(Glynn, 2001). Sea-surface perturbations associated with
the warm phase of ENSO have the strongest effect on
corals in the eastern tropical Pacific (Glynn et al., 2001);
however, corals in the Central and Western Pacific
(Hoegh-Guldberg, 1999), Indian Ocean (Wilkinson, 2000),
and Caribbean Sea (Coffroth et al., 1990) are also affected.
These perturbations include elevated SSTs, elevated sea
level, depressed main thermocline, diminution and reversal
of surface and subsurface currents, increased wave assault,
decreased nutrients and productivity, and increased rainfall
(and concomitant increased sedimentation in nearshore
environments) (Philander, 1983; Fiedler et al., 1992). During ENSO cool phase (La Niña), corals in the Eastern
Pacific are exposed to opposite conditions; depressed SSTs,
lower sea level, elevated main thermocline, intensification
of westward-flowing currents, normal wave action,
increased nutrients and productivity, and decreased rainfall.
SST anomalies and coral mortality
Sea-surface warming associated with ENSO is implicated
as the primary cause of coral bleaching and mortality
(Glynn et al., 1988; Glynn and D’Croz, 1990). Thermal
impacts are more related to temperature anomalies (differences from long-term mean temperatures) than absolute
temperature. For example, during the 1982–1983 ENSO,
mean coral mortality was higher in the Galapagos Islands
(99%) than in Costa Rica (51%) even though mean
monthly SSTs were lower (28.5 vs. 31
C). Temperature
anomalies ranged from þ3 to þ4
C in the Galapagos
Islands where corals were strongly affected, compared
to þ1 to þ2
C in Costa Rica (Glynn, 1990). In the Indian
Ocean, temperatures 3–5
C above normal were reported,
and mortality up to 90% in shallow habitats was observed
(Wilkinson et al., 1999).
Though less well studied, cooling can also stress corals,
resulting in mortality. Populations of Pocillopora at Devil’s
Crown, Galapagos Islands, were reduced by approximately
85% following exceptionally cool conditions in 2007
(Feingold, unpublished data). Bleaching and mortality were
reported in Costa Rica during cooling associated with
a 1985 La Niña event (Guzmán and Cortés, 2001).
Combined effects of ENSO can result in regional-scale
extirpation of corals and dramatic change to reef communities. Reductions of corals and subsequent bioerosion of
reef framework in the Galapagos Islands have eliminated
the few reefs that occurred there (Glynn and Ault, 2000).
Coral bleaching
ENSO-related coral bleaching occurs when endosymbiotic
dinoflagellates (zooxanthellae) either diminish in number
within the coral host tissues, or lose their photosynthetic
pigment. Since zooxanthellae are an important source of
energy, reef-building corals will die unless sufficient
populations of the endosymbiont become re-established.
Bleaching severity shows species-specific trends, with
some corals being sensitive (e.g. Pocillopora) and others
resistant (e.g. Psammocora) (Glynn, 1990). Bleaching
occurs when coral is physiologically stressed, and is most
often associated with positive SST anomalies (warming),
although other perturbations such as cooling, lower sea
level, salinity decrease, and sedimentation contribute.
Bleaching sensitivity is also related to the endosymbiont clade; some zooxanthellae are more tolerant to elevated temperatures than others. For example, in Panama,
pocilloporid corals with zooxanthellae in clade D did not
bleach, whereas those with clade C did (Baker, 2004).
Thus, coral survivors of the 1982–1983 ENSO predominantly harbored clade D endosymbionts, and when these
corals were exposed to highly elevated temperatures again
in 1997–1998, they were not as severely affected as they
were in 1982–1983 (Glynn et al., 2001).
Sea level decrease also results in coral bleaching and
mortality, particularly severe when combined with spring
low tides. Sea level is low in the west during ENSO warm
phase, and low in the east during ENSO cool phase
(La Niña). For example, reef flats were exposed in Guam
during warm phase ENSO in 1972–1973 (Yamaguchi,
1975), and corals were affected in French Polynesia and
the Tokelau Islands during the 1982–1983 and 1993
events (Coffroth et al., 1990). La Niña conditions in
1989 and 1993 resulted in sub-aerial exposure of coral
on the reef flat and high coral mortality at Uva Island,
Panama (Eakin, 2001).
Mitigation by depth and light
Coral reefs and coral communities are more common in
shallow waters (<10 m depth) where positive temperature
anomalies are strongest. However, corals also live in
deeper water where sea-surface warming is not so pronounced. In the Eastern Pacific, corals living >15 m in
depth were not so strongly affected by ENSO-related
warming (0% mortality) as those in shallow waters, due
to periodic shoaling of cooler water from the subsurface
mixed layer (Feingold, 1996). Wilkinson et al. (1999)
reported less coral mortality at depths >20 m (50%) compared to shallower habitats (90%) in the Indian Ocean.
Lower levels of light at deeper depths may contribute to
lessening impacts, since combined effects of elevated
levels of light and temperature together are more detrimental to corals than either one alone (Jokiel and Coles, 1990).
Coral reproduction and dispersal
Reproductive activity (gametogenesis) in some important
reef-building coral families (e.g. Pocilloporidae, Poritidae,
and Agariciidae) in the Eastern Pacific can either be detrimentally affected or enhanced by ENSO-related seawater
warming. Moderate to weak events can improve conditions for reproductive success since reproduction typically
occurs under warmer conditions; however, strong events
can cause reproductive failure if temperatures rise too high
(Colley et al., 2006). Corals disperse to the tropical eastern
Pacific via countercurrents that transport water from the
west to the east. During ENSO warm phase, the intensity
of these currents increase, possibly allowing a more rapid
366
EL NIN ˜ O, LA NIN ˜ A, AND ENSO
the warm phase of ENSO have the strongest effect on
corals in the eastern tropical Pacific (Glynn et al., 2001);
however, corals in the Central and Western Pacific
(Hoegh-Guldberg, 1999), Indian Ocean (Wilkinson, 2000),
and Caribbean Sea (Coffroth et al., 1990) are also affected.
These perturbations include elevated SSTs, elevated sea
level, depressed main thermocline, diminution and reversal
of surface and subsurface currents, increased wave assault,
decreased nutrients and productivity, and increased rainfall
(and concomitant increased sedimentation in nearshore
environments) (Philander, 1983; Fiedler et al., 1992). During ENSO cool phase (La Niña), corals in the Eastern
Pacific are exposed to opposite conditions; depressed SSTs,
lower sea level, elevated main thermocline, intensification
of westward-flowing currents, normal wave action,
increased nutrients and productivity, and decreased rainfall.
SST anomalies and coral mortality
Sea-surface warming associated with ENSO is implicated
as the primary cause of coral bleaching and mortality
(Glynn et al., 1988; Glynn and D’Croz, 1990). Thermal
impacts are more related to temperature anomalies (differences from long-term mean temperatures) than absolute
temperature. For example, during the 1982–1983 ENSO,
mean coral mortality was higher in the Galapagos Islands
(99%) than in Costa Rica (51%) even though mean
monthly SSTs were lower (28.5 vs. 31
C). Temperature
anomalies ranged from þ3 to þ4
C in the Galapagos
Islands where corals were strongly affected, compared
to þ1 to þ2
C in Costa Rica (Glynn, 1990). In the Indian
Ocean, temperatures 3–5
C above normal were reported,
and mortality up to 90% in shallow habitats was observed
(Wilkinson et al., 1999).
Though less well studied, cooling can also stress corals,
resulting in mortality. Populations of Pocillopora at Devil’s
Crown, Galapagos Islands, were reduced by approximately
85% following exceptionally cool conditions in 2007
(Feingold, unpublished data). Bleaching and mortality were
reported in Costa Rica during cooling associated with
a 1985 La Niña event (Guzmán and Cortés, 2001).
Combined effects of ENSO can result in regional-scale
extirpation of corals and dramatic change to reef communities. Reductions of corals and subsequent bioerosion of
reef framework in the Galapagos Islands have eliminated
the few reefs that occurred there (Glynn and Ault, 2000).
Coral bleaching
ENSO-related coral bleaching occurs when endosymbiotic
dinoflagellates (zooxanthellae) either diminish in number
within the coral host tissues, or lose their photosynthetic
pigment. Since zooxanthellae are an important source of
energy, reef-building corals will die unless sufficient
populations of the endosymbiont become re-established.
Bleaching severity shows species-specific trends, with
some corals being sensitive (e.g. Pocillopora) and others
resistant (e.g. Psammocora) (Glynn, 1990). Bleaching
occurs when coral is physiologically stressed, and is most
often associated with positive SST anomalies (warming),
although other perturbations such as cooling, lower sea
level, salinity decrease, and sedimentation contribute.
Bleaching sensitivity is also related to the endosymbiont clade; some zooxanthellae are more tolerant to elevated temperatures than others. For example, in Panama,
pocilloporid corals with zooxanthellae in clade D did not
bleach, whereas those with clade C did (Baker, 2004).
Thus, coral survivors of the 1982–1983 ENSO predominantly harbored clade D endosymbionts, and when these
corals were exposed to highly elevated temperatures again
in 1997–1998, they were not as severely affected as they
were in 1982–1983 (Glynn et al., 2001).
Sea level decrease also results in coral bleaching and
mortality, particularly severe when combined with spring
low tides. Sea level is low in the west during ENSO warm
phase, and low in the east during ENSO cool phase
(La Niña). For example, reef flats were exposed in Guam
during warm phase ENSO in 1972–1973 (Yamaguchi,
1975), and corals were affected in French Polynesia and
the Tokelau Islands during the 1982–1983 and 1993
events (Coffroth et al., 1990). La Niña conditions in
1989 and 1993 resulted in sub-aerial exposure of coral
on the reef flat and high coral mortality at Uva Island,
Panama (Eakin, 2001).
Mitigation by depth and light
Coral reefs and coral communities are more common in
shallow waters (<10 m depth) where positive temperature
anomalies are strongest. However, corals also live in
deeper water where sea-surface warming is not so pronounced. In the Eastern Pacific, corals living >15 m in
depth were not so strongly affected by ENSO-related
warming (0% mortality) as those in shallow waters, due
to periodic shoaling of cooler water from the subsurface
mixed layer (Feingold, 1996). Wilkinson et al. (1999)
reported less coral mortality at depths >20 m (50%) compared to shallower habitats (90%) in the Indian Ocean.
Lower levels of light at deeper depths may contribute to
lessening impacts, since combined effects of elevated
levels of light and temperature together are more detrimental to corals than either one alone (Jokiel and Coles, 1990).
Coral reproduction and dispersal
Reproductive activity (gametogenesis) in some important
reef-building coral families (e.g. Pocilloporidae, Poritidae,
and Agariciidae) in the Eastern Pacific can either be detrimentally affected or enhanced by ENSO-related seawater
warming. Moderate to weak events can improve conditions for reproductive success since reproduction typically
occurs under warmer conditions; however, strong events
can cause reproductive failure if temperatures rise too high
(Colley et al., 2006). Corals disperse to the tropical eastern
Pacific via countercurrents that transport water from the
west to the east. During ENSO warm phase, the intensity
of these currents increase, possibly allowing a more rapid
366
EL NIN ˜ O, LA NIN ˜ A, AND ENSO