gulf.
On the Great Barrier Reef, this mass bleaching coincided with the highest sea surface temperatures ever recorded. It was also at this time that 500-year-old Porites colonies died, strong evidence that mass bleaching had human causes.
The third major mass bleaching event took place in 2001/02, again affecting many countries. By this time it had become clear that there was a causal link between the periodicity of global bleaching and changes in ocean temperature associated with El Niño Southern Oscillation cycles. The gap between these events appears to be closing as the difference between El Niño years and non-El Niño years diminishes, a process that has started occurring and is destined to continue on into this century. Importantly, while 2006 was not an El Niño year, there was significant mass bleaching of corals on the Great Barrier Reef. Extensive mass bleaching occurred in several countries of the Caribbean in both 2005 and 2006. Present indications are that increases in global temperatures will lead to mass bleaching in all years by 2030. The latest global event which occurred from 2015-17 was the most severe on record, and does nothing to assuage these concerns.
Some of the important features of mass bleaching are as follows.
There is no clear link between enhanced greenhouse warming and the frequency or intensity of El Niño events. Analyses of historical records and projections from General Circulation Models are both ambivalent on the subject. The general climatic changes accompanying El Niño development are fairly well understood, although the factors controlling their initiation, intensity and periodicity remain obscure. The 1997-98 El Niño event was the most extreme in recorded history yet it is still possible that this and the two other major events in the past two decades (1981-82 and 2001-02) were exacerbated by other, slower, climatic cycles which are part of the natural variability of the Earth's climate and not a response to greenhouse warming. The recent global events of 2016 and 2017, however, have clear causal links to our warming planet, above and beyond that of the underlying El Niño cycles.
Although any direct causal link between enhanced greenhouse warming and El Niño intensity and frequency is uncertain, it is clear beyond doubt that El Niño cycles and mass bleaching are connected. Mass bleaching is not caused by a direct overall increase in ocean temperature but by short term concentrations of heat in the affected areas. On the Great Barrier Reef these temperature increases can be caused by El Niño events which pulse oceanic water from the Western Pacific Warm Pool, perhaps 1-2°C above what was once normal, into coastal regions. If this water is then trapped in the lagoon of the Great Barrier Reef it can warm still further, exacerbating the effects of the original pulse.
Essential points about El Niño, global ocean temperatures, and mass bleaching are:
Acclimatisation (where the individual's tolerance of environmental conditions increases during their lifetime) and adaptation (an evolutionary process involving natural selection through differential reproduction and survival) are seemingly the only escape routes corals have from the warm world of the future. As introduced above, the recent discoveries of multiple types of zooxanthellae, and corals' inherent capacities to shuffle and/or switch zooxanthellae, may provide additional avenues for both acclimation and adaptation to increasing climate disruption, ocean acidification and other impacts this century.
Acclimatisation There is evidence on both local and global scales that the same and/or closely related coral species show different tolerances to temperature in different locations. On local scales, good examples are corals that tolerate the very high temperatures found in intertidal pools, in water around natural thermal vents or close to thermal outlets of power stations. Normal maximum water temperatures found in particular geographic areas play a large role in determining tolerance to bleaching. Whole suites of corals can survive short-term peaks of 36°C in the Arabian Gulf, parts of the southern Red Sea and sporadically elsewhere. Like most animals, corals may acclimate to tolerate these temperatures by altering biochemical pathways. On local scales this process is likely to be due to acclimatisation whereas across widely separated geographic areas there may be a larger component of genetic selection, especially where local tolerance to extreme conditions is involved.
Adaptation Corals were probably once adapted to higher temperatures in the geological past. However the template of todays' oceans is so different from those of the remote past that most meaningful comparisons are questionable. It is nevertheless worth revisiting the fossil record at this point, and particularly the major 'reef gaps' that extended for millions of years following the mass extinctions. The Scleractinia first rose to prominence after one such extinction, the end-Permian, and have survived those of the Mesozoic, albeit with significant changes in lineages via reticulate evolution and natural selection, and major reductions in reef-building during periods of major climatic instability. Today, the largest uncertainties relate to future rates of global warming and ocean acidification. If our collective global emissions of fossil fuels and other sources of greenhouse gases continue, along with positive climate feedbacks including loss of polar albedo, melting of permafrost and release of 'ice gas' methane clathrates off continental shelves, the climate system will likely be driven ever more rapidly beyond a tipping point. Under this scenario, it is unlikely that corals will have time to adapt. Levels of future extinctions may be significant, and reefs will cease to grow - effectively forming another 'reef gap' in the fossil record of the distant future.