How Gaia and Coral Reefs Regulate Ocean pH

Although some researchers have raised concerns about possible negative effects of rising CO2 on ocean surface pH, there are several lines of evidence demonstrating marine ecosystems are far more sensitive to fluxes of carbon dioxide from ocean depths and the biosphere’s response than from invasions of atmospheric CO2. There is also ample evidence that lower pH does not inhibit photosynthesis or lower ocean productivity (Mackey 2015). On the contrary, rising CO2 makes photosynthesis less costly. Furthermore in contrast to researchers arguing rising atmospheric CO2 will inhibit calcification, increased photosynthesis not only increases calcification, paradoxically the process of calcification produces CO2 and drops pH to levels lower than predicted by climate change models. A combination of warmer tropical waters and coral reef biology results in out-gassing of CO2 from the ocean to the atmosphere, making coral reefs relatively insensitive to the effects of atmospheric CO2 on ocean pH.

Sixty million years ago proxy evidence indicates ocean surface pH hovered around 7.4. If surface pH was in equilibrium with the atmosphere, then CO2 concentrations would have hovered around 2000 ppm, but there is no consensus that CO2 reached those levels. However as will be discussed, there are biological processes that do lower surface pH to that extent, despite much lower atmospheric CO2 concentrations.

Over the next 40 million years corresponding with the rearrangement of the continents and ocean currents, the formation of the Antarctic Circumpolar Current and initiation of Antarctic glaciers, the evolutionary expansion of diatoms and their increasing abundance (diatoms are the most efficient algae for exporting carbon to ocean depths), ocean carbonate chemistry was greatly altered. As a result ocean surface pH gradually rose above pH 8. Then for our last 20 million years, ocean surface pH has fluctuated within this new equilibrium between 8.4 and 8.1, as seen in Figure 1 below (Pearson and Palmer 2000). For the past 400,000 years, pH rose to about 8.35 during the depths of each ice age. Then during each warm interglacial period, when both land and marine productivity increased, pH fell to ~8.1 (Honisch 2005).

60 million years of ocean pH

Although it is commonly assumed atmospheric CO2 and ocean surface pH are in equilibrium, studies examining various time frames from daily and seasonal pH fluctuations (Kline 2015) to the millennial scale transitions from the last ice age to our warm interglacial (Martinez-Boti 2015), demonstrate surface ocean pH has rarely been in chemical equilibrium with atmospheric CO2. Because oceans contain over 50 times as much CO2 as the atmosphere, surface pH is more sensitive to changes in the rates of upwelling of low-pH, carbon-rich deep waters. It is the response of photosynthesizing organisms and the food webs they support that largely determines how much carbon is sequestered in the surface layers and then sent to deeper waters (the biological pump).

As discussed in an earlier essay, the “biological pump” modulates how much CO2 is sequestered and how much CO2 will out-gas to the atmosphere. It has been estimated that without the biological pump, pre-industrial atmospheric CO2 would have out gassed and raised atmospheric CO2 to 500 ppm, instead of the observed 280 ppm. Ironically the processes that build coral reefs also increase surface CO2 concentrations and lower regional pH to levels lower than expected by equilibrium with atmospheric CO2. This biological control of the earth’s chemistry is the essence of Gaia theory.

Gaia theory stimulated great scientific interest (as well as controversy) since the 1970s, and stimulated more extensive investigations into how the biosphere affects the earth’s chemistry. Gaia’s founding scientist James Lovelock formulated Gaia theory while working for NASA seeking chemical signatures of life on other planets. For example, due to living organisms our atmosphere maintains about a 21% concentration of oxygen. Without photosynthesizing organisms, the atmosphere would contain extremely low amounts of oxygen. Thus Lovelock argued, “if life has merely a passive role in cycling the gases of the air, then the concentrations will be set by equilibrium chemistry; in fact they most certainly are not.” Shedding the mystical connotations that many “New Age” adherents attributed to Gaia, several universities have now created departments studying Gaia’s effects, but under less anthropomorphic titles such as Earth System Sciences or Biogeochemistry.

Unfortunately Gaia is often misrepresented as a conscious super-being deserving of religious devotion, with some adherents even advocating Gaia should replace the earth’s major religions. Gaia’s deification was resented both in established religious circles, and by Gaia’s scientific proponents like Dr. Lynn Margulis. She stressed Gaia is simply “an emergent property of interactions among organisms". Or as one of her graduate students suggested, Gaia is simply “symbiosis as seen from space”.

Gaia theory also weighed in on climate change debates and was advocated by Al Gore and climate scientists such as Stephen Schneider. While basic Gaia theory simply argues a variety of biological interactions provide negative feedbacks from which a degree of self-regulating homeostasis emerges, those with a more alarmist view of the earth’s changing climate argued those self regulating processes had been pushed to a disastrous tipping point by rising CO2.  In contrast climate skeptics like world-renowned physicist Freeman Dyson also embraced the concepts of Gaia as a “great force for good” uniting people to save natural habitat and endangered species. But Dyson also bemoaned, “I am horrified to see the environmental movement hijacked by a bunch of climate fanatics, who have captured the attention of the public with scare stories.”

Despite Lovelock’s belief that life regulates earth’s chemistry via a variety of negative feedbacks, his logic was at first swayed by those CO2 scare stories. In a more fearful state of mind Lovelock published books like “The Revenge of Gaia” and in newspaper interviews predicted fast-approaching, global-warming doom stating, “Billions of us will die” and only the “few breeding pairs of people that survive will be in the Arctic”.

More recently however Lovelock recanted stating, “I was 'alarmist' about climate change & so was Gore!” 'The problem is we don't know what the climate is doing. We thought we knew 20 years ago”.

Putting politics and religion aside, the Gaia perspective provides a valuable framework that incorporates the biosphere as a critical active player in global climate and chemical cycles. And only from that framework can we fully account for oscillations in the oceans’ pH on daily, annual, decadal and millennial timeframes.

pH in a Lifeless World

Global climate models, such as used by Caldeira and Wickett 2005, estimated that ocean pH has dropped by (0.09 pH) from 8.2 to ~ 8.1 since preindustrial times due to rising anthropogenic carbon dioxide emissions. They then predicted a further pH drop of 0.3 to 0.4 by 2100 as emissions increase. This claim has been cut and pasted into nearly every journal article that hypothesizes an impending catastrophe driven by “ocean acidification”. However an average pH of 8.1 is typical for interglacial periods such as the one we are now experiencing.  But more importantly Caldeira and Wickett’s modeling experiments only examined geochemical processes and erroneously assumed 1) ocean surface CO2 is in equilibrium with the atmosphere; and 2) the biosphere was a neutral participant.  Caldeira’s model was based on their non-Gaia assumption that ocean surface pH is “affected only by air-sea fluxes and directly injected carbon.”  Indeed, if sequestration of CO2 by photosynthesis is immediately offset by the release of CO2 in the surface layers via respiration, then such an assumption may hold some validity. However that is never the case. And according to the IPCC if there were no biological pump transporting carbon to the ocean depths, oceans would now be experiencing an 8.0 pH.

Relationship between Atmospheric CO2 and Ocean pH

As seen in the graph above from Cohen and Happer models that suggest ocean pH should have declined over the past 150 years as atmospheric CO2 concentrations rose are supported by an abiotic chemical analysis. Modulated by ocean alkalinity, at 400 ppm atmospheric CO2, surface seawater declines to pH 8.2 or 8.1 (blue curve).  For un-buffered rainwater (or river outflows without buffering) pH drops to 5.5 (red dashed curve). However even without any modulating biological effects, the graph suggests a degree of chemical homeostasis where increasing CO2 concentrations have an increasingly smaller effect on ocean pH. For example when CO2 concentrations increase from 0 to 100 ppm, pH rapidly drops from over 11.0 to 8.7. In contrast a quadrupling of atmospheric CO2 since pre-industrial times (~250 to 1000 ppm) would only lower ocean surface pH from 8.3 to 7.9 (blue curve). Counter-intuitively the different dissolved CO2 species exert strong buffering effects. Furthermore far from being catastrophic, not only is a pH range between 8.4 and 7.7 experienced daily in thriving coral reefs, that range appears to be an optimal balance that supports both photosynthesis and calcification!

Extreme views by researchers like Hoegh-Guldberg (2014) have speculated 95% of the coral will be lost by 2050, and he argues our current high levels of CO2 are creating conditions coral have not experienced for millions of years. Yet in terms of pH (and temperature) such “scientific” claims are pure nonsense. First a modeled average surface pH tells us very little about the pH that directly affects marine organisms locally. Due to the counteracting effects of photosynthesis, respiration and calcification, coral reefs can experience a pH hovering around 8.5 or higher during the day followed by a low pH of 7.8 or lower at night. Kline 2015 acknowledged, “As with many other reefs, the nighttime pH minima on the reef flat were far lower than pH values predicted for the open ocean by 2100.” Elsewhere researchers concluded that in addition to atmospheric pH, the complex interactions controlling pH especially in coastal zones, make detection of any trends towards acidification “not trivial and the attribution of these changes to anthropogenic CO2 emissions is even more problematic.” (Duarte 2013)

Why More Acidic Conditions Benefit Photosynthesis

Shallow-water reef-building corals are able to thrive in low-nutrient tropical waters via their symbiosis with a genus of photosynthesizing algae (discussed here.) In order to sustain photosynthesis, corals actively pump hydrogen ions (H+) into the vesicles encapsulating their algal symbionts. This lowers its internal pH to truly acidic levels between pH 4 and 5  (Barott 2015). This increases H+ concentrations up to 10,000 times greater than any theoretical contributions to surface waters by atmospheric CO2. If coral do not acidify their symbionts’ surroundings, the limiting supply of CO2 would dramatically decrease the rate of photosynthesis.

Why does an acidic environment benefit photosynthesis?

To understand the benefits of corals’ purposeful acidification, we must first review how CO2 reacts when dissolved in water. Dissolved CO2 can take 3 forms (or “species”) collectively referred to as Dissolved Inorganic Carbon (henceforth DIC):

1) Carbonic acid (H₂CO₃),

2) Bicarbonate ion (HCO₃^-) after losing one H+

3) Carbonate ion (CO₃^-2) after losing a second H+ .

When CO2 first dissolves, a small proportion bonds to water molecules and forms a weak carbonic acid (H₂CO₃). But the bond is weak causing carbonic acid to convert back and forth with its CO2 form so rapidly, most researchers treat these two forms as the same chemical species.  Carbonic acid is a weak acid, and weak acids are critical buffering agents for most living organisms precisely because its species can rapidly and reversibly change form. Carbonic acid and phosphoric acid are the 2 most critical buffering agents for maintaining a narrow pH range in humans and other animals. In the form of carbonic acid, water’s 2 H+ ions can more easily detach to form bicarbonate and carbonate ions when pH rises. Buffering happens because those added H+ ions counteract a rising pH. (Higher pH means lower H+ concentrations.) Conversely when pH falls (Lower pH means higher H+ concentrations), the excess H+ ions recombine with and are sequestered by any existing carbonate and bicarbonate ions to counteract the falling pH.

Figure 2 illustrates how changes in pH alter the species composition of DIC. For example during photosynthesis CO2 is consumed causing pH to rise. Between pH 7.0 and 8.6, over 90% of the dissolved CO2 naturally converts to bicarbonate ions (HCO₃^-). But bicarbonate ions cannot be directly used in photosynthesis. Photosynthesizing organisms can only use CO2. Thus if photosynthesis drives pH to 8.2 or higher, the requisite CO2 species approach zero. In addition to competing for a dwindling supply of CO2, photosynthesis consumes the limited supplies of nutrients. Thus photosynthesis creates negative feedbacks that inhibit additional photosynthesis.

The relationship between pH and proportion of CO2 species

To overcome the limiting supply of CO2, organisms like coral concentrate bicarbonate ions in compartments into which they pump H+ ions and lower the pH. As seen in Figure 2, at pH 5 or lower, 90% of the DIC converts to CO2. Once bicarbonate ions are imported and concentrated, the conversion to CO2 is also accelerated by the ubiquitous enzyme carbonic anhydrase. However bicarbonate ions cannot simply diffuse into a cell or pass through internal membranes. The ions must be pumped. However pumping and concentrating those ions requires transporters and an expenditure of energy. In contrast whenever surrounding waters experience a lower pH, it makes CO2 more available so that the energy expenditures drop because CO2 freely diffuses into cells and through membranes.

The same carbonate chemistry reactions that provide more CO2 for photosynthesis also explain how some pharmaceutical antacids work and how DIC buffers ocean pH. Bicarbonate is a common ingredient in antacids like Alka-seltzer. When H+ ions increase due to acid indigestion, ingested bicarbonate ions rapidly bond to H+ to form CO2 gas, which can then be carried away by the blood or by a good belch. Likewise when ocean concentrations of H+ ions increase, they more readily bond to the bicarbonate and carbonate ions to minimize the drop in pH and form more CO2, which can be quickly utilized during photosynthesis.

However below pH 7.0, nearly all carbonate ions  (CO₃^-2) will be converted to bicarbonate (HCO₃^-), so that carbonate ions no longer serve as buffering agents. (CO₃^-2  + H+ forms HCO₃^- ). However in coral reefs, that loss of buffering capacity at lower pH is counteracted to a degree by increased dissolution of calcium carbonate minerals. Dissolution of calcium carbonates counter-intuitively absorbs CO2 and releases carbonate ions to increase the water’s buffering capacity, thus exerting a negative feedback that tries to raise pH (Morse 2007). Nonetheless the concept that a lower pH reduces the concentration of carbonate ions evoked climate fears amongst some researchers who incorrectly believed calcifying organisms require carbonate ions.  But research shows no such requirement. All calcifiers use the more abundant bicarbonate ions and bicarbonate ions will be plentiful even if pH unrealistically fell to 6.0

Outside of coral reefs, other marine ecosystems also benefit from lower pH. For example diatoms now account for 40% of the world’s ocean primary productivity and flourish in upwelling waters that bring abundant CO2 and DIC from the ocean’s dark depths into sunlit surface regions. Although this upwelling deceases surface pH and provides more CO2, diatoms still rely on bicarbonate transporters and carbonic anhydrase to ensure an adequate supply of CO2 for photosynthesis. Hopkinson et al. (2011) calculated a doubling of ambient CO2 levels would save diatoms ~20% of the energy they expended on importing bicarbonates. Globally different photosynthesizing organisms have demonstrated a variety of responses to rising CO2 but altogether there appears to be few negative effects on photosynthesis due to elevated CO2 and depending on the species small to large benefits (Mackey 2015).

The Omega Myth

In a lifeless ocean when carbonate ions rise to a certain concentration, they react with ever-present calcium ions to form calcium carbonate minerals like aragonite and calcite. Those minerals are used to make shells, skeletons and reefs. If carbonate ion concentrations are lower, calcium carbonate minerals are more likely to dissolve. When there is a balance between formation and dissolution of those minerals, the water is said to be saturated with respect to that mineral, and saturation is represented by the omega symbol (W). The oceans are currently oversaturated with respect to calcium carbonate minerals, but some researchers became fearful that a falling pH could lower the supply of carbonate ions, and eventually drive the ocean’s saturation point so low that calcium carbonate minerals will dissolve faster than they form. However biologically controlled calcification reveals that simple metrics of chemical equilibriums and saturation points do not accurately demonstrate the biologically controlled calcification process. In that regard several researchers have now published evidence demonstrating the “Omega Myth”.

First biologically controlled calcification does NOT depend on, or directly utilize seawater carbonate ions. Nor does calcification depend on observed saturation states of the oceans (Maranon 2016). Transporters are required for carbonate ions to cross any membrane, but no carbonate transporters have ever been detected. Instead, as with photosynthesis, calcifiers actively uptake the more abundant bicarbonate ions and concentrate them in compartments. Most calcifying organisms have evolved mechanisms to “up-regulate” their internal pH by pumping H+ ions out of the compartment and raising internal pH. In addition pumping  H+ ions out of the calcifying compartments is beneficial because it maintains an electrical gradient that facilitates importing calcium ions (Ca++) into the calcifying compartment. With a higher internal pH, bicarbonate sheds an H+ and converts into carbonate ions and when concentrated in the presence of concentrated Ca++, calcium carbonate minerals readily form.

Although in some species photosynthesis and calcification compete for bicarbonate ions, photosynthesis generally benefits calcification by providing energy, and by raising external pH, which lowers the cost of pumping internal H+ ions to the surrounding waters. In addition on a per molecule basis, the cost of calcification requires less than 1% of the energy produced by photosynthesis (McCulloch 2012). Accordingly numerous studies have reported that greater rates of photosynthesis correlate with greater rates of calcification. The same holds true for other calcifying organisms. For example across the tropical ocean, the ratio of net calcification to net photosynthesis for coccolithophores remained constant despite regions of widely varying surface pH and calcite saturation levels (Maranon 2016).

Past hypotheses arguing calcification was dependent on carbonate ion concentration, or aragonite and calcite saturation levels, were most likely misled by the fact that higher carbonate ion concentrations are a daily “side effect” of photosynthesis. It is the rate of photosynthesis and the energy it provides that typically controls calcification rates. And as reported in the discussion on the coral adaptive bleaching hypothesis, coral are always shifting and shuffling their symbionts to maximize photosynthesis to best adapt to changing local microclimates. The bigger threat to coral photosynthesis is heavy sediment loads from disturbed landscapes that can block the sun and suffocate polyps. 

How Calcification Lowers pH more than Atmospheric CO2

Strangely enough, although some researchers fret higher CO2 concentrations will reduce calcification, it is the very process of calcification that results in the “alkalinity pump.” Calcification removes buffering bicarbonate and carbonate ions from the surface and pumps them to the deep. Calcification also releases CO2 in the surface waters and in combination with less buffering capacity, lowers pH to a much greater extent than possible by surface exchanges with rising atmospheric CO2.

Assuming the modeled background pH of 8.1, and if all else is equal, we would expect pH to rise during the day due to photosynthesis and then fall back to pH 8.1 at night due to respiration. As seen in the graph below for daily (diel) pH values on Heron Island in the Great Barrier Reef (from Kline 2015), coral reefs rarely spend any time at Caldeira’s modeled pH value of 8.1. When photosynthesis and carbonate dissolution outweigh respiration and calcification, surface pH can rise to 8.4 or higher as would be expected. Furthermore when surface pH is above 8.1, the concentration of surface CO2 is lower than atmospheric CO2, and this difference allows CO2 to diffuse into the ocean.  However any absorbed CO2 is quickly sequestered into organic molecules via photosynthesis during which surface pH remains high and never comes into equilibrium with atmospheric CO2 during the day.

Daily Changes in pH on Heron Island Great Barrier Reef

Conversely without photosynthesis, nighttime respiration and calcification increase surface CO2 concentrations and lower pH. Reefs benefit because those processes replenish the depleted CO2 required for photosynthesis on the following day. Furthermore if more organic molecules are formed and sequestered than subsequently respired, we would expect surface pH to remain above 8.1. Indeed photosynthesis produces a large reservoir of dissolved and particulate organic molecules that may persist for decades, centuries, and millennia. When those stored molecules eventually return to the surface, pH can be lowered due to respiration of ancient carbon, independent of atmospheric CO2. Other organic molecules are also formed that resist decomposition for millions of years. And molecules like DMS are out-gassed to the atmosphere where they serve as cloud condensation nuclei and inhibit further warming of ocean surface temperatures.

Thus due to long-term sequestration of CO2 that exceeds respiration we would expect surface pH to remain above 8.1 for the short term. However due to the release of CO2 during calcification, reef pH drops far below 8.1. Calcification infuses the surface waters with an excess of CO2 largely driving the nighttime pH down as low as 7.7.  Furthermore at a pH below 8.1, CO2 concentrations in the ocean’s surface rise higher than the atmosphere’s, and this results in nighttime out-gassing of CO2. Instead of CO2 invading the ocean and affecting coral, overall measurements show coral reefs are net sources of CO2 from the ocean to the atmosphere. Similar dynamics from calcifying coccolithophores likewise promotes CO2 fluxes from the open ocean, and inhibits uptake from the atmosphere. Again as Gaia predicts, biological processes control carbonate chemistry and when or where atmospheric CO2 enters or leaves the ocean.

Although studies in the waters around Hawaii (Dore 2009) reported an increasing trend in DIC that was “indistinguishable” from what rising atmospheric CO2 predicts researchers observed, “Air-sea CO₂ fluxes, while variable, did not appear to exert an influence on surface pH variability. For example, low fluxes of CO₂ into the sea from 1998–2002 corresponded with low pH and relatively high fluxes during 2003–2005 were coincident with high pH; the opposite pattern would be expected if variability in the atmospheric CO₂ invasion was the primary driver of anomalous DIC accumulation.”  However that observed pattern is exactly what we would expect to arise from biological effects.

Furthermore oscillating decadal trends in wind strength can further magnify biological effects causing pH to trend independently of atmospheric CO2. CO2 generated by calcification does not completely outgas and thus changes in the rate at which reefs are flushed with open ocean water will modulate how calcification affects surface pH. In contrast to Caldeira’s “lifeless” pH models that suggest pH has dropped from 8.2 to 8.1 since preindustrial times, a study of pH since 1700 AD on Flinder’s Reef in the Great Barrier Reef concluded pH has oscillated between 8.15 and 7.9 every 50 years. During a positive Pacific Decadal Oscillation and El Nino years, trade winds slowed and reduced the flushing rate of the reef. As a result there was a build up of CO2 released from calcification and average pH dropped pH to 7.9. When winds increased during a negative PDO and more La Ninas, the reef was flushed and pH rose to 8.15. Several studies have linked changes in pH driven with multidecadal oscillations.

For example examining surface pH in the Sargasso Sea Goodkin 2015 reported, “from 1950 to 1996, when surface ocean pHs are predicted to decline more rapidly due to anthropogenic CO2 emissions, pH at Bermuda increases in response to a declining AMO.”  They concluded, “ocean pH does not simply reflect atmospheric CO₂ trends but rather that circulation/biogeochemical changes account for >90% of pH variability in the Sargasso Sea and more variability in the last century than would be predicted from anthropogenic uptake of CO₂ alone.”

Similarly Yeakel 2016 reported Bermuda reefs experienced a drop in pH in association with a negative NAO that caused westerly winds to move further south and generate a deeper winter mixed layer just to the north of the Bermuda reefs. Deeper mixing brought more DIC to the surface layers and promoted greater plankton blooms. The resulting organic particles and zooplankton that fed on the blooms, then circulated over the Bermuda reef. The resulting increase in respiration and calcification caused an  “acidification event”.

Thus to reliably distinguish multidecadal trends in pH driven by ocean oscillations, upwelling and deeper surface mixing versus trends due to rising atmospheric CO2, it will require 60 to 100 years of observation; far longer than any data series to date.

Ocean Surface pH is More Sensitive to Ventilated CO2 Stored at Ocean Depths

Published estimates of anthropogenic CO2 now stored in the upper ocean layers and affecting pH has been based on “the assumption that ocean circulation and the biological pump have operated in a steady state since preindustrial times” (Sabine 2010). The problem is such assumptions are faulty and misleading. The biological pump and ocean circulation are not in a steady state. Regional upwelling has increased since the Little Ice Age (Gutiérrez 2009) and during the past 3 decades (Varela 2015). Multidecadal changes in hurricane frequency and intensity affect upwelling. Changes in surface winds due to El Nino and La Nina, the North Atlantic Oscillation and Pacific Decadal Oscillation affect upwelling (Ishii 2002). Coastal and equatorial upwelling bring an enormous amount of DIC to the surface, with subsequent transport to the gyres of the open ocean, causing declines in open ocean surface pH at rates that are much faster than possibly attributed to atmospheric diffusion.

While 50% of the sequestered carbon formed during photosynthesis is respired before sinking into the dark depths, a tremendous pool of dissolved organic carbon has been created that may not be respired for decades, centuries or millennia and slowly contributes to the pool of DIC at various depths and locations (Giorgiou 2002). This further complicates any attribution of trends in surface pH. For example upwelling of stored CO2 is believed to have been the main driver of the rise in atmospheric CO2 and the fall in ocean surface pH during the transition from the glacial maximum to our interglacial.

As discussed in the article on natural cycles of ocean “acidification”, and illustrated in the graph below by Martinez-Boti, over the past 15,000 years proxy data (thick lines) has determined surface pH has rarely been in equilibrium with expectations (green line) based on models driven by atmospheric CO2. As illustrated, surface pH was more sensitive to the upwelling of subsurface DIC. The venting of stored carbon led to a drop in average regional pH from the 8.3 during glacial times to a pH fluctuating between 8.1 and 8.2 during our current interglacial.

Difference between ocean surface pH and modeled pH from atmospheric CO2

The mechanisms that lowered surface pH to 8.3-8.4 during the Last Ice Age is a matter of considerable debate, but clearly more carbon was being sequestered at depth and less carbon was being pumped to the surface. Several authors have reported less upwelling during the Ice Age. While colder temperatures and less upwelling would reduce rates of photosynthesis, colder temperatures also reduce rates of respiration and calcification. A lower rate of respiration would allow more organic carbon to sink to deeper depths before being completely consumed. Sinking to deeper depths prevents a quick return to the surface during winter mixing or mild upwelling.

It has also been speculated that the loss of coral reefs during the last Ice Age contributed to the higher pH. Research has estimated that during the cold nadir of each ice age, coral reef extent was reduced by 80% and carbonate production was reduced by 73% relative to today. Lower calcification rates would reduce the alkalinity pump, reduce surface CO2 and increase the buffering capacity of surface waters. Conversely the growth of coral reefs as the earth warmed and sea levels rose would contribute to rising CO2 concentrations and falling pH. Vecsei 2004 concluded, “The pattern of reef growth that emerges suggests that emission of CO2 resulting from carbonate production was important particularly during the late stages of deglaciation.”

Overall observations of the effects of photosynthesis and calcification reveal coral reefs are not victims of a fall of pH from 8.2 to 8.1 pH as suggested by Caldeira and Wickett 2005, Doney 2009 or Hoegh-Guldberg (2014). 

On the contrary as Gaia theory would suggest, coral reefs are actively regulating surface pH.

The Coral Bleaching Debate: Is Bleaching the Legacy of a Marvelous Adaptation Mechanism or A Prelude to Extirpation?

A Warm Evolutionary Legacy

Despite increasing confirmation of the Adaptive Bleaching Hypothesis and its ability to explain coral resilience, most people are unaware of its debate within the scientific community. The ability to rapidly adjust to changing environments by modifying their symbiotic partnerships has been the key to their success for millions of years. As one expert wrote, the “flexibility in coral–algal symbiosis is likely to be a principal factor underlying the evolutionary success of these organisms”.

Our modern day reef-building corals first evolved in exceedingly warm and stable climates when deep ocean temperatures were 10°C higher than today and palm trees dotted the Antarctic coast. As ice caps began to form in Antarctica ~35 million years ago sea levels fell and warm epi‑continental seas dried. After ocean depths had cooled for another 30 million years, Arctic ice caps began to form and the earth entered an age with multiple episodes of glacier advances and retreats causing sea levels to rise and fall. Just eighteen thousand years ago during the last glacial maximum, all our shallow reefs did not exist, as sea levels were 400 feet lower than today.

The 35 million year cooling trend increasingly restricted reef-building corals to more tropical latitudes where winter water temperatures remain above 16 to 18 °C. As their evolutionary history would predict, today’s greatest concentrations and greatest diversity of corals are found in the earth’s persistently warmer waters, like the Indo-Pacific Warm Pool. Likewise species inhabiting our warmest waters have undergone the fewest episodes of severe coral bleaching. Given their evolutionary history, coral’s greatest achievement has been enduring bouts of sustained climate cooling and rapid temperature swings. Even during warm interglacials coral battled cold temperatures dips. Studies of 7000-year-old fossil coral reefs in the South China Sea revealed high coral mortality every 50 years due to winter cooling events. Indeed most researchers believe past coral extinctions were most commonly due to cold events. Accordingly research has estimated that during the cold nadir of each ice age, coral reef extent was reduced by 80% and carbonate production was reduced by 73% relative to today.

Holocene Thermocline Temperatures in Indo Pacific warm Pool

As the last ice age ended, coral expanded their range with warming temperatures. At the peak of the Holocene Optimum 10,000 years BP  (Before Present), coral adapted to tropical ocean temperatures in the heart of the Coral Triangle were 2.1 °C warmer than today. As illustrated above, temperatures cooled since then but frequently spiked or plummeted by 2 to 3 degrees over the course of a few centuries. One thousand years ago during the Medieval Warm Period, coral thrived in Pacific water masses that were ~0.65° warmer than in recent decades, then cooled ~0.9°C by the 1700s. Given coral’s evolutionary history, it is unlikely coral were better adapted to 1800s Little Ice Age temperatures versus Medieval Warm Period or 20^th century temperatures.  Emerging research now suggests coral bleaching has been an integral part of corals’ adjustment mechanisms to an ever-changing environment.

Coral Mortality and Resilience

There are 4 widespread misconceptions about bleaching propagated by tabloid media hyping climate doom and researchers like Hoegh-Guldberg, that I correct here:

1      Bleaching is not always driven by warming temperatures 

2      Bleaching is not responsible for most coral mortality.

3      Coral can rapidly respond to disturbances and replace lost cover within a decade or less.

4      Bleaching, whether or not it results in coral mortality, is part of a natural selection process from which better-adapted populations emerge.

1.  Multiple Causes of Bleaching

In contrast to researchers like Hoegh-Guldberg who emphasizes coral bleaching as a deadly product of global warming, bleaching is a visible stage in a complex set of acclimation mechanisms during which coral expel, shift and shuffle their symbionts, seeking the most beneficial partnership possible. Bleaching can be induced by stressful interactions between temperatures, disease, heavy rains, high irradiance from clear skies and competition with seaweeds. Indeed abrupt warm water events like El Nino have induced widespread bleaching and high mortality. But cold winters or La Nina induced upwelling of colder waters have also induced bleaching.

NOAA has also contributed to these misconceptions by overemphasizing just warm-event bleaching. On NOAA‘s web page “What is Coral Bleaching”, NOAA reported, “the U.S. lost half of its coral reefs in the Caribbean” in one year due to warmer waters. But the Caribbean’s main cause of lost reefs was due to an outbreak of the White Band disease in 1981-82. White band specifically targets members of the genus Acropora, like the Staghorn and Elkhorn coral, reducing by 80% of their cover that once dominated the Caribbean reefs. However since the mid 80s experts reported coral cover has changed relatively little.

NOAA also downplayed cold temperature bleaching stating the 2010 cold event just “resulted in some coral death.” However NOAA’s statement stands in stark contrast to coral experts who reported the January 2010 cold snap was the worst coral bleaching and mortality event on record for Florida’s Reef Tract. They reported, “the mean percent coral mortality recorded for all species and subregions was 11.5% in the 2010 winter, compared to 0.5% recorded in the previous five summers, including years like 2005 where warm-water bleaching was prevalent.” Globally there has been an increase in observed cold bleaching events and 2010 was Florida’s first cold bleaching since the 1970s. Globally there have been several more reports of cold induced bleaching and then recovery as the waters warmed. 

There is a perception that bleaching suddenly became more common only since the 1980s, leading some to speculate bleaching is due to rising CO2 and global warming. However, whether warming since the Little Ice Age is natural or anthropogenic, warming does not explain the increased observations of cold bleaching. More frequent observations of bleaching events may be partially due to the advent of remote sensing satellites that have allowed greater global coverage only since the 1980s. Furthermore determination of bleaching severity and mortality requires teams of divers to ground truth satellite data and fine-tune percentages of affected reefs. But SCUBA diving only became possible in the decades after Jacques Cousteau invented the Aqualung in the 1940s. Although natural rates of warming during the 30s and 40s were similar to today, coral reef studies were also hampered by the unsafe battleground between Japan and the Allies. War-time efforts such as the Battle of the Coral Sea, and fights to control the islands of Peleliu, Midway, Iwo Jima, the Philippines, or subsequent nuclear testing on the Bikini Atoll. The resulting reef devastation likely obscured any natural bleaching events.

We now know bleaching regularly happens due to seasonal fluctuations between high solar irradiance and warm temperatures of summer versus lower irradiance and cooler temperatures in winter. High irradiance can damage the corals’ symbiotic algae when photosynthesis runs too rapidly, while low irradiance detrimentally reduces photosynthetic output. Thus coral undergo natural adjustments to seasonal changes by expelling a portion of their symbiotic algae in summer. This leads to temporary or partial bleaching. Low light and colder temperatures slow photosynthesis, so coral increase their symbiont density in winter.

Similarly in response to changes in sunlight, the same species will alter their symbiotic partnerships as irradiance declines at increasing depths or when and where water turbidity alters irradiance. Bleaching is often temporary and mild as coral shuffle and switch their symbiotic algae in order to adapt, but sustained extremes, warm or cold, can prolong bleaching and starve the coral. Whether coral die or not depends on how quickly new symbionts are acquired relative to how much energy the coral has stored, or coral’s ability to feed on plankton as an alternative energy source.

All recent global bleaching events have been driven by El Nino events. The 1998 El Nino caused widespread mortality, an estimated 16% globally. Observed bleaching in response to warm tropical waters invading cooler regions aroused fears that climate change had contributed to this “unprecedented” event. However researchers have noted the relationship between warmer ocean temperatures and “bleaching has been equivocal and sometimes negative when the coolest regions were not in the analyses.” In other words coral living in the warmest waters were well acclimated to the warmest waters redistributed by an El Nino. Furthermore mortality did not always occur during periods with the warmest temperatures, but during the winter or ensuing cold La Nina conditions. Such observations suggest the rapid swings between anomalously warm El Nino and anomalously cold La Nina conditions are the most stressful.

Stressful rapid temperature variations due to El Nino events have occurred throughout the past 10,000 years. As illustrated below from Zhang 2014, the frequency of El Ninos during the past century has been neither extremely high, nor extremely low. Most living coral species have survived over a million years of climate change and have endured the extreme El Nino frequencies of the past 3000 years including the Little Ice Age. El Nino events are a function of natural ocean variability and there is no consensus regards any effect from rising CO2 on El Nino frequency or intensity. To survive extremes from past natural variability, coral species had to be extremely resilient in ways that are just now being understood.

Holocene Frequency of El Nino Events

2. Bleaching Causes the Least Mortality

Most extreme bleaching events are associated with El Ninos, but the high mortality rates are not just a function of higher temperatures. Due to associated flooding and high rainfall, the resulting change in salinity disrupts coral osmosis, which can result in coral death. Furthermore tropical storms and heavy wave action are a major cause of lost coral reefs, but storms also bring heavy rains that also induce bleaching. Although some try to link storm-related mortality to climate change, there is no evidence of an increasing trend in tropical storms. As illustrated by the pie graph from Osborne 2011, in the Great Barrier Reef the explosion of the coral-eating Crown of Thorns starfish (A. planci) and tropical storms contributed to the greatest loss of coral colonies, 70.5%. Bleaching is a very minor contributor to coral mortality, just 5.6%, and that bleaching can be induced by warm or cold temperatures, heavy rains and floods or high irradiance from anomalously clear skies.

Causes of Mortality on Great Barrier Reef from Osborne 2011

Due to coral’s symbiotic efficiency and recycling of nutrients, corals dominate in nutrient-limited tropical waters. Normally those low nutrient conditions also prevent predators like the Crown of Thorns starfish (COTS) from rapidly reproducing because their plankton-feeding larvae typically starve. But increased inflow of nutrients due to landscape changes, agriculture run-off and sewage, has increased plankton blooms and thus the survivorship of COTS’ larvae. The ensuing population explosions of coral eating adults have decimated many reefs. COTS does not exist in the Caribbean. Instead coral there are battling bacterial diseases like white-band that can be spread by coral-eating snails. Humans have indeed tipped the balance in favor of COTS and in addition to destructive over fishing with dynamite and cyanide, those causes of coral death are the only factors we can remedy.

To understand coral resilience in the face of the variety of onslaughts, coral reefs must be seen as dynamic systems that oscillate over decadal periods, as well as centuries and millennia. Snapshots focused only on a few years when coral reefs decline misrepresents coral resilience and promotes false gloom and doom, as well as useless management plans. A long-term study of coral ecosystems of an island in French Polynesia demonstrates corals’ dynamics response to 32-years of storms, Crown of Thorns starfish and bleaching. Coral mortality is often measured as a function of the change in “coral cover”, and 45 to 50% of the healthy reef system around the island of Tiahura was covered with coral.

As illustrated below in Figure 1 from Lamy 2016, an outbreak of COTS removed 80% of the live coral cover between 1979 and 1982, reducing total coral cover to 10% of the reef. However by 1991 the coral had fully recovered. As designated by the small gray arrows at the top, three bleaching events occurred during that recovery period. Later destruction from a 1991 cyclone again reduced coral cover but again coral recovered reaching its greatest coverage of 50% by the year 2000. And again during that recovery there were 3 more bleaching events. Since 2006 the coral suffered their greatest loss due to another outbreak of COTS, quickly followed by another cyclone. High mortality promoted high seaweed cover (dotted green line) that has inhibited coral recovery. Over that time, coral bleaching was associated with periods of recovery, suggesting little if any detrimental effects. As will become clear shortly, one also could reasonably argue those bleaching events were beneficial.

Cycles of Decline and Recovery at Tiahura from Lamy 2016

3. Rapid Coral Recovery: 

Tiahura’s coral recovery periods typically required 7 to ten years, and appeared to be unaffected by the 1998 El Nino. Several other studies have reported similar recovery periods, but some locations required 10 to 20 years to fully recover. In Australia’s Great Barrier Reef (GBF), the 1998 El Nino induced above average sea surface temperatures and salinity changes for 2 months triggering massive coral losses in the reef’s upper 20 meters. At the GBF’s Scott Reef, the upper 3 meters lost 80 to 90% of its living coral and the disappearance of half of the coral genera. Yet researchers observed, “within 12 years coral cover, recruitment, generic diversity, and community structure were again similar to the pre-bleaching years.”  A similar long-term study in the Maldives observed a dramatic loss of coral during the 1998 El Nino but by 2013 the reefs also had returned to “pre-bleaching values”. Although a reef’s recovery sometime requires re-colonization by larvae from other reefs, a process known as re-sheeting or Phoenix effect can facilitate a reef’s speedy recovery. Often a small percentage of living “cryptic” polyps with a more resilient symbiotic partnership were embedded within a “dead” colony and survive extreme bleaching. They then multiply and rapidly “re-sheet” the colony’s skeletal remains.

In addition to rapid recovery of coral cover, researchers are finding bleached reefs have been increasingly less susceptible to subsequent bleaching. For example studies in Indonesian waters determined that two coral species, highly susceptible to bleaching, had experienced 94% and 87% colony deaths during the 1998 El Nino. Yet those same species were among the least susceptible to bleaching in the 2010 El Nino, with only 5% and 12% colony deaths despite a similar increase in water temperatures. Similarly, changes in resilience were observed in response to cold water bleaching in the Gulf of California. Increased resilience in response to a variety of bleaching events prompted the Adaptive Bleaching Hypothesis first proposed in 1993. The hypothesis suggests that although bleaching events are a response to stress, it creates the potential for coral to acquire totally new and different symbionts that are better suited to those stressful conditions.  Contrary to Hoegh-Guldberg’s claim that coral reef systems will “experience near annual bleaching events that exceed the extent of the 1998 bleaching event by the year 2040”, scientists are increasingly observing the exact opposite. After reefs recover from severe bleaching, colonies have evolved enhanced resilience to future bleaching.

4.  Coral Symbiosis, Symbiont Shuffling and Rapid Adaptation

Coral Polyps

A single coral colony is comprised of 100s to millions of individual “polyps” (seen above). Each polyp can be visualized as an upside down jellyfish (coral’s close cousins) with their backs cemented to a surface and tentacles extended outward to capture passing food particles, live prey, or new symbionts. However because coral live in nutrient depleted environments, in addition to filter feeding, polyps harbor single-celled photosynthesizing symbionts inside their cells. Those symbionts (aka zooxanthellae) typically provide ~90% of the coral’s energy needs. Just 40 years ago it was believed all corals were host to just one photosynthesizing symbiont, a single species from the dinoflagellate genus Symbiodinium. But thanks to technological advances in genetic sequencing, we now know a coral species can harbor several potential species or types of Symbiodinium algae, each capable of responding optimally to a different set of environmental conditions and coral physiology. As predicted by the adaptive bleaching hypothesis, improved genetic techniques have revealed a wondrously diverse community of symbionts that coral can choose from. Coral can no longer be viewed as organisms that only adapt slowly over evolutionary millennia via genetic mutation and natural selection. Coral must be seen as an “eco-species” (aka holobiont) that emerges from the synergy of the coral and its varied symbionts.  And we now know those emergent eco-species can rapidly evolve with changing climates by shuffling and shifting those symbionts.

A single colony’s polyps are typically all clones resulting from asexual reproduction and on their own offer the colony scant genetic versatility. However within a colony, a wide variety of symbionts can be harbored within a small percentage of polyps, although one symbiont type typically dominates. That small percentage of “cryptic” polyps often survive severe bleaching episodes and then multiply rapidly over the skeletal remains in a process known as the Phoenix effect. Just one square centimeter of coral tissue typically harbors a million individual symbionts and on average those symbionts can double every 7 days. Thus after severe colony bleaching, a more resilient colony can arise in just a few years with better-adapted symbionts now dominating. Likewise symbiont variability within a reef results in some colonies bleaching while adjacent colonies of the same species do not. And similarly a varied symbiont and coral community allows neighboring reefs to adapt to their unique regional climates.

Colony on the left remains unbleached

Variations in coral reproduction can conserve an “ecospecies” or rapidly promote greater ecospecies diversity. Twenty-five percent of the coral species produce larvae inoculated directly from their parent’s symbionts. However 75% of the species produce larvae that initially lack a symbiont. Only after coral larvae settle on a surface, do those larvae engulf one or more different types of free-living Symbiodinium, drawing them inside their cells. As the larvae develop into mature polyps, coral typically keep the symbiont types best suited to the local microclimate and expel the others. In this manner completely new eco-species emerge.

Furthermore as conditions change, all species can shuffle their symbionts as polyps will expel their current residents and acquire a different type that had been harbored by a neighboring polyp. A colony can also shift its symbiont population by acquiring new types not yet hosted by the colony but are present in the reef. Due to improving genetic techniques, previously undetected types of symbionts with greater thermal tolerance are now being detected after bleaching events. Thus a combination of symbiont shuffling and shifting is the key to corals’ rapid adaptation. Although bleaching can result in coral death due to starvation when new symbionts are not acquired quickly enough, surviving polyps with their altered symbiont community have the potential to re-direct the reef on a trajectory that is better suited to the new environment. Or if conditions return to those prior to an extreme event, coral can re-acquire their old symbiont types.

Scientists have found that coral colonies nearer the surface often harbor a different type of symbiont than colonies living just a few meters deeper. The symbionts residing closer to the surface may be better adapted to high irradiance by making proteins that protect against too much ultra violet light or by modifying their photosystem.  Conversely symbionts living at greater depths may photosynthesize more efficiently under low light conditions but are more susceptible to UV damage. Transplant experiments revealed that when coral colonies growing at greater depths were relocated closer to the surface, the polyps expelled their symbionts resulting in temporary bleaching. Bleaching allowed polyps to acquire new symbionts better adapted to higher irradiance. However colonies adapted to high-light surface conditions, photosynthesized much more slowly when transplanted to lower depths. Bleaching never happened and the coral died. Although experiments can force bleaching by raising temperatures, other controlled laboratory experiments found that in the absence of stress from high solar irradiance, anomalous temperatures 4 degrees above average still did not induce bleaching.

According to the adaptive bleaching hypothesis we can infer that bleaching events are not simply the result of recent global warming. Bleaching should have been ongoing for millions of years, as background temperatures have risen and fell. Thus we would expect that as the Little Ice Age ended and naturally temperatures rose, there should be observations of bleaching in the early 1900s. And indeed there are albeit limited. For example bleaching was reported in Florida on hot days in the early 1900s. But more telling, enough warm weather bleaching had been observed in the early 20^th century that the Great Barrier Reef expedition of 1928-29 focused on warm weather coral bleaching when oceans were cooler than today and long before any possible CO2 warming effect.

Coral Response to Climate Change

Since his first Greenpeace-funded 1999 study, Hoegh-Guldberg has promoted catastrophic climate change as the biggest threat to coral reefs. His papers are frequently cited as evidence of climate related coral demise by some researchers and hyped by media outlets that boost readership by promoting climate catastrophes. The bases for his claims relied on 3 simplistic assumptions that a) bleaching is evidence that coral have reached their limit of maximum thermal tolerance, b) bleaching will increase due to global warming, and c) coral cannot adapt quickly enough to temperatures projected by climate models.

In 1999 Hoegh-Guldberg argued “thermal tolerances of reef-building corals will be exceeded within the next few decades” and coral reefs "could be eliminated from most areas by 2100" due to climate change. In his 2014 paper he continued to dismiss the emerging science supporting the adaptive bleaching hypothesis, belittling it as a “persistent mirage”. His catastrophic claims also intensified, suggesting “as much as 95% [of the world’s coral] may be in danger of being lost by mid-century.” To support his extirpation claim he cited two of his own previously published papers. Hoegh-Guldberg’s history of exaggeration and circular reasoning has led other coral experts to accuse him of “popularizing worst case scenarios”, while others have accused him of persistently misunderstanding and misrepresenting the adaptive bleaching hypothesis. Furthermore other researchers have pointed out the pitfalls and weaknesses in framing threats to coral based on a simplistic temperature threshold. They argue, “A view of coral reef ecosystems that emphasizes regional and historical variability and acclimation/adaptation to various environments is likely to be more accurate than one that sees them as characterized by stable and benign temperature regimes close to their upper thresholds.”

As one of many examples of his deceptive misstatements, in his 2014 paper Hoegh-Guldberg wrote, “there is little evidence that acclimatisation has resulted in a shift or extension of the upper thermal tolerance of reef-building corals [42].” His citation simply referenced a paper he had co-authored. But in that paper he admitted never identifying the symbionts or trying to detect any symbiont shuffling or shifting. Furthermore his methodology removed coral from their potential symbiont community during experimental heat stress treatments, minimizing any possibility for the coral to switch symbionts. But it is symbiont shifting that allows coral to shift their upper thermal tolerance levels. Hoegh-Guldberg’s basis for claiming  “little evidence” was totally irrelevant, if not dishonest.

In contrast, improved genetic sequencing is increasingly providing evidence that in response to warm water bleaching events coral begin acquiring new heat resistant symbionts. The results below from Boulotte 2016 show that over the course of 2 years, colonies radically altered their symbionts. The pie charts represent the changing percentage of dominant symbiont types due to shuffling in a single reef species. The bar graphs list just the rarer symbionts and stars identify types not previously detected suggesting an ongoing shift. Symbionts “types” are characterized first by their genetic lineages known as clades. When the adaptive bleaching hypothesis was first proposed, only 4 clades were known. Now at least nine have been identified. The most heat resistant symbionts belong to clade D, but other heat resistant types have evolved within other clades. Many earlier acclimation studies simply identified a symbiont’s clade. But we now know each clade can harbor hundreds of types (potential species) and improved detection of those species is uncovering more shifting. The most heat resistant species identified to date belonged to clade C. As seen here, different types/species are identified as D_I:6 or D1.12.  As illustrated below after 2 bleaching episodes, a new symbiont species from clade C began to dominate and previously undetected clade D symbionts began to appear more frequently in just 2 years.

Changes in symbionts induced by Bleaching from Boulotte 2016

Nevertheless Hoegh-Guldberg 2014 continues to dismiss coral’s ability to rapidly adapt arguing, “current rates of change are unprecedented in the past 65 Ma [million years] if not 300 Ma.” But such exaggeration is pure nonsense. Ocean temperatures were warmer just 1000 years ago, and paleo-studies of temperatures in the Great Barrier Reef suggest local reef temperatures were higher between 1720 and 1820 as illustrated below from Hendy 2003. (Their luminescence index measures changes in salinity associated with monsoons). Perhaps CO2 concentrations are higher now than over the last 300 Ma. But given the extreme warmth just 65 million years ago, that is evidence that our climate is not very sensitive to CO2 concentrations, as realized by more researchers. In contrast to IPCC models that predict more warming that Hoegh-Guldberg ties to coral demise, climate experts note the Holocene temperature conundrum. While CO2 driven models simulate 6000 years of warming due to rising CO2, all the proxies indicate a cooling trend interrupted only by warming spikes.

Temperatures on Great Barrier Reef from 1630 to 2000

Although coral genomes may evolve slowly, their symbionts have extremely fast generation times, averaging every 7 days. Furthermore the symbiont community consists of hundreds of symbionts that have already adapted to a wide variety of temperature, irradiance and salinity variables within different microclimates over the past million years. Symbiont shuffling and shifting is an evolutionary masterpiece that circumvents plodding evolutionary mechanisms of most organisms with long generation times and enables immediate adaptation. To counter the emerging science, Hoegh-Guldberg can only invoke silly semantics to argue symbiont shifting is not “true adaptation”. But again his arguments evoke criticism from his colleagues who wrote, “flexibility in coral–algal symbiosis is likely to be a principal factor underlying the evolutionary success of these organisms”. But Hoegh-Guldberg seems less interested in embracing the emerging science of coral resilience, in order to cling to his belief in catastrophic climate change.