Biology and geology of eastern Pacific coral reefs - Springer Link

14 downloads 113 Views 1MB Size Report
Acknowledgements. I thank Nancy Knowlton for the honor of ask- ... James MJ (ed), Gala´pagos Marine Invertebrates: Taxonomy, biogeography, and ..... 1163—1175. Reyes-Bonilla H (1993) Biogeografi´a y ecología de los corales her-.
Coral Reefs (1997) 16, Suppl.: S39—S46 (1997)

Biology and geology of eastern Pacific coral reefs J. Corte´ s CIMAR, and Escuela de Biologı´ a, Universidad de Costa Rica, San Pedro, Costa Rica Accepted: 19 December 1996

Abstract. The tropical eastern Pacific region has historically been characterized as devoid of coral reefs. The physical conditions of the region are apparently not conducive to reef growth: low temperatures, low salinity, and high nutrient loads. But recent work has demonstrated persistent coral growth in some locations at relatively high accretion rates, dating at least 5600 y before present. Coral reefs of the eastern Pacific are typically small (a few hectares), with discontinuous distribution and low species diversity. On a global scale, the eastern Pacific reefs may be considered minimum examples of coral reefs, as they have developed in possibly one of the most restrictive environments in the history of coral reefs. Disturbances are frequent, bioerosion intense, and recovery seems to be extremely slow. There is a general paucity of fossil corals and reefs on the American Pacific coast, probably due to the low preservation potential. In this review, distinct characteristics of the eastern Pacific and its coral reefs are highlighted. These factors make the region one of the smallest natural marine laboratories to study coral community structure and function on a regional level. The eastern Pacific is not only a testing ground for biological theory, but it is also a laboratory for paleoclimatic and oceanographic reconstruction.

Introduction The tropical eastern Pacific extends from the Sea of Cortez (Gulf of California) to the northern coast of Peru´, including several offshore islands (Fig. 1). Ever since Darwin’s (1842) classical work on coral reef structure and distribution, followed by Stoddart’s (1969) ecology and morphology of modern coral reefs, to recent textbooks (e.g. Lalli and Parsons’ 1993 Oceanography), the eastern Pacific has been depicted as devoid of coral reefs. Even so, the presence of corals in the region has been known for a long time. Pourtale`s (1875, in Durham and Barnard 1952) recorded the first coral species found in the eastern

Pacific. Other research was conducted in the nineteenth (Verrill 1868—70) and early twentieth century (Durham 1947), and culminated with the monograph by Durham and Barnard (1952) on stony corals of the eastern Pacific. More recent coral species accounts are found in Wells (1983), Guzma´n and Corte´s (1993), Reyes-Bonilla (1993), and Glynn et al. (1996). In the early 1970s, the presence of coral reefs in the eastern Pacific was firmly established with the work by Glynn et al. (1972) in Panama´. Since then, numerous reports have been published describing the reef types of the region. In this study, some outstanding features related to the geology and biology of eastern Pacific coral reefs are described. This should shed light on complex species interactions, community level processes and the evolution of coral reefs in the region.

Geology Prior to 3.5 million years ago The eastern Pacific Basin started taking shape around the end of the Mesozoic, when the Caribbean Plate was implanted between the North American and South American plates (Astorga 1994). Some isolation of this region from the rest of the Pacific existed at that time (Grigg and Hey 1992), but there was a connection with the Caribbean-Atlantic Province until around 3.5 million years ago, when the isthmus of southern Central America emerged (Coates et al. 1992). Before the closure of the isthmus, the coral fauna on the western side of the American continent was similar to that of the Caribbean, but now the Recent eastern Pacific corals have a strong affinity with the Central Pacific (Glynn and Wellington 1983; Corte´s 1986; Budd 1989; Glynn et al. 1996; Glynn in press). Cretaceous and Tertiary coral faunas of the eastern Pacific region were widespread (Glynn and Wellington 1983) and diverse (Durham 1966). Subsequently, both distribution and diversity have progressively decreased

S40

extremes. There was intense upwelling and cooling, which limited reef growth (Glynn and Stewart 1973; Glynn and Macintyre 1977; Glynn et al. 1983), but there were also warming events that may have reduced live coral cover (Glynn 1988a, 1990a, 1992). Both the warming and cooling events may have resulted in the extinction and later colonization of several coral species (Dana 1975; Glynn and Wellington 1983; Corte´s 1986). The Pliocene-Pleistocene boundary was also a period of molluscan faunal turnover (Jackson et al. 1993). Holocene growth history

Fig. 1. Map of the eastern Pacific region, showing the main currents

(Glynn in press). Late Tertiary corals have been dredged from a guyot on the Nasca Ridge, about 2700 km south of the Gala´pagos Islands, and from the Imperial Formation, inland from the extreme north end of the Sea of Cortez (Glynn and Wellington 1983; Budd 1989). Today, eastern Pacific reefs range from the Gala´pagos Islands, on the south, to the southern end of the Sea of Corte´s on the north (Glynn and Wellington 1983). During CretaceousOligocene time 36 coral genera existed, 18 during the Miocene, and 6 remain at the present time (Durham 1966). The last 3.5 million years The rise of the southern Central American isthmus altered the oceanographic conditions of the tropical eastern Pacific. Upwelling in the Gulf of Papagayo and Panama may have started at that time, and the conditions were set for the development of El Nin8 o events (Colgan 1990). What happened following the closure of the isthmus is a matter of controversy. On one hand, Dana (1975) stated that the recent eastern Pacific coral fauna is the product of immigration from the Central Pacific. On the other hand, Heck and McCoy (1978) argued that the present day coral fauna of the eastern Pacific is the product of vicariance, the result of speciation and extinctions (see biogeography section later). The Pleistocene was a period of turmoil in the tropical eastern Pacific. Sea level oscillations greatly changed the available area for reef development, because the continental shelf is narrow and the continental slope steep (Corte´s 1986). It was, as it is today, a period of temperature

The thickness of coral reef frameworks in Costa Rica, Panama´, Colombia and Ecuador (reviewed in Guzma´n and Corte´s 1993) has been determined with metal probes or tubes and by drilling cores. Reef thickness ranges from 0.2 to 13.4 m, with an average for the region of 4.5$0.31 m. Ages range from 200 to 5600 years (Corte´s et al. 1994). Accretion rates range from 0.5 to 14.3 m/1000 y (Glynn and Macintyre 1977; Corte´s 1990a). Maximum thickness, age and accretion rates were found in the non-upwelling Gulf of Chiriqui´ , Panama´ (Glynn and Macintyre 1977). Two types of Holocene coral reefs can be recognized in the eastern Pacific region, based on their age and thickness (Macintyre et al. 1992). The first type is reefs exposed to temperature extremes (upwelling and El Nin8 o warming), where growth discontinuities are common. These reefs have minimal ages and thicknesses. For example, in the Gala´pagos Islands, average reef thickness is 1 m (Glynn and Wellington 1983), and the maximum age is 1000 years (Macintyre et al. 1992). The second type of reefs protected from temperature extremes have few growth discontinuities, have grown for longer periods of time and are thicker. For example, at Punta Islotes, Costa Rica, average reef thickness is 6.3 m, and maximum age is 5500 years (Corte´s et al. 1994). There is a general paucity of fossil corals on the Pacific coast of America, with some exceptions in the Gala´pagos Islands (Glynn and Wellington 1983) and Me´xico (ReyesBonilla 1992). Modern eastern Pacific coral reefs are made up of interlocking, branching corals, with no cementation (Corte´s et al. 1994) or by massive corals that in most areas are either extensively bioeroded at the base (Scott and Risk 1988) or are unattached to the substrate (Corte´s 1990b). Once dead, some of these frameworks can be completely obliterated by sea urchin erosion (Glynn et al. 1979; Glynn 1988b; Colgan 1990; Glynn and Colgan 1992; Eakin 1996; Reaka-Kudla et al. 1996) (see Bioerosion section later). These observations suggest that the preservation of eastern Pacific coral reefs is low (Corte´s 1993), and this probably accounts for the scarcity of fossil corals and reefs along the Pacific coast of the American continent. Biogeography Traditionally, the eastern Pacific region is divided into four biogeographic provinces: Cortez, Mexican, Panamic

S41

and Gala´pagos, based on isolation and endemism mainly observed in mollusks. But in terms of the scleractinian corals, the whole tropical eastern Pacific is a subprovince of the Indo-Pacific faunal province (Stehli and Wells 1971; Glynn and Wellington 1983; Guzma´n and Corte´s 1993; Veron 1995). Four positions have been considered with respect to the biogeographic connections of the eastern Pacific coral fauna. Dana (1975) and Grigg and Hey (1992) defended the position that the modern eastern Pacific coral fauna is a product of immigration from the Central Pacific. Heck and McCoy (1978) argued that the present day coral fauna of the eastern Pacific is a product of vicariance. Veron (1995) claimed that coral distribution patterns are ancient when compared with the age of the present fauna. The fourth position, first stated by Glynn and Wellington (1983), and updated by Glynn et al. (1996) and Glynn (in press), suggests that these view- points are not mutually exclusive, because all the hypotheses describe events that have actually taken place. To distinguish among these hypotheses, more detailed studies on the genetics of corals, on the transport and settlement of larvae (Richmond 1990), and on the few fossil reefs (Budd 1989) have been recommended by Glynn and Wellington (1983). Oceanographic setting The tropical eastern Pacific is one of the most isolated regions of the world oceans. To the north and south it is limited by cool water currents and upwelling, and to the west by the eastern Pacific Barrier, a large expanse of deep water (Chavez and Brusca 1991; Grigg and Hey 1992; Veron 1995). Tropical eastern Pacific coral reefs are exposed to extremes in temperature, salinity, and nutrients. Coastal upwelling, a product of the trade winds, is prevalent at the Gulf of Tehuantepec, Gulf of Papagayo, and Gulf of Panama´ (McCreary et al. 1989). These cold waters inhibit coral and reef growth (Glynn and Stewart 1973; Glynn 1977a; Glynn and Macintyre 1977). The best coral reef development is attained along stretches of the coast protected by high mountains, that reduce the winds that cause coastal upwelling (Glynn et al. 1983). The Gala´pagos Islands are also exposed to cool waters coming from the south and upwelling of the Equatorial Undercurrent (Cromwell Current) (Glynn and Wellington 1983; Chavez and Brusca 1991). The whole region has a very shallow thermocline (Dana 1975; Fiedler 1992) that results in the intrusion of of cold water that impacts on the deeper coral reef zones. The other thermal extreme of the region is the normally high temperature during the non-upwelling season (Fiedler 1992). High temperatures are pushed to the extreme during strong El Nin8 o years causing widespread death of marine life, including scleractinian corals (Glynn 1984a, 1988a, 1990a). El Nin8 o associated warming events can raise the water temperature to 30 °C or more over several weeks to months (Glynn 1990a, 1992), which in laboratory simulations have resulted in coral death (Glynn and D’Croz 1990). The extent of coral bleaching in the region during the 1982—83 El Nin8 o was correlated with the

magnitude and rate of increase in temperature anomalies and their duration (Glynn et al. 1988). El Nin8 o disturbances have been considered as one of the main limiting factors for reef development in the tropical eastern Pacific over long time scales (Glynn and Colgan 1992). Low salinity (between 20 and 30 parts per thousand) also characterizes sections of the coastal eastern Pacific. The Panama´ Bight is an area of low salinity, due to high regional rainfall (Fiedler 1992). Golfo Dulce, on the southern coast of Costa Rica, is also an area where coral reefs are exposed to low salinity (Corte´s 1990b), caused by changes in river discharge patterns over about 500 years (Corte´s et al. 1994). In the second half of 1985, several coral reefs of the eastern Pacific region were affected by phytoplankton blooms (Guzma´n et al. 1990). Also, all shallow reef flats of the region’s reefs are subaerially exposed during periodic extreme low tides (Glynn 1976; Eakin and Glynn 1996). These two events have caused noticeable coral mortality. Biology As noted, coral reefs of the eastern Pacific region grow under extreme environmental conditions. These reefs are small and structurally simple compared to other areas but have complicated biological interactions. Coral diversity is low and perturbances frequent and strong, resulting in slow recovery of these reefs. Coral reefs and diversity Based on the predominant reef-building coral, two main types of coral reefs can be recognized in the eastern Pacific: pocilloporid reefs (Fig. 2) and poritid reefs (Fig. 3). Smaller reefs (less than 50 m2) are also found in the region and are constructed by other species: Psammocora stellata Verrill at Punta El Bajo, Golfo Dulce, Costa Rica (Corte´s 1990b); Pavona gigantea Verrill in the upwelling area north of Peni´ nsula de Santa Elena, Costa Rica (Corte´s 1996); ¸eptoseris papyracea (Dana) in Bahi´ a Culebra, Guanacaste, Costa Rica (Jime´nez in press); Pavona clavus Dana in the Gala´pagos Islands (Glynn and Wellington 1983) and Costa Rica (Corte´s and Jime´nez in preparation). Coral reefs of the eastern Pacific are characterized by their small size (a few hectares), discontinuous distribution, and low species diversity (Glynn and Wellington 1983; Guzma´n and Corte´s 1993). From a global perspective, eastern Pacific reefs may be considered minimum examples of coral reef. Most of these reefs are constructed by one to three coral species (Glynn and Wellington 1983; Guzma´n and Corte´s 1993), a feature that has not changed since initiation of reef growth thousands of years ago (Corte´s et al. 1994). Along the mainland of the eastern Pacific, coral reefs are located at the entrance of the Sea of Cortez (Squires 1959; Brusca and Thomson 1977; Wilson 1988, 1990; Robinson and Thomson 1992; Reyes-Bonilla 1993); at Los Co´banos, El Salvador (Orellana 1985); on the mainland of Costa Rica (Glynn et al. 1983; Corte´s and Murillo 1985;

S42

Biological interactions

Fig. 2. Pocilloporid coral reef from Uva Island, Panama´

Fig. 3. Poritid coral reef from Isla del Coco, Costa Rica

Guzma´n and Corte´s 1989; Corte´s 1990b); Panama´ (Glynn et al. 1972; Glynn 1976; Guzma´n et al. 1991); Colombia (Glynn et al. 1982; Prahl and Erhardt 1985; Vargas-Angel in press); and Ecuador (Glynn and Wellington 1983). There are also coral communities or reefs on the offshore islands: Revillagigedo (Bautista-Romero et al. 1994; Reyes-Bonilla and Carriquiry 1994; Glynn et al. 1996); Clipperton (Sachet 1962; Glynn et al. 1996); Isla del Coco (Bakus 1975; Guzma´n and Corte´s 1992); Malpelo (Birkeland et al. 1975), and Gala´pagos Islands (Glynn and Wellington 1983; Glynn 1994; Feingold 1995).

Among the interesting aspects of eastern Pacific coral reefs are the complex interactions between their biological communities. Two examples are described for illustration. The first one is the importance of asexual reproduction in Porites lobata aided by a fish. This phenomenon was first reported by Glynn and Wellington (1983), expanded by Guzma´n (1988), and is under long-term study by HM Guzma´n. Primary productivity in the eastern Pacific is higher than in other reef areas, and coral colonies are proportionally more infested by boring bivalves (Highsmith 1980). High nutrient input leads to intense competition between algal turf and corals. Usually the corals do not win, thus asexual reproduction becomes important to reef growth and extension. Colonies of P. lobata typically are infested by boring bivalves, ¸ithophaga spp., with densities of up to 100 individuals per 100 cm2 (Scott and Risk 1988). The triggerfishes, Sufflamen veres (Gilbert and Starks) and Pseudobalistes naufragium (Jordan and Starks), in their search for ¸ithophaga, bite into the coral and remove fragments, 2 to 5 cm in diameter. These fragments are discarded by the fish, and a high percentage of the P. lobata fragments survive and grow adjacent to the parent colonies (Guzma´n personal communication 1990). This may be the dominant means of asexual reproduction of this important reef building coral (Guzma´n 1988; Glynn et al. 1994). The second example illustrates the level of complexity of biological interactions that can be reached in the eastern Pacific. This case involves branching corals, Pocillopora spp., a corallivorous sea star, Acanthaster planci (Linnaeus), several species of xanthid crabs, ¹rapezia spp., an alpheid shrimp, Alpheus lottini Guerin, an amphinomid polychaete worm, Pherecardia striata (Kinberg), and a harlequin shrimp, Hymenocera picta Dana. Pocillopora spp., important reef builders in the eastern Pacific, is one of the most commonly consumed coral genera by Acanthaster planci (Glynn 1973, 1974; Guzma´n 1988). However, Acanthaster never reaches outbreak levels in the eastern Pacific. The branching corals are defended from the sea star by crustacean guards and the alpheid shrimp, in a mutualistic relationship (Prahl et al. 1978; Glynn 1983a, b, 1987; Stimson 1990). But not only that, within the interlocked skeletons of Pocillopora lives an amphinomid worm, Pherecardia striata, and a harlequin shrimp, Hymenocera picta, that together apparently control the populations of Acanthaster. The harlequin shrimp inflicts small (1 cm) linear wounds on the arms or aboral surface of Acanthaster and feed on its tissue. The wounds themselves are usually not fatal, but are used by the amphinomid worms to gain entry into the body cavity where they consume soft organs, eventually killing the sea star. Where both the worm and the shrimp are abundant, there are no Acanthaster outbreaks (Glynn 1977b, 1981, 1984b). The presence of crustacean guards limits predation by Acanthaster and often prevents the sea star from reaching unprotected coral species (Glynn 1985a).

S43

Bioerosion The biological destruction of eastern Pacific coral reefs has been extremely high (Highsmith 1980; Glynn et al. 1979), specially after the 1982—83 El Nin8 o (Glynn 1988; Eakin 1996). Recent studies indicate that bioerosion exceeds carbonate deposition, resulting in the slow erosion of the reef structures (Glynn 1988; Colgan 1990; Eakin 1996; Reaka-Kudla 1996). Reefs in Panama´, Gala´pagos Islands, and Isla del Coco are being destroyed by external bioeroders, mainly sea urchins (Glynn et al. 1979; Glynn 1988; Colgan 1990; Guzma´n and Corte´s 1992; Eakin 1996; Reaka-Kudla et al. 1996). In Costa Rica, most of the bioerosion is internal, primarily by boring bivalves (Scott and Risk 1988; Corte´s 1991; Fonseca and Corte´s in press). External bioerosion by sea urchins was between 5 and 6 times higher than internal excavation in the Gala´pagos Islands (Reaka-Kudla et al. 1996). Coral reef frameworks in the Gala´pagos Islands (Colgan 1990; Reaka-Kudla et al. 1996), Panama´ (Glynn 1988; Eakin 1996), Isla del Coco (Guzma´n and Corte´s 1992), and possibly in other areas of the eastern Pacific are being reduced in height by the action of the bioeroders. Some of those reef structures could be eliminated entirely in one to several decades (Glynn 1988; ReakaKudla et al. 1996).

Fig. 4. Dead Pocillopora framework at the north Pacific coast of Costa Rica

mechanism for coral reef recovery in the eastern Pacific (Guzma´n 1991). Discussion

Recovery Recovery of eastern Pacific coral reefs appears to be slower than in other regions (Pearson 1981; Colgan 1987). Twelve years after the devastating 1982—83 El Nin8 o warming event, where 50 to 100% of living coral was killed (Glynn et al. 1988), most reefs of the region show little sign of recovery. Estimates of recovery time range from one to two hundred years before reefs in this region will assume pre- 1982—83 levels of development (Glynn 1985b; Richmond 1985), and this will occur only in areas with suitable environmental conditions for reef recovery, e.g., Gulf of Chiriqui´ (Panama´), Isla del Can8 o and Isla del Coco (Costa Rica). Areas of marginal coral reef development, such as the upwelling area of northern Costa Rica (McCreary et al. 1989), show even slower recovery rates. Coral reefs in this area were affected by low temperatures during the Little Ice Age, 350 to 400 years ago (Glynn et al. 1983). Today, it is still possible to locate and observe the dead Pocillopora frameworks (Fig. 4), because some of these cover large areas (several hectares). After four centuries, there is little recovery of these coral reefs, even though local coral growth rates and survival of fragments are high. The main reef building coral species of the eastern Pacific produce gametes and larvae (Glynn et al. 1991, 1994, 1996), yet there is little to no recruitment. To aggravate the problem, frameworks are being destroyed by sea urchins (Colgan 1990; Glynn and Colgan 1992; ReakaKudla et al. 1996). The destruction of frameworks is detrimental to the long-term development of reefs in the eastern Pacific (Colgan 1990). Even so, survival of coral fragments is high and has been suggested as an important

Eastern Pacific coral reefs have developed under restrictive environmental conditions, representing possibly one of the most extreme situations in the history of coral reefs. Coral diversity is low and reef recovery seems to be extremely slow. In other words, the limited biological diversity results in these systems having a low resilience (Odum 1993). Examples include the disappearance of entire reefs during the 1982—83 El Nin8 o (Glynn 1988b; Colgan 1990; Glynn and Colgan 1992), and the slow recovery of reefs after the Little Ice Age (Glynn et al. 1983). In addition to the limiting conditions for reef growth in the eastern Pacific, anthropogenic stresses are being added, such as the extraction of corals (Corte´s and Murillo 1985; Glynn 1994), pollution (Glynn et al. 1984), tourist impact (Jime´nez in preparation), siltation from land alteration (Corte´s 1990b), and anchor damage (Glynn 1994; personal observation). Some corals and coral reefs of the eastern Pacific are probably being damaged beyond recovery. The eastern Pacific region and its coral reefs represent possibly the smallest natural laboratories of the oceans to study coral community structure and function. The eastern Pacific is not only a testing ground for biological theory (e.g. Wellington and Victor 1985; Eakin 1987; Glynn 1988c, 1990b), but also serves as a laboratory for paleoclimatic and oceanographic reconstructions. For example, stable isotopes and geochemical tracers in coral skeletons have been used to identify previous El Nin8 oSouthern Oscillation events (Druffel et al. 1990; Carriquiry et al. 1994; Wellington and Dunbar 1995), to determine water conditions in which corals grew (Shen et al. 1992), and for paleoclimatic reconstructions (Dunbar et al. 1994; Linsley et al. 1994).

S44

A few of the coral reefs of the eastern Pacific are in relatively good condition and several of them are found in protected areas (e.g., Coiba, Panama´; Gala´pagos Islands; Isla del Coco, Costa Rica). We now know much more about the eastern Pacific, its oceanography and coral reefs, compared to 25 years ago when Peter Glynn began his studies of eastern Pacific coral reefs. While much has been learned, many questions remain about how these coral reefs function. The answers to these questions may shed light on the understanding of larger, more diverse and complex coral reef systems, and may contribute to better management of these ecosystems. Acknowledgements. I thank Nancy Knowlton for the honor of asking me to deliver this plenary talk at the 8th International Coral Reef Symposium. I will always be in debt to my mentor Dr. Peter W. Glynn, and my colleagues and friends H. Guzma´n and I. Macintyre. I thank my students for their help and motivation: Carlos Jime´nez, Odalisca Breedy and Ana C. Fonseca. Research in the eastern Pacific has been possible thanks to the economic support of the Vicerrectori´ a de Investigacio´n and ProAmbi, Universidad de Costa Rica, CONICIT (Costa Rica, 90—326 BID), and the US National Science Foundation (grants to PW Glynn). The manuscript greatly benefited from the reviews by CE Jime´nez, O Breedy, PW Glynn, SCC Steiner, J Mateo, GM Wellington, IG Macintyre, H ReyesBonilla, CM Eakin, M Colgan, and specially the iterative reviews by RW Parkinson.

References Astorga A (1994) El Mesozoico del sur de Ame´rica Central: consecuencias para el origen y evolucio´n de la Placa Caribe. Profil 7:171—233 Bakus GJ (1975) Marine zonation and ecology of Cocos Island, off Central America. Atoll Res Bull 179:1—9 Bautista-Romero J, Reyes-Bonilla H, Lluch-Cota DB, Lluch-Cota SE (1994) Aspectos generales sobre la fauna marina. In: OrtegaRubio A, Castellanos-Vera A (eds), La Isla Socorro, Reserva de la Bio´sfera, Archipie´lago de Revillagigedo, Me´xico. CIBNOR, La Paz, pp 247—275 Birkeland C, Meyer DL, Stames JP, Buford CL (1975) Subtidal communities of Malpelo Island. Smithson Contrib Zool 176:55—68 Brusca RC, Thomson DA (1977) Pulmo Reef: the only ‘‘coral reef ’’ in the Gulf of California. Cienc Mar 2:37—53 Budd AF (1989) Biogeography of Neogene Caribbean reef corals and its implications for the ancestry of eastern Pacific reef corals. Mem Ass Australas Palaeontols 8:219—230 Carriquiry JD, Risk MJ, Schwarcz HP (1994) Stable isotope geochemistry of coral from Costa Rica as proxy indicator of the El Nin8 o/Southern Oscillation (ENSO). Geochim Cosmochim Acta 58:335—351 Chavez FP, Brusca RC (1991) The Gala´pagos Islands and their relation to oceanographic processes in the tropical Pacific. In: James MJ (ed), Gala´pagos Marine Invertebrates: Taxonomy, biogeography, and evolution in Darwin’s Islands. Topics In geobiology, vol 8, Plenum, New York, pp 9—33 Coates AG, Jackson JBC, Collins LS, Cronin TM, Dowsett HJ, Bybell LM, Jung P, Obando JA (1992) Closure of the Isthmus of Panama: the near-shore marine record in Costa Rica and western Panama. Geol Soc Am Bull 104:814—828 Colgan MW (1987) Coral reef recovery on Guam (Micronesia) after catastrophic predation by Acanthaster planci. Ecology 68:1592—1605 Colgan MW (1990) El Nin8 o and the history of eastern Pacific reef building. In: Glynn PW (ed), Global ecological consequences of the 1982—83 El Nin8 o-Southern Oscillation. Elsevier, Amsterdam, pp 183—229

Corte´s J (1986) Biogeografi´a de corales hermati´ picos: el istmo centroamericano. Anal Inst Cienc Mar Limnol UNAM 13:297—304 Corte´s J (1990a) Coral reef decline in Golfo Dulce, Costa Rica, Eastern Pacific: anthropogenic and natural disturbances. PhD dissertation, University of Miami 147p Corte´s J (1990b) The coral reefs of Golfo Dulce, Costa Rica: distribution and community structure. Atoll Res Bull 344:1—37 Corte´s J (1991) Los arrecifes coralinos de Golfo Dulce, Costa Rica: aspectos geolo´gicos. Rev Geol Am Central 13:15—24 Corte´s J (1993) Comparison between Caribbean and eastern Pacific coral reefs. Rev Biol Trop, 41 Supl. 1:19—21 Corte´s J (1996) Comunidades coralinas y arrecifes del Area de Conservacio´n Guanacaste, Costa Rica. Rev Biol Trop 44:623—625 Corte´s J, Murillo MM (1985) Comunidades coralinas y arrecifes del Paci´ fico de Costa Rica. Rev Biol Trop 33:197—202 Corte´s J, Macintyre IG, Glynn PW (1994) Holocene growth history of an eastern Pacific fringing reef, Punta Islotes, Costa Rica. Coral Reefs 13:65—73 Darwin C (1842) The structure and distribution of coral reefs. Reprinted by The University of Arizona Press, 1984 Dana T (1975) Development of contemporary eastern Pacific coral reefs. Mar Biol 33:355—374 Druffel ERM, Dunbar RB, Wellington GM, Minnis SA (1990) Reef building corals and identification of ENSO warming episodes. In: Glynn PW (ed). Global ecological consequences of the 1982—83 El Nin8 o-Southern Oscillation. Elsevier, Amsterdam, pp 233—254 Dunbar RB, Wellington GM, Colgan MW, Glynn PW (1994) Eastern Pacific climate variability since 1600 A.D.: stable isotopes in Gala´pagos corals. Paleoceanogr 9:291—315 Durham JW (1947) Corals from the Gulf of California and the North Pacific coast of America. Geol Soc Am Mem 20:1—46 Durham JW (1966) Coelenterates, especially stony corals from the Gala´pagos and Cocos Islands. In: Bowman RI (ed) The Gala´pagos. University of California Press, Berkeley, pp 123—135 Durham JW, Barnard JL (1952) Stony corals of the eastern Pacific collected by the Velero III and Velero IV. Allan Hancock Pac Exped 16(1):1—110 Eakin CM (1987) Damselfishes and their algal lawns: a case of plural mutualism. Symbiosis 4:275—288 Eakin CM (1996) Where have all the carbonates gone? A model comparison of calcium carbonate budgets before and after the 1982—1983 El Nin8 o at Uva Island in the eastern Pacific. Coral Reefs 15:109—119 Eakin CM, Glynn PW (1996) Low tidal exposures and reef mortalities in the eastern Pacific. Coral Reefs 15:120 Feingold JS (1995) Effects of elevated water temperature on coral bleaching and survival during El Nin8 o disturbance events. PhD dissertation University of Miami, pp 1—236 Fiedler PC (1992) Seasonal climatologies and variability of eastern tropical Pacific surface waters. NOAA Technical Report NMFS 109:1—65 Fonseca AC, Corte´s J (in press) Coral borers of the eastern Pacific: the sipunculan Aspidosiphon (A.) elegans and the crustacean Pomatogebia rugosa. Pac Sci Glynn PW (1973) Acanthaster: effect on coral reef growth in Panama´. Science 180:504—506 Glynn PW (1974) The impact of Acanthaster on corals and coral reefs in the eastern Pacific. Environ Conserv 1:295—304 Glynn PW (1976) Some physical and biological determinants of coral community structure in the eastern Pacific. Ecol Monogr 46:431—456 Glynn PW (1977a) Coral growth in upwelling and nonupwelling areas off the Pacific coast of Panama´. J Mar Res 35:567—585 Glynn PW (1977b) Interactions between Acanthaster and Hymenocera in the field and laboratory. Proc 3rd Int Coral Reef Symp 1:209—215 Glynn PW (1981) Acanthaster population regulation by a shrimp and a worm. Proc 4th Int Coral Reef Symp 2:607—612

S45 Glynn PW (1983a) Crustacean symbionts and the defense of corals: coevolution on the reef ? In: Nitecki MH (ed) Coevolution. University of Chicago, Chicago, pp 111—178 Glynn PW (1983b) Increased survivorship in corals harboring crustacean symbionts. Mar Biol Lett 4:105—111 Glynn PW (1984a) Widespread coral mortality and the 1982/1983 El Nin8 o warming event. Environ Conserv 11:133—146 Glynn PW (1984b) An amphinomid worm predator of the crown-ofthorns sea star and general predation on asteroids in eastern and western Pacific coral reefs. Bull Mar Sci 35:54—71 Glynn PW (1985a) Corallivore population sizes and feeding effects following El Nin8 o (1982—1983) associated coral mortality in Panama´. Proc 5th Int Coral Reef Cong 4:183—188 Glynn PW (1985b) El Nin8 o-associated disturbance to coral reefs and post disturbance mortality by Acanthaster planci. Mar Ecol Prog Ser 26:295—300 Glynn PW (1987) Some ecological consequences of coral-crustacean guard mutualisms in the Indian and Pacific Oceans. Symbiosis 4:301—324 Glynn PW (1988a) El Nin8 o-Southern Oscillation 1982—1983: nearshore population, community, and ecosystem responses. Ann Rev Ecol Syst 19:309—345 Glynn PW (1988b) El Nin8 o warming, coral mortality and reef framework destruction by echinoid bioerosion in the eastern Pacific. Galaxea 7:129—160 Glynn PW (1988c) Predation on coral reefs, some key processes, concepts and research directions. Proc 6th Int Coral Reef Symp 1:51—62 Glynn PW (1990a) Coral mortality and disturbance to coral reefs in the tropical eastern Pacific. In: Glynn PW (ed) Global ecological consequences of the 1982—83 El Nin8 o-Southern Oscillation. Elsevier, Amsterdam, pp 55—126 Glynn PW (1990b) Feeding ecology of selected coral-reef macroconsumers: patterns and effects on coral community structure. In: Dubinsky Z (ed) Ecosystems of the World 25: Coral Reefs. Elsevier, Amsterdam, pp 365—400 Glynn PW (1992) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1—17 Glynn PW (1994) State of coral reefs in the Gala´pagos Islands: natural versus anthropogenic impacts. Mar Poll Bull 29:131—140 Glynn PW (in press) Eastern Pacific reef coral biogeography and faunal flux: Durham’s dilemma revisited. Proc. 8th Int Coral Reef Symp Glynn PW, Colgan MW (1992) Sporadic disturbances in fluctuating coral reef environments: El Nin8 o and coral reef development in the eastern Pacific. Am Zool 32:707—718 Glynn PW, D’Croz L (1990) Experimental evidence for high temperature stress as the cause of El Nin8 o-coincident coral mortality. Coral Reefs 8:181—191 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, 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, Wellington GM (1983) Corals and coral reefs of the Gala´pagos Islands (with annotated list of the scleractinian corals of Gala´pagos by JW Wells). University of California Press, Berkeley, California Glynn PW, Druffel EM, Dunbar RB (1983) A dead Central American coral reef tract: possible link with the Little Ice Age. J Mar Res 41:605—637 Glynn PW, Prahl H von, Guhl F (1982) Coral reefs of Gorgona Island, Colombia with special references to corallivores and their influence on community structure and reef development. An Inst Inv Mar Punta Beti´ n 12:185—214 Glynn PW, Stewart RH, McCosker JE (1972) Pacific coral reefs of Panama´: structure, distribution and predators. Geol Rundsch 61:483—519 Glynn PW, Veron JEN, Wellington GM (1996) Clipperton Atoll (eastern Pacific): oceanography, geomorphology, reef-building coral ecology and biography. Coral Reefs 15:71—99

Glynn PW, Wellington GM, Birkeland C (1979) Coral reef growth in the Gala´pagos: limitation by sea urchins. Science 203:47—49 Glynn PW, Corte´s J, Guzma´n HM, Richmond RH (1988) El Nin8 o (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 Glynn PW, Howard LS, Corcoran E, Freay AD (1984) The occurrence and toxicity of herbicides in reef building corals. Mar Poll Bull 15:370—374 Glynn PW, Colley SB, Gassman NJ, Black K, Corte´s J, Mate´ JL (1996) Reef coral reproduction in the eastern Pacific: Costa Rica, Panama, and Gala´pagos Islands (Ecuador) — III. Agariciidae (Pavona gigantea and Gardineroseris planulata). Mar Biol 125:579—601 Glynn PW, Gassman NJ, Eakin CM, Corte´s J, Smith DB, Guzma´n HM (1991) Reef coral reproduction in the eastern Pacific: Costa Rica, Panama, and Gala´pagos Islands (Ecuador), Part I — Pocilloporidae. Mar Biol 109:355—368 Glynn PW, Colley SB, Eakin CM, Smith DB, Corte´s J, Gassman NJ, Guzma´n HM, Rosario JB DEL, Feingold J (1994) Reef coral reproduction in the eastern Pacific: Costa Rica, Panama, and Gala´pagos Islands (Ecuador) — II. Poritidae. Mar Biol 118:191—208 Grigg RW, Hey R (1992) Paleoceanography of the tropical eastern Pacific Ocean. Science 255:172—178 Guzma´n HM (1988) Distribucio´n y abundancia de organismos corali´ voros en los arrecifes coralinos de la Isla del Can8 o, Costa Rica. Rev Biol Trop 36: 191—207 Guzma´n HM (1991) Restoration of coral reefs in Pacific Costa Rica. Conserv Biol 5: 189—195 Guzma´n HM, Corte´s J (1989) Coral reef community structure at Can8 o Island, Pacific Costa Rica. PSZNI: Mar Ecol 10: 23—41 Guzma´n HM, Corte´s J (1992) Cocos Island (Pacific of Costa Rica) coral reefs after the 1982—83 El Nin8 o disturbance. Rev Biol Trop 40: 309—324 Guzma´n HM, Corte´s J (1993) Los arrecifes coralinos del Paci´ fico Oriental Ecuatorial: Revisio´n y perspectivas. Rev Biol Trop 41: 535—557 Guzma´n HM, Robertson DR, Di´ az ML (1991) Distribucio´n y abundancia de corales en el arrecife de Isla Iguana, Panama´. Rev Biol Trop 39: 225—231 Guzma´n HM, Corte´s J, Glynn PW, Richmond RH (1990) Coral mortality associated with dynoflagellate blooms in the eastern Pacific (Costa Rica and Panama). Mar Ecol Prog Ser 60: 299—303 Heck KL, McCoy ED (1978) Long-distance dispersal and the reefbuilding corals of the eastern Pacific. Mar Biol 48: 349—356 Highsmith RC (1980) Geographic patterns of coral bioerosion: a productivity hypothesis. J Exp Mar Biol Ecol 46: 177—196 Jackson JBC, Jung P, Coates AG, Collins LS (1993) Diversity and extinction of tropical American mollusks and emergence of the Isthmus of Panama. Science 260: 1624—1626 Jime´nez CE (in press) Corals and coral reefs of Culebra Bay, Pacific coast of Costa Rica: anarchy in the reef. Proc 8th Int Coral Reef Symp Lalli CM, Parson TR (1993) Biological oceanography: an introduction. Pergamon Press, Oxford, UK Linsley BK, Dunbar RB, Wellington GM, Mucciarone DA (1994) A coral based reconstruction of intertropical convergence zone variability over Central America since 1707. J Geophys Res 99: 9977—9994 MacIntyre IG, Glynn PW, Corte´s J (1992) Holocene reef history in the eastern Pacific: mainland Costa Rica, Can8 o Island, Cocos Island, and Gala´pagos Islands. Proc 7th Int Coral Reef Symp 2: 1174—1184 McCreary JP, Lee HS, Enfield DB (1989) The response of the coastal ocean to strong offshore winds: with application to circulation in the gulfs of Tehuantepec and Papagayo. J Mar Res 47: 81—109 Odum EP (1993) Ecology and our endangered life-support systems. Sinauer Asso, Sunderland Orellana JJ (1985) Marine fishes of Los Cobanos. Sigma Foundation, New York

S46 Pearson RG (1981) Recovery and recolonization of coral reefs. Mar Ecol Prog Ser 4: 105—122 Prahl H von, Erhardt H (1985) Colombia: Corales y arrecifes coralinos. Editorial Presencia, Bogota´ Prahl H von, Guhl F, Gro¨gl M (1978) Crusta´ceos deca´podos comensales del coral Pocillopora damicornis L. en la Isla de Gorgona, Colombia. An Inst Inv Mar Punta Beti´ n 10: 81—93 Reaka-Kudla ML, Feingold JS, Glynn PW (1996) Experimental studies of rapid bioerosion of coral reefs in the Gala´pagos Islands. Coral Reefs 15: 101—107 Reyes-Bonilla H (1992) New records for hermatypic corals (Anthozoa:Scleractinia) in the Gulf of California, Mexico, with an historical and biogeographic discussion. J Nat Hist 26: 1163—1175 Reyes-Bonilla H (1993) Biogeografi´a y ecologi´ a de los corales hermati´ picos (Anthozoa:Scleractinia) del Paci´ fico de Me´xico. In: Salazar-Vallejo SI, Gonza´lez NE (eds) Biodiversidad Marina y Costera de Me´xico. CIQRO, Me´xico, pp 207—222 Reyes-Bonilla H, Carriquiry JD (1994) Range extension of Psammocora superficialis (Scleractinia: Thamnasteriidae) to Isla Socorro, Revillagigedo Archipelago, Colima, Me´xico. Rev Biol Trop 42: 383—384 Richmond RH (1985) Variations in the population biology of Pocillopora damicornis across the Pacific ocean. Proc 5th Int Coral Reef Cong 6: 101—106 Richmond RH (1990) The effects of the El Nin8 o/Southern Oscillation on dispersal of corals and other marine organisms. In: Glynn PW (ed) Global ecological consequences of the 1982—83 El Nin8 oSouthern Oscillation. Elsevier, Amsterdam, pp 127—140 Robinson JA, Thomson DA (1992) Status of the Pulmo coral reefs in the lower Gulf of California. Environ Conserv 19: 261—264 Sachet MH (1962) Geography and land ecology of Clipperton Island. Atoll Res Bull 86:1—115 Scott PJB, Risk MJ (1988) The effect of ¸ithophaga (Bivalvia: Mytilidae) boreholes on the strength of the coral Porites lobata. Coral Reefs 7: 145—151

Shen GT, Cole JE, Lea SW, Linn LJ, McConnaughey TA, Fairbanks RG (1992) Surface ocean variability at Gala´pagos from 1936—1982: calibration of geochemical tracers in corals. Paleoceanogr 5: 563—588 Squires DF (1959) Results of the Puritan-American Museum of Natural History expedition to western Mexico: 7. Corals and coral reefs in the Gulf of California. Bull Am Mus Nat Hist 118: 371—431 Stehli FG, Wells JW (1971) Diversity and age patterns in hermatypic corals. Syst Zool 20: 115—126 Stimson J (1990) Stimulation of fat-body production in the polyps of the coral Pocillopora damicornis by the presence of mutualistic crabs of the genus ¹rapezia. Mar Biol 106: 211—218 Stoddart DR (1969) Ecology and morphology of recent coral reefs. Biol Rev 44: 433—498 Vargas-Angel B (in press) Distribution and community structure of the reef corals of Utria, Pacific of Colombia. Rev Biol Trop Verrill AE (1868—70) Review of the corals and polyps of the west coast of America. Trans Connect Acad Sci I: 377—567 Veron JEN (1995) Corals in space and time: the biogeography and evolution of the Scleractinia. New South Wales Press, Sydney Wellington GM, Dunbar RB (1995) Stable isotopic signature of El Nin8 o-Southern Oscillation events in eastern tropical Pacific reef corals. Coral Reefs 14: 5—25 Wellington GM, Victor BC (1985) El Nin8 o mass coral mortality: a test of resource limitation in a coral reefs damselfish population. Oecologia 68: 15—19 Wells JW (1983) Annotated list of the scleractinian corals of Gala´pagos. In: Glynn PW, Wellington GM (eds) Corals and coral reefs of the Gala´pagos Islands. University of California Press, Berkeley, California. Wilson EC (1988) The hermatypic coral Pocillopora at Cabo San Lucas, Me´xico. Bull So Calif Acad Sci 87: 79—83 Wilson EC (1990) Mass mortality of the reef coral Pocillopora on the south coast of Baja California Sur, Mexico. Bull So Calif Acad Sci 89: 39—41