Coral Reefs (1990) 8:181-191
Coral Reefs
@ Springer-Verlag 1990
Experimental evidence for high temperature stress
as the cause of El Nifio-coincident coral mortality
P.W. Glynn 1 and L. D'Croz z
1 Divisionof Biologyand LivingResources, RosenstielSchoolof Marine and AtmosphericScience,Universityof Miami,
Florida 33149, USA
2 Centro de Cienciasdel Mar y Limnologia,Universidadde Panamfi,Repfiblicade Panamfi
Accepted 29 May 1989
Abstract. High temperature tolerance experiments performed on Pocillopora damicornis, a major reef-building
coral in the tropical eastern Pacific, resulted in loss of
zooxanthellae, histopathological abnormalities, and
mortality similar to that observed during the severe 198283 E1 Nifio-Southern Oscillation (ENSO) event. Coral vitality declined significantly at 30-32 ~ C during a 10-week
period, but remained high at normal temperatures (2628 ~ C). Laboratory time courses to coral morbidity and
death were similar to those observed in the field. Experimental high temperatures had a greater negative effect on corals from the Gulf of Panama, which experiences seasonally cool upwellings, than on corals from the
nonupwelling Gulf of Chiriqui. The condition of obligate
symbiotic crustaceans (Trapezia, Alpheus) associated
with experimental corals declined with their host's declining condition. All Gulf of Panama corals subjected to
32~ C were dead after 5 weeks, and all of their associated
crustacean symbionts were dead after 9 weeks. Gulf of
Chiriqui corals at 30 ~ C survived for 9 weeks and 42% of
their crustacean symbionts were still alive after 10 weeks.
Coral mortality in the Gulf of Panama was significantly
higher (68.5%) after E1 Nifio warming than after subsequent episodes of unusually intense cool upwellings
(10.4%). Low temperature stress (cool currents and upwelling) has been generally suggested as the critical limiting condition that prevents extensive coral reef development in the eastern Pacific. Our results suggest that infrequent but severe ENSO sea warming events also may
limit reef development in this region.
Introduction
Cool eastern boundary currents and local upwellings
have been acknowledged, for over a century, to be the
main cause of poor development of coral reefs in the
tropical eastern Pacific (J. D. Dana 1843; Yonge 1940;
T.F. Dana 1975; Glynn and Wellington 1983). At 18 ~ C
and below, reef-building corals generally are affected ad-
versely and compete poorly for space with other benthic
organisms (Yonge 1940; Birkeland 1977; Porter et al.
1982). The widespread and significant coral mortality
that occurred coincidently with the severe 1982-83
ENSO (El Nifio-Southern Oscillation) event suggested
that prolonged sea warming could also have major impacts on reef corals in this region (Cort6s et al. 1984;
Glynn 1984; Robinson 1985; Prahl 1986; Glynn et al.
1988). This study presents experimental evidence that
links the prolonged warming conditions of E1 Nifio with
the coral stress and mortality observed in the eastern Pacific in 1983. Our results indicate that upper thermal tolerance limits also should be considered as limiting to
coral reef development and distribution.
Sea surface warming and extensive coral mortality accompanied the 1982-83 ENSO event. Zooxanthellae expulsion ("bleaching") and coral mortality that occurred
throughout the eastern Pacific were closely correlated
with the timing and geographic pattern of sea surface
warming (Glynn 1984; Robinson 1985; Glynn et al.
1988). Corals first showed signs of stress in February
1983, at the height of the sea warming (mean sea surface
temperatures, 30-31 ~ C, i.e. 3-4~ above normal seasonal values) and corals died in areas affected by the E1
Nifio (Costa Rica, Panama, Colombia and Ecuador) until the end of the disturbance in October. Warming in the
Gulf of Panama was delayed by 3 months - until after local, seasonal upwelling (January-April) - and the stress
response of corals there showed a similar lag, starting in
June rather than February.
The initial response of stressed corals involved partial
to full-colony bleaching (Glynn et al. 1985 a). Numerous
confounding effects also accompanied sea warming and
coral death in 1983, namely, seismic activity and high tissue pesticide loads in reef organisms in Panama (Glynn
1983; Glynn et al. 1984); freshwater dilution, increased
sedimentation and high sea level and wave assault in the
Galapagos Islands (Robinson 1985). Such disturbances
have been previously implicated in coral bleaching and
death (Endean 1976; Dodge and Vaisnys 1977; Egafia
and DiSalvo 1982; Glynn et al. 1984; Robinson 1985).
182
However, the consistently high association of coral death
with E1 Nifio warming, and the demonstrated effects of
high temperature stress on corals in the central and western Pacific (Jokiel and Coles 1977; Yang et al. 1980; Yamazato 1981; Kamezaki and Ui 1984), were consistent
with the results of E1 Nifio simulation experiments reported in the present study. More recently, beginning in
the summer of 1987, a bleaching of zooxanthellate cnidarians occurred throughout the Caribbean and surrounding areas (Williams et al. 1987). Unusually high sea
water temperatures, in some cases in combination with
other stressful conditions (e.g., increased irradiance, sedimentation and/or pollution) were again implicated in
this disturbance (Ogden and Wicklund 1988).
Materials and methods
Unattached colonies (8-10 cm diameter) of Pocillopora damieornis
(Linnaeus) that survived the 1983 mortality event served as the test
corals. Sixty colonies were collected at 2-5 m depth from the patch
reefs at Uraba Island (8~
79~
Gulf of Panama, 13
August 1985, and Uva Island (7~
81~
Gulf of
Chiriqui, 17 November 1985 (Fig. 1). Corals were transported to the
laboratory in insulated coolers supplied with aerated sea water.
Transit time for Uraba corals was 2 h and for Uva corals 15 h. Although all transported corals appeared healthy, the crustacean symbionts in the Uva group experienced about 40% mortality. The
crustacean symbionts monitored in this study were the xanthid
crabs Trapezia eorallina Gerstaecker and Trapezia ferruginea Latreille, and the alpheid shrimp Alpheus lottini Guerin. The corals and
crustaceans were allowed to acclimate for 1 week before beginning
each experiment.
Forty-eight apparently healthy colonies with their associated
crustaceans were selected for each experiment. From the end of the
E1 Nifio disturbance to the initiation of the warming experiments,
Uraba and Uva corals had survived for 22 mo and 25 mo respectively. Twelve colonies were maintained, and monitored daily, in
each of 4 outdoor 130 liter (85 x 85 cm) tanks receiving ca. 50% ambient light and supplied with aerated, filtered sea water at ca. 1 liter/
min. The sea water was passed through Strainrite polyester felt filter
bags with a filter pore size of 1 g rating. All but one (the control or
ambient temperature tank) of the tanks was supplied with inflowing
water from a heated reservoir. The corals were evenly spaced in each
tank and separated from each other by 12-15 cm. Crustacean symbionts were free to move among host colonies, which they did. Tank
water temperatures were measured 4-5 times daily (at 0800, 1000,
1200, 1400 and 1700) to the nearest 0.1~ C with precision grade mercury thermometers. Actual mean experimental temperatures (-+
s.e., n = 353 observations per treatment) experienced by the Uraba
corals were: ambient, 27.87~1770.04); 28 ~ C, 28.44~ 0.04); 30 ~ C,
29.61~
0.03); 32 ~ C, 31.68~
0.04). Mean temperatures (n=320
observations per treatment) experienced by the Uva corals were:
ambient, 26.21~
0.07); 26 ~ C, 26.44~
0.07); 28 ~ C, 27.89~
0.08); 30 ~ C, 30.37~
0.07). Anova testing indicated a significant
difference among the temperatures (P<0.001), and a posterior•
SNK testing indicated that all mean temperatures were significantly
different from each other (c~= 0.10).
Coral sampling was determined by strict random assignment;
2 cm branchlets were selected and clipped from each of 3 colonies
per treatment weekly. Visual inspection and the response of the
crustaceans to tactile stimuli revealed the numbers and condition of
the crustacean symbionts. One subsample comprising ca. 20 polyps
was separated from each branchlet for histological examination.
These were placed in Helly's fixative, rinsed and preserved in 70%
ethanol. After decalcification, the tissues were embedded, sectioned
(6 gm thick) and stained separately with Heidenhain's aniline blue,
modified Movat's Pentachrome technique, and Harris's hemato-
!!i
.........................
o
30 40 5 o K .
N-
/
.UVA
Contreras Islands
,~
ISLAND
~
~ ~ : : ~
"
Coiba Island
, I~
_
Cebaco Island
A
. : !!! i : : ~
Gulf of Chiriqu[
i
'
URABA ISL
SABOGA ISLAND
9
f
iiI;"
Pearl Islands
.t
B Gulf of Panamd
78
~
9 ~
IO0
200
3 0 0 KM
PANAMA
Fig. 1. Location of principal collection and study sites off the Pacific
coast of Panama
xylin and eosin. At least 10 subapical polyps per treatment were examined at 400 x magnification, The remaining coral branchlets
were stripped of tissues utilizing a Water Pik with distilled water (Johannes and Wiebe 1970), and the zooxanthellae were separated
from coral tissues by centrifugation (3,000 x g, 10 rain). Zooxanthellae were counted using a hemacytometer (Neubauer chamber)
and light microscope, and chlorophyll concentration determined
after the method of Jeffrey and Haxo (1968). The soluble protein
concentration of coral tissues was determined by Lowry's method
(Peterson 1977).
Coral surface area was determined by relating the mass of paraffin adhering to corals as follows. Pre-weighed, dried coral branchlets
were immersed in 60 ~ C paraffin for 5 seconds and then dried and
183
weighed to obtain the paraffin mass. This was then compared with
a standard curve relating the mass of paraffin adhering to aluminum
foil squares of known area. This method's precision is indicated by
repeated paraffin weight measures of a coral branchlet (n= 6):
mean=0.6594 gm (+ 0.0256, 0.95 conf. lim. of mean). Zooxanthellae densities are expressed in terms of coral surface area and coral
protein. Zooxanthellae densities, coral protein/surface area, and
chlorophyll a/number zooxanthellae were transformed (ln + 1) and
then tested for temperature effects with Model I, 2 factor (temperature, time) anovas with replication and Model I least squares linear
regressions.
The condition of Pocillopora darnicornis at the Saboga Island
coral reef (8~
79~
Fig. 1) was determined at the end
of the E1 Nifio warming (12 September 1983) and the upwelling
cooling (19 March 1985) periods. Sampling was conducted on the
seaward reef flat and forereef slope (1-8 m depth), comprising an
area of about 0.1 ha. Chain-transect sampling, utilizing a 10 m long
chain with 73 sampling points (links) per meter (Porter 1972), was
performed in 1983 when live coral cover was high (ca. 80%). The
condition of whole pocilloporid colonies was assessed in 1985 because of the low abundance of these corals following the 1983 disturbance (Glynn 1984; Glynn et al. 1988). Noted were (a) extent and
pattern of bleaching, (b) polyp expansion/retraction, (c) presence of
invading algae, (d) tissue sloughing, and (e) coral mortality.
Results
Corals at experimental temperatures of 30~
(2=
29.6~
and 32~
(2=31.7~
from the Gulf of
Panama, and 30 ~ C (2 = 30 .4~ C) from the Gulf of Chiriqui exhibited bleaching, coincident with the progressive
loss of zooxanthellae expressed in terms of coral surface
area and coral protein (Fig. 2). Bleaching was severe at
32 ~ C, resulting in stark white colonies; all of these (n = 12
colonies) died after 4 weeks. The only other mortality involved all of the Gulf of Chiriqui corals at 30 ~ C (n--12
colonies) that died after 9 weeks. Anova analyses indicate
a highly significant influence of temperature as time progressed in both experiments (Tables I and 2). Zooxanthellae loss was largely inconsequential at slightly lower
temperatures. At mean temperatures of 27.9~ (ambient) and 28.4 ~ C, number of zooxanthellae/coral protein and chlorophyll a concentration/number of zooxanthellae did not exhibit significant declines over time
(P > 0.05) for Gulf o f Panama corals. And at mean temperatures of 26.2 ~ C (ambient) and 26.4 ~ C, number of
zooxanthellae/coral surface area and number of zooxanthellae/coral protein did not decline significantly over
time (P > 0.05) for G u l f of Chiriqui corals (Fig. 2, Tables
1 and 2), indicating favorable laboratory conditions at
optimal temperatures.
Coral tissue protein levels also demonstrated significant declines with increasing temperature and time in all
cases (Fig. 2, Tables 1 and 2). Chlorophyll a content/
zooxanthellasing cell decreased significantly with time at
32 ~ C in Gulf of Panama corals, and at all experimental
temperatures but ambient (26.2 ~ C) in Gulf of Chiriqui
corals (Fig. 2, Tables I and 2), indicating that the coral
bleaching response was due probably to both loss of
zooxanthellae and a reduction in the concentration of
chlorophyll pigments within zooxanthellae remaining
with the coral host.
At 30 ~ C, the loss of zooxanthellae and coral tissue
protein were more pronounced in Gulf of Panama than
Gulf of Chiriqui corals. The mean experimental temperature was actually slightly higher for the G u l f of Chiriqui
(2=30.37 ~ C) than the G u l f o f Panama (2=29.61 ~ C)
corals.
Histopathological analysis revealed that the few remaining zooxanthellae present in stressed corals were
generally necrotic with unstained nuclei. With increasing
time and temperature, the following lesions were observed in the coral tissues of both experimental groups:
(a) deterioration of epidermal mucous secretory cells;
(b) erosion of epidermal and gastrodermal cell layers;
(c) atrophy of longitudinal retractor muscles; (d) loss of
mesogleal pleat structure; (e) appearance of necrotic nuclei in calicoblastic layer and epidermal and gastrodermal
cells; (f) disappearance of spermaries and developed ova.
Some o f these changes are illustrated in Fig. 3 a-f. The
epidermal mucous secretory cells decreased in size and incorporated less of the Pentachrome stain as the experiments progressed, indicating that corals were secreting
less mucus. A notable degeneration of the cellular architecture and integrity of the epidermal and gastrodermal
cell layers was evident (Fig. 3 b, d and f). For example, at
30 ~ C the mean (n = 20 measurements/week) thickness o f
both epidermal and gastrodermal layers in Gulf o f Chiriqui corals had decreased significantly (P<0.001, t-test)
from 16.2 and 23.4 gm at the beginning of the experiment
to 4.8 and 15.6 gm by week 6, respectively. In contrast,
at 28 ~ C the mean thickness of the epidermal layer was
13.5 gm in weeks I and 6, and reduction of the gastrodermal layer was not significant (20.7 gm in week 1, 18.3 gm
in week 6).
In Gulf of Panama corals held at 32 ~ C, longitudinal
muscle bundles began degenerating by week 2 and by
week 4 no trace of muscle fibers remained. At 30 ~ C, in
both Gulf of Panama and Gulf of Chiriqui corals, muscle
degeneration began later (by weeks 3-4) and by week 6
no muscle bundles were found. At high temperatures (30 ~
and 32 ~ C), more of the mesoglea stained red than the
usual blue with Heidenhain's aniline blue stain, indicating a change in composition of the collagen, and by weeks
2-3 this layer appeared swollen and disoriented. The mesogleal pleat structure was also disoriented and had
largely disappeared by weeks 3 4 . Concordant with the
above-noted changes was the common occurrence o f necrotic nuclei in calicoblastic and epidermal + gastrodermal cells.
Gonads, often both spermaries and oocytes in the
same polyp, were present in both coral groups at the
lower experimental temperatures. For example, oocytes
with cytoplasm around the nuclei, but no vitelline membrane, were present until the third week at 28 ~ C in corals
from the Gulf of Panama, and until the second week in
corals from the Gulf of Chiriqui. Spermatocytes with
large nuclei (stage II, after classification of Szmant-Froelich et al. 1985) were present in several corals through the
third week, and spermatocytes with small nuclei (stage
III) were observed until the fifth week in both experiments. At temperatures of 30 ~ C and 32 ~ C, gonads were
observed in week I samples only.
184
GULF OF PANAMA
/2
GULF OF CHIRIQUl
x
x
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x~
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x=2
I
I
x=
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(Weeks)
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Fig.2. Condition o f experimental corals (zooxanthellae densities,
coral tissue protein and chlorophyll a concentrations) at four temperature treatments over a 10 week period from the Gulf o f P a n a m a
(18 August-21 October 1985) and the Gulf o f Chiriqui (25
N o v e m b e r 1985-27 January 1986). Symbols denoting the different
temperatures for the Gulf o f P a n a m a corals are: x - ambient, 9 28 ~ C, o - 30 ~ C, 9 - 32 ~ C; and for the Gulf o f Chiriqui corals: x
0
I
2
I
4
Time
I
6
I
8
I0
(Weeks)
- ambient, 9 - 26 ~ C, o - 28 ~ C, 9 - 30 ~ C. All u n b r o k e n regression
lines are nonsignificant (P > 0.05, F test). The n u m b e r o f observations are noted at superimposed data points. Negative off-scale
points are also labeled. A l t h o u g h all coral sampling was performed
on the same date, data points at different temperatures were displaced horizontally for easier discrimination
185
Table 1. S u m m a r y results o f a n o v a a n d least s q u a r e s regression analyses, G u l f o f P a n a m a t e m p e r a t u r e e x p e r i m e n t
Variables
Two-way anova
Temps.
• weeks
L e a s t s q u a r e s linear regression
Time
Temp.
Inter.
MCT b
3x10
Zoox./Area
F test
o f line
r2
(in % )
Slope
4•
4 • 4
***"
***
***
***
***
***
Amb.
28 ~ C
30 ~ C
32 ~ C
**
***
***
***
26.98
45.77
88.47
95.90
- 0.0691
- 0.1113
-0.2832
- 1.2379
Zoox./Pro.
3 x 10
4x 4
***
***
***
***
***
***
Amb.
28~
30 ~ C
32 ~ C
ns
ns
***
***
10.48
8.10
71.41
92.46
-0.1436
- 0.9066
Pro#Area
3 x 10
4x4
***
***
***
***
*
*
Amb.
28 ~ C
30~
32 ~ C
*
***
***
***
18.85
39.66
80.46
73.64
- 0.0463
- 0.0824
-0.1385
- 0.3315
Chlor./Zoox.
3 x 10
4x4
**
***
ns
**
ns
**
Amb.
28 ~ C
30 ~ C
32 ~ C
ns
ns
ns
**
0.12
0.58
1.90
66.95
-0.9795
a
3 x 10
Temp.
treat,
Significance levels: * P < 0 . 0 5 ; ** P < 0 . 0 1 ; *** P < 0 . 0 0 1 ; n s = n o n s i g n i f i c a n t
u A posteriori S t u d e n t - N e w m a n - K e u l s test o f differences a m o n g t e m p e r a t u r e s ; 3 x 10 = 3 t e m p e r a t u r e t r e a t m e n t s by 10 weeks, 4 x 4 =
4 t e m p e r a t u r e t r e a t m e n t s by 4 weeks
Table 2. S u m m a r y results o f a n o v a a n d least s q u a r e s regression analyses, G u l f o f Chiriqui t e m p e r a t u r e e x p e r i m e n t
Variables
Two-way anova
L e a s t s q u a r e s linear regression
Temps.
x weeks
Time
Temp.
Inter.
Zoox./Area
4x 9
***a
***
Zoox./Pro.
4x 9
*
Pro./Area
4x 9
Chlor./Zoox.
4x9
MCT b
4x 9
Temp.
treat,
F test
o f line
r2
(in %)
Slope
***
Amb.
26 ~ C
28 ~ C
30~
ns
ns
**
***
10.56
5.01
22.47
77.13
- 0.0506
-0.1769
***
***
Amb.
26 ~ C
28 ~ C
30 ~ C
ns
ns
ns
** *
4.83
10.92
2.63
60.45
- 0.0947
***
**
*
Amb
26 ~ C
28 ~ C
30 ~ C
***
**
**
***
39.56
24.05
28.19
49.55
-0.0473
- 0.0417
-0.0577
-0.0825
***
ns
ns
Amb.
26 ~ C
28 ~ C
30~
ns
**
*
***
3.72
24.52
15.35
51.80
- 0.1123
-0.0845
-0.1785
a Significance levels: * P < 0 . 0 5 ; ** P < 0 . 0 1 ; *** P < 0 . 0 0 1 ; n s = n o n s i g n i f i c a n t
b A posteriori S t u d e n t - N e w m a n - K e u l s test o f differences a m o n g t e m p e r a t u r e s ; 4 • 9 = 4 t e m p e r a t u r e t r e a t m e n t s by 9 weeks
The histopathological
condition of all experimental
corals at the initiation of this study was compared with
n o r m a l ( n o n - b l e a c h e d ) s a m p l e s ofPoeillopora damieornis
c o l l e c t e d a t U r a b a I s l a n d o n 14 J u n e 1 9 8 3 ( G l y n n e t a l .
1985a). With reference to characteristics (a)-(e) noted
above, the condition of the 1983 corals was generally superior to those collected in 1985 (E. C. Peters, personal
communication).
Crustacean
s y m b i o n t s (Alpheus lottini a n d Trapezia
spp.) associated with Gulf of Panama corals had declined
to 14.3% and 0% of their initial abundances by the ninth
week of the simulation experiment at 30 ~ C and 32 ~ C res p e c t i v e l y ( F i g . 4). T h e s y m b i o n t m o r t a l i t y r a t e s w e r e s i g nificantly different at the three temperature
regimes
(P<0.05,
Friedman
two-way
analysis of variance by
ranks). Pairwise statistical testing of ambient vs 30 ~ C
186
Fig. 3 a-f. Photomicrographs of Poeillopora damicornis illustrating
condition of polyps during the E1 Nifio simulation experiment.
a Section near bottom of stomodaeum showing spermaries and
oocytes present on mesenteries, week 1 (27 August 1985), temperature treatment = 30 ~ C, Gulf of Panama, stained with Movat's Pentachrome, b Section through gut, mucosecretory cells of epidermis
greatly reduced in number and size, week 6 (1 October 1985), 30 ~ C,
Gulf of Panama, Movat's Pentachrome. e Section through upper
gut showing oocytes, spermaries and numerous zooxanthellae in
gastrodermis, week 2 (1 December 1985), 28 ~ C, Gulf of Chiriqui,
Heidenhain's aniline blue. d Section through gut showing disorgan-
ized tissue layers, week 6 (1 October 1985), 30 ~ C, Gulf of Panama,
Movat's Pentachrome. e Upper gut showing normal-appearing
epidermis with distended mucosecretory cells and gastrodermis with
numerous zooxanthellae, week I (27 August 1985), 30 ~ C, Gulf of
Panama, Movat's Pentachrome. f Longitudinal section of mesenteries showing thinning of epidermal and gastrodermal tissues,
week 6 (1 October 1985), 32 ~ C, Gulf of Panama, Movat's Pentachrome. Legend: ep = epidermis; gs = gastrodermis; gvc = gastrovascular cavity; m f = mesenterial filament; oc = oocyte; sp =
spermary; z = zooxanthellae. A, B, C and F bar = 100 gm; D and
E bar = 50 gm
187
GULF OF PANAMA
~-
n
16
14
28 ~ C
--0-- 30 ~ C
I00
" ' ~ \ , . ~
~
32~ C
GULF OF CHIRIQUI
I00
50 ~
90
80
8O
70
7O
60
6O
'.
50
\
40
40
50
5~
o "$
20
\
\~
2C
\
I0
01
,b
2'0
3'o
4b
5'o
26~
- 28 ~ C
18
90
50
-~--o
6'0
IE
T;o!
810
O(
,b
2'0 A
40
5'o ~
v'o 8'o
Fig. 4. Percent mortality of crustacean
symbionts associated with experimental
corals from the Gulf of Panama
(18 August-21 October 1985) and the
Gulf of Chiriqui (25 November 198527 January 1986). N refers to the total
number of crustaceans (Alpheus lottini
and Trapezia spp.) at beginning of each
temperature treatment. The periods
during which crustaceans were
associated with dead coral hosts are
indicated by thick broken line segments
at 32~ C after 40 days (Gulf of Panama)
and at 30~ C after 60 days (Gulf of
Chiriqui)
Days
Days
Table 3. Response of Poeillopora damicornis to extreme warming (1983 E1 Nifio) and cooling (1985 upwelling) events at Saboga Island reef,
Pearl Islands, Gulf of Panama
Disturbance event
(sampling date)
E1 Nifio - warming (12 September 1983)
Upwelling - cooling (19 March 1985)
Normal coral before
the event
2,080 a links
125b individuals
Coral condition after the event
Normal
Bleached
Dead
Number
%
Number
%
Number
%
202
78
9.7
62.4
454
34
21.8
27.2
1,424
13
68.5
10.4
a Counts refer to number of 1.3 cm chain links touching coral
b Number of individual colonies examined
and ambient vs 32 ~ C indicated a significant difference
between the latter temperatures only (P < 0.01, Wilcoxon
matched-pairs signed-ranks test), suggesting that
crustacean mortality was highest at 32 ~ C. The numbers
of crustacean symbionts associated with G u l f of Chiriqui
corals surviving after 10 weeks had declined at comparable rates ( P > 0 . 0 5 , Friedman test) to between 40.042.9% of initial abundances at all temperatures. Some
crustaceans remained alive on their dead coral hosts for
up to 3 weeks.
By the end of the E1 Nifio warming event, 68.5% of
pocilloporid corals had died that were alive at the Saboga
Island reef (Gulf of Panama) before the disturbance
(Table 3). Sixteen m o n t h s after the warming event (by
J a n u a r y 1985), upwelling began that was more intense
than any observed since 1972 (Glynn and Stewart 1973;
Glynn 1977, 1984). F o r example, the mean monthly sea
surface temperature at Balboa in March, 1985 was
20.1 ~ C, or 0.6 ~ C lower than the previous M a r c h lows
(1939 and 1923) recorded since the initiation of hydrographic observations in 1908 (courtesy P a n a m a Canal
Commission). R e e f b o t t o m (7 m depth) water temperatures of 17.0 ~ C were recorded at Saboga Island in midMarch 1985. These low thermal conditions consisted of
pulses of cool, upwelled water. The longest period of sus-
rained low sea surface temperatures ( < 20 ~ C) at Balboa
was 5 days. Reef morphology, solar heating and tidal influences have important effects on local thermal regimes,
often resulting in daily warming (Glynn and Stewart
1973). Sampling the same population of pocilloporid
corals that survived the 1983 warming event indicated a
10.4% mortality during the extreme low temperature period (Table 3). E1 Nifio related coral mortality was significantly greater than that resulting from intense upwelling (P < 0.001, 2 x 3 contingency table testing). N o additional mortality occurred within the following m o n t h
(mid-April, R . H . Richmond, personal communication).
CorMs that died during the E1 Nifio period sloughed
stark white tissues devoid o f zooxanthellae. In contrast,
corals that died during the upwelling period sloughed
partially bleached tissues still containing zooxanthellae.
Discussion
Slightly elevated sea temperatures (30-32 ~ C) over a period of several weeks led to declines in coral health and
eventually death in laboratory experiments. The coral's
response to these prolonged high temperatures included
188
rapid loss of symbiotic zooxanthellae, which was accompanied by declines in chlorophyll a and coral tissue protein. Although only temperatures were manipulated in
this study, there is evidence that both conditions are affected by high irradiance levels as well. For example,
Hoegh-Guldberg and Smith (1988) concluded from a laboratory study that the loss of zooxanthellae was more
likely at high temperature and the decline of photosynthetic pigment per zooxanthella was induced by high
light. Also, a natural coral bleaching event at St. Croix
(U.S. Virgin Islands) in 1987 resulted in the loss of zooxanthellae from host tissues and a reduction in chlorophyll pigment concentration per zooxanthella (Gladfelter
1988). This bleaching event was correlated with elevated
sea water temperature, but high light was suspected to be
a contributing factor (Sandeman 1988). The critical influence of light on pigment concentration has also been
demonstrated at low quantum flux (about 10% sunlight),
resulting in an increase in chlorophyll a concentration per
algal cell in Pocillopora damicornis when grown under
blue light (Kinzie et al. 1984).
It is not clear if the gradual deterioration of coral tissues after bleaching (see below) was due to direct coral
tissue damage by the thermal stress or to a nutritional
deficit following zooxanthellae loss. [There could even be
an indirect effect involving the loss of zooxanthellae and
possibly the source of UV-B absorbing compounds
(Dunlap et al. 1986)]. While the metabolic dependence of
pocilloporid corals on their zooxanthellae has been well
documented (Franzisket 1970; Muscatine et al. 1981,
1984; Wellington 1982; Davies 1984), the survival of numerous bleached colonies in the field indicates a capacity
to overcome thermal stress if this kind of disturbance is
not too intense and/or prolonged.
Panamanian pocilloporid corals that experienced severe bleaching in 1983 typically died 2-4 weeks later
(Glynn 1984), a similar period to that observed in the
simulation experiments. Sea warming preceded many of
the bleaching events reported in 1982-83 and during the
Caribbean-wide bleaching disturbance in 1987-88. During both disturbances the warming period often persisted
for 2-3 months (Glynn 1984; Williams et al. 1987; Williams and Bunkley-Williams 1988; Jaap 1988; Ogden and
Wicklund 1988; Coffroth et al., in press). Similar slight,
long-term temperature increases did not precede the simulated E1 Nifio experiments. Further, the experimental
corals were necessarily survivors of the 1982-83 bleaching event and therefore were probably in an altered state
compared with pre-1982 corals. On one hand, it could be
argued that surviving corals were more tolerant of high
temperatures, and on the other that the condition of survivors was weakened by the stress event (see below).
Coles and Jokiel (1978) have presented evidence suggesting that the pigmentation state and thermal history of an
Hawaiian coral (Montipora) were critical in determining
its survival of a subsequent thermal stress. A high acclimation temperature was shown to increase coral survival
to subsequent thermal stress. Since the experimental
corals in Panama survived a period of strong selection in
1983, about 2 years before the present study, and otherwise appeared normal in 1985 (but see below for evidence
of subtle tissue changes), we suspect that our results are
best interpreted to represent upper tolerance limits for
these coral populations.
Corals from the Gulf of Chiriqui that were held at a
mean experimental temperature of 30.37 ~ C experienced
less change (zooxanthellae loss and coral tissue protein
decline) than did corals from the Gulf of Panama at
29.61 ~ C. This difference is not unexpected in that the
Gulf of Chiriqui is a nonupwelling environment and thus
experiences a less variable and higher annual temperature
regime than the upwelling Gulf of Panama (Glynn et al.
1972; Glynn 1977; Dana 1975; Kwiecinski and Chial Z.
1983). Differences in coral thermal tolerances between
Hawaii and Enewetak were found to correspond to the
ambient temperature regimes of those two areas (Coles et
al. 1976; Coles and Jokie11977), and temperature adaptations of calcification rates also have been demonstrated
(Clausen and Roth 1975). Because the experiments in our
study were not conducted simultaneously, present results
are only suggestive of local differences in temperature tolerance.
Coral bleaching has been attributed to a variety of
disturbances, e.g. high and low temperature, subaerial exposure, calm sea conditions, freshwater dilution, high
and low turbidity, sedimentation, storm shock, high and
low light levels, UV radiation, parasite infections, and
pollutants (Brown 1987; Ogden and Wicklund 1988; Williams and Bunkley-Williams 1988; Coffroth et al., in
press). Additionally, numerous branching corals were
uprooted and killed in the Galapagos by strong seas associated with the E1 Nifio event (Robinson 1985). The
marked sea temperature increases observed in the tropical eastern Pacific in 1982-83 corresponded closely with
coral bleaching and mortality events observed in several
areas (Cort6s et al. 1984; Glynn 1984; Prahl 1985; Robinson 1985), suggesting that prolonged sea warming might
be the principal cause of the disturbance in this region.
Moreover, the magnitudes of SST (sea surface temperature) deviations also corresponded significantly with the
severity of coral mortality observed in Costa Rica,
Panama and the Galapagos Islands. In Costa Rica and
western Panama, areas with normally high and stable
temperatures, mean coral mortality was 51.2% and
76.1% respectively, in central Panama and the Galapagos Islands, areas with normally lower and more variable temperatures, coral mortality was 84.7% and 97.0%
respectively (Glynn et al. 1988).
While several reports noted a close correspondence
between coral bleaching and high sea temperatures in the
Caribbean region in 1987 (Ogden and Wicklund 1988;
Williams and Bunkley-Williams 1988), one analysis of
off-shelf SST anomalies indicated no consistent warming
trend at that time (Atwood et al. 1988). The latter study
conceded that temperatures likely reached 30 and 31 ~ C
in shallow, protected waters, but concluded that such
temperatures are not unusual and were probably not responsible for the coral bleaching event. No alternative explanations were offered.
More severe bleaching on the summits of massive
corals than in fissures and the partially shaded sides of
colonies in Costa Rica (Cort6s et al. 1984), Panama
189
(Glynn 1984), the Galapagos Islands (Robinson 1985),
and Jamaica (Sandeman 1988) suggest that light levels
may also have had an impact. In Hawaii, high natural
light was shown to aggravate the damage sustained by a
coral at high water temperature (Coles and Jokiel 1978).
While coral disturbance events in 1982-83 were not
strongly correlated with SST increases or high irradiation
levels in some reef areas outside of the eastern Pacific, e.g.
the Great Barrier Reef system, Australia (Fisk and Done
1985; Harriott 1985; Oliver 1985), a synergistic effect involving both factors was often suggested as the possible
cause of coral bleaching.
Generally, the condition of coral tissues before the
1982-83 E1 Nifio disturbance appeared healthier than
"normal" corals collected about two years later and utilized in the E1 Nifio simulation experiments (Glynn et al.
1985a). It is possible that corals surviving the E1 Nifio
warming period still had not recovered fully after two
years. Also, crustacean symbiont reproductive activities
and densities in surviving corals were unusually low up to
three years after the disturbance (S. L. Gilchrist, unpublished paper). Since these symbionts increase the survivorship of their hosts, by means of surface cleansing
and irrigation (resulting from respiratory and feeding
currents) activities (Glynn 1983 b), the subnormal condition of coral hosts could be due in part to these changes.
Pocilloporid corals affected during periods of intense
upwelling, both in 1985 and 1972 (Glynn and Stewart
1973), were not so severely bleached as corals that were
affected during the E1 Nifio warming event. Coral tissues
subjected to cooling spells still contained numerous zooxanthellae. Perhaps for this reason the symbiotic flora retained by cool-stressed corals was capable of rapid repopulation, thus enhancing the survival and recovery of
host corals.
The histopathological abnormalities observed in this
study, a general atrophy and necrosis of coral tissues,
were similar to those reported in corals that bleached during the 1982-83 E1 Nifio event on eastern Pacific reefs
(Glynn et al. 1985a) and in reef coelenterates that
bleached in the Caribbean during the same period
(Lasker et al. 1984). Foreign organisms, such as bacteria,
fungi, algae and protozoans, were found only occasionally in coral tissues in these studies.
Some crustacean symbionts outlived their coral hosts
at the elevated laboratory temperatures. This result was
observed in another laboratory study that focused on the
condition of crustacean symbionts on coral hosts of variable vitality (Glynn et al. 1985 b), and in the field during
the 1982-83 E1 Nifio disturbance (Glynn 1985). Observations by S. Gilchrist (personal communication) in
Panama (Uva Island reef) during the bleaching event indicate that Trapezia can switch to plankton feeding while
inhabiting dead corals. Plankton-feeding activities (peraeopod waving followed by their movement to mouth
parts and cheliped sweeping producing currents moving
toward mouth parts) were observed in several individuals
and gut analyses of field specimens indicated the ingestion of zooplankton. This plankton-feeding behavior
also was duplicated in the laboratory with natural
zooplankton.
The catastrophic and widespread coral mortality observed during the severe E1 Nifio sea warming event, possibly causing three species of corals to suffer local extinctions in 1983, suggest that marine extinctions can result
from slight temperature increases (Emiliani et al. 1981) as
well as from marked temperature decreases (Stanley
1984). It has been amply demonstrated that most tropical
marine organisms live closer to their upper than lower
thermal tolerance limits (Mayer 1914; Edmondson 1928;
Moore 1972; Johannes 1975). For example, the 1983 high
temperature coral mortalities occurred in Panama during
departures of only 3~4~ above optimum (based on
maximum skeletal growth rates in the field) temperatures
of 27 28~ (Glynn and Stewart 1973; Glynn 1977),
whereas the less marked 1985 low temperature mortalities occurred during departures of 10-11 ~ C below normal. In Florida, coral bleaching and death have occurred
at 2-3 ~ C above optimum temperatures [27-28 ~ C (Jaap
1985; Causey et al. 1988)] and at 11-12~ C below optimum during a winter chilling event (Walker et al. 1982).
In contrast with Edmondson's (1928) findings, Jokiel and
Coles (1977) reported that decreases in water temperature are more harmful to Hawaiian corals than are temperature increases of the same magnitude. They attributed this difference to the length of the experimental exposure times: Edmondson's exposures were for 1 week or
less, whereas those conducted by Jokiel and Coles were
for several weeks. The natural warming (El Nifio) and
cooling (upwelling) disturbances observed in Panama
were of very different durations: stressful high temperatures in 1983 persisted for 5 6 months, whereas extreme
low temperatures in 1985 lasted for only 1 week or less on
different occasions during the 3 month upwelling season.
The severity of coral mortality caused by E1 Nifio events
would seem to be greater than that due to upwelling, at
least under present-day conditions. However, longer periods of intense upwelling could have acted as potent
agents of coral mortality during the Little Ice Age (Glynn
et al. 1983).
While coral reef development is notoriously weak in
the tropical eastern Pacific, coral skeletal growth rates
(Glynn and Stewart 1973; Glynn 1977) and reef accumulation rates (Glynn and Macintyre 1977; Glynn and Wellington 1983, Table 26) are among the highest reported
anywhere (Chave et al. 1972; Kinsey 1982). It is possible
that catastrophic natural warming disturbances of the
magnitude of the 1982-83 E1 Nifio event play an important role in limiting reef growth in the eastern Pacific region.
Acknowledgements.J. Gil, G. Justine A., E.C. Peters and O. Vallarino providedsignificantassistanceduringthe laboratoryphase of
this work. We thank I. Angulo, J. Rosario B. and A. Velarde for
helpingwithlogisticalarrangementsand the fieldstudies.Adviceon
statisticalanalyseswas offeredby N. M. Ehrhardt, S. S. Shapiro and
C.M. Eakin. Commentsby M.W. Colgan,J. Cort6s, C.M. Eakin,
J. S. Feingold,H.R. Lasker,L. Muscatine,E. C. Peters, R. H. Richmond, B. Rinkevich,D. B. Smith,A. M. Szmant, G. M. Wellington
and P.J. Walsh improvedthe clarity of this report. We also thank
J. B. C. Jackson, SmithsonianTropical Research Institute,for logistical and facilitysupport. The participation of personnel from the
Direcci6n General de Recursos Marinos, Ministeriode Comercio e
190
Industrias (Republic of Panama) is gratefully acknowledged. This
research was funded by NSF grant OCE-8415615. Contribution
from the University of Miami, Rosenstiel School of Marine and Atmospheric Science.
References
Atwood DK, Sylvester JC, Corredor JE, Morell JM, Mendez A,
Nodal WJ, Huss BE, Foltz C (1988) Sea surface temperature
anomalies for the Caribbean, Gulf of Mexico, Florida reef track
and the Bahamas considered in light of the 1987 regional coral
bleaching event. Proc Assoc Is Mar Lab Carib 21:47
Birkeland C (1977) The importance of rate ofbiomass accumulation
in early successional stages of benthic communities to the survival of coral recruits. Proc 3rd Int Coral Reef Symp 1:15-21
Brown BE (1987) Worldwide death of corals - natural cyclical
events or man-made pollution? Mar Poll Bull 18:9-13
Causey B, Halas JC, Hudson JH, Jaap WC (1988) Zooxanthellae
expulsions in Florida reefs during 1987. Proc Assoc Is Mar Lab
Carib 21:51
Chave KE, Smith SV, Roy KJ (1972) Carbonate production by
coral reefs. Mar Geol 12:123-140
Clausen CD, Roth AA (1975) Effect of temperature and temperature adaptation on calcification rate in the hermatypic coral
Poeillopora damicornis. Mar Biol 33:93-100
Coffroth MA, Lasker HR, Oliver JK (in press) Coral mortality outside of the eastern Pacific during 1982-1983: relationship to E1
Nifio. In: Glynn PW (ed) Global ecological consequences of the
1982-1983 E1 Nifio-Southern Oscillation. Elsevier Oceanography Series, Amsterdam
Coles SL, Jokiel PL (1977) Effects of temperature on photosynthesis
and respiration in hermatypic corals. Mar Biol 43:209-216
Coles SL, Jokiel PL (1978) Synergistic effects of temperature, salinity and light on the hermatypic coral Montipora verrueosa. Mar
Bio149:187-195
Coles SL, Jokiel PL, Lewis CR (1976) Thermal tolerance in tropical
versus subtropical Pacific reef corals. Pac Sci 30:159-166
Cortrs J, Murillo MM, Guzmfin HM, Acufia J (1984) Pbrdida de
zooxantelas y muerte de corales y otros organismos arrecifales
en el Caribe y Pacifico de Costa Rica. Rev Biol Trop 32:227231
Dana JD (1843) On the temperature limiting the distribution of
corals. Am J Sci Arts 45:130-131
Dana TF (1975) Development of contemporary eastern Pacific
coral reefs. Mar Biol 33:355-374
Davies PS (1984) The role of zooxanthellae in the nutritional energy
requirements of Poeillopora eydouxi. Coral Reefs 2:181-186
Dodge RE, Vaisnys JR (1977) Coral populations and growth patterns: responses to sedimentation and turbidity associated with
dredging. J Mar Res 35:715-730
Dunlap WC, Chalker BE, Oliver JK (1986) Bathymetric adaptations of reef-building corals at Davies Reef, Great Barrier Reef,
Australia. III. UV-B absorbing compounds. J Exp Mar Biol
Ecol 104:239-248
Edmondson CH (1928) The ecology of an Hawaiian coral reef.
Bernice P Bishop Mus Bull 45:1-64
Egafia AC, DiSalvo LH (1982) Mass expulsion of zooxanthellae by
Easter Island corals. Pac Sci 36:61~53
Emiliani C, Kraus EB, Shoemaker EM (1981) Sudden death at the
end of the Mesozoic. Earth Planet Sci Lett 55:317-334
Endean R (1976) Destruction and recovery of coral reef communities. In: Jones OA, Endean R (eds) Biology and geology of coral
reefs 3, Biology 2. Academic Press, New York, pp 215-254
Fisk DA, Done TJ (1985) Taxonomic and bathymetric patterns of
bleaching in corals, Myrmidon Reef (Queensland). Proc 5th Int
Coral Reef Cong 6:149-154
Franzisket L (1970) The atrophy of hermatypic reef corals maintained in darkness and their subsequent regeneration in light.
Int Rev Ges Hydrobiol 55:1-12
Gladfelter EH (1988) The physiological basis of coral bleaching. In:
Ogden J, Wicklund R (eds) Mass bleaching of coral reefs in the
Caribbean: a research strategy. NOAA's Undersea Res Prog, St
Croix, U S Virgin Islands. Res Rpt 88-2:15-18
Glynn PW (1977) Coral growth in upwelling and nonupweUing
areas off the Pacific coast of Panama. J Mar Res 35:567-585
Glynn PW (1983 a) Extensive "bleaching" and death of reef corals
on the Pacific coast of Panama. Environ Conserv 10:149-154
Glynn PW (1983b) Increased survivorship in corals harboring
crustacean symbionts. Mar Biol Lett 4:105-111
Glynn PW (1984) Widespread coral mortality and the 1982/83 E1
Nifio warming event. Environ Conserv 11:133-146
Glynn PW (1988) E1 Nifio-Southern Oscillation 1982-1983: nearshore population, community, and ecosystem responses. Ann
Rev Ecol Syst 19:309-345
Glynn PW, Stewart RH (1973) Distribution of coral reefs in the
Pearl Islands (Gulf of Panama) in relation to thermal conditions. Limnol Oceanogr 18:367-379
Glynn PW, Macintyre IG (1977) Growth rate and age of coral reefs
on the Pacific coast of Panama. Proc 3rd Int Coral Reef Symp
2:251-259
Glynn PW, Wellington GM (1983) Corals and coral reefs of the
Galapagos Islands. University of California Press, Berkeley,
p 330
Glynn PW, Stewart RH, McCosker JE (1972) Pacific coral reefs of
Panama: structure, distribution and predators. Geol Rundschau 61:483-519
Glynn PW, Druffel EM, Dunbar RB (I 983) A dead Central American coral reef tract: possible link with the Little Ice Age. J Mar
Res 41:605-637
Glynn PW, Howard LS, Corcoran E, Freay AD (1984) The occurrence and toxicity of herbicides in reef building corals. Mar Pollut Bull 15:370-374
Glynn PW, Peters EC, Muscatine L (1985a) Coral tissue microstructure and necrosis: relation to catastrophic coral mortality
in Panama. Dis Aquat Org 1:29-37
Glynn PW, Perez M, Gilchrist SL (1985 b) Lipid decline in stressed
corals and their crustacean symbionts. Biol Bull 168:276-284
Glynn PW, Cortes J, Guzman HM, Richmond RH (1988) E1 Nifio
(1982-83) associated coral mortality and relationship to sea surface temperature deviations in the tropical eastern Pacific. Proc
6th Int Coral Reef Symp 3:237-243
Harriott VH (1985) Mortality rates of scleractinian corals before
and during a mass bleaching event. Mar Ecol Prog Ser 21:8188
Hoegh-Guldberg O, Smith GJ (1988) Physiological correlates of
light and temperature stress in two pocilloporid corals. Proc Assoc Is Mar Lab Carib 21:57
Jaap WC (1985) An epidemic zooxanthellae expulsion during 1983
in the lower Florida Keys coral reefs: hyperthermic etiology.
Proc 5th Int Coral Reef Cong 6:143-148
Jaap WC (1988) The 1987 zooxanthellae expulsion event at Florida
reefs. NOAA's Undersea Res Prog. Res Rpt 88-2:24-29
Jeffrey SW, Haxo FT (1968) Photosynthetic pigments of symbiotic
dinoflagellates (zooxanthellae) from corals and clams. Biol Bull
135:149-165
Johannes RE (1975) Pollution and degradation of coral reef communities. In: Ferguson Wood EJ, Johannes RE (eds) Tropical
Marine Pollution. Elsevier Oceanogr Ser 12:13-51
Johannes RE, Wiebe WJ (1970) A method for determination of
coral tissue biomass and composition. Limnol Oceanogr
15:822-824
Jokiel PL, Coles SL (1977) Effects of temperature on the mortality
and growth of Hawaiian reef corals. Mar Biol 43:201-208
Kamezaki N, Ui S (1984) Bleaching of hermatypic corals in
Yaeyama Islands. Mar Parks J 61:10-13
Kinsey DW (1982) The Pacific/Atlantic reef growth controversy.
Proc 4th Int Coral Reef Symp 1:493-498
Kinzie RA III, Jokiel PL, York R (1984) Effects of light of altered
spectral composition on coral zooxanthellae associations and
on zooxanthellae in vitro. Mar Biol 78:239-248
191
Kwiecinski B, Chial-Z B (1983) Algunos aspectos de la oceanografia
del Golfo de Chiriqui, su comparaci6n con el Golfo de Panam/t.
Rev Biol Trop 31:323-325
Lasker HR, Peters EC, Coffroth MA (1984) Bleaching of reef coelenterates in the San Blas Islands, Panama. Coral Reefs 3:183190
Mayer AG (1914) The effects of temperature upon tropical marine
animals. Pap Tortugas Lab 6:1-24
Moore HB (1972) Aspects of stress in the tropical marine environment. Adv Mar Biol 10:21%269
Muscatine L, McCloskey LR, Marian RE (1981) Estimating the
daily contribution of carbon from zooxanthellae to coral animal
respiration. Limnol Oceanogr 26:601-611
Muscatine L, Falkowski PG, Porter JW, Dubinsky Z (1984) Fate of
photosynthetic fixed carbon in light- and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc R Soc
Lond B 222:181-202
Ogden J, Wicklund R (eds) (1988) Mass bleaching of coral reefs in
the Caribbean: a research strategy. NOAA's Undersea Res
Prog, Res Rpt 88-2, 51 pp
Oliver J (1985) Recurrent seasonal bleaching and mortality of corals
on the Great Barrier Reef. Proc 5th Int Coral Reef Congr
4:201-206
Peterson GL (1977) A simplification of the protein assay method of
Lowry et al. which is more generally applicable. Anal Biochem
83:346-356
Porter JW (1972) Patterns of species diversity in Caribbean reef
corals. Ecology 53:745-748
Porter JW, Battey JF, Jason Smith G (1982) Perturbation and
change in coral reef communities. Proc Natl Acad Sci USA
79:1678-1681
Prahl H yon (1985) Blanqueo masivo y muerte de corales hermatipicos en el Pacifico Colombiano atribuidos al fen6meno de
E1 Nifio 1982-83. Bol Erfen 12:22-24
Prahl H von (1986) Crecimiento del coral Pocilloporadamicornis durante y despu6s del fen6meno E1 Nifio 1982-1983 en la Isla de
Gorgona, Colombia. Bol Erfen 18:11-13
Robinson G (1985) Influence of the 1982-83 E1 Nifio on Galfipagos
marine life. In: Robinson G, del Pino EM (eds) E1 Nifio en las
Islas Galapagos: el evento de 1982-1983. Quito, Ecuador, pp
153-190
Sandeman IM (1988) Coral bleaching at Discovery Bay, Jamaica: a
possible mechanism for temperature-related bleaching. In:
Ogden J, Wicklund R (eds) Mass bleaching of coral reefs in the
Caribbean: a research strategy. NOAA's Undersea Res Prog, St
Croix, U S Virgin Islands, Res Rpt 88-2:4648
Stanley SM (1984) Marine mass extinctions: a dominant role for
temperature. In: Nitecki MH (ed) Extinctions. University of
Chicago Press, Chicago, pp 69-117
Szmant-Froelich A, Rnetter M, Riggs L (1985) Sexual reproduction
of Faviafragum (Esper): lunar patterns of gametogenesis, embryogenesis, and planulation in Puerto Rico. Bull Mar Sci
37:880-892
Walker ND, Roberts HH, Rouse LJ Jr, Huh OK (1982) Thermal
history of reef-associated environmentsduring a record cold-air
outbreak event. Coral Reefs 1:83-87
Wellington GM (1982) An experimental analysis of the effects of
light and zooplankton on coral zonation. Oecologia (Bed)
52:311-320
Williams EH Jr, Bunkley-WilliamsL (1988) Bleaching of Caribbean
coral reef symbionts in 1987-1988. Proc 6th Int Coral Reef
Syrup 3:313-318
Williams EH Jr, Goenaga C, Vicente V (1987) Mass bleachings on
Atlantic coral reefs. Science 238:877878
Yamazato K (1981) A note on the expulsion of zooxanthellae during summer, 1980 by the Okinawan reef-buildingcorals. Sesoko
Mar Sci Lab Tech Rep 8:9-18
Yang R-T, Yeh S-Z, Sun C-L (1980) Effects of temperature on reef
corals in the Nan-Wan Bay, Taiwan. Inst Oceanogr Nat Taiwan
Univ (Special Publ) 23:1-27
Yonge CM (1940) The biology of reef-buildingcorals. Br Mus (Nat
Hist), Sci Repts Gr Barrier Reef Exped 1928-1929 1:353-391