How does rising atmospheric CO2 affect marine organisms?

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Carbon Dioxide and Earth's Future: Pursuing the Prudent Path

9. Frequent Coral Bleaching

The claim: Rising ocean temperatures driven by CO2-induced global warming is killing the world's corals.

Bleaching is the name of the phenomenon given to the process whereby the corals inhabiting earth's seas expel the algal symbionts or zooxanthellae living within their tissues (upon which they depend for their sustenance) when subjected to various environmental stresses, one of the most discussed of which is excessive warmth. And as a result of this discussion, primarily among climate alarmists, global warming has long been claimed by them to be one of the primary reasons for mandating reductions in anthropogenic CO2 emissions, in order to prevent our driving numerous species of corals to extinction. But is this contention based on sound science?

With respect to corals adapting to greater warmth, Adjeroud et al. (2005) documented -- in a study of 13 islands in four of the five archipelagoes of French Polynesia -- the effects of natural perturbations on various coral assemblages over the period 1992-2002, during which time the reefs were subjected to three major coral bleaching events (1994, 1998, 2002). Finding that the impacts of the bleaching events were variable among the different study locations, and that "an interannual survey of reef communities at Tiahura, Moorea, showed that the mortality of coral colonies following a bleaching event was decreasing with successive events, even if the latter have the same intensity (Adjeroud et al., 2002)," they concluded that the "spatial and temporal variability of the impacts observed at several scales during the present and previous surveys may reflect an acclimation and/or adaptation of local populations," such that "coral colonies and/or their endosymbiotic zooxanthellae may be phenotypically (acclimation) and possibly genotypically (adaptation) resistant to bleaching events," citing the work of Rowan et al. (1997), Hoegh-Guldberg (1999), Kinzie et al. (2001) and Coles and Brown (2003) in support of this conclusion.

Other researchers have confirmed the phenomenon of thermal adaptation in coral reefs. Guzman and Cortes (2007), for example, studied reefs of the eastern Pacific Ocean that "suffered unprecedented mass mortality at a regional scale as a consequence of the anomalous sea warming during the 1982-1983 El Niņo." In a survey of three representative reefs they conducted in 1987 at Cocos Island, for example, they found that remaining live coral cover was only 3% of what it had been prior to the occurrence of the great El Niņo four years earlier (Guzman and Cortes, 1992); and based on this finding and the similar observations of other scientists at other reefs, they predicted that "the recovery of the reefs' framework would take centuries, and recovery of live coral cover, decades."

In 2002, however, nearly 20 years after the disastrous coral-killing warming, they returned to see just how prescient they might have been after their initial assessment of the El Niņo's horrendous damage, quantifying the live coral cover and species composition of five reefs, including the three they assessed in 1987. And in doing so, they found that overall mean live coral cover had increased nearly five-fold, from 3% in 1987 to 14.9% in 2002, at the three sites studied during both periods, while the mean live coral cover of all five sites studied in 2002 was 22.7%. In addition, they found that most new recruits and adults belonged to the main reef building species of the past, suggesting that a disturbance as outstanding as the 1982-1983 El Niņo "was not sufficient to change the role or composition of the dominant species."

The most interesting aspect of their study, however, was the fact that a second major El Niņo had occurred between the two assessment periods; and Guzman and Cortes report that the 1997-1998 warming event around Cocos Island was more intense than all previous El Niņo events, noting that temperature anomalies above 2°C lasted 4 months in 1997-1998 compared to 1 month in 1982-83. Nevertheless, they found that "the coral communities suffered a lower and more selective mortality in 1997-1998, as was also observed in other areas of the eastern Pacific (Glynn et al., 2001; Cortes and Jimenez, 2003; Zapata and Vargas-Angel, 2003)," which is indicative of some form of thermal adaptation in the wake of the 1982-83 El Niņo.

One year later, Maynard et al. (2008) described how they analyzed the bleaching severity of three genera of corals (Acropora, Pocillopora and Porites) via underwater video surveys of five sites in the central section of Australia's Great Barrier Reef in late February and March of 1998 and 2002, while contemporary sea surface temperatures were acquired from satellite-based Advanced Very High Resolution Radiometer data that were calibrated to local ship- and drift buoy-obtained measurements, and surface irradiance data were obtained "using an approach modified from that of Pinker and Laszlo (1991)."

With respect to temperature, the four researchers report that "the amount of accumulated thermal stress (as degree heating days) in 2002 was more than double that in 1998 at four of the five sites," and that "average surface irradiance during the 2002 thermal anomaly was 15.6-18.9% higher than during the 1998 anomaly." Nevertheless, they found that "in 2002, bleaching severity was 30-100% lower than predicted from the relationship between severity and thermal stress in 1998, despite higher solar irradiances during the 2002 thermal event." In addition, they found that the "coral genera most susceptible to thermal stress (Pocillopora and Acropora) showed the greatest increase in tolerance."

In discussing their findings, Maynard et al. wrote that they were "consistent with previous studies documenting an increase in thermal tolerance between bleaching events (1982-1983 vs. 1997-1998) in the Galapagos Islands (Podesta and Glynn, 2001), the Gulf of Chiriqi, the Gulf of Panama (Glynn et al., 2001), and on Costa Rican reefs (Jimenez et al., 2001)," and they report that "Dunne and Brown (2001) found similar results to [theirs] in the Andaman Sea, in that bleaching severity was far reduced in 1998 compared to 1995 despite sea-temperature and light conditions being more conducive to widespread bleaching in 1998."

As for the significance of these and other observations, the Australian scientists stated that "the range in bleaching tolerances among corals inhabiting different thermal realms suggests that at least some coral symbioses have the ability to adapt to much higher temperatures than they currently experience in the central Great Barrier Reef," citing in this regard, the work of Coles and Brown (2003) and Riegl (1999, 2002). In addition, they note that "even within reefs there is a significant variability in bleaching susceptibility for many species (Edmunds, 1994; Marshall and Baird, 2000), suggesting some potential for a shift in thermal tolerance based on selective mortality (Glynn et al., 2001; Jimenez et al., 2001) and local population growth alone." Above and beyond that, they said their results suggest "a capacity for acclimatization or adaptation."

In concluding their paper, Maynard et al. wrote "there is emerging evidence of high genetic structure within coral species (Ayre and Hughes, 2004)," which suggests, in their words, that "the capacity for adaptation could be greater than is currently recognized." Indeed, as stated by Skelly et al. (2007), "on the basis of the present knowledge of genetic variation in performance traits and species' capacity for evolutionary response, it can be concluded that evolutionary change will often occur concomitantly with changes in climate as well as other environmental changes." Consequently, it can be appreciated that if global warming were to start up again (it has been in abeyance for about the last decade), it need not spell the end for earth's highly adaptable corals.

But how is it done? How do corals adjust to rising temperatures?

One adaptive mechanism that corals have developed to survive the thermal stress of high water temperature is to replace the zooxanthellae expelled by the coral host during a stress-induced bleaching episode by one or more varieties of zooxanthellae that are more heat tolerant. Another mechanism is to produce heat shock proteins that help repair heat-damaged constituents of their bodies (Black et al., 1995; Hayes and King, 1995; Fang et al., 1997). Sharp et al. (1997), for example, demonstrated that sub-tidal specimens of Goniopora djiboutiensis typically have much lower constitutive levels of a 70-kD heat shock protein than do their intertidal con-specifics; and they have shown that corals transplanted from sub-tidal to intertidal locations (where temperature extremes are greater and more common) typically increase their expression of this heat shock protein.

Similar results have been reported by Roberts et al. (1997) in field work with Mytilus californianus. In addition, Gates and Edmunds (1999) observed an increase in the 70-kD heat shock protein after six hours of exposure of Montastraea franksi to a 2-3°C increase in temperature, which was followed by another heat shock protein increase at the 48-hour point of exposure to elevated water temperature. And in their case, they wrote that the first of these protein increases "provides strong evidence that changes in protein turnover during the initial exposure to elevated temperature provides this coral with the biological flexibility to acclimatize to the elevation in sea water temperature," and that the second increase "indicates another shift in protein turnover perhaps associated with an attempt to acclimatize to the more chronic level of temperature stress."

So how resilient are earth's corals to rising water temperatures? No one knows for sure; but they've been around a very long time, during which earth's climatic conditions have changed dramatically, from cold to warm and back again, over multiple glacial and interglacial cycles. And in this regard, we see no reason why history cannot be expected to successfully repeat itself, even as the current interglacial experiences its "last hurrah."

With respect to corals finding salvation via symbiont shuffling, we note that although once considered to be members of the single species Symbiodinium microadriacticum, the tiny 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). Consequently, a particularly ingenious way by which almost any adaptive response to any type of environmental stress may be enhanced in the face of the occurrence of that stress would be for corals to replace the zooxanthellae they expel during a stress-induced bleaching episode by one or more varieties of zooxanthellae that are more tolerant of the stress that caused the bleaching.

Rowan et al. (1997) 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) 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) 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) 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 suggested that coral bleaching events "may be frequent and part of the expected cycle." Gates and Edmunds (1999) additionally reported that "several of the prerequisites required to support this hypothesis have now been met," and after describing them in some detail, they concluded "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 produced the long-sought proof that transformed 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, 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. (2002) wrote 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 stated 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 described 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 noted 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 wrote 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 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 continued, "the corals started to recover quickly in August 2002 and as much as 52% recovery could be noticed." By comparison, they noted 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 said that "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 concluded 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) 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."

Clinching the concept was 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 Niņo-Southern Oscillation (ENSO) bleaching event." Along the coasts of Panama, they studied 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 indicated 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 showed 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 writing 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" that was observed by both groups "represents a mechanism for rapid acclimatization of the holobiont to environmental change." Consequently, the results of both studies demonstrated 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."

In the years that followed, numerous other studies further elevated the symbiont shuffling hypothesis to a full-fledged theory, if not a proven fact.

Chen et al. (2005), for example, studied 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 their 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. Furthermore, 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 say their work revealed "the first evidence that the symbiont community within coral colonies is dynamic ... involving changes in Symbiodinium phylotypes."

Contemporaneously, 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 were 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 said "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 said they suspected 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.

Also 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." Then, two years later, working with an expanded group of scientists (Jones et al., 2008), the same two researchers reported similar findings following the occurrence of a natural bleaching event.

Prior to this bleaching event, Jones et al. reported 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 further reported that "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; and they reported that "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 reported 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. wrote 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 noted that "a shift from bleaching-sensitive type C2 to clade D increased the thermal tolerance of this species by 1-1.5°C." Therefore, they said 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." In fact, they said 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," a finding that bodes especially well for earth's corals in a warming climate.

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 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." And 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 with environmental heterogeneities and survive the consequences (e.g., recover from coral bleaching)."

At about the same time, Mieog et al. (2007) utilized a newly developed real-time polymerase chain reaction assay -- which they said "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 this 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." And as a result, they suggested that symbiont shuffling is likely to play a role in the way earth's "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 alarmists 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). The results of their 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 reported 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 far-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 discounted the argument that symbiont shuffling is not an option for most coral species, because, as they indicated, 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." Thus, 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; for Baird et al. indicated 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. suggested 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 noted that "juveniles of Acropora tenuis regularly harbor mixed assemblages of symbionts, whereas adults of the species almost invariably host a single clade," and they indicated 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 concluded there is no need for an acute disturbance, such as bleaching, to induce clade or sub-clade change. Instead, if it happens that 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 reported that "the majority of mixed genotypes observed during this survey were usually harbored by the smallest hosts." As a result, they speculated 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 protists 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 to 90% of adult coral colonies were severely bleached during the event, only 25% 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.

In light of these several observations, it is logical to believe that earth's corals will 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, the Roman Warm Period, and the Holocene Optimum, as well as throughout numerous similar periods during a number of prior interglacial periods; and there is no reason to believe they cannot do it again, if the need arises.

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