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AMER. ZOOL., 34:115-133 (1994) Biodiversity of Coral Reefs: What are We Losing and Why?1 KENNETH P. SEBENS Department of Zoology, University of Maryland, College Park, Maryland 20742 Coral reefs are threatened by numerous anthropogenic impacts, some of which have already had major effects worldwide. These unique tropical environments harbor a high diversity of corals, reef invertebrates, fish and other animals and plants. In most taxa, the species diversity of reef-associated organisms is poorly understood because many of the species have yet to be collected and described. High coral mortality has been associated with natural events such as hurricanes, predator outbreaks and periods of high temperature, but has also resulted from excess nutrients in sewage and from specific pollutants. Reef corals and associated organisms are also threatened by the possibility of global warming which will result in rising sea levels and periods of increased temperature stress, and which may also bring increased storm frequency and intensity. Although the recent extensive episodes of coral bleaching in the Caribbean and eastern Pacific cannot be causally related to global warming at this time, the close link between bleaching and temperature suggests that global warming will result in severe changes in coral assemblages. Major reef destruction has followed outbreaks of the predatory seastar Acanthaster planci in the Pacific. Although this is considered part of a natural disturbance cycle, there are indications that altered land use patterns and reduction of predators on this seastar by human activities may have increased the severity of outbreaks. Recreational and commercial use of reefs has also increased, and has caused extensive damage, especially near areas of high population density. One of the most obvious and widespread losses to reef biota is the reduction in fish populations from intense overfishing in most reef areas of the world. Coasts without adequately managed reefs have suffered intense overfishing for both local and export purposes, to the point where the positive effects offishon those reefs have been compromised. The combination of these destructive factors has altered reefs in all localities, and many that were once considered protected by distance and low population density are now being exploited as well. On the positive side, improved understanding of ecological processes on reefs combined with concerted conservation efforts have managed to protect some extensive areas of reef for the future. SYNOPSIS. INTRODUCTION the past few decades. Coral reefs are frequently described as the marine equivalent Coral reefs of the world: Distribution and diversity of tropical rain forests, given their high spej i L- i • * L * J cies diversity and the similarity of certain !-,•„ y Ecolog,stsand coral biologists have noted s t n l c l u r i rocesses ( C o n n e | | ^ , 7 8 J a c k . son.99, Thepara.Se,sdono,end,here, co r a , reefs £ most parts Jf the wortd over i n s Z L & ^ u ^ ^ & W beleaguered terrestrial ecosystems as humans seek to exploit their numerous ^sources. Coral itself is used as a building the American Society of Zoologists, 27-30 December 1992, at Vancouver, Canada. material, reefs are destroyed by coastal development, and reef fish are being severely 115 116 KENNETH P. SEBENS depleted in all parts of the world (Hutchings, 1986; Russ, 1991; Wilkinson, 1993). In some regions, fish and invertebrates, including the coral framework, are harvested extensively for the pet and curio trades. Meanwhile, researchers are just beginning to understand the real diversity of reefs, the processes that maintain and destroy them, and the basic biology of corals themselves. Coral reefs are distributed throughout the world tropics, although a few coral species reach the Arctic, the Antarctic and the deep sea. Reef growth, the deposition and accretion of calcium carbonate skeletal material, is limited to regions which average at least 20°C year round. The diversity of corals (Fig. 1) and reef associated species declines north and south of the equator, with high latitude reefs dominated by the few hearty coral species able to survive periodic winter chills (Stehli and Wells, 1971;Veron, 1986). In the Caribbean, about 80 species of reefbuilding corals are found in the southern portion, about two thirds of those are still common in the Florida Keys, and only 21 occur in Bermuda. In the Indo-Pacific, the equatorial regions with large land masses and extensive island groups support over 390 species, whereas southern Japan has from 363 to 25 species moving northward from 27 to 35° latitude (Veron, 19926), and southern Australia has only 72 percent of the northern Great Barrier Reef coral species, near the southern limit of reefs on the eastern coast (Veron, 1986). The diversity of other reef invertebrates and reef fish (Fig. 2) mirrors this pattern in most parts of the world. Another major diversity gradient occurs moving away from high diversity centers in the Pacific, one in the Red Sea and the other in the Philippines, New Guinea and the surrounding region. Eastward from New Guinea, for example, the number of coral genera drops from over 70, to 30 in Tahiti and French Polynesia, to a low of 15 in the separated islands of the eastern Pacific such as the Galapagos and the coast of Central America (Veron, 1992a). Reef fish display the same pattern with a high of close to 900 species in the western Pacific, to about half that in the eastern Pacific, and a third that number in the Atlantic (Thresher, 1991). This diversity gradient, also present for other reef fauna, is the result of several factors, including the large dispersal distances limiting species colonization of islands, the small land masses and high local extinction probabilities, and the geological history of the region, including the effects of numerous large fluctuations in sea level over the past 150,000 years or more (Rosen, 1981). Corals have been collected throughout the world and new species have been described FIG. 1. Worldwide distribution of hermatypic coral genera. Lines connect regions with equal numbers of genera; there is a maximum of over 70 genera (>390 species) in northern Australia, New Guinea, the Philippines and bordering regions. Other areas of high diversity (>50 genera) occur in the Red Sea and in the Indian Ocean. CORAL REEF BIODIVERSITY 117 for over two hundred years. Only in the last species (described and undescribed species) two decades, however, have there been pro- that showed almost no sign of decreasing ductive attempts to examine the validity of even after totals of over 500 species in five all such descriptions, and to find out how years of intensive collecting (Gosliner, many such species are "real." The number 1993). The interstices of coral reefs provide of described species of scleractinian corals abundant and varied habitats for cryptic now accepted as good species has thus species; the number of undescribed polydeclined recently as researchers have rec- chaete worms, small crustaceans, bryozoognized that so-called different species ans, hydroids and other small invertebrate described from separate island groups are species cannot even be estimated with any in fact the same (Veron, 1986). In the Carib- degree of confidence. Shelled mollusks are, bean, polymorphic species have recently of course, well collected and described in been recognized as species complexes (e.g., most parts of the world and populations Montastrea annularis, Knowlton et al, have been decimated to provide shells for 1992) thereby increasing the number of spe- sale. Their diversity often depends on the cies known for that region. Rapid advances habitats created by corals and other reef in molecular systematics will undoubtedly dwellers (Kohn and Leviten, 1976). Fish alter the present species lists further. Related have received even more attention than have anthozoan groups such as the octocorals, sea corals, however, and species rearrangeanemones and zoanthids have never ments are more common than the discovery received the attention directed at sclerac- of many new species, yet patient underwater tinian corals even though they are common observation and collecting continues to turn reef inhabitants. New species and genera are up new species regularly. The taxonomic still being discovered at a rate limited only status of coral reef fauna and flora is thus by the time available for the few experts on extremely similar to that of diverse and each group to collect, quantify characters, remote terrestrial habitats, including tropical rain forests, where new birds and mamand publish. mals continue to be recognized, and hunOther invertebrate groups are incom- dreds to thousands of species of insects, pletely described to a similar extent. A recent plants and simpler life forms await discovestimate from New Guinea produced an ery and description. annual accumulation rate of nudibranch The eastern Pacific is extremely depauperate and the Caribbean, with less than 80 species, reaches only one fourth the generic diversity of the western Pacific (from Veron, 1992b). 118 KENNETH P. SEBENS I I 1000 800 o> 'o a. 600 - <D 400 - in 200 - ov 8 5 40 - 1 5 4 7 1 1 15 1 2 10 9 13 14 16 2 18 17 30 - 19 2 20 1 3 20 10 n Indian Pacific Atlantic FIG. 2. Coral reef fish diversity (species and families) in all coral reef locations of the world. Note the high diversity in the western Pacific (as in Fig. 1 for corals) and the low number of species in the Atlantic and eastern Pacific. The number of families represented shows less of a spread, suggesting that most "guilds" are represented in each reef area, but with fewer species each (redrawn from Thresher, 1991). 119 CORAL REEF BIODIVERSITY Coral Body Wall Environment Dissolved Organics, Amino Acids Demersal Plankton, Particulates, Bacteria 2 .3? 0) Zooxanthellae Ammonia, Host waste Demersal Plankton Corals, Other Invertebrates Zoox. Amino Acids, etc. Zoox. • Host FIG. 3. Interactions between corals, their symbiotic algae (zooxanthellae) and the environment. A section of coral body (or tentacle) wall is represented, with three tissue layers. The gastrodermal layer contains the algae and cells that take in and digest dissolved and paniculate food substances from the internal cavity (coelenteron). The epidermis contains mucus gland cells and nematocysts (stinging cells). Inorganic nutrients reach the algae by diffusion through the epidermis and mesoglea (collagenous structural layer). Organic compounds are absorbed by active uptake, and particulates (including zooplankton) are captured by nematocysts and mucus and are then ingested. Bacteria growing on the coral surface are sloughed off in mucus layers which are either ingested or become food for other reef fauna. These bacteria and other microorganisms also use dissolved nutrients otherwise available to the coral. Symbiotic algae recycle host nitrogen by using waste ammonia to form amino acids and other compounds which are translocated to the host cell. with algal symbionts (hermatypic) accrete carbonate much faster than do those withReef corals (Phylum Cnidaria: Class out the algae (ahermatypic) because algal Anthozoa) build calcium carbonate skeletons (and are termed "scleractinian" corals), photosynthesis creates a chemical environand most derive at least some of their nutri- ment conducive to precipitation and crystion from photosynthesis by symbiotic algae tallization. Corals without symbionts must (dinoflagellates, termed "zooxanthellae") in expend energy to lay down skeleton, and do their gastrodermal cell layer (Fig. 3). Corals so very slowly; they therefore do not conCORAL REEF ECOLOGY 120 KENNETH P. SEBENS pounds (energy sources) for daily metabolism, growth and reproduction; they also recycle host wastes efficiently. Wastes contain elements (nitrogen, phosphorus, etc.) needed as building blocks (amino acid, proteins) for algal and coral tissue growth (reviewed by Sebens, 1987). Even with maximum photosynthetic activity, however, corals must capture zooplankton or other paniculate matter to gain enough nitrogen and phosphorus to build new tissue. In deeper reef zones, photosynthesis cannot supply all necessary energy and zooplankton or other paniculate matter must be consumed to provide both energy and limiting nutrients. Tropical oceanic environments are generally very low in dissolved nutrients (oligotrophic), although coastal environments can be much richer (D'Elia et al, 1981; Lapointe and Clark, F = feeding/scraping mortality 1992; LaPointe et al, 1993). Limiting nutriG = growth rate enhancement ents can also be gained by active uptake, through the coral's body wall (Fig. 3), of FIG. 4. Relationships between corals, macroalgae, nutrients, and consumers. Corals prevent macroalgal compounds dissolved in sea water (e.g., propagules from finding attachment sites, and may have nitrate, nitrite, ammonia, amino acids) allelopathic effects on algae, whereas algae shade and although the amount available is highly abrade corals by overgrowth of coral edges. Increasing dissolved nutrients (e.g., N, P from sewage) increases variable. Addition of nutrients to coastal algal growth ( + + ) and has a slower positive effect on waters might thus seem advantageous to coral growth (+), thus favoring algae. Herbivores corals, and could stimulate growth. How(including omnivorous urchins and fish) remove algae ever, such enrichment (eutrophication) rapidly ( ) and favor coral growth, except within affects benthic algae as well, and they grow damselfish territories where corals can be either faster, damaging corals by shading and destroyed, protected, or allowed to be overgrown by abrasion and limiting coral recruitment by algae. Corals can be removed by omnivores, especially by urchins (-), but corals also provide structural refreducing larval contact with the rock suruges for herbivorous fish. Human exploitation of fish face. results in high urchin densities which reduce both corals and alga. After urchin die-offs (epidemics), algae are strongly favored by low herbivory and high nutrient conditions. If pollutants include pesticides, hydrocarbons, metals or other toxicants, they can have a direct negative effect on corals also. tribute much to reef growth. Ahermatypic corals are usually limited to dark environments on reefs, to deep water, and to high latitudes where temperatures are low. In addition to the scleractinian corals, reef surfaces can be dominated by octocorals, gorgonians and soft corals which usually grow as upright "trees" and maintain flexibility by limiting their skeleton to networks of fused and unfused spicules. Symbiotic algae provide shallow water corals with more than enough carbon com- The diversity of reef corals and associated fauna varies along depth and habitat gradients. In general, the richest zones for coral diversity are at or just below the zone of strongest wave action and highest urchin densities (reviewed by Hughes, 1989; Huston, 1985; Jackson, 1991). In very shallow forereef and lagoonal environments, single species often dominate large areas (e.g., Caribbean and Eastern Pacific). The same is true of deep reef slopes, especially in the Caribbean where plating species (Agaricia spp.) dominate. The combination of high growth rates and disturbance from storms acts to enhance diversity in the zones affected by wave action. This includes wave-exposed reef flat communities of the Great Barrier Reef and central Indo-Pacific which often CORAL REEF BIODIVERSITY display high diversity. Below this zone, the cover and diversity of other invertebrates, such as sponges and ascidians, often increase. In the surf zone, coralline algae rather than corals, can occupy most of the substratum. Disturbance is best defined as any process that clears primary substratum, including the effects of storms, predators, or disease. Coral predators include the Crown-ofThorns seastars {Acanthaster planci, discussed later) which clear large reef areas, fireworms, certain snails, and a variety of corallivorous fish. Such disturbance is as important to coral reefs as it is to any other community, because it opens up space and resets a patch of substratum to an earlier successional stage, allowing the cycle of recovery to begin again. Without significant disturbance, each depth zone of a reef could theoretically become dominated by a single coral species able to outcompete all others. Corals compete by numerous mechanisms, including direct overgrowth and use of sophisticated agonistic structures such as modified tentacles and digestive organs (mesenterial filaments) to kill the tissue of neighboring corals and other cnidarian species (Lang and Chornesky, review, 1988). Any reef, at a given time, comprises a set of "patches" of substratum at different stages of recovery from small to large disturbances. The term "equilibrium" is frequently used to denote the climax or undisturbed community state. The actual "equilibrium" community, however, is a landscape of all successional stages, for a given pattern and rate of disturbance over time (Paine and Levin, 1981), rather than an undisturbed "climax" with almost complete space cover by competitively dominant species. In fact, disturbance at some optimum intermediate level allows the greatest number of species to coexist (Connell, 1978). If there is too little disturbance, a few species take over all the space and if there is too much disturbance, most species cannot recruit and grow fast enough to persist, so the community is dominated by a few "weedy" or opportunistic species with high rates of reproduction and recruitment, but often with poor competitive ability. 121 encrusting invertebrates. Patches can remain algal-dominated indefinitely when they are within territories defended by damselfish, which actively remove other grazers and sometimes damage and kill coral (Lobel, 1980). The interactions between damselfish, schooling herbivorous fish and other grazers, such as sea urchins, are complex (Fig. 4). When fish populations are reduced, urchin populations expand with negative effects on coral cover because urchins remove coral as well as algae (Hay and Taylor, 1985). Corals usually take longer to recruit and to cover large areas, with a few appearing rapidly and regularly because of high larval production and high recruitment rates. Corals reproduce by asexual fragmentation, by brooding planula larvae, and by releasing egg and sperm, often in bundles that burst as they rise to the surface, where fertilization and development to a planula stage occur. When many species spawn over a few nights of the year, spectacular "mass spawnings" result (Babcock et al., 1986) and waves of larvae can be observed from the air, moving from one reef to another as a "surface slick." Whether or not a reef with recently cleared areas is in the path of such a larval mass could determine the number and species of new coral colonists in a given year. Anything (higher or lower temperature, altered currents, poor water quality) that interferes with the regulation and timing of spawning could potentially produce a total failure of recruitment that year, or a significant reduction in the number of recruits of particular species. Sufficient water movement affects the movement of larvae, and is also critical to coral growth because rapid flow or strong wave action removes sediments from coral surfaces, delivers prey organisms to coral tentacles, and reduces the thickness of the "boundary layer" over coral tissue surfaces thus allowing rapid diffusion of oxygen, carbon dioxide and dissolved nutrients (Patterson et al., 1991; Sebens and Johnson, 1991). Corals in lagoons, backreef environments and deep reef zones may be severely limited by the low flows characteristic of Following a disturbance, open space can those habitats (Sebens and Done, 1993), thus be colonized rapidly by algae and by some limiting the number of species that can per- 122 KENNETH P. SEBENS linked the large scale bleaching phenomena observed in the field to temperature as a primary mechanism, and to increased ultraviolet light (during periods of calm clear water) as a potential secondary factor (Glynn et ai, 1993). As temperature increases, the photosynthetic activity of symbiotic algae increases as well resulting in high concentrations of oxygen inside host cells. This has two negative effects, an increase in host metCORAL BLEACHING AND GLOBAL WARMING abolic rate because cnidarians are metabolic In 1983 massive fields of Pocillopora conformers (reviewed in Sebens, 1987) and damicornis and other less abundant species an increase in toxic forms of oxygen (superalong the Pacific Coast of Panama turned oxide radicals, peroxides) that can damage white and later died (Glynn, 1988, 1991; host cell nucleic acids and interfere with Glynn and D'Croz, 1990). This was coupled biochemical pathways (Lesser et ai, 1990). with an extreme ENSO (El Nino Southern Following even a strong bleaching response, Oscillation) event which raised tempera- the host contains a residual population of tures over a broad geographic region of the algae that serve as a source population durEastern Pacific. In 1987, a similar bleaching ing the recovery period, which can take at event was observed throughout the Carib- least a year (Goreau and MacFarlane, 1990; bean (Williams and Bunkley-Williams, Fitt et ai, 1993; Savina, 1993). If the initial 1990; Lang et ai, 1992, reviews), involving shock is severe enough, the entire coral or numerous species (Fig. 6), although it is not parts thereof can die, as occurred extenknown how much mortality ensued. This sively in Eastern Pacific reefs in 1983 (Glynn, was followed by a second similar event in 1988). Coral death was also observed in 1989 and another in 1990. Although sig- mapped colonies of Agaricia on Jamaican nificant coral reef research has been con- reefs, especially when the same coral colony ducted in the Caribbean since the 1950s, suffered repeated bleachings (Savina, 1991). and the bleaching phenomenon can be seen Although significantly higher sea surface from a small boat on a calm day, only geo- temperatures have not been demonstrated graphically isolated bleachings had been during the three periods of bleaching for the reported previously. In the few places where Caribbean as a whole (Atwood et ai, 1992), quantitative observations were carried out the bleachings occurred at the warmest time with good temperature measurements, it was of year and in years when temperatures clear that the Caribbean bleaching events above 30°C lasted longer than usual. Temcoincided with temperatures (30-31°C) peratures measured in Jamaica were well about two degrees above the normal annual maxima (28-29°C). The extensive bleach- above 30°C during the three bleaching events ings, repeated over such a short period, (Gates, 1990; Savina, 1993), and bleaching raised concern that global warming would was particularly common in deep reef (> 30 m) corals {Agaricia lamarcki and Monsoon lead to widespread reef destruction. tastrea annularis) where temperatures were Bleaching occurs when symbiotic algae high but ultraviolet penetration would have (zooxanthellae) are lost from the gastroder- been comparatively low. This does not rule mal tissues of a host organism (corals, out the possibility that increased ultraviolet, anemones, zoanthids, octocorals, etc.), even at low levels, could enhance bleaching sometimes accompanied by loss of host gas- of corals not normally exposed to much trodermal cells (Muscatine et ai, 1993). This ultraviolet light. In a recent series of detailed phenomenon can occur as a response to high experiments, Glynn et ai (1993) tested the temperature, low temperature, high ultra- effects of ultraviolet radiation and temperviolet light, and several other stimuli (Glynn ature on two Pacific coral species, finding et ai, 1993; Hoegh-Guldberg et ai, 1987; that temperature alone (30 and 31°C) had Lesser et ai, 1990). Recent studies have significant bleaching effects and that added sist under such conditions. Habitat alterations that increase sedimentation, or reduce flow (breakwaters, coastal modification, eutrophication) can thus have negative effects on coral growth and diversity. At the other extreme, violent water motion during storms can totally change the composition of coral assemblages, with effects lasting many decades (Woodley et ai, 1981). CORAL REEF BIODIVERSITY ultraviolet increased the effect, but that ultraviolet alone did not cause the corals to bleach. Partially bleached corals generally recovered in these experiments whereas many of the fully bleached colonies died. Are the mass bleaching events a "signal" that global warming has progressed to the point where certain species face local extinction (Glynn and de Weerdt, 1991) and major marine habitats are being degraded? It is impossible to answer this question at present. The increase in carbon dioxide in the atmosphere is well documented (Dickinson and Cicerone, 1986; Gates et ai, 1992), yet the predicted increase in mean air temperature has been harder to confirm, even though a clear signal exists for some localities. This measurement is confounded by the heating effect of spreading urban areas, where many sensors are located, and by the unreliability of old data sets. For sea surface temperature, it is even more difficult to demonstrate a trend, and there is no evidence at present for an increasing mean temperature in the Caribbean over the past decades or century. Despite the lack of firm data, the mechanistic model (Greenhouse Model) predicts that increasing carbon dioxide (already substantial) will eventually cause higher temperatures. The idea that bleaching episodes could act as a "signal" of global warming was tested recently by a model where the increase in temperature over a period of decades and the ability to detect the "signal" (bleaching) were varied (Ware, 1992). If, indeed, we have not missed detecting any mass bleachings over the past half century, and have picked up three clear events in the late 1980s and 1990, such a signal could theoretically be a significant indicator of a period of slowly increasing mean temperature and thus higher annual maxima. This model predicts that, if warming is real, such a signal will be highly significant in approximately another two decades. What will happen to reefs if sea surface temperatures actually do increase, as predicted by the Greenhouse Model? Corals have faced periods of rapid temperature change many times over geological history, and some species are likely to adapt whereas others will become more restricted in geo- 123 FIG. 5. An example of a structurally diverse Acropora cervicornis stand typical of Caribbean reefs at mid depths (above). This zone of reefs along the north coast of Jamaica was destroyed by hurricanes followed by the sea urchin die-off, leaving a pavement of A. cervicornis fragments (below) with heavy algal growth. graphic range. From recent events, it is clear that susceptibility to bleaching differs among species, with some of the common species showing no response at all so far. Some of the most common species on Caribbean reefs, Montastrea annularis, Agaricia lamarcki, Porites porites, as examples, have been severely affected. Other common species, such as Acropora cervicornis and A. palmata, have suffered high local mortality from the "band" diseases over the past decade at many sites in the Caribbean 124 KENNETH P. SEBENS FIG. 6. Examples of severely bleached corals, Montastrea annularis (above) and Agaricia lainarcki (below) in Jamaica (1988). Most colonies of the former species survived whereas a large number of the latter species died, especially after suffering two or three bleachings. CORAL REEF BIODIVERSITY 125 FIG. 7. A fish trap in Jamaica. Note the small mesh size and the size of fish trapped. (Edmunds, 1991), although this is not clearly linked to temperature as far as is known. Continued loss of these important structural and reef-accreting species will certainly change the character of Caribbean reefs. Already, Jamaica and similar localities provide a model of what the future may hold. The combined effects of two hurricanes (Fig. 5), massive algal overgrowth, heavy overfishing, and three bleaching events have produced reefs of severely depleted coral cover, high algal abundance and reduced structural heterogeneity (Hughes, 1989; Liddell and Ohlhorst, 1993). Even stormrelated damage could become worse with global warming, since the severity and frequency of hurricanes and other tropical storms are expected to increase. The bleaching events since 1987 appear to have been worse on Caribbean reefs than in other parts of the world. This might be explained by the small geographic area of the Caribbean. Also, the Caribbean is well north of the equator and corals are probably adapted to generally lower temperatures including temporary periods of much colder water along the northern limits of coral distribution. The small area and close connections between islands in the Caribbean may also make disease effects more severe as well, as in the case of the urchin (Diadema) dieoff which spread from the southern Caribbean throughout the region in less than a year (Lessios, 1988). The Pacific is so large, and some island groups so small, that it may be hard for a substantial patch of water to warm up sufficiently to cause bleaching. However, just such an event happened in Tahiti and Moorea in 1991. This bleaching corresponded to a period of low winds, very still water and high sea temperatures. Tahiti is located at a site where water movement generated by tides is minimal; without wind forcing, water can sit and warm up substantially. The high temperatures caused by ENSO events, by contrast, are restricted to 126 KENNETH P. SEBENS the eastern Pacific, but affect areas far to the north and south of the equator. Bleaching events along the Australian coast, on the other hand, have been linked to localized low temperature events. Extensive events comparable in geographic extent to those in the Caribbean have not been observed in the Indo-Pacific region to date. CROWN OF THORNS AND CROWDS OF TOURISTS was as follows: High rainfall during storms causes massive runoff from high islands and decreases local salinity in surrounding lagoonal and backreef areas. The low salinity triggers spawning by Acanthaster already present at low population density, and the runoff carries nutrients which enhance local phytoplankton growth, providing better food and growth conditions for Acanthaster larvae. The juvenile starfish that result remain hidden within reef cavities for about three years, at which time they are large enough to avoid most predators and emerge onto open reef surfaces. They then become visible to casual observers and begin to consume massive amounts of coral tissue. Low islands and atolls lack the land surface to produce substantial runoff (and nutrients), are less likely to experience significant local salinity reductions, and therefore never experience the outbreaks. The critical anthropogenic factor is forest clearing on high islands, and fertilizer addition to fields, making runoff worse and the nutrient input higher. This could increase the probability of a large outbreak of Acanthaster. Other human activities may also affect the severity of outbreaks, including removal of natural predators such as "Triton shell" gastropods and certain fish (reviewed in Birkeland and Lucas, 1990). This theory seems to apply well to the scattered islands of the Pacific, but not to the Great Barrier Reef of Australia where outbreaks are common and where they move in waves from north to south as larvae produced on one reef are advected southward to continue the march (Moran et ai, 1988). Recent research on Acanthaster larvae indicates that abnormally high phytoplankton concentrations are not necessary for their survival (Olson, 1987), but does not change the overall pattern of outbreaks identified by Birkeland. There may be some other aspect of low salinity or high runoff that causes high recruitment, such as spawning synchrony and enhanced probability of fertilization, or modified coastal circulation patterns that retain larvae. Should fires be allowed to burn in national parks, or should they be controlled to preserve "climax" (incorrectly termed "equilibrium") communities? This has been a hotly debated question for managers of terrestrial forest communities. The best marine example of the same debate comes from the spread of Crown of Thorns seastars (starfish) (Acanthaster planci) on coral reefs of the Indo-Pacific. In the 1960s, researchers in Australia observed massive outbreaks of this predatory echinoderm, and noted almost complete denudation of live coral in reef areas where outbreaks occurred (reviewed in Birkeland and Lucas, 1990). The immediate fears were that major areas of living coral reef would be destroyed, taking centuries to recover, and that this was an unprecedented event somehow connected to human activity. The first fear has been confirmed numerous times as outbreaks have been studied throughout the Pacific, although the spatial extent of outbreaks has been limited and the recovery from major damage can be more rapid than originally predicted (Colgan, 1987). Evidence that Acanthaster outbreaks are caused by human activity is circumstantial at present, although there is plenty of evidence that outbreaks of this species have occurred episodically for hundreds of years in areas where human perturbations have been minimal (reviewed in Birkeland and Lucas, 1990). The most persuasive explanation for outbreaks comes from Birkeland (1982) who noted an amazing pattern of outbreaks occurring only around high islands in Micronesia, never on atolls. A second correlation placed outbreaks three years after When the first major Crown-of-Thorns major tropical storms (typhoons), and was outbreaks occurred, recovery was predicted even used to predict the next one correctly. to take many decades, probably more than Birkeland's explanation for these patterns a century. Grigg and Maragos (1974) exam- CORAL REEF BIODIVERSITY ined lava flows of known age around the island of Hawaii and determined that it would take that long to develop a fully diverse coral community following complete denudation. However, even very severe Acanthaster outbreaks leave some corals in their wake, especially in the shallow "surf zone" where the sea stars have difficulty feeding. Colgan (1987), working on reefs on the island of Guam, found substantial recovery of denuded reefs only 15 years after a major outbreak. We know that many reef corals are hundreds of years old and form massive colonies, yet it appears that coral reefs can develop high cover and normal diversity in a few decades. Is this a paradox? Probably not, just an illustration of the successional processes that occur on reefs. Colonization occurs first by rapidly growing "opportunistic" species that cover reef rock quickly and produce what looks like a very healthy reef. Slower growing species are generally also slow to recruit and do, in fact, take centuries to reach their full size and to replace some of the earlier colonists. A goodlooking diverse reef can thus develop in a few decades, but it is not equivalent to the pre-disturbance "climax" condition because it lacks the larger colonies of long-lived species. Should reefs be managed by removing Acanthaster? First, it is a difficult and very expensive task to remove enough of the seastars to actually prevent major coral damage. Over a large geographic area, some reefs will be severely damaged, others will be recovering, and yet others will be undamaged for many decades and will have essentially intact coral assemblages. This pattern has characterized Australia's Great Barrier Reef even though several waves of Acanthaster outbreaks have gone through the reefs in the past three decades. However, when there is a particular reef that is of great interest to a local tourist industry, intervention may be worthwhile. For example, if there is an island close to a major tourist area and it has excellent reefs, it may be worth the effort of preventing extreme damage during an outbreak. This is partly an economic decision, but it has major conservation consequences. If enough people get excited by seeing one well-preserved and heavily vis- 127 ited reef, these same people are likely to be proponents of reef conservation in the future. POPULATION AND POLLUTION Coral reefs located near areas of high population density have suffered worse than those in isolated regions with small populations, based on observations and historical information, although the data on which to base this claim are generally unavailable or have not been collected using comparable methods (Wilkinson, 1993). Nonetheless, heavy fishing pressure, harvesting of coral and mollusks, and the effects of coastal pollution are all much higher near population centers. The pollutants that affect reefs include oil spills (Loya and Rinkevich, 1980), heavy metal concentrations from industrial and mining sources, pesticides and herbicides, high sediment loads, and increased nutrient loading from sewage and agricultural sources (Lapointe and Clark, 1992; LaPointe et al, 1993). Although there are case studies of negative effects on corals and reefs for all such pollutants, the most widespread effects probably come from the last category, as demonstrated for sewage input into Kaneohe Bay in Hawaii (Banner, 1974; Smith et al., 1981), Barbados (Tomascik and Sander, 1985) and Australia (Bell, 1992). Increased nutrients (inorganic and organic nitrogen and phosphorus compounds) may initially benefit corals, for which they can be limiting to growth, but these nutrients benefit macroalgae as well and the latter have much higher tissue growth rates. The result is algal overgrowth and damage to existing corals and a reduction of surface area available for coral recruitment (Fig. 4). Recent studies along the Florida Keys reef tract have demonstrated levels of certain nutrients, chlorophyll, and turbidity in the water column approximately three times the usual values for reefs in less impacted areas throughout the region (Lapointe and Clark, 1992; LaPointe et al., 1993). During the same period, coral cover has decreased in some localities (Dustan and Halas, 1987; Porter and Meier, 1992), although coral declines may also be linked to particular disease events and high levels of human activity on certain reefs. Eutrophication in 128 KENNETH P. SEBENS the Florida Keys begins with sewage leaching into groundwater and moving laterally through porous carbonate rock into the many channels cut through the Keys. When there is a large amount of freshwater input after heavy rains, the water entering canals can be severely hypoxic (<1 ppm O2), and carries high nutrient loads. The reefs in the Florida Keys are several kilometers offshore, so pulses of high nutrient water must move through mangroves and seagrass beds first, taking several days to reach the reefs. The mangroves and grasses act as a filter removing some nutrients, passing others through, and releasing and transforming still others (LaPointe and Clark, 1992). The net result is an enriched phytoplankton standing crop and organic detritus in the water column cutting down light penetration and increasing the sediment load on corals and other sessile organisms. To these effects are added enhancement of algal growth and biomass, with resultant negative effects on sessile invertebrates through overgrowth, abrasion, and shading. High algal growth rates can support high urchin population densities and, since urchins are omnivores, increased rates of urchin predation and incidental damage to corals and other invertebrates. FISHING THE FINAL FRONTIER Diverse "unaltered" fish assemblages have positive effects on corals and on reefs. Herbivorous fish remove benthic macroalgae which compete for space with corals and other invertebrates (Hay, 1984; Hay and Taylor, 1985; Neudecker, 1977), and large schools of herbivores periodically destroy damselfish "gardens" (Robertson et al, 1976) in which algal biomass is high and coral survival is usually poor. Schooling fish which take shelter in coral heads can increase the growth rate of those corals by supplying nitrogenous waste products (Meyer et al, 1983), which can be limiting to the growth of algae and corals in oligotrophic tropical seas. Large predatory fish also control populations of benthic invertebrates, and of smaller reef fish, thus potentially enhancing diversity of both groups by limiting competitive dominants. The physical structure of coral reefs can enhance fish diversity by providing physical refuges from predators, microhabitat differences, and numerous sites for recruitment. Although the expected relationship is an increase of fish diversity with structural complexity, not all studies of natural reefs have demonstrated a strong correlation (Sale, 1991). At scales of tens to hundreds of meters, reef fish are segregated more or less predictably by habitat and over depth zones (Goldman and Talbot, 1976). At smaller scales, however, there is some evidence that only certain fish guilds subdivide the reef by physically or biologically different microhabitats (e.g., anemones as habitat for anemonefish, branching corals versus mounding forms). Experimental work has demonstrated a "lottery" effect for other guilds; when a resident damselfish is removed, for example, the fish that replaces it is not necessarily of the same species, nor is the replacement predictable (Sale, 1977). Live coral cover appears to be important for high fish diversity (Bell and Galzin, 1984). Simplification of reef structure through direct damage, increased bioerosion, and reduced coral growth all lead to a lack of branching structures, filling of holes, and a general increase in habitat similarity. These modifications reduce the number of fish that can find refuge, the number of distinct habitat types, and probably the suitability of settlement sites for the larvae of particular species. Experiments with artificial reefs have amply demonstrated the importance of physical habitat architecture (variety of shelter sizes) in attracting fish and maintaining diverse assemblages, although factors such as reef size and location may be even more critical (Bohnsack, 1991). Two forms of intensive fishing threaten coral reefs, their fish populations, and the species controlled by interactions with fish. The first is subsistence fishing in areas of relatively high human population density. This includes the provision of fish for fishermen's own families, for sale to other locals, and for sale to hotels and restaurants catering to tourists. A prime example is the intensive trap fishing (Fig. 7) and spear fishing as practiced in Haiti (Ferry and Kohler, 1987) and Jamaica (Koslow et al, 1988), CORAL REEF BIODIVERSITY which is carried out almost completely in reef habitats, and results in the harvesting of all fish and mobile invertebrates that cannot escape through chicken-wire a few centimeters in mesh size. On reefs along the north coast of Jamaica, it is quite common never to see a fish over about 30 cm length in an hour of diving (also in Haiti: Ferry and Kohler, 1987). Every community along the coast of Jamaica practices this type of fishing, with obvious results to the reef fish populations (Munro et ah, 1987), and less obvious effects on the reefs themselves. Overfishing has definite effects on the rest of the reef community. The epidemic destruction of Caribbean sea urchin (Diadema antillarum) populations in 1983 (Lessios, 1988), combined with the low numbers of herbivorous fishes remaining on Jamaican reefs, led to a particularly severe growth of benthic algae (Hughes et ai, 1987). This threatens the survival and recruitment of corals and has slowed the recovery of these reefs from hurricane damage in 1980 and 1988(LiddellandOhlhorst, 1993). Recently, protected zones in which fishing is not allowed have been established in areas, such as Montego Bay, which benefit from diving tourism. However, such areas have been in existence only a few years and the overall effects are not yet known. In the Florida Keys, protection of reef fish from spear fishing had rapid positive effects on fish populations (Bohnsack, 1982). The nearest island group to the west of Jamaica is the Cayman Islands, just over 100 km away. This group of small islands has a low population density, and has had protected reefs for at least a decade. Fishing has not had the decimating effect on these reefs that is so evident in Jamaica, and the Cayman Islands are one of the prime destinations for diving tourism in the Caribbean. In 1988, I had the chance to take a university class to Jamaica and to the Cayman Islands where we sampled coral and fish populations. The contrast was remarkable. On every dive in the Cayman Islands, we observed numerous large grouper, snapper, and other fish rarely seen on our dives in Jamaica. We observed that coral cover was much higher and algal cover much lower here than in Jamaica. This may be due partly 129 to the lesser effect of both recent hurricanes on the Cayman Islands, but is probably also an effect of the more "normal" fish assemblages. The same pattern was seen when coastal fish populations were compared to those on the Pedro Bank southwest of Jamaica (Koslow et ai, 1988). The second type of fishery affects even the most remote and underpopulated reefs of the central Pacific and the rest of the world. This is export fishing of both reef and offshore species for shipment to developed countries, often by airplane, soon after they are caught. This type of fishery has become popular in areas where, even recently, there was no threat of local overfishing for subsistence, and where the ratio of people to reef area was so low as to prevent significant negative impact onfishpopulations. With the strong economic incentives supplied by developed countries, every source of harvestable fish and shellfish is being explored and in many cases is already overexploited (Russ, 1991; Russ and Alcala, 1989). Where once there was some hope that distance and low human population density would protect certain reefs, now even those areas are at great risk. Management of coastal fisheries is certainly the only viable way to prevent decimation of a local fish fauna and ensuing changes to the reef communities. Such management can take the form of limits on trap sizes, numbers and mesh size, limits to catch, and limits to areas fished. One intriguing proposal (Randall, 1982) holds that refuge areas, where all fishing is prevented, can provide a number of immediate benefits. First, such areas will be of great interest to diving and snorkeling tourists, who admire the beautiful coral and invertebrates but who spend much of their time fish-watching and photographing fish. The tourist industry also provides jobs for guides and boat operators, who might alternatively add to the local fishing pressure. Second, such refugia provide a source offish that can grow large then migrate out into adjacent fished areas. Ferry and Kohler (1987) stress that providing improved fishing methods and gear for offshore fishing may reduce fishing pressure on reefs because the fish available offshore are larger and of greater value. However, this 130 KENNETH P. SEBENS approach could also result in the formation of two groups of fishermen, each exploiting its target habitat to the maximum. A major limitation to reef fish populations is recruitment from distant locations, which can be highly variable in space and time (Doherty, 1987; Doherty and Williams, 1988; Sale, 1991, review), followed by local survival to adult size. This is especially limiting on isolated islands hundreds of kilometers from a source of larvae. Refugia from fishing provide areas where these processes can be enhanced. For species with locally generated offspring, refugia also provide a local breeding stock, and better recruitment to adjacent areas. Lobel and Robinson (1986), for example, described a situation where larvae produced by reef fish on the island of Hawaii were trapped in large offshore eddies and passively returned to the coast to settle. Local success and the resultant crowding of adults in refuges will again result in migration of large fish out of the refuge area. Finally, the primary reason that protected areas (parks or conservation areas) should be encouraged is that this is the most conservative option in a system where the effects of each alternative type of management are poorly understood. Many of the countries experiencing overfishing problems also have few resources to enforce limits and gear restrictions. Completely protected areas, spread out along a coastline, are relatively easy to manage and to observe. Locals benefitting from increased tourism, including tour operators and diving concerns, can be expected to assist in the process of discouraging illegal use of protected areas. Therefore, the establishment of such areas is probably the quickest and best first step any country can take to ensure the continuation of its fishery and the preservation of its reefs. THE FUTURE: FAR FROM PERFECT It is hard to be optimistic about the future of the world's coral reefs. At present, humaninduced changes have already caused major reef deterioration, especially near dense population centers. The combined effects of pollution and exploitation have altered the species assemblages present on such reefs, and have affected the reef framework itself in many regions. Added to the obvious localized effects, the effects of global warming could include local or regional loss of species abundance and diversity due to differences in thermal tolerance, loss of species and reef framework from increased storm frequency or severity, and submergence of some reefs by rising sea level. The forces that will produce such widespread change are already in motion and cannot be stopped over the short term. If the present increase in carbon dioxide has indeed caused a long term warming trend, and if the general aspects of the Greenhouse Theory are correct, the first results will be evident in the next several decades. Although we can slow the rate of increase, there is no foreseeable way to reverse the trend in carbon dioxide concentration in the atmosphere and in its effects on global temperature fast enough to avoid its effects on ecosystems. At a practical level, there are many things that can be done to alleviate human-induced effects on particular reefs and reef systems. Decreasing the input of organic and inorganic nutrients that cause eutrophication is an obvious improvement that can happen within a decade or even in a few years following construction of adequate treatment facilities. Managing fisheries such that at least some reefs in each geographic area can attain their full complement of species and population size structure again is another. Prevention of physical damage to heavily visited reefs by permitting, placing fixed moorings, and regulating visitor density and activity are also positive ways to reduce impact on particular reefs. Coral reefs, in common with other complex communities, are changing on all time scales. In ecological time (decades, centuries) any particular reef is being disturbed or is at some stage of recovery from a large past disturbance (hurricane, Crown-ofThorns outbreak, over-harvesting) and can thus be expected to change its species abundances as it follows a successional sequence, then to change again after another disturbance. 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