Henderson State University
Rapid, widespread changes in coral reef community composition, overall health, and metabolism have become increasingly obvious over recent years. Even before the advent of recent, highly publicized, global coral bleaching events, changes in percent coral cover were well-documented and of concern to some researchers. Numerous causes have been implicated in the observed changes, but the relative importance of most of them has yet to be established. These include changes in water temperature, eutrophication, overfishing, toxic chemicals, disease organisms, and algal growth. The extent to which these changes reflect long-term natural cycles is also unknown, although some studies (Greenstein et al. 1998) have demonstrated that the changes observed in recent decades are inconsistent with long-term taxon abundance characterizing the Pleistocene/Holocene periods.
We seem to know little of the incidence and importance of disease as a force in community structure in marine ecosystems. It appears, however, that diseases are potentially important factors involved in structuring these systems. Seagrass, corals, seals, fish, mollusks, and kelp have all experienced major disease events in recent years, and the frequency of such events seems to be increasing. In the Caribbean alone, 28 major epidemics have been documented in a wide variety of taxa since 1980 (Harvell et al. 1999). In most cases, however, a lack of baseline data and observations makes interpretation of these events in a temporal perspective nearly impossible. Numerous causes contribute to the occurrence of such events, including climatic variability, environmental stresses, and long-range transport introducing pathogens into new habitats.
Diseases of coral, such as black-band disease, have been conclusively linked to significant, rapid changes in reef community composition (e.g. Bruckner and Bruckner 1997). One of the more dramatic events to impact coral and the reef communities over a wide geographic area, however, was not a disease of coral at all. It was the mass mortality of the sea urchin Diadema antillarum in 1983-84. This still unexplained event appears to be strongly affecting the state of Caribbean reefs, long after the disease itself disappeared.
Diadema antillarum Philippi (Echinodermata: Echinoidea) is an omnivorous species of sea urchin that occurs throughout the Caribbean, and in tropical regions of the Western and Eastern Atlantic Oceans. This conspicuous organism, known as the black sea urchin, or long-spined black urchin, is easily recognized by its long, black spines, which may radiate up to 30 cm from a relatively small (7.5 cm) test. The spines are coated with a mildly toxic, irritating mucous.
D. antillarum has been found in a wide variety of habitats, but most often occupies moderately shallow coral reef and seagrass communities. Typically, this animal remains in more sheltered areas, such as depressions in coral, during the day, and migrates out, often to more open seagrass areas, to feed during night (Kaplan 1988). Patch reefs located in seagrass beds can often be found with denuded areas (halos) immediately surrounding them; this clearing action is attributed to the grazing activity of Diadema (Ogden et al. 1973). This urchin has also been implicated as a major bioeroder of reef structure.
D. antillarum has been established as a major herbivore in reef and seagrass habitats. Its preferred food appears to be benthic algal turf and macroalgae, but when those are not available, it will feed on other materials, including live coral. Carpenter (1981;1986) demonstrated its preference for algae, its optimal foraging behavior, and documented some control of algal abundance by the grazing activity of this urchin.
The occurrence of unusual mortality of Diadema was first observed in mid-January, 1983, on the Caribbean coast of Panama, close to the mouth of the Panama Canal (Lessios et al. 1984). Death appeared to occur rapidly, soon after symptoms appeared, and virtually all individuals died. Affected organisms initially developed an accumulation of sediment, and lost pigment and some spines. As the disease progressed, the animals were unable to remain attached to their substrates. Eventually, they literally seemed to fall apart. Behavioral changes were also noted, as the animals did not typically seek shelter during daylight, and were observed being preyed on by fish not normally seen feeding on healthy Diadema. Within days of the first observation of the disease, most individuals in this population were dead, reduced to bleached tests.
After a lag of several months, the disease was noted in other locations. First affected were Diadema in the San Blas Islands of Panama. Populations across the Caribbean were eventually affected by this spreading disease, which traveled in a pattern consistent with major surface currents. The disease moved from Panama in both a westward and an eastward direction on these currents. The disease spread at a rate of roughly 2000 km/ yr to the east, and nearly 3000 km/yr to the west (Lessios 1988a). Eventually, the entire Caribbean was involved, as the disease spread to Florida and north to Bermuda. 3.5 million square kilometers of ocean habitat were affected, and it does not appear that any population of D. antillarum in this area escaped massive mortality. Populations of this species in the eastern Atlantic, and a sibling species in the Eastern Pacific were apparently not affected. The Pacific species might be assumed to be at risk due to potential transmission of the pathogen through the canal. In practice, such movement of organisms appears to be very rare, probably due to the fresh-water nature of the canal, and the fact that water flows from the continental divide at the high point of the canal out into both oceans.
The disease was not only widespread, but highly virulent. The actual intensity of the disease across the 3.5 million square kilometers affected is difficult to compare, due to variations in sampling protocol, but Lessios (1988a) reports that mortality averaged 98%, exceeding 93% at all locations examined, and ranging to over 99.9%. The disease seemed to stop affecting urchins in February, 1984, roughly one year after it appeared. It did re-appear, however, in October-December of 1985. At this time, the disease seemed much less virulent, with less than 1% of the surviving populations in affected Panama and St. Croix developing symptoms.
No causative agent for the disease has been conclusively identified. Lessios (1988a) cites strong circumstantial evidence that a waterborne, host-specific pathogen was responsible. This evidence includes the tendency of the outbreaks to follow the direction and speed of water currents, the involvement of captive Diadema populations in aquaria fed by seawater, lack of decrease in the mortality with distance, development of symptoms when healthy individuals were experimentally exposed to affected animals, and the apparent limitation of the disease to a single species. Two species of spore-forming Clostridium were cultured from an affected population of urchins (Bauer and Agerter 1987). Healthy individuals died when injected with these bacteria, but the connection between the epidemic and these bacteria was not considered conclusive. Mortality appeared to be density independent. Overall, there does not seem to have been a significant relationship between initial population density and the intensity of the die-off at individual locations (Lessios 1988a).
FOLLOWING THE EPIDEMIC
Recovery of Diadema populations following the disease has been surprisingly slow. Studies in Panama (Lessios 1995) indicate that densities remained below 3.5% of pre-mortality population levels, ten years following the epidemic. Some populations were still at only 0.04% of their original densities. In St. Anne’s Bay, Jamaica, densities have recovered only slightly since the epidemic (Morrisey, personal communication). Hodgson (1999) conducted a major survey of coral reefs around the world, examining major organisms present. He found Diadema densities consistently low across the Caribbean. Over 80% of the sites had Diadema at densities less than 5/100m2, 45% had none at all.
Life history characteristics of Diadema would seem to make it a good candidate for fairly rapid recovery from a catastrophic decrease in population. Females produce large numbers of eggs throughout the year, and the planktonic larvae are well-suited to dispersal. Additionally, the reduction of intraspecific competition, and a surprising lack of numerical response in presumed heterspecific urchin competitors following the die-off would seem to encourage more rapid increase in numbers. That has obviously not occurred, but the reason for this is unknown. Lessios (1995) was able to demonstrate that low levels of Diadema in reef habitats are not responsible for poor juvenile recruitment. Because, in some marine species, the presence of adults is important in providing settlement cues to juveniles, this was a definite possibility. His inclusion/exclusion experiments demonstrated that juvenile settlement was not higher in habitats where Diadema density was artificially increased to pre-mortality levels. He speculates that low densities of adults over large areas may result in sufficiently reduced fertilization success for the eggs produced, so that the resulting number of larvae from “upstream” locations is insufficient to overcome naturally high larval mortality. The picture, however, may be more complicated that Lessios suggests. Liddell and Ohlhorst (1986) describe a situation in which an area from which Diadema were experimentally removed in 1972 had failed to reestablish well in the subsequent 12 years. The low fertilization effect offered by Lessios would not seem to explain the slow re-colonization in this case.
Despite the slow recovery of populations, there is some evidence that reduced densities have given existing individuals an advantage. Hughes (1994) found a significant increase in the mean and maximum size of individuals ten years following the die-off, a change attributed to reduced intraspecific competition.
As important herbivores, with controlling effects on algal abundance (Carpenter 1981) the loss of Diadema from reef systems where they had previously been abundant would be predicted to encourage growth of the benthic algae on which they feed. The epilithic algal community on coral reefs is generally considered to be an important component of productivity, but one that is normally kept in check by strong herbivory. Across the Caribbean, there were numerous cases in which cover by species of fleshy benthic algae (Turbinaria, Lobophora, Dictyota, Padina) and filamentous algae increased drastically following the urchin mortality. This appears to be a long-term effect of great importance.
Liddell and Ohlhorst (1986) documented changes in the composition of the benthic community on shallow Jamaican reefs immediately following the mass mortality of Diadema. Due to the proximity of the Discovery Bay Marine Laboratory, good data were available on urchin density and algal /coral cover prior to the die-off. Mortality on these reefs was catastrophic, with urchin densities reduced from 6.6/m2 to 0.0/m2. Dramatic increases in benthic turf algal cover followed the urchin mortality, increasing from approximately 31% before the die-off, to nearly 50% within 2 weeks afterwards. A maximum coverage of 72% was observed 4 months after the event, then declining somewhat. Hughes et al. (1987; 1994) describe drastic changes in community structure on Jamaican reefs in the years immediately following the urchin die-off. A survey of well-studied sites along the North coast of Jamaica shows a consistent decrease from more than 50% coral cover in the late 1970’s to less than 5% in 1993. This is portrayed as a major ecological phase shift from a coral dominated system to an algal dominated system. In perhaps the most telling sentence in the literature surrounding the growth of algae on coral in the Caribbean, Hughes (1994) writes: “Indeed, the classic zonation patterns of Jamaican reefs, described by Goreau and colleagues just two to three decades ago, no longer exist”.
This is not to suggest that reduction of herbivory on epilithic algae is responsible for all observed changes in coral/algal cover. Some researchers stress that the “top down” control of algae by herbivory should not be cause to ignore the “bottom up” control that results from nutrient concentrations in these typically nutrient poor habitats. In many of the Caribbean systems in which algal cover has increased, nutrient concentrations from run-off have also increased (Lapointe 1997). Despite these arguments, however, the seemingly immediate response of algal communities following the Diadema mortality argues strongly for a causal relationship. One recent study (Russ and McCook 1999) failed to document an increase in standing crop following a hurricane-related increase in nutrient availability. Productivity increased, but was not sufficient to saturate grazers, so that no biomass accumulation of the epilithic algal community occurred. The response of grazers appeared to be functional, rather than numerical, with individuals probably adjusting their grazing intensity. Such a functional response was reported by Carpenter (1986) in an increase in fish grazing behavior following Diadema mass mortality. Additionally, even on remote reefs, with no evidence of eutrophication and little fishing pressure, changes in coral cover have been substantial. Such a series of patch reefs in Belize (McClanahan and Muthiga 1998) has experienced a 75% reduction in hard coral cover, and a 315% increase in fleshy algal cover since 1973. Acropora species were particularly affected, with a 99% decrease in cover over the 25-year span, although white-band disease may be responsible for much of this decline. Although there are no pre-die-off Diadema density estimates, current densities are <1/1000 m2.
In an elegant paper, Jeremy Jackson (1997) makes a plea for a reconsideration of the widely accepted relationship between Diadema, overfishing, mortality, and turf algae on coral reefs. In particular, he criticizes the assumption that recent overfishing has allowed an unnaturally high population of Diadema to develop, with the Diadema taking over the algal herbivory previously carried out by the fish. Using Jamaica as an example, he argues that Diadema was abundant in the 17th century, before significant overfishing. He also argues that “recent overfishing” is an incorrect view, as the reef and seagrass communities throughout much of the Caribbean were strongly influenced by human fishing pressure by the first half of the 1700s.
ADDITIONAL SCIENTIFIC BENEFITS OF THE EPIDEMIC
Population genetics. Severe decreases in population size are generally believed to reduce overall genetic diversity in a “bottleneck effect” that persists even after recovery of population numbers. Some data on allozyme diversity in this Diadema antillarum existed prior to the epidemic, allowing Lessios (1985) to make comparisons before and after just such a bottleneck. The predicted decrease in average heterozygosity and number of alleles was not observed. It was suggested, however, that due to the small sizes of remaining populations, the low observed levels of larval recruitment, and certain reproductive characteristics of this species, bottleneck conditions may be experienced over a longer period of time (Lessios 1988b).
Competition. Lessios’s (1995) inclusion/exclusion experiments provided an interesting example of existing assumptions concerning interspecific competition being incorrect. The urchin Echinometra viridis was assumed a competitor with D. antillarum, based on food and habitat preferences. Manipulation of both species densities, however, demonstrated that the presence of E. viridis actually appears to facilitate settlement of D. antillarum juveniles. The grazing of this herbivore may create an algal-free substrate that is more conducive to successful Diadema larval recruitment. (Somewhat surprisingly, the presence of D. antillarum adults has no significant effect. The mechanism for this effect is unknown.) In general, it appears that the drastic decrease in herbivory by Diadema has not resulted in a substantial, widespread increase in other urchins. In some cases, species such as Tripneustes ventricosus have increased somewhat in number, and occur in some previously Diadema-dominated habitats where these species had been rare (Woodley and Gale 1999)
Certainly, the drastic changes in coral community composition observed in the Caribbean in recent years cannot be attributed entirely to effects of the mass mortality of Diadema. Coral diseases, bleaching, increased sedimentation, anthropogenic chemicals, and overfishing all may contribute to the shifts observed. Different systems are certainly responding to differing pressures. It seems clear, however, that the Diadema epidemic has provided us with a unique opportunity to observe a natural experiment involving mass removal of an important herbivore from a complex system. The intensity of the community response, and the long-term changes apparent have been surprising to many researchers in this field.
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