Coral Communities and their Modifications Relative to Past and Prospective Central American Seaways

Ado. Mar. Biol., Vol. 19, 1982, pp. 91-132

CORAL COMMUNITIES AND THEIR MODIFICATIONS RELATIVE TO PAST AND PROSPECTIVE CENTRAL AMERICAN SEAWAYS P. W. GLYNN Smithsonian Tropical Research Institute, A PO Miami 34002, U.S.A. I.

Introduction

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11. Panamic Isthmian Setting

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A. Paleoecological background B. Character of extant reefs . .. .. , . , , C. Availability of colonists , . , . ., .. .. D. Access through the Panama Canal and the proposed inter-ocean seaway 111. Theoretical Considerations .. .. .. .. .. .. .. .. A. Attributes of good colonists . . .. .. .. , . .. .. B. Establishment in relation t o the biotic community , .. .. .. IV. Speculations on Some Potential Ecological Interactions . . .. .. .. A. Feeding relations , . , . ., , . ., , . , . .. ., B. Competition. .. .. .. .. .. .. .. .. .. C. Symbiosis . . , . .. .. ., .. , . ., .. , . D. Diseased organisms , . .. .. .. ., .. .. .. E. Biotic disturbance . ., ., .. .. .. , . .. .. V. Conclusions. , . , . ., ., , , , . .. .. , . , , VI. Acknowledgements .. ., .. .. .. , . ., ., . . VII. References . .. , . ., .. ., .. .. .. .. ..

The risk of adverse ecological consequences stemming from construction and operation of a sea-level Isthmian canal appears to be acceptable. (Atlantic-Pacific Interoceanic Canal Study Commission, Interoceanic Canal Studies, 1970, p. 62.) As an example of the worst thing that biologists might let slip by them, consider the possibility t h a t the Atlantic and Pacific biotas could be mingled by migration through the new Panamanian sealevel canal proposed for construction in the 1980s. (E. 0. Wilson and E . 0. Willis, Ecology and Evolution of Communities, 1975, p. 522.)

92 93 93 94 100 102 103 103 105 106 107 113 118 119 120 121 122 122

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I. INTRODUCTION During the past century man’s activities have resulted in the accidental or intentional introduction of numerous exotic species in marine, brackish and freshwater environments. Some of these introductions have been beneficial, some neutral (as presently understood) and others clearly undesirable. Commercially important fin fish and shell fish species have been transplanted on a grand scale over many parts of the world. Many of these introductions have resulted in highly successful fisheries, providing oysters, salmonids, shad, etc. to new areas (Elton, 1958; Bardach et al., 1972). Exotic fin fish have also migrated to the Mediterranean through the Suez Canal and now contribute importantly to the eastern Mediterranean fisheries (Ben-Tuvia, 1966, 1978; Ben-Yami and Glaser, 1974). Unfortunately, such redistributions may also lead to the establishment of undesirable pest species and, thus, result in serious disruptions to assemblages of native species. The slipper limpet and oyster drill, gastropod molluscs native to the North American east coast, were accidentally introduced with oyster transplants to Europe and the Pacific coast of North America (Elton, 1958; Yonge, 1960). I n British and other northern European waters, the slipper limpet became a serious competitor for space in oyster beds and reduced the population size and even replaced native oysters. The American oyster drill is a serious predator of oysters, and, because of its relatively greater tolerance to cold winters than native oyster drills, has achieved a dominant status in English oyster communities. Construction of the Erie and Welland Canals permitted the establishment of the alewife and sea lamprey in the Great Lakes (Aron and Smith, 1971). These exotic species brought about a major disruption in the native Great Lakes fish fauna. The species interactions that have occurred since these introductions are complex and have at times been influenced by over-exploitation and pollution (Christie, 1974). One unfortunate result was a serious decline of large piscivores, such as the Atlantic salmon and the lake trout, brought about in part by the predatory sea lamprey. This reduction in salmon and trout has allowed an explosive increase in the alewife, a migratory marine herring that has largely replaced the lake herring. The lake herring in the past provided forage for desirable predators and was also a valuable commercial species. If sufficient attention had been focused on the possible consequences of the introductions noted above, these ecological problems might have been anticipated and avoided. The application

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of quarantine and cleansing procedures can greatly restrict the movement of problematical species. Such screening measures would surely have prevented the introduction of the slipper limpet and oyster drill into European oyster communities. Measures t o restrict the movements of marine species (alewife and sea lamprey) into the Great Lakes could have prevented the serious problems t h a t occurred there as well. Although i t would be naive t o pretend t h a t all problem species can be identified and their movements prevented, this article will offer a tentative identification of some potentially troublesome species in American coral reef ecosystems if these Atlantic and Pacific biotas are allowed t o mingle through a sea-level canal.

ISTHMIAN SETTING 11. PANAMIC A. Paleoecological background The isthmian* region of Central America is a significant biogeographic focal point because i t is here t h a t the last portal existed through which Atlantic and Pacific coral reef biotas mingled (Woodring, 1954; Durham and Allison, 1960; Newell, 1971). When the isthmus emerged i t isolated the eastern Pacific region from t h e Caribbean Sea and the Tethyan realm, the great tropical seaway in existence since the Triassic. A restriction of flow across Centrd America occurred by the early t o mid Miocene (Holcombe and Moore, 1977; Mullins and Neumann, 1978). It has generally been held that communication of marine species, via the Panama-Costa Rica and Bolivar Troughs, ceased sometime during the Pliocene epoch, between 1 million (Olsson, 1972) and 5.7 million (Emiliani et al., 1972) years ago. Changes in the direction of coiling of planktonic foraminifera from the Atlantic and the Indo-Pacific Oceans (Saito, 1976) and the major interchange of mammalian faunas between North and South America (Webb, 1976), indicate the emergence of the Isthmus of Panama, and complete intercontinental terrestrial connection 3.5 and 3.0 million years ago, respectively. The latest cohabitation of Pacific and Caribbean reef coral biotas presently known on the isthmus is from the Panama Formation of early Miocene age (Woodring, 1957). The latest outpost of a former panneotropical (Caribbean and eastern Pacific) coral fauna probably occurred in the Pliocene, as evidenced by the Caribbean genera present in the Imperial Formation at the head of the Gulf of *Isthmian, when used alone or otherwise unqualified, refers to both t h e t'aribbean and Pacific marine ecosystems of Panama

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California (Vaughan, 1919; Durham and Allison, 1960). The existence of this assemblage was ephemeral for these corals became extinct shortly thereafter. Although post-Tethyan events are geologically recent, paleontological reconstructions in this region are limited by a meagre fossil record (Durham, 1966). Therefore, any interpretation of the evolutionary development of coral reef communities in Central America must] be viewed cautiously. During the Pliocene and Quaternary evidence indicates a general deterioration of the environmental conditions favouring reef corals, such as warm water and gradual eustatic sea-level changes (Wells, 1956; Durham and Allison, 1960; Newell, 1971). Contrasted with the Caribbean, which supported extensive coral reef development during the interstadial periods in the Pleistocene (Vaughan, 1919; Mesolella et al., 1970; James et al., 1971), and probably significant reef accretion during glacial periods (Macintyre, 1972), very few fossil reef deposits of comparable age are known from the eastern Pacific (Durham, 1980). It has been postulated that the eastern Pacific reef coral biota is a relict assemblage, surviving since its separation from the Caribbean Province after closure of the isthmian portal (McCoy and Heck, 1976; Heck and McCoy, 1978). However, Hubbs (1952, 1960) has marshalled evidence suggesting that tropical environments were severely reduced in size, if not entirely eliminated, in the eastern Pacific during Pleistocene glacial advances. Dana (1975) has suggested that eastern Pacific reef corals became extinct at such times, and extant corals and reefs in the eastern Pacific are derived largely from recent colonists from the central Pacific (Line Islands). The faunal affinity of eastern Pacific and central Pacific corals, the virtual absence of fossil Quaternary reefs on American Pacific shores, and the age of formation of extant eastern Pacific reefs (4000-6000 years B.P.; Glynn and Macintyre, 1977) are consistent with this view.

B. Character of extant reefs Many differences are evident in the general appearance of coral reefs on opposite shores of Central America. Extant Pacific reefs, which have formed during Holocene time (over the past 6000 years), are small (one to a few hectares) compared with Caribbean reefs which often cover tens to hundreds of hectares. I n addition, reef development in the eastern Pacific is attenuated in upwelling areas (Gulfs of Panama, Papagayo, Tehuantepec), along stretches of sand beach (southern Mexico to El Salvador; Springer, 1958) and near

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large river mouths and coastal areas of high rainfall (e.g. northwestern Colombia; Glynn, 1974a). A corollary of this fact is that Pacific coral reef habitats tend to be discontinuous and very limited in extent. Pacific coral reefs also show limited vertical framework construction (11-12 m maximum; Glynn and Macintyre, 1977) compared with Caribbean reefs, the largest of the latter having attained 33 m in thickness (Macintyre et al., 1977). Additionally, Pacific reefs are usually confined to protected (wave-sheltered) habitats and are restricted to shallow depths ( 1 H 5 m, as opposed to Caribbean reefs which show constructional activity to 60 m; Goreau and Goreau, 1973; Lang, 1974), particularly along Pacific continental coastlines (Porter, 1972; Dana, 1975; Glynn, 1976). As regards habitat diversity, zonation is limited on Pacific reefs, with only three to four zones present (Glynn, 1976); on well-developed Caribbean reefs, as many as 11 habitat zones are recognized (Goreau and Goreau, 1973). Submerged bank reefs, often present on insular and continental shelves in the Caribbean (Macintyre, 1968, 1972), have not yet been observed in the eastern Pacific. Thus, Caribbean reefs are much more varied and are formed under a greater range of conditions (i.e. on protected and exposed coasts and in shallow and deep environments) than those in the Pacific. Eastern Pacific reefs contain few frame-building species, usually ten or fewer scleractinian and hydrozoan corals, per reef (Fig. 1). Caribbean reefs often contain 30-50 hermatypic corals (and as high as 70 species in some areas) on a single reef (Fig. 2). Mangrove and sea grass communities, which commonly intermingle with Caribbean reefs, do not generally occur in reef habitats in the eastern Pacific. Except for Clipperton Island, the constructional contribution of crustose coralline algae appears to be less in the case of Pacific relative t o Caribbean reefs. This difference may be due, in part, to the fact that eastern Pacific reefs are generally absent from environments of high wave energy where coralline algae flourish (Adey, 1978; Dawson, 1966). A rich crustose coralline algal flora is present in the eastern Pacific (Earle, 1972; Silva, 1966; Taylor, 1945), and has undergone significant accretionary development in some areas, e.g. at Clipperton Island (Sachet, 1962), in the Galapagos Islands (Wellington, 1975), and in Colombia and Costa Rica (Glynn, personal observations): however, coral framework construction and algal buildups do not generally occur together. I n addition to the significant difference in number of reef-building corals, there is also a greater species representation in many diverse taxa on Caribbean as opposed to Pacific reefs. Absent or rare in

F I ~ 1. Windward upper slope zone ( 3 m d e p t h ) o f a n actiwl? atcreting Pacific coral reef corals are the only discernible macrobenthic species

Secas Islands Gulf of Chiriqui (24J u n e

1978) Pocilloporid

FK 2 Windward upper slope zone (7 m depth) of an activel) accreting Caribbean coral reef. Korbiski Island, San Blas Islands (19 August 1978) Scleractinian corals, hydrocorals And gorgonacean coelenterates are vivible

Eastern Pacific Physical Thermocline and high nutrient environment levels occur a t shallow depths. Upwelling areas and cool water currents are widespread. Tidal amplitude large (up to 6 m j and predictable. Turbidity high near coast with increasing clarity on offshore islands. Nature of reefs

Reefs small, one to a few ha in area. Reefs are discontinuous and relatively isolated (island-likej. Maximum Holocene framework thickness 12 m. Mean reef frame accumulation rates = 1.3-75 m 1000/yr Reefs form in sheltered habitats and are not well-consolidated. Framework construction occurs a t shallow depth, usually no deeper than 10-15 m; submerged reefs on insular and continental shelves are unknown.

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Habitat diversity is low with three to four vertical zones per reef. Number of reef-building corals is low with eight to ten species per reef. Sea grass and mangrove communities are not present near coral reefs. Crustose coralline algae rarely form an algal ridge.

Caribbean Thermocline and high nutrient levels occur to lower depths. Upwelling areas and cool currents are limited in extent. Tidal amplitude small (c. 1 in j and unpredictable. Light penetration moderate to high.

Reefs large, from one to hundreds of ha in area. Reefs are widespread and often occur continuously over large geographic areas. Maximum Holocene framework thickness -33m. Mean reef frame accumulat,ion rates = 06-39 m 1000/yr Reefs form in low to high energy environments and are well-consolidated. Framework construction occurs in shallow and deep water, to 60 m depth; submerged bank or barrier reefs on insular and continental shelves are common. Habitat diversity is high, with up to 11 vertical zones per reef. Number of reef-building corals is high, with 30-50 species per reef. Sea grass and mangrove communities overlap extensively with coral communities. Crustose coralline algae commonly serve as cementing agents and often construct algal ridge features.

TARLF: 1 (cmt.) Eastern Pacific Ecological attributes

Impoverished with respect t o numerous sedentary taxa, i.e. calcareous green algae, large fleshy algae, sea grasses, large fleshy sponges, hermatypic corals, sclerosponges, gorgonaceans," actiniarians, zoanthids,b crinoids, colonial tunicates. Number of individuals per species is generally high. Corallivores are abundant with significant effects on coral growth and relative abundances of corals. Predation on motile, invertebrate corallivores is high. Sponge predators (cowries, asteroids, fishes) abundant and possibly responsible for low sponge cover on reefs. Competition for space among corals is intense. Branching corals contain protective symbiotic crustaceans. Pathogens are presently unknown in eastern Pacific coral communities. Organisms capable of binding calcareous skeletal remains are generally rare

Bioerosion is intense.

Caribbean With relatively rich and diversified sedentary biota.

Number of individuals per species is low to moderately high. Corallivores relatively insignificant. Predation on motile, invertebrate corallivores is low. Sponge predation is limited.

Competition for space between corals and other benthic taxa is intense. Branching corals without ( ? ) protective symbiotic crustaceans. Pathogenic blue-green algae and bacteria are reported in reef corals and associated fauna. Biotic binding agents (e.g., encrusting red and calcareous green algae, sea grasses, sponges, zoanthids, gorgonaceans) are abundant. Bioerosion is moderate.

"Gorgonians are abundant on Pulmo Reef in the Gulf of California (Squires, 1959; Brusca and Thomson, 1977). 'An extensive (several hundred m2) carpet of zoanthids was observed on a pocilloporid reef near Machalilla, Ecuador (1" 28's; 80"47'W) (Glynn, personal observations). Carlgren (1951) also noted abundant zoanthid (Palythm)coverage in the Gulf of California.

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eastern Pacific reef environments are calcareous green algae, sea grasses, large fleshy sponges, and gorgonacean (horny corals), actinarian (sea anemones) and zoanthidean coelenterates, all of which are prominent on most Caribbean reefs. Whereas Pacific reefs can be fairly categorized as paucispecific, they are not sub-normal (relative to Caribbean and Indo-west Pacific reefs) in growth rate (Glynn, 1977; Glynn and Macintyre, 1977), in live hermatypic surface coverage or in the biomass of their associated biota (Glynn et al., 1972; Porter, 1974; Glynn, 1976). Consequently, the relatively few species often occur at higher population densities than do their Caribbean counterparts. The generally greater abundance of reef fishes in the Pacific, compared with the Caribbean, is probably related to the greater productivity resulting from the shallow distribution of nutrients in the upper layers of the sea and periodic upwelling in certain areas. These differences between isthmian coral reefs, notwithstanding the inevitable exceptions that will come to light, are summarized in Table I . Additional attributes that are discussed below are also included in Table I . C. Availability of colonists The distribution of extant coral reefs, and some noteworthy reef associates on opposite sides of Panama, were presented in synoptic form in 1972 by Glynn (1972) and Porter (1972). A t that time, structural coral reefs were indicated near the Caribbean entrance to the Panama Canal and in the Gulf of Chiriqui, about 360km southwest of the Pacific entrance (Fig. 3). More recent findings have shown that flourishing coral reefs are also present in several areas in the Gulf of Panama (Glynn and Stewart, 1973; Glynn and Macintyre, 1977). Small patch reefs occur in the Taboga Island group, 15 km south of the Pacific entrance to the canal. Porter (1972) lists 36 species of scleractinian and hydrozoan reef builders near the Caribbean canal terminus and eight species at Taboga Island on the Pacific side. The movement of coral reef species through the Suez Canal is not favoured because of the absence of coral reefs at either end of that canal (Por, 1971). It is obvious from the above that the situation in Panama is otherwise. Although live reef communities occur near the present canal, these communities are relatively impoverished when compared with reef assemblages elsewhere in Panama. For example, reefs in the San Blas area on the Caribbean coast comprise up to 50 species of coelenterate hermatypes (Porter, 1972), and in the Gulf ofchiriqui 15

C A NA L

C A R IB B E A N

E NT R A NC E

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PANAMA C I T Y

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C A N A L ENTRANCE

FIG.3. Location of coral reefs, volcanic rock substrata and mangroves in relation to Pacific a n d Caribbean entrances of present locks canal and proposed sea level canal routes 10 and 14. Distance scale applies to both maps.

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species (Glynn et al., 1972; Porter, 1972). This trend is evident in other, but not all (Abele, 1976) taxa. Reef fishes, for example, are also represented by more species on coral reefs in the Gulf of Chiriqui than in the Gulf of Panama (Rosenblatt et al., 1972).

D. Access through the Panama Canal and the Proposed Inter-ocean Seaway Pacific and Caribbean coral reefs are presently separated by less than 100 km across the Central American isthmus. Nonetheless, Gatun Lake has served as an effective freshwater barrier since the Panama Canal opened in 1914 (Rubinoff, 1970; Jones and Dawson, 1973). Few documented cases of marine species moving through t h e Panama Canal waterway are known-nine fishes had transited the canal by 1971 (McCosker and Dawson, 1975).The saline waterway of the Suez Canal has permitted the migration of nearly 200 marine species in the 100-year period 1869-1970 (Aron and Smith, 1971). The colonization of species via ship’s bottoms (Menzies, 1968) is also a likely possibility. Following drought conditions on the isthmus in the early 1970s, a plan was considered to pump sea water into Gatun Lake to increase the supply of lockage water. Even minimal salinization (to 2-3%,) would greatly reduce the effectiveness of the Gatun barrier (McCoskerand Dawson, 1975).Another way the Gatun barrier might be circumvented is by transport of marine organisms (including their spores, cysts, larvae, etc.) in the ballast water of tankers (Chesher, 1968; Dawson, 1973). Increasing numbers of oil tankers are now dumping clean (i.e. chemically, but not biologically, clean), Caribbean water, up to 20-30000 tons each, in Parita Bay, Gulf of Panama (N. Smythe, personal communication). Given an inter-oceanic seaway across Central America and an array of potential coral reef colonists, there still remain numerous circumstances that could hinder or promote migrations. While no single set of physico-chemical parameters is optimal for all species, reef-dwelling organisms generally do best in shallow, warm, sun-lit waters of high (oceanic) salinity and adequate circulation (Wells, 1957; Stoddart, 1969a).A firm substratum and low sediment load are additional factors that favour survival of corals and associated species. The impoverished character of coral communities in the Gulf of Panama is probably due in large part to the seasonal upwelling regimen in this area. The increased turbidity in the dry season, due largely to the resuspension of mud-rich sediments, is believed to be a

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significant limiting condition for reef growth around the Caribbean canal entrance (Macintyre and Glynn, 1976). Certain conditions are likely to occur across a Panamanian seaway: (1) a mean Pacific sea level elevation 30cm higher on the Pacific than the Caribbean would result in net water movement into the Caribbean; (2) canal water will oscillate in response to changing tides; (3) most water transport would be from the Pacific to the Caribbean, but some small amounts of Caribbean water would probably also reach the Pacific (Sheffey, 1972). If mean volume transport from the Pacific to the Caribbean is 9.6 x lo7m3 (78000 acre-feet) per day, unrestricted flow (Sheffey, 1972), it is likely that, the temperature-salinity characteristics in a sea-level canal would approximate those surrounding the canal entrances. Sea surface temperatures of 23-28°C and salinities of 28-35%0, which delimit the mean long-term ranges on either side of the canal (Glynn, 1972), are not expected to interfere with the movement of most marine species. On the other hand, oscillating tidal currents may produce unfavourable conditions-high sediment transport and resuspension regimes, reduced light levels in the water column-for many coral reef species. Harleman (1972) calculated that a parcel of water would move from the Pacific to the Caribbean side of a sea-level canal in 2.5 days. Since the majority (80-85%) of tropical, shallow-water benthonic species produce planktotrophic larvae with pelagic phases of from 1 to 26 weeks (Thorson, 1950, 1961; Mileikovsky, 1971; Scheltema, 1977), it is reasonably certain that a mass transport of young stages will take place. The likelihood that adult benthonic reef species can establish “stepping-stone” populations in the proposed sea-level waterway is probably considerably less than the movement of species via currents. While numerous adult coral reef species (including Acanthaster and hermatypic corals, inter alia) can be maintained in aquaria throughout the year a t the present Pacific terminus, surviving seasonally low water temperatures (20-22°C) and salinities (l8-20%,) (Glynn, 1974a), it seems unlikely to me that they could establish viable populations under the high sedimentary regimes envisioned in or near a sea-level canal.

111. THEORETICAL CONSIDERATIONS

A. Attributes of good colonists Successful colonists often possess one or more of the following attributes: (1) a greater dispersal ability, (2) ability to produce a

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propagule, i.e. the minimal number of individuals of a species necessary to allow for continued reproduction (MacArthur and Wilson, 1967), ( 3 ) a high intrinsic rate of natural increase (e.g. early age at first reproduction, repeated reproduction, high fecundity and rapid development, Steams, 1976) and (4) a generalized behaviour and physiology (sensu Slobodkin, 1968) allowing for adjustments to new environmental circumstances. Many of these characteristics are shared by opportunists, i.e. species that prosper in temporary and unpredictable environments (MacArthur, 1972; Pianka, 1974). Vermeij ( 1 978) summarizes evidence indicating that many long-lived marine organisms, which often occupy constant and predictable environments, also have exceptional powers of dispersal. Because both opportunists and long-lived species are probably involved in colonization events, Vermeij suggested that the attributes of potential isthmian migrants can be best understood from an analysis of how migrating species from a donor source (e.g. Red Sea to Mediterranean or central Pacific to eastern Pacific) differ from species that have not migrated. With respect to propagule size (2, above), certain larval traits deserve further notice. A t least some planktonic larvae test surfaces and delay settlement and metamorphosis until an appropriate substratum is found (Crisp, 1974; Wilson, 1960). Further, larval settlement is often gregarious (aggregated), occurring among previously settled larvae or adults of the same species (Wilson, 1968). Such larval behaviours will allow freely dispersing species to settle on suitable surfaces in close enough proximity to ensure reproductive success. The capacity of invading species to tolerate new environmental conditions (an aspect of 4, above) was suggested by Por (1975),t o play an important role in the Lessepsian migration through the Suez Canal. Por believes that the dominant movement of species from the Red Sea to the eastern Mediterranean, is due in large part to a greater tolerance to physical stress of the northern Red Sea biota which evolved under harsh glacial episodes in the Pleistocene. I n contrast, the eastern Mediterranean biota, which is largely a product of mild interglacial periods, is not preadapted to cope with t h e physical rigors of the Suez waterway. In Panama, Pacific species inhabiting rigorous environments, e.g. the intertidal zone and upwelling areas, may have a greater tolerance and potential for establishment than Caribbean species. However, stressful conditions, such as unpredictable tidal exposures and periods of severe wave action, also occur frequently on the Caribbean reefs of Panama.

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Organisms reproducing by means of planktonic larvae-probably the bulk of coral reef species-commonly possess adaptations correlated with good colonists ( 1 , 2 and 3, above). Therefore, i t seems reasonable to postulate that isthmian coral reef communities of both coasts offer a great potential for reciprocal colonization. If the eastern Pacific biota contains many elements that arrived by longdistance transport from the central Pacific (and I believe the evidence for this, referred to in part below, is very good), then one may assume that such species are predisposed to invade accessible and suitable Caribbean environments. Invasion, however, does not guarantee the successful establishment of a species. An invading population must also overcome a multitude of obstacles to insure colonization.

B. Establishment in relation to the biotic community Evidence, based on the colonizing and replacement-success t h a t has occurred between mammal and bird assemblages of different regions (Simpson, 1947; Darlington, 1957, 1965; Mayr, 1965; Patterson and Pascual, 1972), and marine fish faunas and other groups (Briggs, 1970, 1974), has been synthesized into a general zoogeographic theory, namely t h a t concerning the evolutionary centres of origin. This concept maintains that there exist evolutionary centres of high species diversity; from these, advanced, competitively dominant species disperse and tend to displace older established species occupying marginal areas. The general competitive ability of a biota is positively correlated with provincial diversity. Briggs (1969)applied this view to a reciprocal interoceanic migration scenario in Panama and predicted the mass extinction (one to 5000 species) in the relatively species-poor eastern Pacific region by the richer western Atlantic tropical biota. One must not lose sight of the important contribution of IndoWest Pacific species to east Pacific coral communities, however. Accordingly, from the aforegoing argument, many species of corals, hydrocorals, molluscs, crustaceans, echinoderms and fishes (Wells, 1978; Glynn et al., 1972; Emerson, 1978; Garth, 1974; Chesher, 1972; Rosenblatt et al., 1972 respectively), for example, might be expected t o immigrate and some possibly displace their competitively inferior counterparts in the western Atlantic region. Of course, this prediction must be tempered with the possibility that many IndoWest Pacific migrants became established in the eastern Pacific because of the impoverished nature of the coral communities in this region.

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However, i t is by no means certain that community structure (species composition and relative abundances) is, indeed, largely controlled by competitive processes. I n reviewing mostly experimental evidence, Connell (1975, 1978) concluded that population densities are seldom great enough t o allow competitive displacements between species. Rather, a strong case is made for predation (including eating plants) and disturbance (physical and biotic) as important processes in controlling community structure. Environments subject to natural perturbations or disturbances by man often allow the entry of opportunistic species, i.e. species which share many of the characteristics of successful colonists. Wilson and Willis (1975) suggested that the variable Pacific environment, subject to seasonal upwelling events, would favour the evolution of a high proportion of opportunistic species that could insert themselves into the Caribbean biota. Birkeland’s (1977) analysis of Caribbean and Pacific colonizing species in Panama has, indeed, demonstrated that opportunists predominate in later stages of community development in the Gulf of Panama. Thus, one may envisage a plume of upwelled water extending through a sea-level canal into the Caribbean, and providing suitable conditions for the transit and at least temporary presence of exotic opportunistic species. This hypothesis argues for a biotic migration opposite t o that suggested by Briggs (1969). But Caribbean coral communities also have a multitude of opportunists that invade storm-ravaged reefs (Stoddart, 1969b), reef flat habitats experiencing unpredictable exposures and mass mortalities (Hendler, 1977),and other disturbed habitats. Therefore, it is probable that some opportunistic species would move and colonize in both directions with a somewhat stronger migratory component arising from the Pacific side.

IV. SPECULATIONS ON SOME POTENTIAL ECOLOGICAL INTERACTIONS I t has been argued thus far that potential coral reef colonists occur on both sides of the isthmus near the preferred sea-level canal routes, that many (if not the majority) of these species could transit a sea-level waterway lacking an effective biotic barrier, and that isthmian coral reef communities differ on a variety of levels, e.g. taxonomic affinity, relative abundances of major guilds and ecological processes influencing community structure. These postulates form the basis of a challenging task: to predict the possible

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outcome of the reunion of reef biotas that have been separated for millions of years. A range of interactions and effects of certain coral reef species have been identified, at least in general terms, during the past two decades. From this largely qualitative knowledge, some speculations are offered on possible outcomes of a variety of potential Caribbeanpacific species interactions.

A. Feeding relations Clearly one of the more immediate results that can be expected, in the event of open access between the two oceans, will involve feeding interactions between invading and native species. Predation alone, recalling the dramatic effects of the Crown-of-Thorns sea star, Acanthaster, has been demonstrated to disrupt coral reef ecosystems over great areas (Endean and Stablum, 1973; Vine, 1973; Ormond and Campbell, 1974). Acanthaster has caused local extinctions of corals on some reefs with severe repercussions on the variety of life depending directly or indirectly on live coral. Several animals are now known to feed directly on the tissues of live, reef-building scleractinian and hydrozoan corals (Robertson, 1970; Glynn, 1973; Randall, 1974). Animals having apparently no or only slightly harmful effects on their coral hosts, such as species engaged in capturing food from corals or feeding on mucus and detritus (Patton, 1976), are not considered here. An inventory of the presently known corallivores of American coral reefs is presented in Table 11. Note that the majority of these corallivores (those with asterisks), 26 out of a total of 38 species, have been observed on Pacific or Caribbean reefs in Panama. Many of these corallivores, e.g. Hermodice, Coralliophila abbreviata and Acanthaster, feed on a variety of coral species, or, in the case of Mithrax, Diadema, damselfishes and parrotfishes, on other kinds of organisms as well. These species, with their generalist-type diets (an important attribute of successful colonists), could probably feed on a variety of novel prey in natural habitats [cf. next paragraph]. Preliminary observations on individual corals in aquaria and on coral patches maintained in large laboratory tanks have shown that all corallivores, thus far tested, will consume novel coral prey. (Novel species are here defined as organisms that are not presently members of a particular biota.) The ability of a Pacific corallivore, the gastropod Jenneria, to feed and reproduce on a diet of Caribbean corals was first demonstrated by D'Asaro (1969) and corroborated

TABLE 11. INVENTORY OF AMERICAN CORAI.I.IVORES Ksows TO FEED ON SCLERACTISIAN AND HYDROZOAS HER MA TYPE^ The coral species involved follow the enumeration scheme given at the bottom of the table. Corallivores observed in the isthmian faunas are indicated by asterisks. Note that key numbers of Pacific species are in boldface. Pammic Pam& Taxonmic group

Corallivore species

Coral prey

Polychaetous annelid

Gastropod molluscs

*Jenneria pustulata (Lightfoot)"

Muricopsrs zeteka Hertlein and Strong Lutiaxis (Babelcnnurex) hindsii Carpenter

8, 13 (D'Asaro, 1969)b 4, 12, 14 (personal observation) 2 (Glynn et al., 1972)

4 (Wellington, 1975)

Caribbean- West Indian Corallivore species

Coral prey

*Hermodice earunculata (Pallas)"

10, 11 (Marsden, 1962, 1963) 2 (Glgnn, 1962) 10, 11, 14, 15, 16, 20, 27 (Ott and Lewis, 1972) 25 (D. R. Robertson, personal communication) 3 (Antonius, 1976; Shinn, 1976) 2*, 12 (personal observation)

*Corallawphila abbreointa (Lamarck)

20 (Ward, 1965) 2,3,4,7,9,10,11, 14, 15, 16, 17, 20 (Miller, 1970)' 2, 3, 4 , 8, 15, 16, 20, 24 (Ott and Lewis, 1972) 18 (personal observation)

*Coralliqphilo (caribbaea)Abbott

2, 5, 9, 10, 1 1 . 24 (Miller, 1970)' 3 (J. C. Lang. penonal communication)

*Quoyula madreporarum (Sowerby) Aeolid nudibranch

Crustaceans

Echinoderms

*Trimpagurus magnifeus (Bouvier) *Aniculus elegans Stimpson *Acanthaster plnnci (LiMaeUS)d

*Pharia pyramiduta (Gray) *Nidorellia a r m t a (Gray) *Eueidaris thomrsii (Valenciennes)

2 (Glynn et al.,

1972) * Phestilla sp. 8 . 10 (R. C . highsmith, personal communication)

2 (Glynn et al., 1972) Variety of Pacific hermatypic scleractinians and hy drocorals' (Barham et al., 1973;Dana and Wolfson, 1970; Glynn, 1974a,1976; Porter, 1972) 4, 10, 12 (cited in Porter, 1972)b 3 (Dana and Wolfson, 1970) 4 (Galapagos Iss., personal observation) 2. 4 (Glynn eta!., 1979)

Calliostoma javanieum Lamarck

6,23' (Lang, 1970) 4b (Miller, 1970)

*Mithrax sculptus (Lamarck)

11, 12 (Glynn,1975)

Oreaster reticulatus (Linnaeus)

3,20 (L.Buss, personal communication)b

*Diadems antillarum Philippi

1, 2,3,4,20,27 (Bak and van Eys, 1975) 19 (Dana, 1970)

TABLE I1 (cont.) Taxonomic P U P

FISHES

Spadefish Butterfly fishes and Angelfishes

Damselfishes

Panamic Pacijic Corallivore species

Coral prey

Caribbean- West Indian Corallivore species *Chaetcdipterus faber (Broussonet) *Chaetodm eapistratus Linnaeus

*Microspathodm chrysurus (Cuvier and Valenciennes)

* E u p m e n t r u s planifrons (Cuvier and Valenciennes)

*Eupornncentrus dmsqpunaeans (Poey)

Coral prey 22 (Randall, 1967) 8, 20 ( L . Buss, personal communication)

Bohlke and Chaplin ( 1968) Note that western Atlantic Chaetodontidae browse on reef- building corals 25 eaten by juveniles (Ciardelli, 1967; Glynn, 1973) 2, 13 eaten by juveniles (D. R. Robertson, personal communication) 8, 25 eaten by adults (Glynn, 1973) 3, 1 1 , 18, 20 (Kaufman, 1977) 25 eaten by juveniles (D. R. Robertson, personal communication) 25 eaten by juveniles (D. R. Robertson, personal communica.tion)

Parrotfishes

*Scarus ghobban Forsskll

6 (Glynn et al., 1972)

*Scarus perrico Jordan and Gilbert

3 (Glynn et al., 1972)

*Scarus croicensis Bloch Scarus vetula Bloch and Schneider S p a r i s m viride (Bonnaterre) Scarus taeniopterus Desrnarest Sparisoma aurofrenatum (Cuvier and Valenciennes) Alutera scripta (Osbeck) Cantherhines macrocerus (Hollard) Cantherhines pullus (Ranzani)

Filefishes

Puffers

*Arothrm hispidus (Linnaeus) *Arothron meleagris (LacBpide) *Canthigaster amboinemis (Bleeker)

Unidentified fragments (Randall, 1967)

Scarus coelestinus Cuvier and Valenciennes *Scarus gwmmaia Cuvier

II

8 and probably 2, 3, 4, 12, 20 (Bakus, 1969; Glynn, 1973) 3 (J.Ogden, personal communication) 1, 4, 8, 10, 11, 20, 21, 27 (Frydl, 1977) 1, 4, 8, 10, 11, 20, 21, 27 (Frydl, 1977) 10 (Gygi, 1975)

1, 11 (Frydl, 1977)

26 (Randall, 1967) Unidentified scleractinians (Randall, 1967)

1 , 2 (Glynn et al., 1972, unpublished data) 1 , 5 , 7 (Glynn et al., 1972, unpublished data) Unidentified scleractinians (Hobson, 1974)

Pacific corals: 1-Psammoeora (Stephanuria)stellata (Verrill): 2-Pocilloporid species, including Pocilloporu damicornis (Linnaeus), P. capitata Verrill, P . lacera Verrill, P . robusta Verrill; *Poeillopora sp.; 4--Patma clavzu Dana; 5-Pavma sp.; G P o r i t e s panamensis Venill; 7-Porites californica Verrill: 8-Porites lobata Dana.

TABLE 11 (cont.) Caribbean corals and hydrocorals: 1-Madracis mirabilis (Duchassaingand Michelotti); 2-Acrqpma palmata (Lamarck);3-Acrqpora cervicornis (Lamarck);4-Agaricia agaricites (Linnaeus);5-Agaricia sp.; 6-Agaricia spp.; 7-Helioseris cucullata (Ellis and Solander);8-~’iderastrea siderea (Ellis and Solander); 9-8iderastrea radians (Pallas);1 G P m i t e s astreoides Lesueur; 1 1-Porites porites (Pallas); 12-Porites furcata Lamarck; 13Purites sp.; l4-Favia fragum (Esper); 15-Diploria divosa (Ellis and Solander); 1 6 D i p l m i a strigosa (Dana); 17-Diplmia labyrinthiformis (Linnaeus); 18- Colpqphyllia natans (Miiller); lZ)--Colpqphyllia sp.; 2&Mmstrea annulan’s (Ellis and Solander); 21-Montastrea cuvernosa (Linnaeus);2 2 4 c d i m diffusa Larnarck; 23-Mussa angulosa (Pallas);24-Mycetophyllia lamarckana Milne-Edwardsand Haime; 25-Millepora wmplanatu (Lamarck); 2 6 M i l l e p o r a alcicmnis (Linnaeus): 27-Millepora sp. “Species with asterisks observed in Panama. Laboratory observations. Suggested to play a parasitic role. *Acunthaster ellisii (Gray) is believed to be a junior synonym of A . planci. See Glynn (1974a). ‘Species lists are available in Glynn et al. (1972) and Porter (1972).

CORAL ('OMM~'N11'IES

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and extended to include additional novel coral species (personal observations). Acanthaster has been shown to feed on all Caribbean corals thus far offered (five species).On a small coral patch containing both Pacific and Caribbean corals, Acanthaster fed indiscriminately on all species except the Caribbean coral Porites furcata, which was eaten last; the sea star remained on the patch until every colony was consumed (Fig. 4 ) .The Caribbean polychaete Hermodice, which often feeds on thick (up to 1-5em), branching Caribbean corals (Porites furcata, P. porites and Acropora cervicornis), feeds avidly on Pacific species of Pocillopora, whose colonies are formed of branches less than 1.5cm thick (Fig. 5). In addition, the Caribbean Coralliophila abbreviata is being maintained in our laboratory on a diet of Pacific Pocillopora. The damage caused by many of these corallivores in their native surroundings does not appear to be excessive. However, in the face of an invasion, where native corals may lack adequate defensive mechanisms to cope with exotic corallivores or where predation or competition on corallivores is relaxed, i t is possible that their effects could take on a new destructive dimension. For example, the low rates of predation by fishes on the echinoid Eucidaris in the Galapagos Islands, compared with mainland eastern Pacific populations, has been hypothesized to explain the high population densities of the sea urchin in the Galapagos and its limiting effect on reef development there (Glynn et al., 1979). While it is not possible to consider here other aspects of feeding ecology in coral communities, it must be emphasized that interactions of this genre can have a wide and complex range of effects. Disruptions in coevolved antipredatory adaptations such as those involving skeletal architecture (Vermeij, 1974, 1977), the utilization of noxious and toxic substances (Bakus, 1969; Bakus and Green, 1974; Fenical, 1975), crypsis, aposematism and mimicry (Wickler, 1968; Rubinoff and Kropach, 1970;Edmunds, 1974) are all conceivable effects that could result from a biotic interchange. B. Competition Interspecific competition, a mutual interference interaction between species due to the utilization of common and limiting resources, is an omnipresent and potent ecological factor. The mechanisms of competition are diverse and may be broadly classified into exploitation and interference modes (Miller, 1967). Interference competition, exemplified in sedentary species by allelochemical

FIG.4. Acanthasterplanci feeding in a mixed patch ofCaribbean and Pacific corals. These animals were maintained in isolation in a 115 kl(30 400gal.) tank a t Naos Island. Arrows denote Pacific (Pocillvpora damicornis, (1); Puwona gigantea, ( 2 ) )and Caribbean (Agaricia agaricites, ( 3 ) )corals eaten by the sea stan.

('ORAL ('OMMUNITIES

115

FIG.5. Hermodice

mruncuZatu, a Caribbean polychaete worm, feeding (in isolation) on the Pacific coral Pocilbpora dumicornis. Arrow points to head end of worm over a branch-tip of the coral. Tissues have been stripped by the worm from the three branch-tips at topcentre.

effects, extracoelenteric digestion and overgrowth responses, in'volves a direct interaction whereby one species denies another access to a requisite limiting resource. Exploitative competition is an indirect interaction whose outcome depends on the relative efficiencies of species in utilizing a mutually accessible but limiting resource. A fast-growing species that can gain access quickly to some required minimum amount of space, sunlight or plankton-rich currents may successfully exploit these resources at the expense of its slower growing neighbours. Reef-building corals compete for space by rapid growth and overtopping (exploitative competition) and by extracoelenteric digestion and overgrowth through direct contact (interference competition), Pocilloporid corals, in part because of a relatively high growth rate ( 3 . M . O cm/yr; Glynn, 1977), predominate in the eastern Pacific where they form monogeneric reefs in many areas (Galapagos Islands, mainland Ecuador, Colombia, Panama, Costa Rica and Mexico). Caribbean acroporid corals, which occupy extensive areas in shallow reef zones, are faster growing species than eastern Pacific

116

P. W. GLYNN

corals. Acropora palmata and A . cervicornis grow linearly from 6 to 10 cm/yr (Gladfelter and Monahan, 1977) and 14-27 cm/yr (Lewis et al., 1968), respectively. If linear growth differences should prove to be important, then it is possible that Acropora corals would, to a large extent, replace pocilloporid corals on Pacific reefs in the event of interoceanic access. I n addition, two acroporid species, Acropora palmata and A . prolifera, have a spreading growth habit which frequently leads to overtopping and the death of adjacent slowgrowing or prostrate corals. Another relevant factor involves extracoelenteric feeding, whereby corals growing in close proximity extrude mesenterial filaments and digest and kill their heterospecific neighbours. Such interactions in the Caribbean, where they were studied extensively by Lang (1973), are hierarchical with small, slow-growing species ranking highest in ability to injure neighbouring corals. Thus, if dominant and subordinate juvenile corals grow side by side, the subordinate species could be eliminated in spite of an advantage in growth rate or pattern. Recent observations by Sheppard (1979) in the Indian Ocean indicate that predictions involving the competitive outcomes between Pacific and Caribbean corals will not be a straightforward task. Contrary to the situation in the Caribbean, where dominant members of a hierarchy are present in all reef habitats, but constitute relatively minor components of the reef, many of the highest ranking corals studied in the Indian Ocean are the dominant members of certain reef zones (see also Connell, 1976). Additionally, the capacity of Indo-Pacific corals to damage adjacent species through extracoelenteric feeding is not clearly related to their morphology or taxonomic position (Sheppard, 1979). A further complication arises from the discovery of Wellington (1980) that previously established hierarchies in the eastern Pacific (Glynn, 1974b) can be reversed over longer periods of time. For example, eastern Pacific Pocillopora spp. typically develop elongated sweeper tentacles that eventually (7-60 days) kill initially dominant pavonid species. The recent discovery of Pocillopora in Caribbean fossil deposits of late Pleistocene age (60000-120 000 years B . P . ) indicates that this coral genus survived on Caribbean reefs until relatively recently (Geister, 1977). Paleo-ecological analysis of former habitat conditions (shallow, protected, backreef or lagoonal environments) and species composition of the scleractinian assemblage led Geister to conclude that Pocillopora was competitively inferior to contemporaneous Caribbean coral taxa. This conclusion is compatible with some

CORAL COMMLTNITIES

117

of the known competitive attributes of Pocillopora compared with Caribbean species, i.e. (1) lower growth rate (with respect to Acropora), (2) non-overtopping colony form and (3) poor space competitor, at least in parts of the western Pacific (Maragos, 1972; Connell, 1976). On the other hand, the development of sweeper tentacles in Pocillopora might give these corals an advantage in close encounters. (Some Caribbean corals have sweeper tentacles also; see Richardson et al., 1979). Finally, considering the apparent low abundance of Pocillopora before its extinction in the Caribbean, one cannot discount the possible important effects of predation or disease on remnant populations. While corals often predominate in shallow, well-illuminated zones, reef surfaces typically contain diverse taxa that frequently compete directly with corals for space under these conditions. For example, reef-building corals are commonly overgrown by algae (Birkeland, 1977; Connell, 1973; Glynn, 1973),foraminiferans (Bak et aE., 1977), sponges (Riitzler, 1971, 1972; Glynn, 1973), other coelenterates, such as sea anemones (Ott, 1975; Sebens, 1976), zoanthideans (Glynn, 1973) and gorgonaceans (Kinzie, 1970; Glynn, 1973),and tunicates (Bak et al., 1977). Recalling the low abundances or virtual absence of such groups on eastern Pacific coral reefs, it is possible that non-coral, benthic Caribbean elements could acquire significant space in such habitats if allowed access to them. Competitive outcomes can also be influenced by the feeding activities of animals not directly involved in competition a t that trophic level. Experimental studies have shown that when browsers and grazers are excluded, the community composition of reef surfaces often changes dramatically. The constant cropping of algae by herbivorous fishes allows other benthic organisms to compete and occupy surfaces that would not otherwise be available to them (Stephenson and Searles, 1960; Randall, 1965; Bakus, 1969; Wanders, 1977). Many fishes selectively graze on algae, in some cases avoiding juvenile corals (Birkeland, 1977), and, thereby, prevent rapidly growing plants from monopolizing available substrata. Areas supporting high population densities of sea urchins, which efficiently crop fleshy algae, often contain sparse fleshy algal cover (Sammarco et al., 1974; Benayahu and Loya, 1977),have a high surface coverage of crustose coralline algae (Van den Hoek et al., 1975; Adey and Vassar, 1975), and are probably better suited for the recruitment of corals and other animals that compete with fleshy algae (Dart, 1972). There are also animal feeding behaviours that encourage algal growth, such as the algal gardens defended by damselfishes (Brawley

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P. W. GLYNN

and Adey, 1977).Kaufman (1977)hypothesized that the competitive outcome between two coral species in the Caribbean (Montastrea annularis and Acropora cervicornis) can depend on the territorial feeding behaviour of a damselfish. I n killing coral to extend their algal gardens, the damselfish-induced mortality of corals has a greater effect on Montastrea than on Acropora. Montastrea regenerates slowly and is subject to a high rate of invasion by boring organisms, thus allowing Acropora to increase and monopolize certain reef zones. It is, therefore, necessary to consider possible competitive interactions between Pacific and Caribbean species in relation to predation and, probably, other ecologic processes (see below). It is conceivable that the migration of exotic corallivores and sponge feeders, abundant in the eastern Pacific compared with the Caribbean (Glynn, 1972), into the Caribbean could reduce coral and sponge cover and alter competitive interactions to the advantage of presently minor groups of solitary organisms (Jackson, 1977). C. Symbiosis Symbiosis, here defined as an intimate and mutually beneficial association between species, is a commonly encountered relationship on coral reefs. Crabs and shrimps living as obligate symbionts on Pacific pocilloporid corals, from which they obtain shelter and nutriment, offer protection to their coral hosts by repulsing the corallivore Acanthaster (Pearson and Endean, 1969; Weber and Woodhead, 1970; Glynn, 1976). Large coral colonies containing agonistic crustacean symbionts are virtually immune from predation because the crabs pinch and pluck at the tube feet and the shrimps grip spines and snap explosively at sea stars attempting to mount the coral. Some Caribbean corals also harbour symbiotic crustaceans (e.g. the crab Domecia on Acropora palmata), but it is not known if these act to protect their hosts from novel corallivores. In the case of pocilloporid corals and their crustacean symbionts, which have evolved in the presence of Acanthuster, the selective advantage in protecting an essential resource is obvious. Caribbean species of Acropora, however, are not attacked by corallivores that destroy the entire colony in a natural situation, and it is, therefore, unlikely that a strong defensive behaviour has evolved in this particular coral-crab partnership. Thus, if invading pocilloporid symbionts cannot adapt to Caribbean acroporid corals (and they do not live on sympatric Indo-Pacific acroporids),the latter would be vulnerable to attacks by

CORAL COMMUNITIES

119

Acanthaster. I n fact, Indo-Pacific Acropora species are a preferred food of Acunthaster (Goreau et al., 1972; Endean and Stablum, 1973; Laxton, 1974; Ormond et al., 1976). Laxton (1974) speculated that Acanthaster could seriously damage western Atlantic reefs where Acropora is an important frame-building species. Cleaning symbiosis, in which certain reef fishes allow other fishes or shrimps to clean their bodies of unwanted food, parasites or diseased tissues, is a highly coevolved relationship on coral reefs (Feder, 1966;Ehrlich, 1975).Cleaner stations, focal points of high fish abundance and diversity on reefs (Slobodkin and Fishelson, 1974), are visited by a variety of fish hosts which recognize cleaners by their colour patterns (usually conspicuous) and invitational displays. It is possible that invading naive hosts may not recognize new cleaner species, or may prey intensively on native cleaners in non-cleaning situations (Hobson, 197 1 ), thus disrupting this highly coevolved interaction. However, aquarium observations have demonstrated that some naive hosts can quickly adjust their behaviours to accommodate novel cleaners (G. Barlow in Feder, 1966). Fish predators also interfere with cleaning symbiosis by frightening away the cleanees (Potts, 1973). The introduction of novel predators that may eat cleaners, such as sharks, barracuda, jacks, groupers and snappers, could conceivably affect this system. D . Diseased organisms Considering the significant effect of pathogenic organisms on species populations and communities, it is unfortunate that our knowledge of such interactions in the marine environment is so limited. While two serious epidemics in the sea have been well documented-the devastation of eel grass communities on both sides of the Atlantic in the 1930s (Hopkins, 1957), and of commercial sponges in the Gulf of Mexico and Caribbean in the 1930s and 1940s (Storr, 1964)- the ultimate processes responsible for these upheavals have never been satisfactorily explained. Since the mid- 1970s, several reports have appeared on the incidence of diseases in reef organisms (in sponges, Antonius, 1977; in alcyonarian coelenterates, Antonius, 1977; Morse et al., 1977), especially in reef-building corals. These diseases are widespread in the western Atlantic, having been observed in corals in Bermuda (Garrett and Ducklow, 1975), Florida (Antonius, 1976,1977;Dustan, 1977),the Virgin Islands (Gladfelter, personal communication) and Panama (Glynn, personal observations). The pathogens thus far identified are blue-green algae

120

P. W. GLYNN

(Antonius, 1976, 1977) and bacteria (Garrett and Ducklow, 1975). The diseased corals are often, but not invariably, living under disturbed or stressful conditions. In spite of a recent emphasis on reef studies in this region, no diseased organisms have yet been reported from eastern Pacific reefs. If Pacific species have not been exposed to the disease organisms of the Caribbean, and do not possess protective mechanisms against such forms, the spread of pathogens through a sea-level canal could be disastrous to eastern Pacific coral communities.

E. Biotic disturbance Just as there exists a suite of organisms that bind, cement and otherwise stabilize the reef frame and surrounding sediments, reef communities also contain a variety of burrowing and boring organisms whose activities are destructive to various degrees. Some important binding organisms present in the Caribbean, e.g. calcareous green algae, sea grasses, sponges, zoanthids and gorgonians, are absent or rare in the eastern Pacific. This may explain in part the fragility of Pacific pocilloporid reefs and their usual development in sheltered areas, even outside of the hurricane belt. The insertion of some of these stabilizing Caribbean forms (e.g. see Wulff and Buss, 1979 for evidence on the binding capacity of sponges) into eastern Pacific coral reef communities could conceivably enhance their integrity and allow their expansion into a greater range of habitats. Bioerosion is intense in isthmian coral communities with endolithic algae, sponges, polychaetous annelids, sipunculans, cirripeds, molluscs and echinoids contributing substantially. Highsmith ( 1980) has demonstrated a significant relationship between intensity of boring and primary productivity, which was greater in the eastern Pacific than in the Caribbean. Fishes also appear to have a greater effect on Pacific coral communities as compared with those of the Caribbean (Glynn, 1972, 1973; Bakus, 1969). Pacific puffers and parrotfishes feed directly on live corals, a triggerfish causes extensive damage to massive corals (in the process of extracting boring bivalves) and a jack overturns rubble and corals along the edge of reefs (in search of crustaceans). While much coral is killed in this way, these activities also enhance the asexual propagation and lateral extension of reef communities. Toxopnuestes roseus, a sea urchin present only on Pacific reefs, also plays a significant role in moving coral rubble. The die1

CORAL COMMVNITIES

121

movements (nightly surfacing and daily burial) of large populations of this urchin through rubble sediments topples young corals and commonly churns them into the bottom where they die (personal observations). Moreover, coral recruits are rasped from rubble surfaces by these foraging urchins. These activities of Pacific urchins and fishes, in combination with their cropping of potential binding agents (algae, sponges, etc.), could generate a de-stabilizing effect in Caribbean reef communities. These, and other properties related to species interactions on Pacific and Caribbean reefs, are contrasted in Table I.

V. CONCLUSIONS It is evident that present knowledge permitting insight into the kinds of ecologic interactions that might occur, should isthmian coral reef biotas merge, is decidedly fragmentary. It is also clear that the possible levels and variety of effects are enormous. This creates a dilemma as to the kinds, extent and emphasis of research that should be devoted to this problem. From the standpoint of ecological effects, and without consideration for effort and priorities, I believe it is now* time to initiate studies on two general themes regarding the possible mingling of coral reef biotas across the Isthmus of Panama: ( 1) identification and study of potential colonizing species and (2) assessment (in isolation, but simulating natural systems as closely as possible) of the nature and intensity of the interactions of novel species. The first line of inquiry would provide (a)a n inventory of local coral reef biotas and (b)information on the life history tactics of diverse taxa relevant to colonization. Of particular interest are population growth characteristics, including egg and larval production and development (e.g. frequency and intensity of reproduction, seasonal timing, time spent in water column), the settling behaviour of planktonic larvae and morphological plasticity. Information obtained on species interactions, such as feeding ecology (generalist versus specialist diets, switching behaviour, prey palatability, etc.), competition, symbiosis, parasites and disease organisms, inter alia, could be used to help identify potentially undesirable species. The identification of such forms could also serve as a point of focus for further analysis of the *The main problem areas outlined here were already identified and recommended for study in 1970 by the Committee of Ecological Research for the Interoceanic Canal (CERIC),National Academy of Sciences (Newman, 1972).

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P.

w.

(:LYNN

attributes of colonizing species. I would recommend, as has Vermeij (1978), that such studies also include comparisons with migrations that have occurred elsewhere in the world. Finally, every effort should be made to maintain effective biotic barriers across the Panama waterway. This applies to the existing locks canal-in the light of recent freshwater shortages and proposed salinization of Gatun Lake, and the discharge of increasing amounts of seawater ballast (from the Caribbean into the tropical eastern Pacific) in the trans-shipment of Alaskan oil-as well as to a possible sea-level canal. The uncertainties inherent in the outcome of species introductions demand that the utmost precaution be taken to safeguard the integrity of tropical marine ecosystems. Our present meagre understanding of coral reef ecosystems raises many possibilities, but allows no failsafe judgements to be passed, on the relative risks of potential ecological and environmental effects resulting from transisthmian migrations.

VI. ACKNOWLEDGEMENTS I wish t o thank the following for the suggestions they offered to help improve this essay: L. Buss, J . Cubit, C. E. Dawson, J . W. Durham, M. L. Jones, H. Lessios, W. A. Newman, R . M. Overstreet and G. J . Vermeij. I gratefully acknowledge the following for permission t o include in Table I1 their unpublished feeding observations: L. Buss, R. C. Highsmith, J. C. Lang, J. Ogden and D. R. Robertson. New data were obtained from research supported by the Smithsonian Research Foundation. I owe a special debt to R. W. Grigg, and D. R. Stoddart, who provided the initial stimulus to examine the problem of Panamic marine migrations. It is also a pleasure to acknowledge the encouragement and support provided by I. Rubinoff, director. Smithsonian Tropical Research Institute.

VII. REFERENCES Abele, L. G. (1976). Comparative species richness in fluctuating and constant environments: coral-associated decapod crustaceans. Science, Washington, D.C. 192, 461463. Adey, W. H. (1978). Coral reef morphogenesis: a multidimensional model. Science, Washington, D.C. 202, 831-837. Adey, W. H. and Vassar, J. M. (1975). Colonization, succession and growth rates of tropical crustose coralline algae (Rhodophyta, Cryptonemiales). Phycologia 14, 5569.

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Antonius, A. (1976). New observations on coral destruction in reefs. Abstract, Proceedings, Association of Island Marine Laboratories of the Caribbean, 10th Meeting, p. 17. Antonius, A. (1977).Coral mortality in reefs: a problem for science and management. In “Proceedings: Third International Coral Reef Symposium” (D. L. Taylor, ed.), Vol. 11, pp. 617-623. University of Miami, Florida. Aron, W. I. and Smith, S. H. (1971). Ship canals and aquatic ecosystems. Science, Washington, D.C. 174, 13-20. Atlantic-Pacific Interoceanic Canal Study Commission ( 1970). Report of the Atlantic-Pacific interoceanic canal study commission. Interoceanic Canal Studies 1970, 129 pp. + 5 annexes. Bak, R. P. M. and van Eys, G. (1975). Predation of the sea urchin Diadema antillarum Philippi on living coral. Oecologia, Berlin 20, 1 1 1-1 15. Bak, R. P. M., Brouns, J. J. W. M. and Heys, F. M. L., (1977). Regeneration and aspects of spatial competition in the scleractinian corals Agaricia agaricites and Montastrea annularis. In “Proceedings: Third International Coral Reef Symposium” (D. L. Taylor, ed.), Vol. I, pp. 143-148. University of Miami, Florida. Bakus, G. J. (1969). Energetics and feeding in shallow marine waters. International Review of General and Experimental Zoology 4, 275-369. Bakus, G. J. and Green, G. (1974). Toxicity in sponges and holothurians a geographic pattern. Science, Washington, D.C. 185, 951-953. Bardach, J. E., Ryther, J. H. and McLarney, W. 0. (1972). “Aquaculture. The Farming and Husbandry of Freshwater and Marine Organisms”, 868 pp. Wiley-Interscience, New York. Barham, E . G., Gowdy, R . W. and Wolfson, F. H. (1973). Acanthaster (Echinodermata, Asteroidea) in the Gulf of California. Fishery Bulletin, Seattle, Washington 71, 927-942. Benayahu, Y. and Loya, Y. (1977). Seasonal occurrence of benthic-algae communities and grazing regulation by sea urchins a t the coral reefs of Eilat, Red Sea. In “Proceedings: Third International Coral Reef Symposium” (D. L. Taylor, ed.), Vol. I, pp. 383-389. University of Miami, Florida. Ben-Tuvia, A. (1966). Red Sea fishes recently found in the Mediterranean. Copeia 2, 254-275. Ben-Tuvia, A. (1978). Immigration of fishes through the Suez Canal. Fishery Bulletin, Seattle, Washington 76, 249-255. Ben-Yami, M. and Glaser, T. (1974). The invasion of Saurida undosquamis (Richardson) into the Levant Basin-an example of biological effect of interoceanic canals. Fishery Bulletin, Seattle, Washington 72, 35S373. Birkeland, C. (1977). The importance of rate of biomass accumulation in early successional stages of benthic communities to the survival of coral recruits. In “Proceedings: Third International Coral Reef Symposium” (D. L. Taylor, ed.), Vol. I, pp. 15-21. University of Miami, Florida. Bohlke, J. E. and Chaplin, C. C. G. (1968). “Fishes of the Bahamas and Adjacent Tropical Waters”, 77 1 pp. Livingston, Wynnewood, Pennsylvania. Brawley, S. H. and Adey, W. H. (1977). Territorial behavior of threespot damselfish (Eupomacenlrus planijrons) increases reef algal biomass and productivity. Environmental Biology of Fishes, The Hague 2, 45-51. Briggs, J . C. (1969). The sea-level Panama Canal: potential biological catastrophe. Bioscience, Washington, D.C. 19, 4 4 4 7 .

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