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CO2, Global Warming and Coral Reefs
Prospects for the Future

2. Responding to Stress: The Power of Adaptation


Considering the many threats to the health of coral reefs in today’s world of extensive socioeconomic and environmental change – including the global warming of the past century or so, which may or may not be CO2-induced – is there any way that these incomparable repositories of underwater biodiversity can ever be expected to escape irreversible bleaching and death?

In an illuminating response to this important question, Glynn (1996) answered with an observation that is pertinent to concerns about predictions of future CO2-induced increases in air and water temperatures. Glynn began by pointing out that “numerous reef-building coral species have endured three periods of global warming, from the Pliocene optimum (4.3-3.3 million years ago) through the Eemian interglacial (125 thousand years ago) and the mid-Holocene (6000-5000 years ago), when atmospheric CO2 concentrations and sea temperatures often exceeded those of today.” In fact, Glynn went so far as to state that “an increase in sea warming of less than 2°C would result in a greatly increased [our italics] diversity of corals in certain high latitude locations.”

So how does it happen? Why, with so many local and global threats to their continued existence, do reefs persist and sometimes even flourish? To what do they owe their amazing resilience? And how do they meet the physiological challenges presented by the combination of high light intensities and water temperatures that many climate alarmists consider to be the primary cause of mass coral bleaching? In a word, the answer is adaptation.

Living organisms are resilient. Various lifeforms can tolerate temperatures from below freezing to the boiling point of water; while others inhabit niches where light intensity varies from complete darkness to full sunlight. One reason for this great versatility is that, given time to adapt, nearly all living organisms can learn to survive in conditions well outside their normal zones of environmental tolerance. As noted by Gates and Edmunds (1999), results of numerous studies indicate that “corals routinely occupy a physically heterogeneous environment,” which “suggests they should possess a high degree of biological flexibility.” And indeed they do, as evidenced by their successful responses to the different threats that cause coral bleaching, which are examined in the following subsections.

2.1. Response to Solar Radiation Stress

With respect to coral responses to stress imposed by high solar irradiance, one simple example of such adaptation comes from studies of corals that exhibit a zonation of their symbiont taxa with depth, where symbiont algae that are less tolerant of intense solar radiation grow on corals at greater depths below the ocean surface (Rowan and Knowlton, 1995; Rowan et al., 1997). It has also been demonstrated that zooxanthellae in corals possess a number of light quenching mechanisms that can be employed to reduce the negative impacts of excess light (Hoegh-Guldberg and Jones, 1999; Ralph et al., 1999). Both the coral host and its symbionts also have the capacity to produce amino acids that act as natural “sunscreens” (Hoegh-Guldberg, 1999); and they can regulate their enzyme activities to enhance internal scavenging systems that remove noxious oxygen radicals produced in coral tissues as a result of high light intensities (Dykens and Shick, 1984; Lesser et al., 1990; Matta and Trench, 1991; Shick et al., 1996).

Another adaptive mechanism proposed to lessen the stress of solar irradiance is coral tissue retraction, according to Brown et al. (1994a), who studied the phenomenon in the scleractinian coral Coeloseris mayeri at coral reefs in Phuket, Thailand, by examining the retraction and recovery of coral tissues over a tidal cycle. Results of their analysis showed that extreme tissue retraction was observed approximately 85 minutes after initial sub-aerial coral exposure. Tissue retraction, however, did not involve any reduction in chlorophyll concentration or algae symbiont abundance; and the tissues expanded over the coral skeletons to pre-retraction conditions following the return of the tide. The adaptive benefits of tissue retraction, according to the authors, "include increased albedo, leading to a reduction in absorbed solar energy of 10%, ... and possible avoidance of photochemical damage or photoinhibition at high solar irradiance."

Another intriguing idea was proposed by Nakamura and van Woesik (2001), who upon evaluating the bleaching of large and small coral colonies along the western coast of Okinawa, Japan, during the summers of 1998 and 2001, argued that small coral colonies should survive thermal and light stress more readily than large coral colonies based on mass transfer theory, which suggests that rates of passive diffusion are more rapid for small colonies than for large colonies. Still another reason why large coral colonies suffer more than small colonies during environmental conditions conducive to bleaching is the fact that small Acropora recruits, according to Bena and van Woesik (2004), "contain high concentrations of fluorescent proteins (Papina et al., 2002), which have photoprotective properties (Salih et al., 2000)," and they note that "a high concentration of photoprotective pigments in early life, when planulae are near the surface and as newly settled recruits, may facilitate survival during this phase as well as during stress events involving both high irradiance and thermal anomalies (van Woesik, 2000)."

In addition to the adaptive phenomena described above, the earth appears to possess an amazingly effective meteorological "ThermoSolarStat" that jumps into operation to suppress the intensity of solar radiation to which corals are exposed whenever dangerously-high water temperatures are approached, and which thereby tends to suppress further increases in water temperature that may be prompted by increases in the intensity of any thermal forcing factor, such as the CO2-augmented greenhouse effect.

How does the mechanism, which is composed of at least two major components, work? According to Hoegh-Guldberg (1999), 29.2°C is the threshold water temperature above which significant bleaching can be expected to occur in many tropical corals. However, as Sud et al. (1999) have demonstrated in elucidating the functioning of the first of the ThermoSolarstat's two primary components (based on data obtained from the Tropical Ocean Global Atmosphere Coupled Ocean-Atmosphere Response Experiment), deep atmospheric convection is typically initiated whenever sea surface temperatures (SSTs) reach a value of about 28°C, so that an upper SST on the order of 30°C is rarely exceeded.

Initially, according to this concept, the tropical ocean acts as a net receiver of energy in its warming phase; but as SSTs reach 28-29°C, the cloud-base airmass is charged with sufficient moist static energy for the clouds to reach the upper troposphere. At this point, the billowing cloud cover reduces the amount of solar radiation received at the surface of the sea, while cool and dry downdrafts produced by the moist convection tend to promote ocean surface cooling by increasing sensible and latent heat fluxes at the air-sea interface that cause temperatures there to decline.

This "thermostat-like control," as Sud et al. describe it, tends "to ventilate the tropical ocean efficiently and help contain the SST between 28-30°C," which is essentially a fluctuating temperature band of ±1°C centered on the bleaching threshold temperature of 29.2°C identified by Hoegh-Guldberg. This particular component of the atmosphere's ThermoSolarstat, i.e., the component that creates towering cumulonimbus clouds at the appropriate critical SST, also greatly reduces the flux of solar radiation received at the surface of the sea, thereby providing a dual approach to relieving the two main stresses (solar and thermal) that may be experienced by corals that are teetering on the brink of potentially irreversible bleaching.

Some other intriguing observations also point to the existence of a natural phenomenon of this nature. Satheesh and Ramanathan (2000), for example, determined that polluted air from south and southeast Asia absorbs enough solar radiation over the northern Indian Ocean during the dry monsoon season to heat the atmosphere there by 1-3°C per day at solar noon, thereby greatly reducing the intensity of solar radiation received at the surface of the sea. Ackerman et al. (2000), however, calculated that this atmospheric heating would decrease cloud-layer relative humidity and reduce boundary-layer mixing, thereby leading to a 25-50% drop in daytime cloud cover relative to that of an aerosol-free atmosphere, which could well negate the surface cooling effect suggested by the findings of Satheesh and Ramanathan. But in a test of this hypothesis based on data obtained from the Extended Edited Cloud Report Archive, Norris (2001) determined that daytime low-level ocean cloud cover (which tends to cool the water surface) not only did not decrease from the 1950s to 90s, it actually increased ... in both the Northern and Southern Hemispheres and at essentially all hours of the day.

Commenting on this finding, Norris remarked that "the observed all-hours increase in low-level cloud cover over the time period when soot aerosol has presumably greatly increased argues against a dominant effect of soot solar absorption contributing to cloud 'burn-off'." Hence, he says, "other processes must be compensating," one of which, we suggest, could well be the one described by Sud et al.

Another process – and our proposed second component of earth's ThermoSolarstat – is the "adaptive infrared iris" phenomenon that has been described by Lindzen et al. (2001). Working with upper-level cloudiness data obtained from the Japanese Geostationary Meteorological Satellite and SST data obtained from the National Centers for Environmental Prediction, the inquisitive atmospheric scientists found a strong inverse relationship between upper-level cloud area and the mean SST of cloudy regions, such that the area of cirrus cloud coverage (which tends to warm the planet) normalized by a measure of the area of cumulus coverage (which tends to cool the planet) decreased about 22% for each 1°C increase in the SST of the cloudy regions.

"Essentially," in the words of the scientists, "the cloudy-moist region appears to act as an infrared adaptive iris that opens up and closes down the regions free of upper-level clouds, which more effectively permit infrared cooling, in such a manner as to resist changes in tropical surface temperatures." So substantial is this phenomenon, Lindzen et al. are confident it could "more than cancel all the positive feedbacks in the more sensitive current climate models," which are routinely used to predict the climatic consequences of projected increases in atmospheric CO2 concentration.

All this is well and good; the meteorological aspects of the ThermoSolarstat are clearly supported by significant bodies of real-world data. But is there any real-world evidence the ThermoSolarstat has actually been instrumental in preventing coral bleaching that would otherwise have occurred during periods of unusually high thermal stress? The answer, of course, is yes; and it comes in an important paper published by Mumby et al. (2001), wherein they examined long-term meteorological records from the vicinity of the Society Islands, which provide what they call "the first empirical evidence that local patterns of cloud cover may influence the susceptibility of reefs to mass bleaching and subsequent coral mortality during periods of anomalously high SST."

With respect to the great El Niño of 1998, Mumby and his colleagues determined that SSTs in the Society Islands sector of French Polynesia were above the 29.2°C bleaching threshold for a longer period of time (two months) than in all prior bleaching years of the historical record. However, mass coral bleaching, which was extensive in certain other areas, was found to be "extremely mild in the Society Islands" and "patchy at a scale of 100s of km."

What provided the relief from extreme sun and heat, without which, Mumby et al. have concluded, "mass bleaching would have occurred"? As he and his associates describe it, "exceptionally high cloud cover significantly reduced the number of sun hours during the summer of 1998," much as one would have expected earth's ThermoSolarstat to have done in the face of such anomalously high SSTs. The marine scientists also note that extensive spotty patterns of cloud cover, besides saving most of the coral they studied, "may partly account for spatial patchiness in bleaching intensity and/or bleaching-induced mortality in other areas."

In conclusion, although the ThermoSolarstat cannot protect all of earth's corals from life-threatening bleaching during all periods of anomalously high SSTs, it apparently protects enough of them enough of the time to insure that sufficiently large numbers of corals survive to perpetuate their existence, since living reefs have persisted over the eons in spite of the continuing recurrence of these ever-present environmental threats. And perhaps that is how it has always been, although there are currently a host of unprecedented anthropogenic forces of site-specific origin that could well be weakening the abilities of some species to tolerate the types of thermal and solar stresses they have successfully "weathered" in the past.

2.2. Response to Temperature Stress

As living entities, corals are not only acted upon by the various elements of their environment, they also react or respond to them. And when changes in environmental factors pose a challenge to their continued existence, they sometimes take major defensive or adaptive actions to insure their survival. A simple but pertinent example of one form of this phenomenon is thermal adaptation, which feature has been observed by several researchers to operate in corals.

Fang et al. (1997), for example, experimented with samples of the coral Acropora grandis that were taken from the hot water outlet of a nuclear power plant near Nanwan Bay, Taiwan. In 1988, the year the power plant began full operation, the coral samples were completely bleached within two days of exposure to a temperature of 33°C. Two years later, however, Fang et al. report that “samples taken from the same area did not even start bleaching until six days after exposure to 33°C temperatures.”

Similar findings have been reported by Middlebrook et al. (2008), who collected multiple upward-growing branch tips of the reef-building coral Acropora aspera from three large colonies at the southern end of Australia's Great Barrier Reef and placed them on racks immersed in running seawater within four 750-liter tanks that were maintained at the mean local ambient temperature (27°C) and exposed to natural reef-flat summer daily light levels. Then, two weeks prior to a simulated bleaching event -- where water temperature was raised to a value of 34°C for a period of six days -- they boosted the water temperature in one of the tanks to 31°C for 48 hours, while in another tank they boosted it to 31°C for 48 hours one week before the simulated bleaching event. In the third tank they had no pre-heating treatment, while in the fourth tank they had no pre-heating nor any simulated bleaching event. And at different points throughout the study, they measured photosystem II efficiency, xanthophyll and chlorophyll a concentrations, and Symbiodinium densities.

Results of the study indicated that the symbionts of the corals that were exposed to the 48-hour pre-bleaching thermal stress "were found to have more effective photoprotective mechanisms," including "changes in non-photochemical quenching and xanthophyll cycling," and they further determined that "these differences in photoprotection were correlated with decreased loss of symbionts, with those corals that were not pre-stressed performing significantly worse, losing over 40% of their symbionts and having a greater reduction in photosynthetic efficiency," whereas "pre-stressed coral symbiont densities were unchanged at the end of the bleaching." In light of these findings, Middlebrook et al. (2008) say their study "conclusively demonstrates that thermal stress events two weeks and one week prior to a bleaching event provide significantly increased thermal tolerance to the coral holobiont, suggesting that short time-scale thermal adaptation can have profound effects on coral bleaching."

Moving out of the laboratory and into the real world of nature, Adjeroud et al. (2005) initiated a monitoring program on 13 islands (eight atolls and five high volcanic islands) in four of the five archipelagoes of French Polynesia, with the goal of documenting the effects of natural perturbations on coral assemblages. For the period covered by their report (1992-2002), these reefs were subjected to three major coral bleaching events (1994, 1998, 2002) and three cyclones (1997), while prior to this period, the sites had experienced an additional seven bleaching events and fifteen cyclones, as well as several Acanthaster planci outbreaks.

Results of the monitoring program revealed that the impacts of the bleaching events were variable among the different study locations. In their ten-year survey, for example, they observed three different temporal trends: "(1) ten sites where coral cover decreased in relation to the occurrence of major disturbances; (2) nine sites where coral cover increased, despite the occurrence of disturbances affecting seven of them; and (3) a site where no significant variation in coral cover was found." In addition, they report 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)."

Commenting on their and other researchers' observations, the seven French scientists say 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 also confirmed the phenomenon of thermal adaptation in coral reefs. Guzman and Cortes (2007) studied coral 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 Niño." At Cocos Island (5°32'N, 87°04'W), in particular, they found in a survey of three representative reefs, which they conducted in 1987, that remaining live coral cover was only 3% of what it had been prior to the occurrence of the great El Niño four years earlier (Guzman and Cortes, 1992). 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, therefore, 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 Niño's horrendous damage, quantifying "the live coral cover and species composition of five reefs, including the three previously assessed in 1987."

So what did they find?

The two researchers report that overall mean live coral cover increased nearly five-fold, from 2.99% in 1987 to 14.87% 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 from pre-1982 ENSO, Porites lobata, suggesting that a disturbance as outstanding as El Niño was not sufficient to change the role or composition of the dominant species."

With respect to the subject of thermal tolerance, however, the most interesting aspect of the study was the fact that a second major El Niño occurred between the two assessment periods; and Guzman and Cortes state that "the 1997-1998 warming event around Cocos Island was more intense than all previous El Niño events," noting that temperature anomalies "above 2°C lasted 4 months in 1997-1998 compared to 1 month in 1982-83." Nevertheless, they report that "the coral communities suffered a lower and more selective mortality in 1997-1998 [our italics], 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 type of thermal adaptation following the 1982-83 El Niño.

One year later in a paper published in Marine Biology, 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. write that they are "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 say 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 say 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 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, however, they say their results additionally suggest "a capacity for acclimatization or adaptation."

In concluding their paper, Maynard et al. say "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, a phenomenon we describe in greater detail in the next section of our report. 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) have 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 is followed by another heat shock protein increase at the 48-hour point of exposure to elevated water temperature. They state 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 corals in this regard? No one knows for sure; but they've been around a very long time, during which 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."

2.3. Symbiont Shuffling

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). 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 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 tolerant of the stress that caused the bleaching.

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, 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 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) 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 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," 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 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."

In the years that have followed since 2004, many more studies have further elevated the symbiont shuffling hypothesis to a full-fledged theory.

Writing in the journal Marine Ecology Progress Series, Chen et al. (2005) 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 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. 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 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. 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.

In 2006, working within Australia's Great Barrier Reef system, Berkelmans and van Oppen 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 further report 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 report 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 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." As a result, 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." In fact, 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," 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 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. 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 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).

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 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 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; for they 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 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, 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; and there is no reason to believe they cannot do it again, if the need arises.

2.4. Bacterial Shuffling

One final adaptive bleaching mechanism is discussed in the literature by Reshef et al., (2006), who developed a case for what they call the Coral Probiotic Hypothesis. 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," that (2) "V. shiloi can no longer be found on the corals," and that (3) "V. shiloi that previously infected corals are unable to infect the existing corals." In fact, they say that "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 the coral probiotic phenomenon, as described by Reshef et al., must be what produced the welcome results.

With respect to the future of earth's corals within 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 [our italics] genetic potential to adapt rapidly [our italics] to changing environmental conditions." In fact, 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 every coral.

2.5. A Role for Elevated CO2?

It is a general principle – applicable to the vast majority of all plants – that as temperatures rise, photorespiration consumes ever more of the recently-fixed products of photosynthesis, creating a decrease in the rate of net carbon uptake (Hanson and Peterson, 1986) and thereby reducing the plant’s ability to withstand any number of environmental stresses. If more CO2 can be delivered to the site of photosynthesis, however, more CO2 can be made available to compete with oxygen for active sites on the carboxylating/oxygenating enzyme rubisco (Grodzinski et al., 1987). Hence, anything that increases the concentration of CO2 at the site of photosynthesis should enhance the net fixation of carbon more at higher temperatures than it does at lower temperatures, as atmospheric CO2 enrichment clearly has been shown to do in numerous terrestrial plants (Idso et al., 1987; Mortensen, 1987; Idso and Idso, 1994).

One of the major consequences of this phenomenon is that the optimal temperature for plant growth generally rises with CO2 enrichment. For terrestrial C3 plants, Long (1991) has calculated that their optimal temperatures should rise by about 5°C for a 300 ppm increase in the air’s CO2 content; while in an analysis of the results of seven studies that experimentally evaluated this response in terrestrial C3 plants, Idso and Idso (1994) found plant optimal temperature to rise by approximately 6°C for such a rise in atmospheric CO2 concentration. In addition, Chen et al. (1994) demonstrated that there may even be a modest increase in terrestrial C4 plant optimal temperature in response to atmospheric CO2 enrichment.

At the highest temperatures experienced by plants, elevated CO2 concentrations are especially helpful. When photorespiration is so high as to drive net carbon fixation all the way to zero, for example, more CO2 can sometimes mean the difference between a plant’s living or dying (Kriedemann et al., 1976; Converse and George, 1987), as it may enable the plant to maintain a positive carbon exchange rate, when plants growing under ambient CO2 concentrations exhibit negative rates that ultimately lead to their demise. Idso et al. (1995) demonstrated this fact explicitly with a terrestrial C3 plant, while Idso et al. (1989) demonstrated it with a floating aquatic C3 plant. Hence, it is not illogical to think that as the air’s CO2 content continues to rise, forcing more CO2 to dissolve in the surface waters of the world’s oceans, this same phenomenon may operate to protect the algal symbionts of the oceans’ corals from dying at what would normally have been a lethal water temperature under pre-industrial atmospheric CO2 concentrations.

A likely major consequence of this phenomenon is that coral reefs would expand their ranges throughout the world in the face of a CO2-induced global warming, or even in the face of a non-CO2-induced global warming, if atmospheric CO2 concentrations rose concurrently for some other reason. With temperatures and CO2 concentrations both rising everywhere, for example, coral symbionts would be able to extend their ranges poleward in response to the global warming; and with the protective effect of higher aqueous CO2 concentrations helping them to withstand the stress of increased temperature at the other end of their latitudinal distributions, they would be able to continue to survive in the warmest regions of their ranges.

But what about the coral animals that act as hosts to the zooxanthellae? Would elevated levels of CO2 help them in some way, so that they too could withstand a temperature increase in the warmest regions of their ranges? Although no experiments have broached this subject, some real-world terrestrial observations suggest that such might well be the case.

A crude terrestrial analogy to the coral/zooxanthellae relationship of the aquatic realm – but where the animal provides little of value to the plant that sustains it – is that of the butterfly and the plant species upon which its larvae feed. It is thus instructive to observe that in a study of shifts in the ranges of more than 50 European butterfly species over the past century, Parmesan et al. (1999) found that most of them moved northward in response to a regional warming of approximately 0.8°C. However, in the words of the authors, “nearly all northward shifts involved extensions at the northern boundary with the southern boundary remaining stable” – such as would be expected for the plants on which they feed in the face of concurrent increases in air temperature and atmospheric CO2 concentration – so that “most species effectively expanded the size of their range when shifting northwards.” Furthermore, this northward range expansion did not displace other butterflies from the southern portions of their ranges, so that the numbers of butterfly species inhabiting many areas of the continent, or butterfly species richness, increased. And in a similar study of shifts in the ranges of an equally large number of British bird species (which feed on such things as butterfly larvae), Thomas and Lennon (1999) found essentially the same behavior: northern boundaries moved northward in response to regional warming and concurrent increases in atmospheric CO2, while southern boundaries remained constant, which thus increased the diversity of bird species inhabiting many of the affected areas.

Thus we see there are a number of ways in which corals may adapt to high temperature and solar radiation stresses. In addition, the rising CO2 concentration of earth’s atmosphere may give them an enhanced ability to successfully cope with the specific stress of global warming. And certain terrestrial plant-animal associations exhibit responses to CO2 and global warming that are in harmony with predictions based upon this latter phenomenon, thereby providing a solid basis for being optimistic about the fate of earth’s coral reef ecosystems in the face of the ongoing rise in the air’s CO2 content.