Biology and geology of eastern Pacific coral reefs - Springer Link

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

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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

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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;

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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).

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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).

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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.

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