Mass bleaching is a recent phenomenon, becoming chronic
D) CONSEQUENCES
Mortality, recovery and long-term consequences
Adaptation and/or selection of host and symbionts
Extinction
Recruitment
Diversity
Ecological interactions
Erosion
Geological comparaison
2) CAUSAL FACTORS
A) IN SITU OBSERVATIONS
Diseases
Temperature
The East Pacific 1982-1983 El Niño event
The Great Barrier Reef event in early 1982
In situ data
Satellite data
Dolldrum time
Light and UV
Others factors
In situ bleaching with obvious local causes
B) LOCAL REEF FACTORS
Water characteristics
Extreme warm temperatures and high salinities
Acidity
Water agitation
Water stratification
Warm oceanic patches and rings
C) LINKS WITH GLOBAL CHANGES
Warming
Other climatic parameters
El Niño-Southern Oscillation
Ultra-violets
Carbon dioxide
Nutrients
ABSTRACT
Since the early 80's, it has been observed a global and
massive dysfunction of major reef organisms. It affects not only
corals but also all the other animal-algae symbioses. The loss of
symbionts and/or their photosynthetic pigments brings a
discoloration, hence the common denomination of "bleaching".
Hereunder is a bibliographic synthesis on this badly
understood recent mass bleaching of reef photosynthetic symbioses,
inattended to be the most comprehensive possible, from biochemical
aspects to global perspectives. Meanwhile it is advocated that CO2
rise is the cause of this phenomenon through symbionts
photoinhibition mechanism.
This bibliographic synthesis is aimed at i) giving an overview
of the problem in its globality; ii) providing support to
reflexion and design of future research; iii) making easier access
to informations for scientists who will join people already
working on the subject, as it is clearly needed. Updated versions
will be regularly delivered by electronic media
(http://www.essi.fr/~sander/articles/Misc/Coral_Reef.html,
also from the Internet reef site,
http://coral.aoml.noaa.gov).
Observations of mass bleaching made in situ were collected by
Williams and Bunkley-Williams and already excellently summarized
by them in 1990. Their synthesis is only completed by more recent
and related works judged noteworthy to be treated. Relevant
informations on local and global factors are examined. All the
physiological and biological aspects of the question are
specifically developed. It is attempted not only to treats direct
data on the bleaching phenomenon, but also to signalle works which
are potentially relevant to it, in spite of the danger of this
approach. This synthesis may appear as a frustrating fragmentary
puzzle, as our state of knowledge is. It is rather a collection of
details, each of which could be important for future
understanding. A special attention is given to carbon process,
even though at the edge of our current knowledge.
Mass reef bleaching is unique amongst the many alarming
threats on earth ecosystems: it is the only one where the primary
level of an ecosystem may collapse all over the world, and for
reasons which are yet unclear, but certainly global. This makes
mass bleaching a prioritary concern.
FIRST PART : FIELD KNOWLEDGE
I) IN SITU OBSERVATIONS ON MASS BLEACHING
A) SPECIFIC AND INDIVIDUAL PATTERNS
Organisms involved
The most stricking feature of recent mass bleaching is that it
affects probably all and quasi-exclusively photosynthetic
symbioses in reefs (last review by Williams and Bunkley-Williams,
1990a, thereafter W90). It is known with certainty that bleaching
affects symbioses of hosts ranging from cnidarians, sponges,
mollusks to foraminifers associated with symbionts which are
either dinoflagellates, diatoms or cyanobacteria:
- all symbiotic cnidarians: hard corals (scleratinian) and
fire corals (Millepora), black, blue and soft corals, anemones,
gorgonians, alcyonaceans and zooanthids. There was even once a
"marked discolouration of many small individuals" of the
free-floating zooxanthellate shyphomedusan Phylloriza punctata.
This was observed in Puerto Rico in 1990, in an inshore coastal
lagoon, for the first time since they were studied in 1986 (J. R.
Garciá, in Goenaga and Canals, 1990). Cnidarian'symbionts
belong to the dinoflagellate genera Symbiodinium
("zooxanthellae"). They live in so-called perialgal vacuoles
inside the endodermic host cells, and also, in the particularly
bleaching-sensitive zoanthid genera Palythoa (as well as in
Protopalythoa and Isaurus) in their outer epidermal cells (Trench,
1971, 1974);
-Tridacna bivalves, although not very currently (W90,
Yellowless et al., in press). Their zooxanthellae live in
diverticula of the digestive tract, which is well irrigated by the
blood system (Norton et al., 1992, abstract, Rees et al., 1992,
abstract). No case of bleaching of the less current symbiotic
bivalve Hippopus have been yet reported, nor of other
molluscs/algae cryptic symbioses such as those of nudibranchs
(Crossland and Kempf, 1985) or Strombus gigas and other
gasteropods (Berner et al., 1986a, 1986b);
- sponges belonging to seven different orders (W90, in annex),
and associated either with cyanobacteria (the red-colored
phycoerythrin-bearing cyanobacteria Aphanocapsa living in the
mixotroph Xestospongia muta, and Petrosia pellasarca, Aplysina sp.
Spheciospongia vesparia) or zooxanthellae (paling noted in
Anthosigmella varians) (Vincente, 1990, Dennis and Wicklund,
1993). Aphanocapsa and zooxanthellae are the only sponge symbionts
living intracellularly, inside specialized cells called cyanocytes
and in "bubble-shaped" cells (Wilkinson, 1982, 1992, Rützler,
1990, and ref. herein). Aphanocapsa are also found in the
intercellular collagenous matrix (mesohyl), as do others symbionts
(chlorophytes, diatoms or red macroalgae), in sponges not yet
known to bleach. Bleaching of sponges appears rather uncommon: the
survey of Vicente (1990) reported a frequency of 10-30% of
bleached X. muta on hard ground at 4-15m depth. Some specimens of
the symbiotic sponge Mycale laevis (or rather the symbiotic M.
laxissima, V. Vicente, com. pers.) in Puerto Rico in 1987 changed
of color from bright orange to dull grey, apparently not due to
zooxanthellae pigment change (?), and they survived (Bunkley
Williams and Williams, 1988, Bunkley Williams et al., 1991).
Another sponge, Aplysilla sp., changed from yellow to blue in
Bahamas, 1987, but this was interpreted as a mere consequence of
their death (R. Wicklung in Williams and Bunkley-Williams, 1989).
This genera lives associated with Aphanocapsa (Rützler,
1990), and Prochloron has been observed as an incidental symbiont
on the outside of this sponge (Parry, 1986). In addition, all
sponges contain non-photosynthetic bacterial symbionts, the status
of which remains unknown during bleaching episodes;
- at least one genera of a large foraminifer, Amphistegina,
with diatom endosymbionts, extensively bleached in Florida, 1991
till 1996, and worldwide in 1992 with the four species A. gibbosa,
A. lobifera, A. lessonii and A. radiata in vicinity of many
bleached cnidarians (Hallock and Talge, 1993, Hallock et al.,
1995, Talge et al., in press). A first observation of bleaching
was made in Bahamas, 1988. Amphistegina are seemingly more prone
to bleaching than adjacent corals (Hallock and Talge, 1993, tab.
4) and bleached in 1992 while corals not (Hallock et al., 1995).
Unexpectedly, it appears that the peak frequency of bleaching is
decreasing, from 20-80% in the 1991 to 20-50% in 1995, though with
greater variability (Talge et al., in press). Standing crop fell
sharply, also in the Gulf of Aqaba (J. Erez, com. pers.). A great
shift in dominance from large symbiotic foraminifers to small
heterotrophic ones has been observed between the decades 1960 to
1990 off Florida, rather related incorrectly in our opinion to
eutrophication rather (Cockey et al., 1996), as between 1974 and
1989 in Mauritius (Hottinger and Pêcheux, 1991). There,
about six months after mass bleaching, white but living, moving,
Heterocyclina tuberculata were collected from 70m depth, and many
other areas were devoid of living large foraminifers while fresh
shells were abundant in sediments (pers. obs.). Informations on
other groups of large foraminifers would be interesting as they
harbour various, sometimes more than one, symbiont groups
(dinoflagellates among them Symbiodinium, rhodophytes,
chlorophytes or isolated chloroplasts, Leutenneger, 1984, Lee,
1990, 1992a, 1992b, Lee et al, 1980, 1982). Many show nowadays
shell abnormalities (see below). Cyclorbiculina, with chlorophyte
symbionts, displayed abnormal orange colors (P. Hallock, com.
pers.). Mass bleaching of symbiotic planktonic foraminifers must
also be logically envisaged (Hallock and Talge, 1993, Hallock et
al., 1995, J. Erez, com. pers.). Large foraminifers are "giant"
unicellulars of a few millimeter size at most and it is not
surprising if they have been overlooked in census, although they
may produce more calcium carbonate than corals themselves (Smith
et al., 1985, Tudhope and Scoffin, 1988, and pers., in prep.).
Their symbionts are, as in corals, harboured inside host vacuoles,
or free in cytoplasm in the cases of Peneroplis associated with
rhodophytes and Elphidium with isolated chloroplast ;
- no observations are yet available on the last but
ecologically minor photosymbiosis, ascidian associated with
cyanobacteria or with the so particular cyanobacterial-eukaryotic
intermediate Prochloron, living extracellularly. In
Curaçao, ascidians increased by nine fold over 1978-1993,
perhaps because of pollution (Bak et al., 1996) but they are
probably non-symbiotic ones (R. Bak, com. pers.).
One non-symbiotic coral, Stylaster roseus, was observed to
discolour in Mona Island (Puerto Rico). This population was
thereafter drastically reduced (C. Kontos, in Williams and
Bunkley-Williams, 1989, W90).
Whereas Merlen (1985) remarks that in Galapagos, July 1983,
the only points of color were from "few beautiful yellow-orange
Tubastrea" (thus probably T. tagusensis), this endemic
non-zooxanthellate species discoloured and may even have
diseappered (Glynn and De Weerdt, 1991). The closely related but
non colored T. coccinea was unaffected (Robinson, 1985, Glynn et
al., 1985a). It must already be emphasized that a wide range of
organisms were affected in Galapagos, 1983, with water
characterized by temperature of at least 2-3°C higher than
normal. Associated with mass bleaching, but restricted to heated
reef flats, death of urchins and mollusks is also reported by
Tsuchiya et al. (1987) in Okinawa, 1986, and together with some
mortality of Strombus gigas, and abnormal behavior of mollusks, of
echinoderms and of polychaetes in Florida, 1987 (Berg in Jaap,
1988). Other reports noted mortalities or unusual behavior of
mollusks and urchins, and occasionally of bryozoans, coralline
algae, tunicates and polychaetes, in Florida, 1983, California and
Kenya, 1987, and Okinawa, 1988, maybe also in inshore area (W90).
Almost no discoloration of photosynthetic non-symbiotic
organisms, i.e. algae, are signalled. Mention of severe damage to
Thalassia near a thermal effluent was done by Jokiel and Coles
(1974), and also of death and/or bleaching (?) of sea grasses in
Florida Keys, 1983 (Causey, in W90). Mastaller (1979, Diss., in
Mergner, 1981) described a "quick massive expulsion of brownish
dyes" by an entire brown algae population, subsequently dying off,
after a daily increase of 8.5°C over the reef flat in the
Gulf of Aqaba.
Interspecific differences
Williams and Bunkley-Williams (1989) and W90 listed around 89
species that bleached, and no new information of interest is to be
added to their analysis. There is great variability between sites
and events. To summarize it briefly, the most currently affected
coral species in the Caribbean zone are Montastrea annularis (more
than M. cavernosa), the 2 Millepora species (M. alcicornis more
than M. complanata, but see Sandeman, 1988, Losada, 1988), and the
various Agaricia sp. in deeper water. Acropora palmata is commonly
cited but is rather resistant, more than A. cervicornis. The
zoanthid Palythoa caribbea emerges as the most sensitive species.
Alcyonarians are also strongly affected (Glynn, 1993). All those
species have high cover in reef. Glynn (1988a) remarked that in
Atlantic realm, massive corals seem more affected than branched
ones (but see W90), whereas the reverse appears to be true in the
Indo-Pacific, in particular with the bleaching of the fast-growing
Pocillopora and Millepora. Newton (in W90) pointed out that the
most extensively bleached host Agaricia lamarcki in Bonaire, 1987,
is a coral of cooler water origin.
Available data confirm the general rule that there are crude
correlations between the various indicators of species
sensitivity: apparition and speed of bleaching, percentage of
affected colonies, percentage of bleached surface of colonies,
percentage of mortality and time of recovery. Exceptions exist: in
Panama, Millepora was the most extensively bleached but recovered
well therafter (Lasker et al., 1989). Noticeable deviations
concern mostly time dynamics : Acropora are often those which
bleach the first but are not the most affected (W90), Porites
panamensis may show delayed response (Glynn, 1984), Pocillopora
had immediate, but lower mortality rate than Acropora in French
Polynesia, 1991 (Salvat, 1992).
Intraspecific differences
Variability between individuals within the same species is
very great: often two similar specimens side by side, one
bleaching, the other not, are observed. It is supposed to result
from the genetic variability of the symbionts (Gladfelter, 1988),
even whithin a single colony (Sandeman, 1988) or of the host, as
showed by clone neighbour analysis (Edmunds, 1994). Genetic
studies suggest that bleached heads of Porites compressa in
Kanehoe Bay, summer 1988, were clone-mates of a genotype that is
extremely sensitive to higher temperature (Hunter and Kinzie in
Jokiel and Coles, 1990). Sensitivity to high light
(500-1300µE/m2.s) of healthy zone of partially bleached
Agaricia tenuifolia was greater than in normal colonies, as
measured by chlorophyll fluorescence (Lovelock et al., 1996). In
Jamaica, Goreau and Macfarlane (1991) suggest that dark colonies
of Montastrea annularis are more resistant (this is opposed to the
finding of Coles and Jokiel, 1978, in experiments, see below).
Thin walled, fused tridents Porites lutea sub-group did not
bleached in summer 1991 in Thailand (Tudhope et al., 1992). Clear
examples of difference in intensity of bleaching of the same
species among localities are given by W90 for the sponge Cliona
and the gorgonian Briarium (cf. also Lang, 1988).
Harriott (1985) states that mortality of smaller individuals
was higher. Survivorship was greater in large massive coral
colonies six years after the El Niño 1983 event in East
Pacific region (Glynn, 1989). In Moorea, French Polynesia, during
bleaching in 1991, it was observed diseappearance of more juvenile
Pocillopora than adults, but this has perhaps other causes
(Gleason, 1993). The opposite pattern of size-dependent bleaching
of fungus corals in Indonesia, 1983, was explained by their
spatial distribution, as big specimens migrate to the more
affected shallow outer reef (Hoeksema, 1991). Preferential death
of small corals was also observed at first after a hurricane
(Knowlton et al., 1981). In the large foraminifer Amphistegina,
bleaching was more frequent in large adults, and small forms less
then 0.6 mm were seldom affected (Hallock et al., 1995, Talge et
al., in press).
In Jamaica, the same M. annularis colonies bleach from years
to years, with others in addition (Goreau, 1990); in Rosario,
Colombia, the few shallow Acropora cervicornis survivors of the
80's events seemed unaffected in 1987 (Lang, 1988), whereas in
East Pacific, coral still alive after the 1983 El Niño
bleached again in 1987, though they recovered in 4-6 weeks (Glynn,
1989). In the Flower Garden Banks, Gulf of Mexico, the same
colonies often bleached each summers 1989-1991, and with the same
pattern (Hagman and Gittings, 1992). The same sponge colonies
affected in Bahamas, 1987, bleached again in 1990, and colonies of
A. cervicornis and Porites, also bleached in 1987, died in 1990
(Dennis and Wicklung, 1993). After 4 years of weekly survey in
Oahu, Hawaii, C. Hunter (Internet reef site) recognizes some
colonies of deeply pigmented Porites and encrusting Montipora
which will bleach for few weeks every spring and fall.
Another interesting observation is that individuals of M.
annularis, A. agaricites, Mycetophyllia and other species with a
particular orange-red color at Negril, Jamaica, a color unusual in
other parts of Jamaica, did not appear to be affected by bleaching
(T. Goreau, unpublished). This suggests that the presence of some
pigments, as carotenoids in symbionts, would make them resistant
to bleaching. It seems that no short-term adaptation exists, as
would be expected with (i) existence of resistant symbionts and
(ii) their selection either from previous host population or free
living ones during bleaching and recovery.
Bleaching affects also the coral larvae : in Bonaire,
September 1995, Morse (1996) observed discolouration of Agariciid
larvae, which was correlated with parent one.
Bleaching at individual scale
It is quite variable, from paling, bleached blotches, to total
bleaching. The surface area bleached ranged generally from 20% to
100% (W90). The most coherent pattern is in relation to light, as
bleaching affects very preferentially the upper faces of corals
and/or let shaded parts intact (Glynn, 1983, Jaap, 1985, Harriott,
1985, Fisk and Done, 1985, Robinson, 1985, Woodley, 1988, Lang et
al., 1989, Williams and Bunkley-Williams, 1989, Goreau and
Macfarlane, 1990, Goenaga and Canals, 1990, Gates, 1990, Yap et
al., 1992, Tudhope et al., 1992). Fine stripes of dead area along
ramets of Acropora after a bleaching event in Mauritius, 1989,
indicated very precisely the zenithal direction (pers. obs.). But
opposite pattern also exists (Woodley, 1988, Tudhope et al.,
1992). Goenaga et al. (1990) counted 64% of corals bleached on
upper part, and 5% on lateral faces. Shaded colonies bleached only
at the end of the 1983 event (Glynn, 1989) or when transplanted to
illuminated places (in Ogden and Wicklung, 1988). Notable
exceptions to this rule is bleaching on the undersides of Agaricia
lamarcki from recessed cave environments (Porter et al., 1989),
and of the gorgonian Pacifigorgia under boulders, in a surge
channel (Robinson, 1985). Gorgonians were also sometimes
white-striped above and below their ramets (W90).
Branched corals may have their peripheral ramets more affected
(Porites elegans, Glynn, 1989) or bleaching can be variable
between branches (Woodley, 1988). The tips are often the first and
the most affected (Glynn, 1984, Lasker et al., 1984, 1989, Glynn
et al., 1985b, Sandeman, 1988, Gates, 1990, Choquette, Reyes-B. in
W90, Rougerie, 1992, Drollet et al., 1995), or verrucae in P.
eydouxi (Drollet et al., 1994, 1995), but Acropora in Andaman
Island bleached from their base toward their tips (Wood in W90). A
colony of A. cervicornis in a public aquarium in St Thomas
bleached in one day from bottom to top (Nunn in W90). A. palmata
has often large, white, irregular blotches (Williams and Williams,
1988). Tabular Acropora bleached from outside to inside, A. valida
in patch, and A. gemmifera only in the coenosteum and not at the
branches (Drollet et al., 1994, 1995). Death of the upper part of
Acropora was also reported following a cold event in Arabian Gulf
(Coles and Fadlallah, 1991).
In massive corals, M. annularis bleached from base to upper
face at San Blas in 1983 (Lasker et al., 1984). Less bleaching was
noted by Glynn (1984) and Hof (in W90) in fissures and or
depressions but Jaap (1988, and in Holling, 1988) indicates an
oppposite pattern. Bleaching patterns of M. annularis differed
with depth in Jamaica (Sandeman, 1988): shallow ones had bleached
areas either in ridges or valleys, on top or side of pillars. Some
colonies had a white 2cm ring at their edge. Below 10 meters, they
were affected only at top, and below 20 meters no bleached
colonies were seen. M. annularis in Mexico after the fall 1995
event were still bleached on top six months later whereas sides
had recovered (R.E. Rodriguez, Internet reef site).
Flat corals as Agaricia and less commonly Leptoseris may
become white from both the edges and the center (Faure et al.,
1984, Bunkley Williams and Williams, 1988) or from edges toward
center (in Williams and Bunkley-Williams, 1989), or in ridges
(Gates, 1990). In Florida, 1987, as well as in Jamaica, deeper
colonies were found striped (Jaap, in Holling, 1988, Jaap, 1988,
Goreau, 1991). Bicolor patterns in recovering corals is signalled
by Newton (in W90).
In Bahamas, among two P. asteroides which bleached in 1991 and
again in 1992, one bleached at the opposite side of previous year
(Lang et al., 1993). A strange pattern of bleaching was carefully
reported by Kobluk and Lysenko (1994), after a cold event in
Bonaire, June 1992, with temperature lowering only from 27°C
to 25°C, in Agaricia agaricites with "ring" bleaching
circling unbleached area of centimeter scale, somewhat located on
ridges.
The large foraminifer Amphistegina were "mottled" to some
degree, ranging from one or more anomalous white spots to nearly
bleached with a few remaining browns areas (Hallock and Talge,
1993). Bleached chambers were not reoccupied by symbionts (as in
DCMU experiments) but new added chambers were colored (Hallock et
al., 1995).
Some bivalvesTridacna gigas bleached only in the central
portion of their mantle (Goggin in W90).
Bleaching in the sponge Xestospongia muta in Belize in 1996
usually starts from the base of the sponge and gradually works
itself up, until the whole sponge is completely bleached out. Then
the sponge just crumbles apart (S. Paz, Internet reef site).
B) THE BLEACHING PHENOMENON AND RELATED REACTIONS
Bleaching: loss of symbionts or of pigments ?
Loss of zooxanthellae was observed under microscope (Glynn,
1983, Faure et al., 1984, Lasker et al., 1984, Glynn et al.,
1985b). Jaap (1985) observed 2 specimens virtually devoided of
pigments. Some symbionts are always still present except in
extremely necrotic coral (Glynn, 1989), and even in the most
highly bleached corals, Jokiel and Coles (1990) could always
detect a few live zooxanthellae through fluorescence microscopy.
Bleached part of one M. annularis colony from Cayman had only
55%-36% of zooxanthellae in June 1988, 9-12 months after bleaching
event, and 88% in December 1988 (Hayes and Bush, 1990).
Different cases were observed:
- both reduction of zooxanthellae density together with a
decrease of pigment content per zooxanthellae : only 10% of
symbionts in bleached M. annularis and Diplora strigosa of St
Croix, 1987, with less chlorophyll a and c per symbionts in M.
annularis (Gladfelter, 1988). Four colonies of M. annularis (from
Florida, collected 5-6 months after bleaching in Dec. 87), had 27%
symbionts, themshelves with a lower level of pigments (chlorophyll
a 36%, chlorophyll c 9%, peridinin 20%, diadinoxanthin 16%)
(Kleppel and al., 1989). Porter et al. (1989) measured in bleached
specimens of M. annularis and A. lamarcki from Florida, 1987,
collected 5 months after bleaching, a reduction to respectively
14% and 43% of zooxanthellae number, together with a reduced
content of chlorophyll a at 52% and 34% of normal level. Coral
biomass decreased to respectively 39% and 73%, photosynthetic rate
to 17% and 74% at saturating light level, but respiration decresed
only slightly. One surprise of their results is that, on a
chlorophyll a basis, photosynthesis was multiplied by about 2.5 in
bleached M. annularis and by 5 in A. lamarcki. In the study of
Brown et al. (1995) of six species just 5 weeks after bleaching in
Thailand, 1991, the counts of zooxanthellae number were very low,
few percent to at most 50% the normal level, and particularly
marked in oral tissue. Pigments analysis 4 months later measured
less chlorophyll per symbionts (0.4-2.1 versus 1.5-4.6 pg chl);
- only a loss of zooxanthellae, down to 25% of normal level,
in 2 colonies of M. annularis of Florida, 1987, collected 9-12
months after bleaching (Szmant and Gassman, 1990);
- more zooxanthellae (about twice) with less pigment (one
tenth) in a third colony;
- less zooxanthellae (19%) with more pigment (+47%, n=8,
p<0.05) in Seriatopora hystrix of Lizard Island, 1987,
collected maybe up to 3 months after bleaching (Hoegh-Guldberg and
Smith, 1989). Bleached Stylophora pistillata from the same place
were more "orthodox" with only loss of symbionts down to 29%.
Lovelock et al. (1996) measured chlorophyll fluorescence of
bleached Agaricia tenuifolia, which was only 2% normal level. A
surprise came from the quantum efficiency (Fv/Fm) which was
identical of that of brown colonies. Jaap (1985) observed an
increase of the chlorophyll a/b ratio in corals bleached in
Florida, 1983. At the same place, in 1987, this ratio rose from
about 2.6 to 10 (Kleppel and al., 1989, if chlorophyll a of
endoliths is not taken into account, as they represent generally a
contamination of less than 10%). Peridinin declined from 34% to
18% of chlorophyll a on a weight basis, whereas the slight
increase of one of the xanthophyll cycle pigments (involved in
photoprotection, see below) is to be confirmed (ratio of
diadinoxanthin/chlorophyll a+c from 11% to 16%).
In addition, whitening of some corals in the field may be the
result of strong tissue retraction, as seen after subaerial
exposure with 10% reduction of absorbance though aspect (Brown et
al., 1994b). One morph of Montastrea annularis with naturally pale
polyps may have been classified as bleached according to Knowlton
et al. (1992). Digitization of color photographies of colonies in
Bahamas showed that bleaching increases the brightness but does
not change the color spectrum (Lang et al., 1993).
In conclusion, the data are quite controversial. Loss of
either symbionts or pigments may be secondary phenomenons, but the
long time lag between the bleaching events and the analysis are
more probably responsible for these discrepencies, as already
advocated by Hoegh-Guldberg and Smith (1989). They consider the
possibility of an initial decline in both the pigment content and
population density of zooxanthellae, followed at first by a
recovery of only the pigment content. In addition, natural daily
variation in pigments may be important, of the order of 50%,
according to Titlyanov et al. (1991), and there is more color in
winter (Lang et al., 1993).
Table 1: Zooxanthellae loss and/or pigment loss in
bleached corals in situ.
Zoox. number
Chlo /Zoox.
Species
Place and date
of bleaching
Delay of analysis
(months)
References
10%
less
M. annularis
D.strigosa
St Croix, 1987
?
Gladfelter, 1988
36%
?
M.annularis
Cayman, 1987
9-12
Hayes and Bush, 1990
27%
9%-36%
M. annularis
Florida, 1987
5-6
Kleppel and al., 1989
14%
52%
M. annularis
Florida, 1987
5
Porter et al.,1989
43%
34%
A. agaricites
Florida, 1987
5
Porter et al.,1989
27%
normal
M. annularis
Florida, 1987
9-12
Szmant and Gassman, 1990
200%
10%
M. annularis
Florida, 1987
9-12
Szmant and Gassman, 1990
19%
147%
S. hystrix
Great Barrier
3
Hoegh-Guldberg and Smith
29%
normal
S. pistillata
Reef, 1987
3
1989
50%
few
6 species
Thailand, 1991
1
Brown et al., 1995
1/4-1/2
6 species
Thailand, 1991
1
Brown et al., 1995
In situ observations of release of zooxanthellae
Massive expulsion of zooxanthellae is at least proved in some
few in situ cases. The first description was made by Fankboner and
Reid (1981), during several incoming very warm tides, giving a
burning sensation, on inshore area of Eniwetak Atoll, Aug. 1979,
in the form of a cloudy-green vertical front, about 2 m deep.
Microscopic examinations revealed numerous zooxanthellae along
with bits of filamentous algae, miscellaneous protozoa, polychaete
setae and molted crustacean cuticules. Samples of a less opaque
cloud contained 5100 zooxanthellae per liter. Large dense
yellowish brown clouds, up to 2 m thick, or golden yellow mucus
above corals, were reported just prior mass bleaching events, and
are surely expulsed zooxanthellae (Bunkley-Williams and Williams,
1987, 1988, 1989, Goenaga and Canals, 1990). They were said "dead
and dying" by Bunkley-Williams and Williams (1990b), without any
further information.
Zooxanthellae and histopathological observations
Coral tissue loss or sloughing has been rarely seen: in Uva
Island, 1983 (Glynn et al., 1985b), in Montastrea annularis and
Diploria spp. in St. Croix, 1988 (Gladfelter, in W90), as well as
in the former species in Florida Keys and Puerto Rico in 1987
(Hudson, 1988, Goenaga et al., 1988), and in Porites evermanni in
Hawaii, 1987 (Jokiel and Coles, 1990).
Desappression of thylakoids is the first observable event
according to M.D.A. Le Tissier (com. pers., 1994). Degenerated
zooxanthellae are commonly observed, but, according to Glynn et
al. (1985b), only after animal necrosis, at contrast to Brown et
al. (1995) observations. They are described as vacuolized (Glynn,
1989), with abnormal empty appearance (Lang, in Holling, 1988), or
as "empty, devoid", with unstained vacuoles, without densely
stained granules, some with a central condensation and peripheral
cytoplasmic clumps (Hayes and Bush, 1990), with loss of
circularity, vacuolization around them, and many empty vacuoles
(Brown et al., 1995). Wide perialgal space was also observed in
"solar bleaching" (Le Tissier and Brown, 1994). Pyrenoids and
assimilation bodies were still visible, except in a few ones of
the oral disk (Szmant and Gassman, 1990). In the transition zone
from bleached to unbleached parts, accumulation bodies were
hypertrophied (Faure et al., 1984). Chloroplasts were reduced or
absent, lipids lacking and membranes ruptured (Jaap, 1985). Host
lipid reserves were seen to increase in mesenterial area (Brown et
al., 1995). Symbionts may be localized in the base of the polyp
and in mesenterial filaments, either as "refugees" or in course of
expulsion (Szmant and Gassman, 1990), or simply due to more
reduction in oral than mesenterial or basal areas (Brown et al.,
1995). Those authors also observed zooxantellae in mesoglea ; and,
as in some laboratory experiments, symbionts were often in
dividing state. No damage of perialgal membrane is reported.
Tissue of bleached corals shows general atrophy and necrosis.
There is 30-50% less tissue per surface, with a normal C:N ratio
(Szmant and Gassman, 1990). Invasion of cell by ovoid dark
inclusions at the base of endoderm was described by Faure et al.
(1984). Jaap (1985) observed abnormal mitochondria in coral
cytoplasm, with mucoid-polysaccharide material. Mucus secretory
cells increased in number and size (Brown et al., 1995), even in
healthy appearing Agaricia (Lasker et al., 1984) and in Pavona
clavus, but decreased in P. gigantea and P. varians (Glynn et al.,
1985b, Glynn, 1989). Based on staining with pentachrome, a change
of mucus composition and of pH in Porites damicornis, P.
panamensis, Psammocora stellata, and Pavona clavus must have
occurred, together with formation of basophilic "blobs" (Glynn et
al., 1985b). One "healthy"-looking Pocillopora was in early stage
of necrosis (loss of architecture, basophilic tinge in mesoglea),
from which it was concluded that the problem is on the animal
side, with maybe thereafter nutrient-starvation of zooxanthellae
(Glynn et al., 1985b). Gonads are reduced and reproduction is
generally impaired, according to health state (Glynn et al.,
1985b, Glynn, 1989, Szmant and Gassman, 1990). Bleached corals had
half normal lipid level (Glynn et al., 1985a). Phenoloxidase, a
biomarker of immune capability, was found to have lower activity
in bleached and semi-bleached M. annularis (Smith, 1992,
abstract). Large foraminifers diplayed abnormal number of large
vacuoles and lysosomes surrounding deteriorating symbionts
(Hallock and Talge, 1993, Talge and Hallock, 1993).
Diseases
Secondary parasites were observed in a few cases, with massive
invasion of fungal hyphae in M. complanata, but not in Acropora
nor Palythoa (Te Starke et al., 1988) or in one colony with ovoid
granular basophilic bodies similar to those of the "White Band
Disease" (Lasker et al., 1984). Coccoid and rod-shaped
bacteria-like objects were observed in the gastrodermis of
bleached corals of East Pacific, 1983, sometimes present in the
vacuoles vacated by zooxanthellae (Glynn, 1989). There is no
transmission of bleaching following iso-, allo- and xenografts,
i.e. between parts of the same colony, between specimens of the
same species or different ones (Glynn, 1983, Glynn et al., 1985b).
Recently, this hypothesis gains support from the finding of
Kushmaro et al. (1996, and oral com., Panama 1996) : in the Israel
mediterranean coast, bleaching was observed in summer in Oculina
patagonensis (a very strange coral, see Zibrowius and Ramos,
1983). Bleached rim zone was infected with Vibrio-like bacteria,
which were cultivated. They revealed to be potent bleaching agent
within one week to one month according to aquarium inoculation.
Antibiotics protected from bleaching. Moreover bleaching was
effective at 25°C but not at 16°C, in resonance with
worldwide "warming" bleaching. Such a peculiar restricted
phenomenon was not unexpected. Although impressive, these data can
be taken in account only when some similar finding are found
somewhere else, and more crucially if infection can be carried out
on other bleaching taxons.
Calcification of corals
During bleaching, there is no visible calcification, as seen
with alizarine marks (Glynn, 1983, Glynn, 1989), nail technique
(Goreau and Macfarlane, 1991), band analysis (no stress band,
Leder et al., 1991, missing or great reduction of deposit, Porter
et al., 1989, Reese et al., 1988) or direct caliper measurements
(at most very reduced growth in coral transplanted to nearshore
area, Shinn, 1966). At contrast, Tudhope et al. (1992) still noted
calcification in 3 weeks Alizarine-stained bleached corals, albeit
extremely limited. Risk and Pearse (1992) were able to observe
daily growth bands in one of the few corals of the west coast of
Costa Rica which survived the El Niño 1983 bleaching event.
It grew 22µm per day before the event, 9µm at maximum in
1983-1984 with possible total cessation of growth, and recovered
to 18µm after 1985. Rougerie et al. (1992) suggest that
fluorescent colonies may continue to calcify. Calcification can
still be negligible even 6 months after recovery of normal color,
suggesting that bleaching inhibits calcification more than
photosynthesis (Goreau and Macfarlane, 1991). About one year after
bleaching event, growth rate of M. annularis was still null for
bleached ones (or 37% for the colony n°67 with twice more
zooxanthellae), 67%-93% for recovering ones, and 81%-98% for those
that did not bleach (Leder et al., 1991).
Thus no clear signals was given by isotopic carbon and oxygen
deviations in skeletal bands. d18O from Porites lobata of Isla del
Caño records a +2°C temperature anomaly during the
1982-1983 El Niño, corresponding to 32°C, whereas in
situ temperature in January 1983 was only 30°C in shallow
areas and 29°C at 15m depth. Salinity interference was
postulated (Carriquiry et al., 1988). In Florida, 1987, the
0.25-0.5°% lighter d18O, corresponding to 0.5-1°C
warming, was seen very only in bleached colonies and unexpectedly
not in the unbleached ones (Porter et al., 1989). Leder et al.,
(1991), studying also M. annularis colonies of Florida, 1987, have
not seen a d18O temperature signal in normal colonies except a
little one in three affected colonies, but again perhaps because
of a salinity effect. A 1°% lighter d13C in bleached
specimens can be interpreted as an effect consecutive to lower
growth rate (Porter et al., 1989), whereas Leder et al. (1991)
interpreted the absence of d13C signal to opposite effects of
photosynthesis reduction and of lower growth rate. The colony
n°67 (with twice more zooxanthellae) has a d13C 1-2°%
heavier than all others. Isotopic deviation and growth rate were
good but not perfect indicators of past ENSO events, because of
would-be cessation of calcification and of other isotope
excursions not linked to ENSO (Druffel et al., 1989, and ref.
therein, Quinn et al., 1993, Dunbar et al., 1994). Ten growth
discontinuities were identified in a record since 1587 (not always
correlated with ENSO), but included the one associated with the
1973 ENSO without bleaching, and none presented bioerosion nor
encrustation observed after the 1983 mass bleaching (Dunbar et
al., 1994).
Shell abnormalities in large foraminifers
At contrast to corals, large foraminifers enregister bleaching
event in their calcification. Spectacular shell abnormalities were
encountred in various genera in Mauritius, 1989, six months after
a bleaching event (cf. Hottinger and Pêcheux, 1991) (see
Annex V). In Florida 1991 to 1996, Amphistegina showed
calcification defects, with extensive shell damages and
deformities: breakage (3-29%), margin chipping, loss of outer
chambers, twisted, elongated or conjoined tests, tests with two
apertures or distended embryo (6% or less) (Hallock and Talge,
1993, Hallock et al., 1995, Talge et al., in press). Strong
abnormalities were also observed in Amphistegina lessoni and A.
bicirculata from Palau on the front reef, 30m-60m depth, in
October 1995 (J. Hohenegger, com. pers.) and in a small sample, in
Amphistegina, Heterostegina and Sorites from Caribbean Panama in
few meters depth in July 1996 (pers. obs.). We are currently
monitoring a population of S. variabilis near Nice, France. They
display 17.9%-27.3% of abnormal forms (supplementary plans,
irregular periphery, twisted disk, twin specimens), but we could
not find old samples to be sure it is a new phenomenon (in prep.).
Those observations are of utmost importance. Minor
irregularities in chamber formation were quantified in normal
population of Operculina (Pêcheux, 1995b), and they appears
as quite distinct phenomenon. Shell abnormalities of symbiotic
foraminifers were known in tidal pools or very shallow water with
temperature, salinity, oxygen and pH excursions (cf. Reiss and
Hottinger, 1984), in culture (Röttger and Berger, 1972, pers.
obs.) or in small foraminifers in heavily polluted areas
(Venec-Peyre, 1981, Yanko et al., 1994, see reviews in Boltovskoy
and Wright, 1976, Alve, 1995) and in planktonic foraminifers
believed to be under stress (Berger, 1972), but never in the
recent past in pristine areas bathed by stable oceanic open
waters. It prooves that bleaching is a new phenomenon.
Moreover, to my knowledge and of many consulted specialists as
well as extensive bibliographic search, such high frequency of
deformities was never observed in geological time. For example, we
checked our collection of Mexican upper Cretaceous-lower Tertiary
large foraminifers, containing circa 20 000 representative
specimens (Pêcheux, 1984). Abnormalities accounted for about
4 per mil, almost always from special facies (very shallow,
deltaic, transgression or emersion ones) and never comparable to
certain monsters today observed. The only similar record is found
just after the Cretaceous/Tertiary catastrophe, not in reef
foraminifers which all disappeared but in planctonic ones, half of
which was abberant during about 50 000 years (Gerstel et al.,
1986), a time of considerable CO2 rise. These abnormalities
indicate that bleaching is truly an unprecedent stress at
planetary evolution scale.
Unusual colors and secondary pigments
Many observers report unusual blue, green, yellow or pink
colors of "bleached" colonies (Goreau, 1990, Salvat, 1992), which
colors were reported before mass bleaching only by Jokiel and
Coles (1974) for local bleaching in the flume of a thermal
effluent, mostly in Pocillopora meandrina. In particular
Siderastrea sidera become lavander, lilac or blue (Jaap, 1988,
Hudson, 1988, Williams and Bunkley-Williams, 1989,
Bunkley-Williams et al., 1991, Rougerie, 1992). Montastrea
annularis turned blue before bleaching, Porites asteroides and P.
porites yellow (Williams and Bunkley-Williams,1989), and
Montastrea cavernosa grey (Goreau, 1991). Some anemons turned
bright yellow or rust, whereas the mouths of Agaricia and
Leptoseris remained yellow (Bunkley Williams and Williams, 1988).
There were some instabilities in this phenomenon, with changes of
color from pink to blue or yellow to pink within weeks in Acropora
(Rougerie et al., 1992).
Those colors are sometime characterized as "fluorescent" or
"iridescent" (Goenaga et al., 1990, Rougerie, 1992). In Moorea,
1991, T. Goreau (unpublished) has observed that unbleached
colonies, and "white" or yellow bleached ones have the same
fluorescence, whereas none was visible in rose-pink, blue or
violet bleached colonies. The fluorescent pigments were localized
in the animal, and were soluble in water but not in acetone and
are probably the mycosporine-like amino-acids. In bleaching due to
thermal effluent in Hawaii, an increase of 330nm-absorbing
pigments have been observed in bleached Montipora verrucosa but
not in other two studied species and was said to be merely due to
the amount of tissue loss (Jokiel and Coles, 1974). In Indonesia,
1983, among the mushroom corals, Heliofungia actiniformis was
unaffected, perhaps because of its green fluorescent pigment, or
alternatively because of its thick gastrodermis (Hoeksema, 1991).
Polyps behavior
Polyps response is variable, from normal behavior, to
extention without prey capure, to total retractation (Williams and
Bunkley-Williams, 1989, Lang in Holling, 1988) probably depending
on the intensity of the perturbation. Fire corals (Millepora) may
or may not inflict pain (Jaap, 1979, 1985, 1988, Losada, 1988,
Goenaga and Canals, 1990). Abnormal expansion of polyps (Faure et
al., 1984), or continuous extension night and day of normally
night species (Glynn, 1989, Williams and Bunkley-Williams, 1989)
were also noticed. Before mass bleaching, it has been observed
that white Montastrea cavernosa (due to reduced light) expanded
their polyps abnormally in the day (Wells et al., 1973). At
opposite, Lasker (1979) found in 1979 one "diurnal" morph of M.
cavernosa with a small bleached region. This region expanded its
polyps at night instead of day, and recovered the normal behavior
of the rest of the colony progressively, in parallel with
pigmentation.
C) SPATIO-TEMPORAL PATTERNS
The remarkable work of W90 summarizes all informations made
available till 1988, and the reader is invited to refer to it.
Recent bleaching events are now signalized on the Internet reef
site (http://coral.aoml.noaa.gov). Table 2 summarizes published
works. An overview is given here for completude.
Time patterns
The first described mass bleaching event sensu stricto (with
no obvious local cause) began in Bonaire (Leeward Islands,
Caribbean) in June 1979 and ended in February 1980 (Hof, in W90).
It occurred extensively on all but the windward coast of the
island from 10 to 40 m depth. Bleaching occurred in summer 1980 in
several areas in the Florida Keys (W90), and in the Great Barrier
Reef (Oliver, 1985). Therafter, mass bleaching events are well
reported, in early 1982 in the Great Barrier Reef, and in 1983
mostly in the Eastern Pacific, clearly associated with El
Niño, and also in Indonesia, Japan, Mayotte, and Caribbean.
Some mass bleaching occurred in 1986 in Hawaii, Mayotte, Puerto
Rico, Barbados and perhaps Bahamas. In 1987-1988, the bleaching
occurred worldwide, and was the "most severe, extensive and
long-term bleaching ever [previously] recorded" (W90). Although a
detailed synthesis is not yet available for more recent years,
mass bleaching was reported in Caribbean and other Indo-Pacific
regions from 1989 to 1995, 1990 being considered as major events
in Carribean. Severe bleaching in Society Islands in 1991 is
clearly related to the 1991-1992 El Niño. From all
evidences, mass bleaching is more and more frequent and
widespread, as in 1995 (Panama 1996 congress abstracts and
Internet reef site).
W90 emphasized the cyclical pattern of mass bleaching in
1979-80, 1982-1983 and 1987-1988, and divided bleaching complex in
preceding, main and following events. It appears that the 1979-80
cycle is far from evident, and that bleaching is becoming more
continuous in the recent years. Once the connection with the El
Niño phenomenon is discarded (W90, Atwood et al., 1992,
1996 and see below), the existence of worldwide cycles in
1982-1983 and 1987-1988 raises more interrogations on their origin
than provides light on the cause of recent bleaching.
Local time dynamic of bleaching
With local heating on reef flats during low tides, the time
response of bleaching may be as fast as a few hours. In most mass
bleaching cases, it ranged from one week to months. In Looe Keys,
Florida, bleaching occurs within a week or so once dolldrum
weather sets (Causey, in Atwood et al. 1992). In Puerto Rico,
September 1990, seas became unusually calm one week before
bleaching (Goenaga and Canals, 1990). According to Dennis and
Wicklung (1993), bleaching appears in Bahamas, 1990, more than a
couple of days, but less than 18 days, after the raise of
temperature. The rate of increase was lower than in other years,
about 3.1°C in 14 days.
If one takes warming as the cause of bleaching, it is
difficult to know when the temperature threshold, if there is one,
is reached during a slowly warming period. Temperature records
before bleaching are rare. The warming may be as long as 17 months
(Glynn, 1989). In Florida, 1987, Cook (in Porter et al., 1989)
recorded warming up to 0.5°C per day, and temperature was
above 30.2°C during two weeks, and bleaching started 5 days
later. (Cook et al., 1990). In East Pacific, 1983, bleaching began
about one month after warming according to Glynn (1984), and after
30°C during three weeks and 32°C during one week at San
Blas (Coffroth et al., 1989). In Indonesia, April 1983, bleaching
took place 4-6 weeks after the end of the wet season and of the
warming (Brown and Suharsono, 1990), and between one and two
months after warming in Society Islands, April 1991 (Rougerie et
al., 1992). In Jamaica, 30°C was reached at least in early
August 1989, and bleaching becames apparent in early October
(Goreau, 1990). The data of Kato (1987) show a warming from
25°C to 31°C in two weeks in a shallow area of Okinawa
in 1986. Bleaching affected 30-40% of the colonies at the end of
this period as well as one month later, but curiously not in
between.
Bleaching may be sudden or progressive (W90), lasting many
months (1 1/2 month in Australia, 1982, Oliver 1985, or increasing
from July to November 1987, Goreau and Macfarlane, 1990) or
lasting more than a year. Glynn (1989) observed a delay of 2-4
weeks between bleaching and death.
Increase of bleaching has been observed after its initiation,
with delay of 4-7 months for Colpophyllia and of 8-11 months of
Palythoa (Lang et al., 1992). Some corals have been seen to
recover while others began to bleach, as Millepora in Bermuda,
1988 (Cook et al., 1990, and see W90). This could be interpreted
as an acclimatation of the corals bleached during the first phase,
or rather as the fact that they were already bleached and thus
unaffected by the conditions which generate the second phase of
bleaching.
Spatial patterns
Mass bleaching affects all regions. The only main exception
today is the Gulf of Akaba, perhaps because of its low
temperature. At lower spatial scale, the perplexing variability of
mass bleaching was well analyzed by W90, and, as they stated, "few
if any trends can be assembled which are not contradicted by some
reports. The patterns and extent of bleaching seem to suggest a
large number of local, unrelated, pratically unique events but
they are too highly coordinated to be coincidental".
At reef scale, bleaching affects large continuous tracts,
spotty areas or isolated colonies (Glynn, 1983, Lang et al., 1984,
W90). There is no trends with depth. Bleaching occurs from near
surface down to 90 m depth (although at a low level of 3%). It may
be more intense in shallow waters, intermediate ones (12-15m) or
deeper ones (10-55m). Opposite depth trends has been even observed
in two adjacent sites in Jamaica (also CARICOMP, 1996). In some
events, bleaching moves deeper with time, but toward shallower
areas in others. In 1994, bleaching was more frequent in shallow
waters in the North-West of Moorea, Society islands, but more in
deeper waters in the North-East, 10 km apart. It seems to be
induced by previous species distribution, in particular of the
resistant Porites (Hoegh-Guldberg and Salvat, 1994). Bleaching is
as often reported in inshore than in offshore zones. The few
coherent indications of bleaching in grooves and channels is
discussed later in relation to dense water formation.
Preferential bleaching on one side of islands is often
reported, but with no emerging pattern, suggesting local
circulation factors. Relative intensity of bleaching at Looe Key
and at Key West in Florida was reversed from 1983 to 1987 (Jaap,
1988). No regional trend is clear, apart for the El Niño
East Pacific 1982-83 event, but even in this region some places
escaped bleaching (Glynn, 1989). W90 indicated that in
January-November 1987, bleaching was centered in northern
Caribbean, Bahamas and south Florida, perhaps because they are
large platforms and/or with poor water circulation. Bleaching
later expanded with less intensity to include all of the greater
Caribbean Islands and eastern Pacific in November 1987-January
1988.
Mass bleaching is a recent phenomenon, becoming chronic
There is almost no doubt that mass bleaching events have
appeared since the early 80's and tremedously increased in
magnitude and frequency. One may argue that there were fewer
observers at the begining of the century, but this objection
certainly does not hold for the 60's and the 70's. It is
significant that almost no mention of bleaching was made in the
reviews on coral reef stress by Johannes (1975), Endean (1976),
Pearson (1981), Peters (1984) and Rogers (1985). A special chapter
first appeared in Brown and Howard (1985). One must be confident
that since the begining of the century, and probably a little
sooner, mass bleaching events similar to the present ones would
have been at least sometimes described, as were reported local
events (see table 2; and below).
Before historical reports, halt of coral calcification during
bleaching and absence of specific mark in the growth bands have
prevented so far a retrospective long-term analysis. A contrario,
in Florida, the apparent lack of missing years in the growth bands
of Solenastrea since 1880, and Montastrea annularis since 1861
(Hudson et al., 1976, 1989) tends to indicate that there was no
widespread previous bleaching event. The maximum reduction of
growth in those two corals was respectively 50% and 30% from the
mean, with only stress bands due to cold winter.
Sclerochronological data are more ambiguous for the east and
central Pacific (Druffel, 1985, Druffel et al., 1989). Growth
discontinuities were identified in a record since 1587, but none
presented bioerosion nor encrustation observed after the 1983 mass
bleaching (Dunbar et al., 1994).
Death of centuries old colonies, at least 200 years, and
perhaps more than 500 years in East Pacific (Glynn, 1985, 1989,
Robinson, 1985) and in Puerto Rico (Goenaga in Goenaga et al.,
1989) reinforces the conviction that mass bleaching is a new
phenomenon. Frequent abnormalities of shell of large foraminifers,
never observed before, support this view.
Is there a normal "back ground" level of bleaching in reefs ?
Natural aposymbioses are known in the temperate coral Astrangia
danae (Peters and Pilson, 1985) and the sea anemone Anthopleura
along the Pacific coast of North America (Muscatine, 1974), and
for sponges in deep waters (Vicente, 1990). Most reefs would
contain a few bleached colonies normally (Williams and
Bunkley-Williams, 1989). Lastly, we found no old reports of the
phenomenon. Goreau and Goreau (1959) judged an opportunity for
experiments their finding of in situ bleached colonies of Manicina
areolata under a large coral head in semi-darkness. Goreau (1964)
has observed temporary and reversible bleaching on the fore-reef
slopes at depths below 30 m, which was described more precisely by
Goreau et al. (1970): "For reasons not yet understood, almost
complete bleaching, i.e. loss of zooxanthellae, is often observed
in deep water reef corals that appears to be otherwise normal. It
is perhaps noteworthy that such corals regain their normal
complement of zooxanthellae within a few days whereas in severely
stressed corals the recovery of the zooxanthellae takes several
months". This casts doubt whether true symbiont expulsion
occurred, and at least indicates an important difference with
recent bleaching phenomenon. Yonge in 1973 stated that "colourless
colonies of hermatypes are from time to time encountred in deep
shade, usually under some man-made erection". During a monitoring
of Montastrea cavernosa at 3 sites on Panama's Caibbean coast over
2 years, Lasker (1979) found only one colony with a small bleached
region, at time of heavy waves in December 1979. Muscatine et al.
(1979) stated: "Most desirable are naturally-occurring
aposymbiotic corals of the same species [for experiments].
Unfortunately these are difficult to obtain, and for most species
may be virtually non-existent. During the course of investigations
(...) we discovered naturally-occurring aposymbiotic colonies of
Madracis mirabilis (...) in Discovery Bay, Jamaica", due to
sediment covering. Upton and Peters (1986) examined 3 species of
corals (A. agaricia, M. cavernosa, M. meandrites) from Puerto Rico
which were found in 1980 with partial or patchy bleaching and
necrosis, and often, but not always, infected. No frequency of the
phenomenon is given but the largest white patch measured 4x5cm. In
1981, some corals in Puerto Rico were bleached but supposely
because of a ciliate attack (Vicente and Goenaga in Williams et
al., 1981, Williams et al., 1987, unpublished).
Fisk and Done (1985) stated that isolated bleached corals are
commonly observed in the Great Barrier Reef, especially on
nearshore reefs. Very low level of bleaching for long periods was
also said to exist in Maldives and Fiji (Wood, 1988, Beckman in
W90). "Chronic level of bleaching since early 80's" is said to
occurs in Colombia (Zea and Duque Tobon, 1989). Bleaching occured
at 1-2% level in Bonaire in the years 1977-1981 and 1985-1992, at
10-30 m depth, outside main events (in part due to cooling also)
(Kobluk and Lysenko, 1994). Deep Agaricia in Jamaica partially
bleached in October months before mass bleaching in 1987 (Porter
in Woodley, 1988). Up to 4.5% bleached colonies in sites of
Florida Keys in July-September 1985 were observed by Glynn et al.
(1989a). Low level of bleaching have occurred in Caribean
throughout 1987-1988 (W90). In winter 1986-1987 in Jamaica,
between summer bleaching events, minimum level of bleaching of M.
annularis and Agaricia sp. was between 5% and 25% in the fore reef
(Gates, 1990). One third of the Favia fragum and Palythoa
?mammilosa was found in a bleached state in Bermuda in spring
1988, between main events (Cook et al., 1988). This must be hardly
considered as a "normal" background level. One is forced to
conclude that a chronic bleaching (Glynn, 1993) had appeared.
D) CONSEQUENCES
Mortality, recovery and long-term consequence
Coral mortality after mass bleaching is highly variable,
affecting up to 97% of corals in Uva Island after 1983 (Glynn,
1989), but in a number of cases recovery seems total (W90, and
Table 2). General discussion of recovery after various
environmental perturbations are found in Johannes (1975), Endean
(1976), Pearson (1981), and Brown and Howard (1985). Recovery time
of reef coral commonities was evaluated to be between 4 to 100
years (Coles, 1984). Long-term consequences of mass bleaching were
particularly discussed by Coffroth et al. (1989), Glynn (1989,
1993), Glynn et al. (1991), Smith and Buddemeier (1992). Given
that causes and mechanisms of mass bleaching are not understood,
few predictions can be made apart of gloomy subjectives guesses.
At ecosystem level, stability is a complex question quite far
beyond current knowledge. It can only be affirmed that mass
bleaching has revealed coral reefs may be surprinsingly fragile.
The 1980-85 period was catastrophic in the Great Barrier Reef but
somewhat better in 1985-90 (Done, 1992). The implications of
bleaching for the carbon cycle is treated in annex IV. A few more
points can be quoted:
Adaptation and/or selection of host and symbionts
Adaptation of corals to chronic or repeated bleaching stress
conditions is probably very slow as they are long-lived species
(Glynn, 1989, 1993, Glynn et al., 1991). Selection of resistant
strains of symbionts, if it occurs, would be important for fast
adaptation. Unbleaching of orange-colored corals in Negril,
Jamaica, is an argument in favor of the existence such strains
(Goreau, 1991). Buddmeier and Fautin (1993) posit that bleaching
allows a host to be repopulated with a different partner. In a
laboratory experiments, Franzisket (1970) described a recovery of
a bleached coral tip with zooxanthellae slowly spreading from a
contact with another tip, and Aiptasia was reinfected with more
resitant zooxanthellae from the sun-loving Cassiopea (Jokiel and
York, 1982). In situ, the observation of recovery from unbleached
area at a rate of 12 mm per month in Cayman M. annularis suggests
an absence of selected residual symbiont population (Hayes and
Bush, 1990). Bleaching of the same colonies every year seems to
infirm change of algal partner.
Extinction
Two species of Millepora (Hydrozoa) were first believed
extinct in the eastern Pacific after the 1983 event, M. boschmai
(described by de Weerdt and Glynn, 1992) and M. platyphylla (known
also in Marquesas Islands), as well as perhaps also Acropora
valida and the non-zooxanthellate coral Tubastrea tagusensis, a
Galapagos endemic (Glynn and De Weerdt, 1991). However, five
little live colonies of M. boschmai of 4-7 years old were
discovered in 1992 at Uva Island (Glynn and Feingold, 1992).
Recruitment
A first step of recovery after coral mortality is recruitment.
Following the East Pacific 1983 El Niño event, the "low
rates of larval recruitment suggest that local populations have
capacity to recover" (Glynn et al., 1991, 1996a). Robinson (1985)
noted high rate of recruitment of black corals. Species can
recover through recruitment in places were they all died, as
Acropora from 1983 to 1988 in Indonesia (Brown and Suharsono,
1990) or Millepora intricata in Uva Island (Glynn and De Weerdt,
1991). Bleached populations of the large foraminifer Amphistegina
gibbosa observed in culture within months after field collection
showed both reduction of clonal reproduction by large adults and
attempt of reproduction by small ones, producing reduced number of
young, frequently non-viable or deformed. Size histogram of
Floridan population in 1993, as well as double normal size of A.
radiata from Caroline Islands, 1992, indicated also partial
suppression of asexual reproduction (Hallock and Talge, 1993,
Hallock et al., 1995, Talge et al., in press).
Diversity
Recovery of diversity, and more fundamentally of the integrity
of the ecological system for which no definition nor measurement
can be proposed, is hardly predictable. Diversity decreased but
not significantly, with the dominant species, tabulate Acropora,
less affected, according to the study of Fisk and Done (1985),
whereas Jaap (1985) observed long term reduction of diversity and
change of dominance. Variability of the effects on diversity
measurements are emphasized by Brown and Suharsono (1990). The
results of the long-term biotic monitoring of Warwick et al.
(1990) in Indonesia after the 1983 event are complex but
promising. They found an approach to recovery till 1985, then a
halt perhaps under an "unidentified stress". At one place (Pari),
the maximum of diversity between quadrats was in 1984 because of a
higher mortality and/or a previous variability in the dominant
species. Shift in coral population structure, different than
dominance or diversity, was also shown up. This shift was roughly
similar at species and genera level at one site, but not at the
other (op. cit., fig. 6).
Ecological interactions
Reefs are basically dominated by coral competition against
algae. It is stricking that in Jamaica, coral cover reduced from
50-80% in the 1970' to less than 5% in 1990, and in the same time
algal cover changed from 1-3% to 60-95%, not only because of mass
bleaching but also because of overfishing, Diadema mortalities and
cyclones (Hugues, 1994), and perhaps eutrophisation as well
(Goreau, 1992). There is rapid algae overgrowth on bleached and
dying corals (W90). After recovery, when healthy, corals dominates
those algae with formation of calcified rims and walls till a
complete enclosure of the algae. Rim formation by brown living
part can be as rapid as one week after bleached tissue is gone,
and recovered corals sometimes showed many nodosities, sometimes
with enclosed H2S-smelling dark liquid (pers. obs.). In Florida,
numerous growth protuberance were also observed on A. palmata,
without identification of the origin (Porter and Meier, 1992)
At an upper ecological level, relative foraging pressure of
the sea urchin Eucidaris increased after bleaching (Robinson,
1985), as well as predation from the sea star Acanthaster and the
Arothron after the 70-95% coral mortality in East Pacific, 1983,
but gasteropod Jeneria population declined (Glynn, 1985a). The
urchin population increase dramatically, from 3-5 to 50-80
individuals/m2 (Glynn and Colgan, 1992). The most beautiful
example of the complexity of the ecological disturbance is the
story of the corals, their crustacean guards, and the sea star
Acanthaster in Uva Island (Glynn, 1985b, Glynn et al., 1985a): the
crustacean Trapezia and Alpheus, obligate partners of Pocillopora
corals, feed on the lipid-rich mucus and in exchange, protect them
efficiently against predation of Acanthaster. Once the corals
bleached and died, the crustacean guards migrated or died.
Acanthaster could go through the circle of pocilloporids
surrounding the lagoon and devasted the area. Another example is
the colonization of algal mats on partially bleached corals after
El Niño 1983: algae were grazed by damselfishes which
inflicted additional coral bite and mortality, thus providing
further substrates for algal mats (Glynn, 1990). Damselfish
interactions are complex as they also protect against Acanthaster
(Glynn and Colgan, 1992).
Erosion
Reef framework destruction was evaluated in the very detailed
analysis of bioerosion conducted by Glynn (1988b), Reaka-Kula et
al. (1996) in Panama and Galapagos. The bioerosion increased to
respectively 10-20 kgCaCO3/m2.year and 20-40 kgCaCO3/m2.year, with
a net erosion of somewhat less than 10 kg/m2.year, or around
7mm/year. In Uva Island, the erosion is now of 22 mm/year, and
even 44 mm/y at the walls (Eakin, 1992, 1996).
Geological comparaison
From a geological point of vue, reef ecosystems recovered
slowly from extinction events (Cowen, 1988, and ref. therein). The
present degradation of coral reefs, with its magnitude and speed,
due both to local and global reasons, has no known equivalent in
the past time, put aside the Cretaceous/Tertiary event. Present
foraminifer shell abnormalities strongly support this comparaison
(see above). Corals survived this probable bolide impact (Grigg,
1992), but the reconstitution of the ecosystem, with reappearance
of hermatypic corals evolving from deep sea ones and of larger
foraminifera from little benthics was a process which needed about
10 millions years (Pêcheux, 1995, Pêcheux and Michaud,
1997 ; Int. Geol. Correl. Prog. 286 "Early Paleogen Benthos",
Jaca, Spain, 1991, verbal conclusion).