From Climate Change Reconsidered, a work of the Nongovernmental International Panel on Climate Change
Although once considered to be members of the single species Symbiodinium microadriacticum, the zooxanthellae that reside within membrane-bound vacuoles in the cells of host corals are highly diverse, comprising perhaps hundreds of species, of which several are typically found in each species of coral (Trench, 1979; Rowan and Powers, 1991; Rowan et al., 1997). One way coral respond to stress is to replace the zooxanthellae expelled by the coral host during a stress-induced bleaching episode with one or more varieties of zooxanthellae that are more tolerant of that particular stress.
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. Buddemeier and Fautin (1993) suggested coral bleaching is an adaptive strategy for “shuffling” symbiont genotypes to create associations better adapted to new environmental conditions. Kinzie (1999) suggested coral bleaching “might not be simply a breakdown of a stable relationship that serves as a symptom of degenerating environmental conditions,” but 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). 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 eight 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, 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 the IPCC 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).” They report that between 1991 and 1992 total coral cover dropped from 51.0 percent to 24.2 percent, 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. 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, Riegl (2003) reviewed what is known about the responses of real-world coral reefs to high-temperature-induced bleaching, focusing primarily on the Arabian Gulf, which experienced high-frequency recurrences of temperature-related bleaching in 1996, 1998, and 2002. In response to these high-temperature events, Riegl notes that Acropora, which during the 1996 and 1998 events always bleached first and suffered heaviest mortality, bleached less than all other corals in 2002 at Sir Abu Nuair (an offshore island of the United Arab Emirates) and actually recovered along the coast of Dubai between Jebel Ali and Ras Hasyan. As a result, Riegl states that “the unexpected resistance of Sir Abu Nuair Acropora to bleaching in 2002 might indicate support for the hypothesis of Baker (2001) and Baker et al. (2002) that the symbiont communities on recovering reefs of the future might indeed be more resistant to subsequent bleaching,” and that “the Arabian Gulf perhaps provides us with some aspects which might be described as a ‘glimpse into the future,’ with … hopes for at least some level of coral/zooxanthellae adaptation.”
In a contemporaneous paper, 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 the 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 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.”
Writing in Nature, Rowan (2004) described 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 noted 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.”
Baker et al. (2004) “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. They concluded their 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.”
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 percent 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 “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,” but 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 “the association is flexible and characterized by a change in (dominant) zooxanthella strains over time.” Lewis and Coffroth concluded that “the ability of octocorals to reestablish symbiont populations from multiple sources provides a mechanism for resilience in the face of environmental change.” Little et al. concluded that the “symbiont shuffling” observed by both groups “represents a mechanism for rapid acclimatization of the holobiont to environmental change.”
Writing in the journal Marine Ecology Progress Series, Chen et al. (2005) reported their study of the seasonal dynamics of Symbiodinium algal phylotypes via bimonthly sampling over an 18-month period of Acropora palifera coral on a reef flat at Tantzel Bay, Kenting National Park, southern Taiwan, in an attempt to detect real-world symbiont shuffling. Results of the analysis revealed two levels of symbiont shuffling in host corals: (1) between Symbiodinium phylotypes C and D, and (2) among different variants within each phylotype. The most significant changes in symbiont composition occurred at times of significant increases in seawater temperature during late spring/early summer, perhaps as a consequence of enhanced stress experienced at that time, leading Chen et al. to state their work revealed “the first evidence that the symbiont community within coral colonies is dynamic … involving changes in Symbiodinium phylotypes.”
Also in 2005, Van Oppen et al. (2005) sampled zooxanthellae from three common species of scleractinian corals at 17 sites along a latitudinal and cross-shelf gradient in the central and southern sections of the Great Barrier Reef some four to five months after the major bleaching event of 2002, recording the health status of each colony at the time of its collection and identifying its zooxanthella genotypes, of which there are eight distinct clades (A-H) with clade D being the most heat-tolerant. Results of the analysis revealed that “there were no simple correlations between symbiont types and either the level of bleaching of individual colonies or indicators of heat stress at individual sites.” However, they say “there was a very high post-bleaching abundance of the heat tolerant symbiont type D in one coral population at the most heat-stressed site.”
With respect to the post-bleaching abundance of clade D zooxanthellae at the high heat-stress site, the Australian researchers say they suspect it was due to “a proliferation in the absolute abundance of clade D within existing colonies that were previously dominated by clade C zooxanthellae,” and that in the four to five months before sampling them, “mixed C-D colonies that had bleached but survived may have shifted (shuffling) from C-dominance to D-dominance, and/or C-dominated colonies may have suffered higher mortality during the 2002 bleaching event” and subsequently been repopulated by a predominance of clade D genotypes.
Working within Australia’s Great Barrier Reef system, Berkelmans and van Oppen (2006) investigated the thermal acclimatization potential of Acropora millepora corals to rising temperatures through transplantation and experimental manipulation, finding that the adult corals “are capable of acquiring increased thermal tolerance and that the increased tolerance is a direct result of a change in the symbiont type dominating their tissues from Symbiodinium type C to D.” Two years later, working with an expanded group of authors (Jones et al., 2008), the same two researchers reported similar findings following the occurrence of a natural bleaching event.
Prior to the bleaching event, Jones et al. report that “A. millepora at Miall reef associated predominantly with Symbiodinium type C2 (93.5%) and to a much lesser extent with Symbiodinium clade D (3.5%) or mixtures of C2 and D (3.0%).” During the bleaching event, they report “the relative difference in bleaching susceptibility between corals predominated by C2 and D was clearly evident, with the former bleaching white and the latter normally pigmented,” while corals harboring a mix of Symbiodinium C2 and D were “mostly pale in appearance.” Then, three months after the bleaching event, they observed “a major shift to thermally tolerant type D and C1 symbiont communities … in the surviving colonies,” the latter of which types had not been detected in any of the corals prior to bleaching. They report “this shift resulted partly from a change of symbionts within coral colonies that survived the bleaching event (42%) and partly from selective mortality of the more bleaching-sensitive C2-predominant colonies (37%).” In addition, they report that all of the colonies that harbored low levels of D-type symbionts prior to the bleaching event survived and changed from clade C2 to D predominance.
In conclusion, Jones et al. say that “as a direct result of the shift in symbiont community, the Miall Island A. millepora population is likely to have become more thermo-tolerant,” as they note that “a shift from bleaching-sensitive type C2 to clade D increased the thermal tolerance of this species by 1-1.5°C.” They say their results “strongly support the reinterpreted adaptive bleaching hypothesis of Buddemeier et al. (2004), which postulates that a continuum of changing environmental states stimulates the loss of bleaching-sensitive symbionts in favor of symbionts that make the new holobiont more thermally tolerant.” They state that their observations “provide the first extensive colony-specific documentation and quantification of temporal symbiont community change in the field in response to temperature stress, suggesting a population-wide acclimatization to increased water temperature.”
In a much larger geographical study, Lien et al. (2007) examined the symbiont diversity in a scleractinian coral, Oulastrea crispata, throughout its entire latitudinal distribution range in the West Pacific, i.e., from tropical peninsular Thailand (<10°N) to high-latitudinal outlying coral communities in Japan (>35°N), convincingly demonstrating in the words of the six scientists who conducted the study, “that phylotype D is the dominant Symbiodinium in scleractinian corals throughout tropical reefs and marginal outlying non-reefal coral communities.” In addition, they learned that this particular symbiont clade “favors ‘marginal habitats’ where other symbionts are poorly suited to the stresses, such as irradiance, temperature fluctuations, sedimentation, etc.” Being a major component of the symbiont repertoire of most scleractinian corals in most places, the apparent near-universal presence of Symbiodinium phylotype D thus provides, according to Lien et al., “a flexible means for corals to routinely cope [our italics] with environmental heterogeneities and survive the consequences (e.g., recover from coral bleaching).”
Also in 2007, Mieog et al. (2007) utilized a newly developed real-time polymerase chain reaction assay, which they say “is able to detect Symbiodinium clades C and D with >100-fold higher sensitivity compared to conventional techniques,” to test 82 colonies of four common scleractinian corals (Acropora millepora, Acropora tenuis, Stylophora pistillata and Turbinaria reniformis) from eleven different locations on Australia’s Great Barrier Reef for evidence of the presence of background Symbiodinium clades. Results of the analysis showed that “ninety-three percent of the colonies tested were dominated by clade C and 76% of these had a D background,” the latter of which symbionts, in their words, “are amongst the most thermo-tolerant types known to date,” being found “on reefs that chronically experience unusually high temperatures or that have recently been impacted by bleaching events, suggesting that temperature stress can favor clade D.” Consequently, Mieog et al. concluded that the clade D symbiont backgrounds detected in their study can potentially act as safety-parachutes, “allowing corals to become more thermo-tolerant through symbiont shuffling as seawater temperatures rise due to global warming.” As a result, they suggest that symbiont shuffling is likely to play a role in the way “corals cope with global warming conditions,” leading to new competitive hierarchies and, ultimately, “the coral community assemblages of the future.”
In spite of the hope symbiont shuffling provides—that the world’s corals will indeed be able to successfully cope with the possibility of future global warming, be it anthropogenic-induced or natural—some researchers have claimed that few coral symbioses host more than one type of symbiont, which has led some commentators to argue that symbiont shuffling is not an option for most coral species to survive the coming thermal onslaught of global warming. But is this claim correct? Not according to the results of Apprill and Gates (2007).
Working with samples of the widely distributed massive corals Porites lobata and Porites lutea—which they collected from Kaneohe Bay, Hawaii—Apprill and Gates compared the identity and diversity of Symbiodinium symbiont types obtained using cloning and sequencing of internal transcribed spacer region 2 (ITS2) with that obtained using the more commonly applied downstream analytical techniques of denaturing gradient gel electrophoresis (DGGE).
Results of the analysis revealed “a total of 11 ITS2 types in Porites lobata and 17 in Porites lutea with individual colonies hosting from one to six and three to eight ITS2 types for P. lobata and P. lutea, respectively.” In addition, the two authors report that “of the clones examined, 93% of the P. lobata and 83% of the P. lutea sequences are not listed in GenBank,” noting that they resolved “sixfold to eightfold greater diversity per coral species than previously reported.”
In a “perspective” that accompanied Apprill and Gates’ important paper, van Oppen (2007) wrote that “the current perception of coral-inhabiting symbiont diversity at nuclear ribosomal DNA is shown [by Apprill and Gates] to be a significant underestimate of the wide diversity that in fact exists.” These findings, in her words, “have potentially far-reaching consequences in terms of our understanding of Symbiodinium diversity, host-symbiont specificity and the potential of corals to acclimatize to environmental perturbations through changes in the composition of their algal endosymbiont community,” which assessment, it is almost unnecessary to say, suggests a greater than previously believed ability to do just that in response to any further global warming that might occur.
In a contemporaneous study, Baird et al. (2007) also discount the argument that symbiont shuffling is not an option for most coral species, because, “as they see it,” it is the sub-clade that must be considered within this context, citing studies that indicate “there are both heat tolerant and heat susceptible sub-clades within both clades C and D Symbiodinium.” Hence, the more relevant question becomes: How many coral species can host more than one sub-clade? The answer, of course, is that most if not all of them likely do; Baird et al. note that “biogeographical data suggest that when species need to respond to novel environments, they have the flexibility to do so.”
So how and when might such sub-clade changes occur? Although most prior research in this area has been on adult colonies switching symbionts in response to warming-induced bleaching episodes, Baird et al. suggest that “change is more likely to occur between generations,” for initial coral infection typically occurs in larvae or early juveniles, which are much more flexible than adults. In this regard, for example, they note that “juveniles of Acropora tenuis regularly harbor mixed assemblages of symbionts, whereas adults of the species almost invariably host a single clade,” and they indicate that larvae of Fungia scutaria ingest symbionts from multiple hosts, although they generally harbor but one symbiont as adults.
Because of these facts, the Australian researchers say there is no need for an acute disturbance, such as bleaching, to induce clade or sub-clade change. Instead, if ocean temperatures rise to new heights in the future, they foresee juveniles naturally hosting more heat-tolerant sub-clades and maintaining them into adulthood.
In a further assessment of the size of the symbiont diversity reservoir, especially among juvenile coral species, Pochon et al. (2007) collected more than 1,000 soritid specimens over a depth of 40 meters on a single reef at Gun Beach on the island of Guam, Micronesia, throughout the course of an entire year, which they then studied by means of molecular techniques to identify unique internal transcribed spacer-2 (ITS-2) types of ribosomal DNA (rDNA), in a project self-described as “the most targeted and exhaustive sampling effort ever undertaken for any group of Symbiodinium-bearing hosts.”
Throughout the course of their analysis, Pochon et al. identified 61 unique symbiont types in only three soritid host genera, making the Guam Symbiodinium assemblage the most diverse derived to date from a single reef. In addition, they report that “the majority of mixed genotypes observed during this survey were usually harbored by the smallest hosts.” As a result, the authors speculate that “juvenile foraminifera may be better able to switch or shuffle heterogeneous symbiont communities than adults,” so that as juveniles grow, “their symbiont communities become ‘optimized’ for the prevailing environmental conditions,” suggesting that this phenomenon “may be a key element in the continued evolutionary success of these protests in coral reef ecosystems worldwide.”
In support of the above statement, we additionally cite the work of Mumby (1999), who analyzed the population dynamics of juvenile corals in Belize, both prior to, and after, a massive coral bleaching event in 1998. Although 70 percent to 90 percent of adult coral colonies were severely bleached during the event, only 25 percent of coral recruits exhibited signs of bleaching. What is more, one month after the event, it was concluded that “net bleaching-induced mortality of coral recruits … was insignificant,” demonstrating the ability of juvenile corals to successfully weather such bleaching events.
Zooxanthellae (symbiotic dinoflagellates of the genus Symbiodinium) are critical to the survival of reef-building corals, providing a major source of energy from photosynthesis for cell maintenance, growth and reproduction of their coral hosts. Cantin et al. (2009) studied the amount of photosynthetic "rent" paid by two different clades of Symbiodinium (C1 and D) to their coral hosts (juvenile Acropora millepora) for the privilege of living within the latter's calcareous "houses." Results indicated that "Symbiodinium C1 exhibited a 121% greater capacity for translocation of photosynthate to A. millepora juveniles along with 87% greater relative electron transport through photosystem II under identical environmental conditions."
As a result of their analysis, Cantin et al. conclude that "the differences in carbon-based energy transfer between symbiont types may provide a competitive advantage to corals associating with Symbiodinium C1, particularly during their early life histories, when greater energy investment into rapid tissue and skeletal growth can prevent overgrowth of juveniles by competitors and mortality from grazers." As the community structure of coral reefs shift in response to global climate change and ocean acidification, corals harboring symbionts may gain a competitive advantage, allowing them the natural provisions to cope with changing environments.
In light of these several observations, earth’s corals will likely be able to successfully cope with the possibility of further increases in water temperatures, be they anthropogenic-induced or natural. Corals have survived such warmth—and worse—many times in the past, including the Medieval Warm Period, Roman Warm Period, and Holocene Optimum, as well as throughout numerous similar periods during a number of prior interglacial periods; there is no reason to believe they cannot do it again, if the need arises.
One final adaptive bleaching mechanism is discussed by Reshef et al., (2006), who developed a case for what they call the coral probiotic hypothesis, and what we call “bacterial shuffling.” This concept, in their words, “posits that a dynamic relationship exists between symbiotic microorganisms and environmental conditions which brings about the selection of the most advantageous coral holobiont.”
This concept is analogous to the adaptive bleaching hypothesis of Buddemeier and Fautin (1993), or what was referred to in the preceding section as symbiont shuffling, wherein corals exposed to some type of stress—such as that induced by exposure to unusually high water temperatures or solar irradiance—first lose their dinoflagellate symbionts (bleach) and then regain a new mixture of zooxanthellae that are better suited to the stress conditions. In fact, the two phenomena work in precisely the same way, in one case by the corals rearranging their zooxanthellae populations (symbiont shuffling) and in the other case by the corals rearranging their bacterial populations (bacterial shuffling).
In seeking evidence for their hypothesis, the team of Israeli researchers concentrated their efforts on looking for examples of corals developing resistance to emerging diseases. This approach makes sense, because corals lack an adaptive immune system; i.e., they possess no antibodies (Nair et al., 2005), and they therefore can protect themselves against specific diseases in no other way than to adjust the relative sizes of the diverse bacterial populations associated with their mucus and tissues so as to promote the growth of those types of bacteria that tend to mitigate most effectively against the specific disease that happens to be troubling them.
Reshef et al. begin by describing the discovery that bleaching of Oculina patagonica corals in the Mediterranean Sea was caused by the bacterium Vibrio shiloi, together with the finding that bleaching of Pocillopora damicornis corals in the Indian Ocean and Red Sea was the result of an infection with Vibrio coralliilyticus. But they then report that (1) “during the last two years O. patagonica has developed resistance to the infection by V. shiloi,” (2) “V. shiloi can no longer be found on the corals,” and (3) “V. shiloi that previously infected corals are unable to infect the existing corals.” They say “by some unknown mechanism, the coral is now able to lyse the intracellular V. shiloi and avoid the disease,” and because corals lack the ability to produce antibodies and have no adaptive immune system, the only logical conclusion to be drawn from these observations is that bacterial shuffling must be what produced the welcome results.
With respect to the future of earth’s corals in the context of global warming, the Israeli scientists note that “Hoegh-Guldberg (1999, 2004) has predicted that coral reefs will have only remnant populations of reef-building corals by the middle of this century,” based on “the assumption that corals cannot adapt rapidly enough to the predicted temperatures in order to survive.” However, they report that considerable evidence has been collected in support of the adaptive bleaching hypothesis, and they emphasize that the hundreds of different bacterial species associated with corals “give the coral holobiont an enormous genetic potential to adapt rapidly to changing environmental conditions.” They say “it is not unreasonable to predict that under appropriate selection conditions, the change could take place in days or weeks, rather than decades required for classical Darwinian mutation and selection,” and that “these rapid changes may allow the coral holobiont to use nutrients more efficiently, prevent colonization by specific pathogens and avoid death during bleaching by providing carbon and energy from photosynthetic prokaryotes,” of which they say there is “a metabolically active, diverse pool” in most corals.
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