I have just finished co-writing a book chapter on the biological effects of increased CO2 levels on corals and coral reefs. It was a fascinating journey for me through much new subject matter, and I felt the subject would also be appropriate for the reefkeeping audience since our hobby is inextricably linked to the health of coral reefs. This month's article is a greatly scaled-down and amended version of that story, and is also, hopefully, a little easier to read than the original version.

Such a project requires a vast amount of literary searching, and in the process I came across quite a few articles that seemed to have some significance to keeping reef aquaria. Because they cover some fairly discontinuous subjects, I will offer them next month as a compendium since they do not lend themselves to a cohesive single article. Just so you all know, my wife and I do not own an SUV, and last year purchased a Mini Cooper - not an electric hybrid, but still an antithesis to the fuel-guzzling vehicles menacing U.S. roadways.

Background

Coral reefs are threatened worldwide, and the threats responsible for this crisis are multiple and often complex. The worldwide rate of coral reef degradation is alarming; 58% are threatened by human activities, 11% have been lost to human activities, and 16% were damaged or lost by the ENSO-related bleaching events of 1997-1998 (Wilkinson 2002). This dramatic tale of coral reef decline has been told in many highly regarded scientific publications (Hoegh-Guldberg 1999; Hughes and Connell 1999; Buddemeier et al. 2004; Knowlton 2001; Hughes et al. 2003; Wilkinson 2002; Pandolfi et al. 2003).

The deterioration of coral reefs is known or believed to be linked mainly to human activities, and perhaps the largest indirect effects occur on a global scale and result from climactic change. The El Niño Southern Oscillation (ENSO) was first reported in Ecuador and northern Perú during the mid to late 1800's (Murphy 1926). Early reports described prolonged periods of high sea surface temperatures, heavy rains, and little wind (doldrums). The El Niño phenomenon was later explained as Pacific-wide changes in sea level resulting from shifts in the trade winds (Bjerkenes 1969; Wyrtki 1973). The severity and frequency of ENSO events have increased in recent years, and the 1997-1998 mass ENSO-related bleaching event affected coral reefs in over 50 countries and resulted in 70-90% total coral mortality at many sites exposed to abnormally elevated seawater temperatures, including the Maldives, Palau, the Seychelles and the Arabian Gulf (Wilkinson 2002; Goreau et al. 2000). These are historically unprecedented coral bleaching events (Glynn 1993, 2000; Brown 1997; Wilkinson 2002; Hoegh-Guldberg 1999; Fitt et al. 2001; Lough 2000; Wellington and Glynn, 2004).

Concurrent with increasingly frequent and common ENSO events, global warming is also occurring and is generally acknowledged as resulting from recent human activities (Mann, et al. 1998; Meehl et al. 2003; Cubasch et al. 1997; Stott et al. 2000; Crowley 2000; Karl et al., 2000; Tett et al. 1999). The 2001 report from the International Panel on Climate Change (IPCC) predicted with 90% certainty that 1.4 - 5.8ºC increases over 1990 levels of global surface temperature will occur by 2100. Tropical oceans are showing the greatest increase in temperature (+0.5ºC/decade), and the increase in coral bleaching events is testimony to this trend. While many factors are involved in global warming, increasing levels of CO2 (primarily from fossil fuel combustion and deforestation) are considered to be the largest factor. The 2001 IPCC report predicts a doubling of pre-industrial CO2 levels by 2065, and the rate of increase in global CO2 since 1990 is unprecedented (Buddemeier et al. 2004).

Effects of CO2 and Seawater Carbonate on Coral Growth

Our oceans are responsible for most of the uptake of anthropogenic CO2 (Sabine et al. 2004). Increasing levels of CO2 change seawater chemistry by altering the carbonate equilibrium and saturation state of the oceans. As more CO2 enters seawater, its pH declines, affecting the carbonate buffering system. Reef growth, and reef survival, depends on the addition of calcium carbonate by corals and other calcifying reef-binders (coralline algae, etc.) at levels that exceed calcium carbonate losses by dissolution and bioersoion (Eakin 1996), although over geological time frames this may not be the "normal" state of reefs (Kleypas et al. 2001). If calcification slows, production-dominated reefs may suffer a net loss of carbonate, and reefs and even small coral islands can completely disappear. Calcification requires calcium and inorganic carbon sources (typically carbonate in seawater), although many factors may influence biogeochemical rates and processes (see this article by Randy Homes-Farley for an excellent review of calcification).

In general, calcium concentrations in seawater are about 100 times higher than carbonate concentrations, and carbon is now generally considered a limiting factor in calcification, despite the supersaturation of oceanic shallow waters with respect to calcium carbonate. With current rates of CO2 increase, tropical seawater's carbonate saturation will drop by approximately 30% with a concomitant 14-40% decrease in reef calcification (Kleypas 1999; Langdon 2000; Kleypas and Langdon 2000; Falter et al. 2001). Historical trends are very telling! A figure by Kleypas (Figure 1) indicates the changes of the carbonate state of world oceans, and Mark Eakin (with whom I had the pleasure of diving in Palau last month) produced an article (Eakin 1996) that is indicative of this change entitled, "Where have all the carbonates gone?"

Decreases in the aragonite saturation state of the oceans will tend to favor organisms that produce the more stable forms of calcium carbonate, such as calcite and high magnesian calcite. Aragonite-forming organisms, like corals, will be more subject to dissolution and bioerosion. Calcification of all groups, however, is negatively affected by reductions in the carbonate saturation of ocean waters (Feely et al. 2004). If CO2 doubles over current levels, a 10-50% reduction in calcification is likely to occur. Various mesocosm studies have confirmed this using calcareous macroalgae, other coral species, coccolithophorids, and whole mesocosm communities, with an average reduction of 28 % for all groups combined. Langdon (2003) found calcification dropping to rates that were from 50% (½) to 17%(1/6^th) of previous levels with a 160% increase of CO2 over current levels, and Marubini et al. (2001, 2003) measured significantly decreased growth in Porites compressa under conditions of a projected doubling of CO2. Direct evidence of the effects of increasing CO2 levels on calcification of various marine calcifying organisms has come mainly from aquarium studies, and of those, most come from work in Monaco and Biosphere II in Arizona (Reynaud et al. 2003; Leclerq et al. 2000, 2002; Langdon et al. 2000, 2003).

There is, however, a possible mollifying effect. Solubility of CO2 is inversely related to water temperature, so the overall effects of increased atmospheric CO2 emissions may be limited by warming temperatures, along with a reduction in the resultant pH drop (Cladeira and Wickett 2003). Drops in pH under increased CO2 concentrations have also been shown to reduce calcification (Marubini and Atkinson 1999).

Coral Reef Bleaching Events

Bleaching is a complex phenomenon that can generally be defined as a breakdown of the symbioses between the host coral polyp and its zooxanthellae, manifested as a loss of symbiotic algae or their pigments in response to a variety of stressors. Coral bleaching was first described in the early 20^th century (Vaughan 1914; Boschma 1924; Yonge and Nichols 1931a, 1931b), with the first mass coral bleaching reported following the 1982-1983 ENSO event (Glynn 1984). Densities of zooxanthellae are normally in flux, and bleaching is actually the extreme of a normal and dynamic gradient of zooxanthellae in coral tissues (Buddemeier et al. 2004). I reviewed coral bleaching in a previous article.

Although many factors may cause the characteristic signs of bleaching (Brown 1997; Coles and Brown 2001), most mass coral bleaching is related to high sea surface temperatures (Fitt at al. 2001; Wellington et al. 2001). The physiological and biochemical processes responsible for temperature-related coral bleaching, including a breakdown in photosystem II, have been fairly well-characterized (Fitt et al. 2001; Warner et al. 1996, 1999; Gates and Edmonds 1999; Jones et al. 1998, 2000).

The impact of most bleaching events worldwide has been a reduction in coral cover. Bleaching has been shown to result in greater than 90% mortality of corals during severe events (e.g. Glynn 1984; Bruno et al. 2001; Wellington et al. 2001; Aronson et al. 2000; Strong 2000). What is remarkable, though, is that in every case of which I am aware, some coral colonies, species, or areas escape the full impacts of bleaching events (Done et al. 2003; Williams and Bunkley-Williams 1988; Glynn and D'Croz 1990, Jokiel and Coles 1990; West 2001; Coles and Brown 2003). They are more resilient or somehow resistant.

Resistance to bleaching may be due to specific physiological tolerance of bleaching stressors, or a result of physical or environmental variables that reduce stresses to the symbioses between coral and zooxanthellae. Shading (clouds, turbidity, physical structures) can provide some resistance, as do fluorescent proteins (Salih et al 2000), mycosporine-like amino acids (Karentz 2001) and heat shock proteins (Downs et al. 2000). A key factor in escaping bleaching events may be the type of zooxanthellae hosted by a coral, with stress- or temperature-tolerant symbionts being more resistant to bleaching conditions (Baker 2003; LaJeunesse et al. 2003; LaJeunesse 2002; Loya et al. 2001; Warner et al. 1999).

Many environmental influences affecting bleaching susceptibility and resistance have been studied (Goreau and Macfarlane 1990; Jokiel and Coles 1990; Williams and Bunkley-Williams 1990; Glynn 1993; Brown 1997; Hoegh-Guldberg 1999; Goreau et al. 2000; Feingold 2001; Glynn et al. 2001; Riegl 2003). Any reduction in the levels of temperature and irradiance stress may limit the cellular damage that can occur during bleaching (Gleason and Wellington 1993, 1995; Wellington and Fitt 2003; Warner et al. 1999; Jones et al. 2000). Upwelling areas, deep areas, areas of strong water flow or flux (Jokiel and Coles 1990; Nakamura and van Woesik 2001), and nearshore regions with highly variable light, nutrients, salinity, and temperature provide refuge from severe bleaching (reviewed in Glynn 2001; West 2001). Nearshore, lagoonal, or turbid habitats, in particular, are interesting in that regular exposure to various stressors, and the resultant acclimatization or adaptation of corals, seem to occur there (many studies, but see Brown and Coles 2001; Craig et al. 2001).

Recovery from bleaching depends on many factors, including the levels of lipid reserves and nutrient availability to corals during stress events. Bleaching results in a nutrient deficit to coral polyps, and corals must rely on other means to meet their energy requirements. Their ability to directly absorb nutrients or capture prey or particulate material sufficiently to sustain them while algal symbiont populations recover may be the critical factor in colony recovery. Another means of recovery is termed the "Phoenix effect." Although colonies may appear completely dead, residual tissue in skeletal recesses allows for a more rapid recovery of some coral colonies (Riegl and Piller 2001). Recovery of reefs, as a whole, depends on how many bleached colonies survive, their method of reproduction, and the populations of upstream colonies that are available to recruit to the bleached reef. Sexual reproduction can be slowed or reversed after bleaching (Szmant and Gassman 1990; Michalek-Wagner and Willis 2001).

Getting up to Date on Zooxanthellae, Revised Edition

Quite a few years ago, I wrote an article on the diversity of zooxanthellae. In the time between then and now, this has become one of the hottest subjects in coral reef research. Coupled with even better molecular methods, our understanding of zooxanthellae diversity has increased greatly. The symbionts of corals, collectively termed zooxanthellae, are a diverse group (50-60 or more types/species) of photosynthetic dinoflagellates mostly from the genus Symbiodinium. Symbiont types have varying physiological attributes, with different tolerance limits for elevated temperature, stress, and irradiance within the six or seven clades (LaJeunesse et al. 2003; LaJeunesse 2002; Baker 2003, 2004). Compare this to the relatively small number I reviewed in the article not that long ago.

Over a decade ago, Buddemeier and Fautin (1993) proposed the "Adaptive Bleaching Hypothesis" (ABH), whereby corals could potentially adapt to moderate bleaching or stress by shuffling their zooxanthellae. This hypothesis was recently reviewed in Buddemeier et al. (2004). Critics argued that bleaching and the sometimes massive resultant mortality could not be considered adaptive, and also that adaptation necessarily involved gene flow (Hoegh-Guldberg et al. 2002; Coles 2001; Coles and Brown 2003). However, Buddemeier et al. (2004) refer to the biological adaptedness of the coral/zooxanthellae association, rather than the ecological or evolutionary definition. This hypothesis is rapidly gaining support. Although some coral species appear inflexible in their associations, with a "one-host, one-symbiont" relationship, it is becoming well recognized that considerable flexibility exists between many coral species and a pool of potential zooxanthellae types (Kinzie et al. 2001; Baker 2001, 2004; Toller et al. 2001a, 2001b; Little et al. 2004). Such flexibility may, in fact, be the norm for many species. The more "adaptive" strains are not necessarily acquired from the environment, but may exist in small numbers within many coral colonies. Loss of one type during bleaching could simply allow for an increase in the population of the more well-adapted strains. Coral populations and even reef structure may well hinge on the relative numbers of flexible and inflexible species. How meaningful and common transient "strain swapping" is to reefs under rapidly changing conditions is yet to be fully understood.

Summary

What is the future of coral reefs under increasing thermal stress, rising CO2 and reduced calcification? The number, extent, and severity of bleaching events will almost certainly worsen with future increases in sea surface warming. The future survival of corals on reefs is difficult to predict, although some genera (e.g. Acropora) are widely acknowledged to be far more sensitive than others to environmental stress (Baird and Marshall 2002); studies exist on the variability of resistance among species (Stimson et al. 2002; Marshall and Baird 2000). Over the long term, only those corals tolerant enough to endure will survive to reproduce (Glynn et al. 2001), but even this may not be adequate to compensate for very severe conditions such as those that occurred during and after the 1997-1998 ENSO event (Riegl 2003, 2004). However, it's possible that the distribution of reefs will change, occurring and forming in higher latitudes or deeper waters (Precht and Aronson. 2004; Done 1999; Veron 1992).

As CO2 levels continue to increase (with the resultant decrease in calcification), corals will grow more slowly and would be expected to be less competitive for space. Increased carbonate dissolution rates and bioerosion will result in more fragile skeletons, likely producing colonies more susceptible to damage or disease. Reef growth would slow as a whole, and some reefs may change from accreting calcium carbonate and growth to experiencing a net loss of calcium carbonate and recession. In the worst scenario, some reefs may be lost entirely. Similar losses of reef-binding calcifiers could also reduce the structural integrity of coral reefs.

Another possible effect of increased CO2 is an increase in phytoplankton. Resulting "greenwater" would decrease in the light available for corals, further decreasing calcification rates, although the reduced irradiance might also limit bleaching. Rising CO2 could also favor the growth of competing macroalgae, already dominant on many reefs around the globe and especially in the Caribbean. The ongoing problem of over fishing on herbivores only compounds the problem.

It is highly likely that significant changes to coral reefs will continue to occur at an increasing rate. Increasing CO2 and seawater temperatures are only two of many threats reefs currently face. Whether reefs are resilient enough to survive a myriad of additional impacts is uncertain. The most probable scenario is that global climactic change and increasing CO2 will strongly affect coral reef systems, having variable but often synergistic effects with other stressors. The results will almost certainly be deleterious, and, in some cases, disastrous. Coastal areas will probably suffer the most, while remote oceanic reefs will be spared some of the coastal-based stresses.

There is a lot of uncertainty over the short-term and even long-term persistence of coral reefs, even if they are unlikely to become extinct as ecosystems. Corals and coral reefs have persisted over geological time frames and they probably will persist long after humans have vanished. But, it is in our best interest, and in the interest of future generations, to act in earnest regarding our contributions - whether they are in the interest of conservation or potentially contributing to their demise.

References

I have left many additional references intact for those who are interested in further readings regarding climate change science.

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