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 20th
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 20th 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.