Rowan et al. (1997) have suggested that this phenomenon occurs in many of the most successful Caribbean corals that act as hosts to dynamic multi-species communities of symbionts, and that "coral communities may adjust to climate change by recombining their existing host and symbiont genetic diversities," thereby reducing the amount of damage that might subsequently be expected from another occurrence of anomalously high temperatures.  In fact, Buddemeier and Fautin (1993) have suggested that coral bleaching is actually an adaptive strategy for "shuffling" symbiont genotypes to create associations better adapted to new environmental conditions that challenge the status quo of reef communities.  Saying essentially the same thing in yet another way, Kinzie (1999) has suggested that coral bleaching "might not be simply a breakdown of a stable relationship that serves as a symptom of degenerating environmental conditions," but that it "may be part of a mutualistic relationship on a larger temporal scale, wherein the identity of algal symbionts changes in response to a changing environment."

This process of replacing less stress-tolerant symbionts by more stress-tolerant symbionts is also supported by the investigations of Rowan and Knowlton (1995) and Gates and Edmunds (1999); and the strategy seems to be working, for as Glynn (1996) has observed, "despite recent incidences of severe coral reef bleaching and mortality, no species extinctions have yet been documented."

These observations accord well with the experimental findings of Fagoonee et al. (1999), who suggest that coral bleaching events "may be frequent and part of the expected cycle."  Gates and Edmunds (1999) additionally report that "several of the prerequisites required to support this hypothesis have now been met," and after describing them in some detail, they conclude "there is no doubt that the existence of multiple Symbiodinium clades, each potentially exhibiting a different physiological optima, provide corals with the opportunity to attain an expanded range of physiological flexibility which will ultimately be reflected in their response to environmental challenge."  In fact, this phenomenon may provide the explanation for the paradox posed by Pandolfi (1999), i.e., that "a large percentage of living coral reefs have been degraded, yet there are no known extinctions of any modern coral reef species."  Surely, this result is exactly what would be expected if periods of stress lead to the acquisition of more-stress-resistant zooxanthellae by coral hosts.

In spite of this early raft of compelling evidence for the phenomenon, Hoegh-Guldberg (1999) challenged the symbiont shuffling hypothesis on the basis that the stress-induced replacement of less-stress-tolerant varieties of zooxanthellae by more-stress-tolerant varieties "has never been observed."  Although true at the time it was written, a subsequent series of studies has produced the long-sought proof that transforms the hypothesis into fact.

Baker (2001) conducted an experiment in which he transplanted corals of different combinations of host and algal symbiont from shallow (2-4 m) to deep (20-23 m) depths and vice versa.  After 8 weeks nearly half of the corals transplanted from deep to shallow depths had experienced partial or severe bleaching, whereas none of the corals transplanted from shallow to deep depths bleached.  After one year, however, and despite even more bleaching at shallow depths, upward transplants showed no mortality, but nearly 20 percent of downward transplants had died.  Why?

The symbiont shuffling hypothesis explains it this way.  The corals that were transplanted upwards were presumed to have adjusted their algal symbiont distributions, via bleaching, to favor more tolerant species, whereas the corals transplanted downward were assumed to not have done so, since they did not bleach.  Baker suggested that these findings "support the view that coral bleaching can promote rapid response to environmental change by facilitating compensatory change in algal symbiont communities."  Without bleaching, as he continued, "suboptimal host-symbiont combinations persist, leading eventually to significant host mortality."  Consequently, Baker proposed that coral bleaching may "ultimately help reef corals to survive."  And it may also explain why reefs, though depicted by climate alarmists as environmentally fragile, have survived the large environmental changes experienced throughout geologic time.

One year later Adjeroud et al. (2002) provided additional evidence for the veracity of the symbiont shuffling hypothesis as a result of their assessment of the interannual variability of coral cover on the outer slope of the Tiahura sector of Moorea Island, French Polynesia, between 1991 and 1997, which focused on the impacts of bleaching events caused by thermal stress when sea surface temperatures rose above 29.2°C.  Soon after the start of their study, they observed a severe decline in coral cover following a bleaching event that began in March 1991, which was followed by another bleaching event in March 1994.  However, they report that the latter bleaching event "did not have an important impact on coral cover," even though "the proportion of bleached colonies ... and the order of susceptibility of coral genera were similar in 1991 and 1994 (Gleason, 1993; Hoegh-Guldberg and Salvat, 1995)."  In fact, they report that between 1991 and 1992 total coral cover dropped from 51.0% to 24.2%, but that "coral cover did not decrease between 1994 and 1995."

In discussing these observations, Adjeroud et al. write that a "possible explanation of the low mortality following the bleaching event in 1994 is that most of the colonies in place in 1994 were those that survived the 1991 event or were young recruits derived from those colonies," noting that "one may assume that these coral colonies and/or their endosymbiotic zooxanthellae were phenotypically and possibly genotypically resistant to bleaching events," which is exactly what the symbiont shuffling hypothesis would predict.  Hence, they further state that "this result demonstrates the importance of understanding the ecological history of reefs (i.e., the chronology of disturbances) in interpreting the specific impacts of a particular disturbance."

In the same year, Brown et al. (2002) published the results of an even longer 17-year study of coral reef flats at Ko Phuket, Thailand, in which they assessed coral reef changes in response to elevated water temperatures in 1991, 1995, 1997 and 1998.  As they describe it, "many corals bleached during elevated sea temperatures in May 1991 and 1995, but no bleaching was recorded in 1997."  In addition, they report that "in May 1998 very limited bleaching occurred although sea temperatures were higher than previous events in 1991 and 1995 (Dunne and Brown, 2001)."  What is more, when bleaching did take place, they say "it led only to partial mortality in coral colonies, with most corals recovering their color within 3-5 months of initial paling," once again providing real-world evidence for what is predicted by the symbiont shuffling hypothesis.

The following year, Kumaraguru et al. (2003) reported the results of a study wherein they assessed the degree of damage inflicted upon a number of coral reefs within Palk Bay (located on southeast coast of India just north of the Gulf of Mannar) by a major warming event that produced monthly mean sea surface temperatures of 29.8 to 32.1°C from April through June of 2002, after which they assessed the degree of recovery of the reefs.  They determined that "a minimum of at least 50% and a maximum of 60% bleaching were noticed among the six different sites monitored."  However, as they continue, "the corals started to recover quickly in August 2002 and as much as 52% recovery could be noticed."  By comparison, they note that "recovery of corals after the 1998 bleaching phenomenon in the Gulf of Mannar was very slow, taking as much as one year to achieve similar recovery," i.e., to achieve what was experienced in one month in 2002.  Consequently, in words descriptive of the concept of symbiont shuffling, the Indian scientists say "the process of natural selection is in operation, with the growth of new coral colonies, and any disturbance in the system is only temporary."  Consequently, as they conclude in the final sentence of their paper, "the corals will resurge under the sea."

Although these several 2001-2003 findings were very significant, a quartet of papers published in 2004 - two in Nature and two in Science - finally "sealed the deal" with respect to establishing the symbiont shuffling hypothesis as a fact of life, and an ubiquitous one at that.

Writing in Nature, Rowan (2004) describes how he measured the photosynthetic responses of two zooxanthellae genotypes or clades -- Symbiodinium C and Symbiodinium D -- to increasing water temperature, finding that the photosynthetic prowess of the former decreased at higher temperatures while that of the latter increased.  He then notes that "adaptation to higher temperature in Symbiodinium D can explain why Pocillopora spp. hosting them resist warm-water bleaching whereas corals hosting Symbiodinium C do not," and that "it can also explain why Pocillopora spp. living in frequently warm habitats host only Symbiodinium D, and, perhaps, why those living in cooler habitats predominantly host Symbiodinium C," concluding that these observations "indicate that symbiosis recombination may be one mechanism by which corals adapt, in part, to global warming."

Clinching the concept, is the study of Baker et al. (2004), who "undertook molecular surveys of Symbiodinium in shallow scleractinian corals from five locations in the Indo-Pacific that had been differently affected by the 1997-98 El Niño-Southern Oscillation (ENSO) bleaching event."  Along the coasts of Panama, they surveyed ecologically dominant corals in the genus Pocillopora before, during and after ENSO bleaching, finding that "colonies containing Symbiodinium in clade D were already common (43%) in 1995 and were unaffected by bleaching in 1997, while colonies containing clade C bleached severely."  Even more importantly, they found that "by 2001, colonies containing clade D had become dominant (63%) on these reefs."

After describing similar observations in the Persian (Arabian) Gulf and the western Indian Ocean along the coast of Kenya, Baker et al. summarized their results by stating they indicate that "corals containing thermally tolerant Symbiodinium in clade D are more abundant on reefs after episodes of severe bleaching and mortality, and that surviving coral symbioses on these reefs more closely resemble those found in high-temperature environments," where clade D predominates.  Hence, they concluded their landmark paper by noting that the symbiont changes they observed "are a common feature of severe bleaching and mortality events," and by predicting that "these adaptive shifts will increase the resistance of these recovering reefs to future bleaching."

Meanwhile, over at Science, Lewis and Coffroth (2004) described a controlled experiment in which they induced bleaching in a Caribbean octocoral (Briareum sp.) and then exposed it to exogenous Symbiodinium sp. containing rare variants of the chloroplast 23S ribosomal DNA (rDNA) domain V region (cp23S-genotype), after which they documented the symbionts' repopulation of the coral, whose symbiont density had been reduced to less than 1% of its original level by the bleaching.  Also, in a somewhat analogous study, Little et al. (2004) described how they investigated the acquisition of symbionts by juvenile Acropora tenuis corals growing on tiles they attached to different portions of reef at Nelly Bay, Magnetic Island (an inshore reef in the central section of Australia's Great Barrier Reef).

Lewis and Coffroth wrote that the results of their study show that "the repopulation of the symbiont community involved residual populations within Briareum sp., as well as symbionts from the surrounding water," noting that "recovery of coral-algal symbioses after a bleaching event is not solely dependent on the Symbiodinium complement initially acquired early in the host's ontogeny," and that "these symbioses also have the flexibility to establish new associations with symbionts from an environmental pool."  Similarly, Little et al. reported that "initial uptake of zooxanthellae by juvenile corals during natural infection is nonspecific (a potentially adaptive trait)," and that "the association is flexible and characterized by a change in (dominant) zooxanthella strains over time."

Lewis and Coffroth thus concluded that "the ability of octocorals to reestablish symbiont populations from multiple sources provides a mechanism for resilience in the face of environmental change," while Little et al. concluded that the "symbiont shuffling" observed by both groups "represents a mechanism for rapid acclimatization of the holobiont to environmental change."  Hence, the results of both studies demonstrate the reality of a phenomenon whereby corals may indeed "grasp victory from the jaws of death" in the aftermath of a severe bleaching episode, which is also implied by the fact - cited by Lewis and Coffroth - that "corals have survived global changes since the first scleractinian coral-algal symbioses appeared during the Triassic, 225 million years ago."

Wonderfully, these four papers (two each from Nature and Science), as well as the important studies that preceded them, not only successfully explain the past, they similarly foretell the future; and that future bears absolutely no resemblance to what the world's climate alarmists claim it will be (largely devoid of corals due to global warming), which, of course, should come as no surprise to anyone who has thoughtfully followed the scientific unfolding of the emotion-laden issue.

References
Adjeroud, M., Augustin, D., Galzin, R. and Salvat, B.  2002.  Natural disturbances and interannual variability of coral reef communities on the outer slope of Tiahura (Moorea, French Polynesia): 1991 to 1997.  Marine Ecology Progress Series 237: 121-131.

Baker, A.C.  2001.  Reef corals bleach to survive change.  Nature 411: 765-766.

Baker, A.C., Starger, C.J., McClanahan, T.R. and Glynn, P.W.  2004.  Corals' adaptive response to climate change.  Nature 430: 741.

Brown, B.E., Clarke, K.R. and Warwick, R.M.  2002.  Serial patterns of biodiversity change in corals across shallow reef flats in Ko Phuket, Thailand, due to the effects of local (sedimentation) and regional (climatic) perturbations.  Marine Biology 141: 24-29.

Buddemeier, R.W. and Fautin, D.G.  1993.  Coral bleaching as an adaptive mechanism.  BioScience 43: 320-326.

Duane, R.P. and Brown, B.E.  2001.  The influence of solar radiation on bleaching of shallow water reef corals in the Andaman Sea, 1993-98.  Coral Reefs 20: 201-210.

Fagoonee, I., Wilson, H.B., Hassell, M.P. and Turner, J.R.  1999.  The dynamics of zooxanthellae populations: A long-term study in the field.  Science 283: 843-845.

Gates, R.D. and Edmunds, P.J.  1999.  The physiological mechanisms of acclimatization in tropical reef corals.  American Zoologist 39: 30-43.

Gleason, M.G.  1993.  Effects of disturbance on coral communities: bleaching in Moorea, French Polynesia.  Coral Reefs 12: 193-201.

Glynn, P.W.  1996.  Coral reef bleaching: facts, hypotheses and implications.  Global Change Biology 2: 495-509.

Hoegh-Guldberg, O.  1999.  Climate change, coral bleaching and the future of the world's coral reefs.  Marine and Freshwater Research 50: 839-866.

Hoegh-Guldberg, O. and Salvat, B.  1995.  Periodic mass-bleaching and elevated sea temperatures: bleaching of outer reef slope communities in Moorea, French Polynesia.  Marine Ecology Progress Series 121: 181-190.

Kinzie, R.A., III.  1999.  Sex, symbiosis and coral reef communities.  American Zoologist 39: 80-91.

Kumaraguru, A.K., Jayakumar, K. and Ramakritinan, C.M.  2003.  Coral bleaching 2002 in the Palk Bay, southeast coast of India.  Current Science 85: 1787-1793.

Lewis, C.L. and Coffroth, M.A.  2004.  The acquisition of exogenous algal symbionts by an octocoral after bleaching.  Science 304: 1490-1492.

Little, A.F., van Oppen, M.J.H. and Willis, B.L.  2004.  Flexibility in algal endosymbioses shapes growth in reef corals.  Science 304: 1492-1494.

Pandolfi, J.M.  1999.  Response of Pleistocene coral reefs to environmental change over long temporal scales.  American Zoologist 39: 113-130.

Rowan, R.  2004.  Thermal adaptation in reef coral symbionts.  Nature 430: 742.

Rowan, R. and Knowlton, N.  1995.  Intraspecific diversity and ecological zonation in coral-algal symbiosis.  Proceeding of the National Academy of Sciences, U.S.A. 92: 2850-2853.

Rowan, R. and Powers, D.  1991.  Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae).  Marine Ecology Progress Series 71: 65-73; 1991.

Rowan, R., Knowlton, N., Baker, A. and Jara, J.  1997.  Landscape ecology of algal symbionts creates variation in episodes of coral bleaching.  Nature 388: 265-269.

Trench, R.K.  1979.  The cell biology of plant-animal symbiosis.  Annual Review of Plant Physiology 30: 485-531.