Copyright © 2008 David Iluz et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
An extensive bleaching event in the summer of the year 1997-1998 affected most
reefs along East Africa's shores. In the aftermath of that episode, the reefs of Île
Alphonse in the Seychelles were examined and it was found that reefs along the seaward
slopes of the island lost >95% of their branching coral colonies, with considerably
higher survival of massive species. Île Alphonse features a nearly circular shallow
lagoon, with steep seaward slopes. Contrary to our expectations, mortality in the warmer
lagoon was far lower than of coral colonies on the surrounding slopes, bathed in deeper
and cooler waters. We suggest that corals in the lagoon were protected from UV radiation by
leachate stemming from seagrass leaves steeped in the lagoon. Our measurements in the
lagoon showed a strong attenuation of ultraviolet radiation, not observed in the waters outside
the lagoon, and laboratory examination confirmed that the strong UV absorption of
substances leached into seawater from decomposing leaves of the seagrass
Thalassodendron (=Cymodocea) testudinaceum. Our findings demonstrate
the synergism between elevated seawater temperature and UV radiation in triggering
bleaching on shallow reefs.
Global warming, possibly accompanied by
increased UV radiation and oceanic acidification [1], is a likely culprit in
the recent worldwide decline of coral reefs. The coral bleaching event of
1997-1998, which spread throughout the Indian Ocean,
Southeast Asia, the Caribbean, and parts of the far eastern and western Pacific,
is probably the most severe such episode in recorded history [2, 3].
Recent field
and laboratory studies have demonstrated that
elevated seawater temperatures can indeed induce bleaching in corals [4–7].
While documenting an
extensive mortality episode that struck East Africa’s coral reefs, we found that,
contrary to our expectations, corals on the seaward slopes of a
small cay in the Seychelles
were
the hardest hit, whereas colonies in a warm and turbid lagoon fared
much better.
The data for the study were
collected in November 1998 during an expedition to Île Alphonse, a coral cay four nautical miles in diameter in the Seychelles
archipelago (see Figure 1). Data were collected by
SCUBA diving as video transects, which were subsequently analyzed with image
processing software. Analysis of live coral colonies and recently-bleached
coral skeletons indicated that, prior to the 1997-1998 bleaching event, the
percent cover of live massive stony corals was much higher than that of
branching corals inside the lagoon, while the reverse pattern occurred on the
outer reef slope (see Figure 2(a)). In contrast, after the bleaching event,
most corals of both growth forms survived within the lagoon, while especially
the branching corals suffered extensive mortality on the outer reef slope,
leading to very low live coral cover (see Figure 2(b)). On the outer reef
slope, the mortality of branching colonies reached 100% near
the
surface, whereas among the massive corals, mortality was about 20% at all
depths (see Figure 2(c)). Many of the massive
colonies were only partially affected and, in such cases, only their
upward-facing portions were bleached. Our observations are in
agreement with recent reports that coral colonies in Phuket have been,
in many cases, only partially affected [8]. However, there the differences in
bleaching resulted from exposure to high light rather than UV radiation, and
previous exposure to solar bleaching protected colony faces from subsequent
thermal bleaching.
Figure 1: The Île
Alfonse lagoon: (a) schematic transects, (b) aerial view.
Figure 2: Stony coral percent
cover and mortality at Ile Alphonse,
Seychelles, surrounding
the 1997-1998 bleaching episode. Comparison of massive and branching
colonies inside the lagoon and on the outer reef slope. (a) Percent cover of
live stony corals prior to the bleaching episode, from analysis
of live coral colonies and recently-bleached coral skeletons that appeared to
have died within the year preceding. (b) Percent cover of live stony corals
after the bleaching episode. (c) Mortality rates following the bleaching
episode. “Lagoon top” refers to corals on the top of shallow reef patches
inside the lagoon, and “lagoon side” refers to corals on the vertical sides of
reef patches in the lagoon. Data were collected during November 1998, from 1-m2 digitized video quadrates ( 12–39) at each location.
Our attention was
drawn to the striking and counterintuitive differences in coral fate between
the turbid and warm (35°C) lagoon
and the clearer, cooler (28°C)
outer-reef slope. All along the lagoon shore, we noticed a huge accumulation of
drying leaves of the seagrass Thalassodendron (=Cymodocea) testudinaceum.
Visible amounts of colored substances were being leached into the lagoon water
out of this decomposing mass of sea grass (see Figure 3). Underwater light
measurements were carried out using a submersion spectroradiometer (Li Cor-1800UW).
Measurements were made in the lagoon which had a high content of leaves of the
seagrass Thalassodendron (=Cymodocea) testudinaceum, and outside the
lagoon there was no effect of these leaves. Upon examination of the spectral
distribution of underwater irradiance, we found that the UV/PAR ratio was
dramatically reduced in the lagoon (see Figure 4). Indeed, laboratory
examination of Thalassodendron (=Cymodocea) testudinaceum leachate
revealed a high absorption in UV range. The leaves were left to extract in Red Sea water at 25°C for 24 hours. The
extract was scanned on a Varian 340 spectrophotometer in quartz cuvettes, with
seawater as the reference (see Figure 5). This result is in agreement with the findings
of Stabenau et al. [9] that the seagrass Thalassia testudinum releases a
UV absorbing substance.
Figure 3: The Ile
Alphonse lagoon. Leaves of the
seagrass Thalassodendron testudinum leaching colored substances.
Figure 4: Comparison of photosynthetically
available radiation, 400–700 nm, (UV/PAR) ratio in the lagoon and on the outer
reef slope, as measured with a LiCor-1800UW submersible spectroradiometer.
Figure 5: Absorbance spectrum
of the leaf extraction of seagrass Thalassodendron (= Cymodocea) testudinum.
Our findings support
previous reports [10]suggesting a synergistic effect of UV
and temperature in triggering coral bleaching. Experiments have shown that an increase in
UV light causes coral bleaching. UV light experienced by corals can increase in
calm waters. The amount of mycosporine-like amino acids in a coral's tissues
helps to determine how much UV it can withstand without bleaching [11, 12].
In the case of Ile Alphonse, it is clear that the reduced mortality of
corals in the lagoon was not related to reduced temperature or PAR levels but
rather to a reduction of UV radiation in lagoonal waters. In general, it seems
that in susceptible corals, bleaching may be triggered by synergism between
high temperatures and other factors, whether UV, as at Ile Alphonse, or high
visible-light insolation. We hypothesize that, although temperatures in the
lagoon exceeded those on the outer slope (28°C), seagrass leachate
rich in UV-absorbing compounds created an effective UV-blocking filter in
lagoonal waters, thereby mitigating bleaching-inducing temperature effects. However,
based on our data we cannot exclude the possibility that zooxanthellae clades
with higher thermal tolerance may be involved. In such case that would confer
additional protection from bleaching on the coral colonies in the lagoon, above
that provided by the “UV filter” we report here. It has been
suggested that some clades have higher thresholds for bleaching than others [13–15]. We suggest that this UV
screening phenomenon, together with long-term adaptive mechanisms developed by
lagoonal colonies exposed to higher temperatures, protected this population
throughout the 1997-1998 bleaching event. The coral populations that survive in
such protected refuges may be a source of propagules for future reef recovery.
Acknowledgments
This research was made possible by an expedition to
the Seychelle Islands sponsored by the Interuniversity Institute for Marine Science in Eilat, Israel.
We thank the former managing director, Dr. Avi Baranes, for logistical and
financial support. This research was supported by NATO-SfP-981883 and Beit Berl College.