Proceedings 9th International Symposium, Bali, Indonesia 23-27 October 2000, Vol. 2.

Effects of the 1997-98 El Niño-Southern Oscillation on Eastern Pacific corals and coral reefs: An overview

P.W. Glynn1 ABSTRACT In magnitude (+ 3-4o C anomalies) and duration (3-4 months), the 1997-98 El Niño-Southern Oscillation (ENSO) was comparable over most eastern tropical Pacific areas to the record-setting ENSO of 1982-83. The effects of these two recent, very strong ENSOs on eastern Pacific coral communities are compared. Both events caused widespread bleaching and mortality of zooxanthellate corals over the entire eastern equatorial Pacific region. High coral mortality occurred from 16o N (southern México) to 2o S (Ecuador, including the Galápagos Islands and mainland) in 1982-83, and from 24o N (northern México) to 2o S in 1997-98. The timing and severity of were closely correlated with positive sea surface temperature (SST) anomalies. Coral community recovery since 1982-83 has been completely reversed in many areas. Certain rare corals suffered extreme reductions in abundance to local extirpations in 1997-98. Likely delayed biotic effects are presently under study at several eastern Pacific sites.

Keywords El Niño 1997-98 sea warming, Coral reported (Goreau et al. 2000). For documentation and bleaching, Eastern Pacific more detailed information on recent disturbances in the eastern Pacific, the reader is referred to work at particular Introduction sites, which is being prepared for a forthcoming special issue of the Bulletin of Marine Science, entitled “Eastern In several respects, the 1982-83 and 1997-98 ENSO Pacific Reef Coral Mortality and the 1997-98 El Niño- events resulted in marked perturbations to eastern Pacific Southern Oscillation”. reef-coral communities. These two very strong events occurred only 16 years apart. Several workers have Methods documented the magnitude and similarities of these recent ENSOs relative to their intensity, duration and far- Long-term (1982-1999) SSTs and SST anomalies reaching effects (Wolter and Timlin 1998, Chavez et al. (SSTA) near 12 coral bleaching sites in 1997-98 were 1999, McPhaden 1999, Enfield 2001). Their impacts on examined utilizing Reynolds data sets (Reynolds and reef-building or zooxanthellate corals were severe in the Smith 1994). These data are weekly SSTs at 1x1o eastern Pacific, but notably different in terms of the extent resolution based on satellite-derived data and ship/buoy of bleaching/mortality and geographic influence. The observations (National Center for Environmental varied short-term and longer-term disturbances to coral Prediction, NCEP 2001). In situ temperature reefs precipitated by the 1982-83 ENSO, not least of measurements were made with calibrated mercury which has been the virtual elimination of coral reefs in the thermometers (± 1o , ± 0.5o C) or with a variety of Galápagos Islands (Glynn 1994, Reaka-Kudla et al. calibrated underwater temperature loggers (e.g. Hobo, 1996), have certainly been unwelcome, but nonetheless Stowaway and Tidbit, ± 0.5o C, Onset Computer well documented. In one sense, ongoing study of the Corporation). Animated SST anomalies (a blended 1997-98 ENSO will broaden our understanding of the satellite product) available on the National Oceanographic damage caused by sea warming episodes, and allow a first and Atmospheric Administration’s web site (NOAA approximation of effects of consecutive disturbances of 1997-98) were also examined. this genre. Twelve areas, each represented by multiple sampling This report offers a preliminary broad sketch of the sites, are noted from 2o south to 24o north (Fig. 1). effects of the 1997-98 ENSO on eastern Pacific corals and Quantitative information on coral condition, i.e. the extent coral reefs. In addition to coral condition, brief mention is of bleaching and mortality in all zooxanthellate corals, also made of coral reproductive activity and skeletal was obtained from interviews with local workers, studies growth during the 1997-98 ENSO. The chief motivation in progress, and manuscripts in press ( caption to Fig. 1). for presenting this synopsis is to provide information on It is cautioned that coral condition, reported here as disturbances in the eastern Pacific region, and to alert percent of affected, is not standardized. For workers of forthcoming studies for comparisons with example, in some studies bleaching and mortality were ENSO 1997-98 effects in other coral reef biogeographic reported as numbers of colonies affected and in others as regions. A recent global analysis has concluded that changes in coral surface cover. Also, data collection at bleaching in 1998 in most of the major coral reef regions - particular sites was not always at comparable times in - western and central Indian Ocean, west and east Pacific, terms of the maximum bleaching and mortality effects. and the greater Atlantic -- has been the most extensive Even though coral condition was estimated near the since 1982, when large-scale bleaching events were first height of greatest impact, some species with delayed

1 Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, Florida, 33149-1095 USA responses (e.g. Porites panamensis Verrill) and others Coral tissues from 10 zooxanthellate species were capable of rapid recovery (e.g. Porites lobata Dana) were sampled repeatedly for reproductive activity during the not included in all assessments. It is further cautioned that 1997-98 ENSO at several sites, including Caño Island, the reporting of general area responses is highly Costa Rica (April 1997, May 1998), Gulfs of Chiriquí dependent on the coral species composition at particular (January, October, September 1997, March 1998) and sites, i.e. the relative abundances of bleaching-susceptible Panamá (January 1997, March 1998), and the and resistant species. southern/central Galápagos Islands (May 1997, 1998). The tissues selected for sampling were from whole, normally-pigmented colonies or from pigmented tissue patches on colonies that experienced only partial bleaching. Collection and fixation procedures, histological processing and assessment of gonadal condition followed Glynn et al. (2000) and earlier studies cited therein. Coral skeletal extension rates reported from Colombia (Vargas-Ángel et al. 2001) were obtained utilizing Alizarin Red S vital stain.

Results The first occurrence of ENSO 1997-98 anomalies of 1-2 o C in the eastern tropical Pacific region, between 80- 100o W, were evident by March to April 1997 (Chavez et al. 1999, McPhaden 1999, Enfield 2001). Stressful SSTs affecting zooxanthellate corals, i.e. prolonged positive anomalies of 2-3o C during the warm season, were observed at equatorial eastern Pacific sites and Mexican sites from early to mid 1997: Galápagos Islands (Glynn et Fig. 1. Coral bleaching and mortality observed in the al. 2001, Podestá and Glynn 2001, Wellington et al. eastern Pacific during the 1997-98 ENSO event. 2001), Colombia (Vargas-Ángel et al. 2001), Panamá Locations and samplng dates: 1 – Galápagos Is, 10-20 (Glynn et al. 2001), Costa Rica (Guzmán and Cortés May 1998, 2 – mainland Ecuador, 19-21 May 1998, 3 – 2001, Jiménez et al. 2001), lower Baja California (Reyes Gorgona I, Colombia, several from May 1997-Aug 1998, Bonilla 2001), and Banderas Bay (Carriquiry et al. 2001). 4 - La Chola and Tebada, Colombia, 6-11 Jun 1998 and Reynolds weekly SST observations for the Galápagos 20-23 Sep 1998, 5 – Malpelo I, Colombia, 14-15 Mar Islands (0o S) showed peak SSTs in early 1998 of 30 o C 1998, 6 - Gulf of Panamá, 25-26 May 1999, 7 – Gulf of (Fig. 2). The Galápagos area experienced a rapid rise in Chiriquí, several from 14 Oct 1997-19 Dec 1998, 8 - SSTAs in early 1997, between 4o to nearly 6o C, which Caño I, Costa Rica, May 1998 and Feb 1999, 9 - persisted for several months then declined rapidly in early Guanacaste, Costa Rica, Jun to Oct 1997, 10 - Huatulco, 1998. Gulf of Chiriquí (7o N) SSTs showed a similar México, Sep 1998, 11 – Banderas Bay, México, Aug-Oct temporal pattern with maximum SSTAs of 2o C. 1997; 12 - Baja California (south), Sep-Nov 1997. Maximum SSTs reached 30o C at three locations off Sources: 1, 2, 6 and 7, Glynn et al. (2001) 3, 4 and 5, México (15 o -24o N), with highest SSTAs of 3o C off Vargas-Ángel et al. (2001) 8, Guzmán and Cortés (2001) Baja California (Fig. 2). The reader is referred to the 9, Jiménez et al. (2001) 10 - Reyes-Bonilla et al. (2001) collection of 12 SST and SSTA plots on the World-Wide 11- Carriquiry et al. (2001) 12 - Reyes-Bonilla (2001). Web at http://www.coral.noaa.gov/glynn2.

Fig. 2 Reynolds NCEP weekly SSTs and SSTAs (1982-1999) near two locations, in the eastern equatorial Pacific and off subtropical México, where coral condition was assessed during the 1997-98 ENSO event. Temperature observations are from 1x1o grids centered at 00o , 90 o W (Galápagos Islands) and 24 o N, 109 o W (Baja California).

Coral bleaching generally occurred from one to three heavily eroded frameworks on the Ecuadorian coast, months following the initial high temperature periods, i.e. remnants of the 1982-83 ENSO, can still be recognized by mid to late 1997. Initiation of bleaching in Galápagos and support a few relatively recent coral recruits. Large corals was unusually prolonged, not occurring until mid sections of pocilloporid reefs in the Gulf of Panamá have December 1997, about 9 months after the ENSO warming fully recovered from the 1982-83 disturbance and were event began. By that time corals had experienced positive unaffected in 1997-98. Pocilloporid reefs at Huatulco and anomalies of 2-4 o C for 9 months, at SSTs of 26-27 o C, in north Banderas Bay, México, experienced nearly total below critically elevated temperatures that induce mortality in 1997-98 (95-99%), thus rendering these reef bleaching over shorter time intervals (Podestá and Glynn frameworks susceptible to bioerosion and physical 1997). Coral bleaching and mortality continued in the damage. Galápagos until May 1998, during which 2-3o C ano- Despite high overall levels of bleaching (32- 97%) malies persisted and SSTs reached 29-30o C. during the 1997-98 ENSO, several coral species sampled The evolution and propagation of elevated SSTAs (3- in the equatorial eastern Pacific revealed significant 5o C) into the equatorial eastern Pacific during 1997-98 gonadal activity. The tissues with gonads and mature were portrayed as on-line, near real-time NOAA weekly gametes evidently were only minimally affected by the animations. These animations also revealed filaments (2- warming event as they displayed normal pigmentation in 3oC anomalies) emerging from the equatorial warm most collections. At Caño Island, Costa Rica, 7 species tongue and propagating northeastward toward the Central [ damicornis (Linnaeus), Pocillopora elegans American coast. These warm pulses, verified by in situ Dana, Porites lobata, Gardineroseris planulata (Dana), temperature recorders, occurred in mid 1997 and early to Pavona gigantea Verrill, Pavona varians Verrill, and mid 1998, and coincided with two coral bleaching Pavona sp.a] contained mature gametes in April 1997 and episodes in Panamá (Glynn et al. 2001), Costa Rica May 1998. In the Gulf of Chiriquí, Panamá 8 species (all (Jiménez et al. 2001) and along the Colombian coast of the preceding species excluding P. damicornis and (Vargas-Ángel et al. 2001). During most of the 1997-98 including Porites panamensis and Pavona clavus Dana) ENSO, the NOAA spatial plots indicated relatively low contained mature gametes in January 1997 and March (0-1.5o C) SSTAs in the Panamá Bight. 1998. In the Galápagos, 6 species (P. damicornis, P. Coral mortality was relatively low in the equatorial elegans, P. lobata, P. varians, Pocillopora sp.a, and eastern Pacific except for the Galápagos Islands (Fig. 1, Diaseris distorta Michelin) produced mature gametes area 1) with 26% overall mortality. Mortality summarized during the ENSO event. for five areas in the Panamá Bight (Fig. 1, areas 2-6) Mean linear skeletal extension rates of Pocillopora ranged from 0% (Gulf of Panamá) to 4.5% (Ecuadorian damicornis measured at two reefs in Colombia were coast). High levels of bleaching, 32.4% to 97.3%, significantly higher by 30% and 43% during the 1997-98 occurred in two non upwelling environments off Costa ENSO period than in previous non-ENSO years (Vargas- Rica and in the Gulf of Chiriquí. These high incidences of Ángel et al. 2001). However, the mean skeletal growth of bleaching, however, resulted in relatively low coral Psammocora stellata (Verrill), measured at one site in mortality, ranging from 2.7% (Caño Island) to 13.1% Colombia, was significantly less (by -18%) during the (Gulf of Chiriquí). The highest coral mortalities occurred 1997-98 ENSO compared with earlier non-ENSO years. along the Mexican coast. Six coral reefs surveyed at Toward the end of 1997, for a brief 6 week period Huatulco, Gulf of Tehuantepec, in September 1998 (September-November), a large warm pool that formed revealed 98.9% mortality. Since SSTs did not exceed the off the eastern Pacific spawned 3 tropical storms that normal seasonal maxima in 1997 or 1998, and the made landfall along the Oaxaca (southern México) coral observed coral bleaching/mortality was coincident with reef tract. Hurricane Pauline, the largest of these storms upwelling, Reyes Bonilla et al. (2001) related this with maximum sustained winds of 213 km hr -1 , caused disturbance to stressful low temperature conditions. Coral extensive branch-tip breakage and occasional dislodgment reefs present in the northern sector of Banderas Bay of pocilloporid reef frame blocks, the chief type in this experienced 71.1% mortality. This event was region (Lirman et al. 2001). The only other known storm- unequivocally linked to elevated SSTs that persisted for related damage occurred in the Galápagos Islands during 11 months (Carriquiry et al. 2001). Coral communities at the 1982-83 ENSO (Robinson 1985). On two occasions in the southern tip of Baja California were less affected with January 1983, large ocean swells from the NW -- the 29.1% bleaching and 17.9% mortality (Reyes Bonilla usual direction is from the SE – swept across coral 2001). communities and patch reefs at northern Floreana Island. Due to the patchy and low-level coral mortality in the This resulted in the dislodgment of large massive corals equatorial eastern Pacific in 1997-98, relatively little (Pavona and Porites), which were deposited above the damage was done to whole reef frames. That is, most live high tide line. Also, Pocillopora corals were torn loose, corals present on frameworks that survived the 1982-83 fragmented and deposited on the shore, along with ENSO were still alive after the 1997-98 bleaching event. numerous coral-associated species such as echinoids and Pocilloporid reef frameworks in Colombia, Panamá and asteroids. Costa Rica were still largely intact after 1998. Some Some zooxanthellate corals were severely affected overall coral mortality amounted to 85%. Upwelling during ENSO 1982-83 and 1997-98. Species with occurred on schedule in 1997-98, lowering sea branching colony morphologies, e.g. pocilloporid corals temperature in the gulf, and no coral bleaching or and milleporid hydrocorals, experienced moderate to mortality were observed. The impact of the 1982-83 extremely high mortalities. Pocillopora damicornis, ENSO off México is largely unknown, but was probably Pocillopora elegans and Glynn minimal considering the generally high coral cover in this suffered 55% to 75% mortality at some sites in the region before 1997 (Reyes Bonilla 2001). Galápagos Islands and mainland Ecuador. Pocillopora However, coral mortality was high in 1997-98, damicornis also experienced exceptionally high mortal- ranging from overall values of 98% at Huatulco to 71% in ities (96%) on reefs in north Banderas Bay, and at north Banderas Bay and 18% off the southern end of the Huatulco, México (99%, five Pocillopora spp. combined, Baja California peninsula. The cause of mortality at Reyes Bonilla et al. 2001). In the aftermath of the 1997- Huatulco has been tentatively associated with a sudden 98 ENSO, the few known colonies of Millepora boschmai drop in SST associated with intense upwelling, which Weerdt & Glynn are now dead, and Millepora intricate occurred during the last quarter of 1998 (Reyes Bonilla et Milne Edwards experienced 99.9% mortality. Leptoseris al. 2001). This hypothesized cold spell is not evident in papyracea (Dana), a rare species known only from three Reynolds’ SSTs . Retrospective analyses of coral density eastern Pacific sites (Glynn and Ault 2000), experienced bands (i.e. the timing of appearance of stress bands), a severe reduction in abundance in Costa Rica, with a isotope thermometry, and trace metals (indicative of decrease in live cover >90%. Porites panamensis upwelling strength) in coral skeletons may shed light on demonstrated mixed responses in 1997-98. This species this explanation. The high mortalities observed at virtually disappeared from coral reefs in the Gulf of Banderas Bay and off Baja California did occur during Chiriquí (Panamá), but suffered only low to moderate periods of extreme elevated SSTs. The maximum SSTA mortality in Costa Rica and México respectively. One of was +6.1o C in Banderas Bay in 1997-98, exceeding by the first scleractinian corals to bleach, Pavona sp.a, lost 26% the +4.5o C anomaly in the Galápagos Islands in significant amounts of surface area from large colonies or 1982-83, which coincided with the near elimination of often died totally if colonies were small. Additional reef corals there. Moreover, Banderas Bay corals in 1997- information on other species is given in Glynn (1997). 98 were subject to a greatly accelerated rate of warming Gardineroseris planulata nearly disappeared from Caño (+3.5 o C mo -1 ) compared with Galápagos corals Island (Costa Rica) reefs in 1982-83, but suffered only (+0.35 oC mo -1 ) in 1982-83. slight mortality during the recent ENSO event (Guzmán High solar irradiance has been shown to cause coral and Cortés 2001). A small population of G. planulata in bleaching, often together with elevated sea temperatures the Galápagos Islands, about 25 colonies, was reduced to (Brown 1997). Since ambient light was not monitored on a few small patches after the 1982-83 ENSO. These did eastern Pacific reefs in 1997-98, it is not possible to not show any appreciable recovery up to the 1997-98 assess its effects. Hopefully, affordable instrumentation ENSO disturbance, and are now believed to be locally for measuring underwater irradiance levels will soon extinct. Populations in the Gulf of Chiriquí and Gulf of become available. Panamá suffered only minor partial mortality at most and Damage to pocilloporid reef frames (i.e. high are now robust (Fong and Glynn 2000). Millepora mortality of live coral cover) in the eastern equatorial platyphylla Hemprich and Ehrenberg, not seen after 1983, Pacific was minor in 1997-98 compared with 1982-83. and Millepora boschmai, all known colonies were dead Pocilloporid reefs off Huatulco and Banderas Bay, after 1998, could now be absent from the eastern Pacific however, were severely damaged in 1997-98, coral fauna. Millepora intricata has recently experienced experiencing up to 95-100% mortality. Three tropical a severe reduction in abundance (>99.9%), but reappeared storms moved past the Huatulco reefs in late 1997, but after a similar setback following the 1982-83 ENSO. caused no significant damage (Lirman et al. 2001). Hurricane Isis, which moved into the Gulf of California in Discussion September 1998, after the ENSO-warming event, caused In general, coral bleaching and mortality in the eastern significant colony mortality (59.4%) to shallow-occurring equatorial Pacific was less than expected considering the (?=1 m depth) Pocillopora corals at Punta Arenas, Baja magnitude (+ 3-4o C) and duration (3-4 mo) of SST California (González Peláez et al. 2001). This storm did anomalies. Compared with the 1982-83 ENSO not result in permanent damage, and coral recruitment has disturbance, which resulted in overall coral mortalities of been observed as early as November 1998. In the long about 50% in Costa Rica (Caño Island), 75% in the Gulf term, if coral recovery is slow at Huatulco and Banderas of Chiriquí (Panamá) and 97% in the Galápagos Islands Bay, bioeroders and physical damage could begin to (Glynn 1990), these same areas in 1997-98 experienced erode and weaken reef frames there, as occurred in only 2.7%, 13.1% and 26.1% mortality, respectively. Panamá, Cocos Island (Costa Rica) and the Galápagos Damage to coral reefs off Coiba Island (Gulf of Chiriquí) Islands following the 1982-83 ENSO event (Glynn and in 1998, assessed from coral mortality data after the Colgan 1992, Guzmán and Cortés 1992, Macintyre et al. disturbance, was considerably less than initially reported 1993). (Goreau et al. 2000). With the cessation of upwelling and With the mortality in 1998 of all known colonies (8) persistent warming in the Gulf of Panamá in 1982-83, of Millepora boschmai that survived the 1982-83 ENSO, it is possible that this endemic hydrocoral is now extinct. Acknowledgements I thank H. Reyes Bonilla, S.B. Since no living colonies of Millepora platyphylla have Colley, P. Fong, J.S. Feingold, C.E. Jiménez, J.D. reappeared in the eastern Pacific since 1983, this species Carriquiry, G.E. Leyte-Morales, and B.Vargas Ángel for appears to have suffered a regional extinction. Millepora allowing me to refer to work in progress. Joan A. Kleypas intricata is also highly susceptible to sea warming kindly supplied temperature data and graphics, and episodes, having disappeared entirely from Panamanian offered a thoughtful critique of this overview. I also coral reefs following the 1982-83 and 1997- 98 ENSO acknowledge helpful comments from S. B. Colley, C.M. events. Recruits of M. intricata reappeared on reefs in Eakin, I.G. Macintyre, J. L. Maté, H. Reyes Bonilla, B. 1986, about three years after their disappearance. Since Vargas Ángel, an anonymous reviewer, and help from the small populations of M. intricata have been found conveners of this session, K.A. Teleki and T. Spencer. recently at depths (12-18 m) below two reefs affected in Financial support was provided by the Biological 1997-98 in the Gulf of Chiriquí, the prospects for Oceanography Program, US National Science recruitment and recovery at shallow depths appear good. Foundation, the Smithsonian Tropical Research Institute, Other eastern Pacific corals that often occur in and the National Geographic Society. relatively deep, inter-reef habitats, where high temperature and irradiance levels are generally less References stressful, include Leptoseris papyracea, Diaseris distorta, Cycloseris curvata (Hoeksema) and Psammocora stellata. Brown B (1997) Coral bleaching: causes and Despite the high loss of live cover (94.7%) of consequences. 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