William F. Precht

One-third of reef-building corals face elevated extinction risk from climate change and local impacts

The conservation status of 845 zooxanthellate reef-building coral species was assessed by using International Union for Conservation of Nature Red List Criteria. Of the 704 species that could be assigned conservation status, 32.8% are in categories with elevated risk of extinction. Declines in abundance are associated with bleaching and diseases driven by elevated sea surface temperatures, with extinction risk further exacerbated by local-scale anthropogenic disturbances. The proportion of corals threatened with extinction has increased dramatically in recent decades and exceeds that of most terrestrial groups. The Caribbean has the largest proportion of corals in high extinction risk categories, whereas the Coral Triangle (western Pacific) has the highest proportion of species in all categories of elevated extinction risk. Our results emphasize the widespread plight of coral reefs and the urgent need to enact conservation measures.

White-band disease and the changing face of Caribbean coral reefs

In recent decades, the cover of fleshy macroalgae has increased and coral cover has decreased on most Caribbean reefs. Coral mortality precipitated this transition, and the accumulation of macroalgal biomass has been enhanced by decreased herbivory and increased nutrient input. Populations of Acropora palmata (elkhorn coral) and A. cervicornis (staghorn coral), two of the most important framework-building species, have died throughout the Caribbean, substantially reducing coral cover and providing substratum for algal growth. Hurricanes have devastated local populations of Acropora spp. over the past 20–25 years, but white-band disease, a putative bacterial syndrome specific to the genus Acropora, has been a more significant source of mortality over large areas of the Caribbean region.Paleontological data suggest that the regional Acropora kill is without precedent in the late Holocene. In Belize, A. cervicornis was the primary ecological and geological constituent of reefs in the central shelf lagoon until the mid-1980s. After constructing reef framework for thousands of years, A. cervicornis was virtually eliminated from the area over a ten-year period. Evidence from other parts of the Caribbean supports the hypothesis of continuous Holocene accumulation and recent mass mortality of Acropora spp. Prospects are poor for the rapid recovery of A. cervicornis, because its reproductive strategy emphasizes asexual fragmentation at the expense of dispersive sexual reproduction. A. palmata also relies on fragmentation, but this species has a higher rate of sexual recruitment than A. cervicornis. If the Acropora spp. do not recover, macroalgae will continue to dominate Caribbean reefs, accompanied by increased abundances of brooding corals, particularly Agaricia spp. and Porites spp. The outbreak of white-band disease has been coincident with increased human activity, and the possibility of a causal connection should be further investigated.

Conservation, precaution, and Caribbean reefs

Some authors argue that overfishing is an important reason that reef corals have declined in recent decades. Their reasoning is that overfishing removes herbivores, releasing macroalgae to overgrow and kill the corals. The evidence suggests, however, that global climate change and emergent marine diseases make a far greater contribution to coral mortality, and that macroalgae generally grow on the exposed skeletal surfaces of corals that are already dead. Macroalgal dominance, therefore, is an effect rather than a cause of coral mortality. Marine protected areas (MPAs), which are usually established to protect stocks of reef fish, foster populations of herbivorous fish under at least some circumstances. Increased herbivory can reduce algal cover, potentially accelerating the recovery of coral populations inside MPAs; however, establishing MPAs will have only a limited impact on coral recovery unless policymakers confront the accelerating negative effects of the global-scale sources of coral mortality.

Climate flickers and range shifts of reef corals

Staghorn coral (Acropora cervicornis) and elkhorn coral (Acropora palmata), are important reef builders in the Caribbean. In the early to middle Holocene (10 000–6000 years ago), when sea temperatures were warmer than today, Acropora-dominated reefs were common along the east coast of Florida as far north as Palm Beach County. The fossil record shows that the northern limits of these two cold-sensitive species subsequently contracted to Biscayne Bay, south of Miami, apparently as a result of climatic cooling. This response of the Acropora species to climate provides a context for interpreting recent shifts in their geographic distribution. Despite recent disease-induced mass mortalities throughout the Caribbean and western Atlantic, the two species are now re-expanding their ranges northward along the Florida Peninsula and into the northern Gulf of Mexico, coincident with increasing sea temperatures. In the face of continued global warming, the northernmost limit of this range expansion will ultimately be...

Stasis, biological disturbance, and community structure of a Holocene coral reef

Disturbances have drastically altered Caribbean coral reefs over the past two decades. Acropora cervicornis (staghorn coral), which predominated at intermediate depths (5-25 m) from the 1950s through the 1970s, has virtually disappeared from most reef environments. Other coral spe- cies have declined as well, and the cover of macroalgae has increased. In apparent contrast, fossil reef sequences suggest that the species composition and zonation of coral assemblages did not change during the Pleistocene and Holocene. One interpretation of these observations is that coral species persisted on Caribbean reefs for hundreds of thousands of years as components of tightly integrated communities, and that a rare or unique combination of disturbances led to the syn- chronous decline of A. cervicornis and other corals throughout the region. The hypotheses of (1) community integration and (2) a unique, recent community transition, were tested by ecological and paleoecological observations in the shelf lagoon of the Belizean Barrier Reef. The reef growing along the flanks of Channel Cay, a lagoonal shoal, was monitored by point counts along transects over a ten-year period (1986-95). This reef was covered primarily by A. cer- vicornis at 3-15 m depth until the late 1980s. After 1986, A. cervicornis experienced a mass mortality from White Band Disease, an epizootic of presumed bacterial origin. The cover of A. cervicornis dropped from -70% in 1986 to nearly 0% in 1993. Agaricia spp. (lettuce corals) responded oppor- tunistically to the availability of free space in the form of A. cervicornis skeletal rubble. Agaricia, which had been a minor constituent of the sessile biota (10% cover in 1986), replaced A. cervicornis as the most common occupant of space on the reef (56% cover in 1995). The percent cover of other coral species and macroalgae remained low throughout the ten-year period. Similar changes were observed on other reefs over an area of at least 250 km2. The Acropora-to-Agaricia transition left a clear signature in the sedimentary record. Trenches dug into the reef at Channel Cay revealed the accretion of a layer of Agaricia rubble with a mean thick- ness of 22 cm in the decade after 1986. Due to the unconsolidated, uncompacted nature of the reef sediments, evidence of previous Acropora-to-Agaricia transitions should have been visible in the fossil record as vertical accumulations of A. cervicornis branches interrupted by layers of imbricated Agaricia rubble. Coring studies at Channel Cay revealed that no other Agaricia layers were deposited during at least the past 3800 years; the recent transition was unique on a time scale of millennia. This result supports the contention that excursions from the Acropora-dominated situation are un- usual in the history of Channel Cay and nearby reefs. However, the dynamics of the transition do not support the community integration hypothesis for the Channel Cay reef, indicating instead that different coral taxa in this assemblage responded differently, or not at all, to a large-scale biotic disturbance. The community transition also underscores the potential for biological factors in gen- eral, and disease in particular, to alter the composition of ecological communities and their sedi- mentary remains.

THE EXPANDING SCALE OF SPECIES TURNOVER EVENTS ON CORAL REEFS IN BELIZE

Beginning in the late 1980s, white-band disease nearly eliminated the stag- horn coral Acropora cervicornis from reefs in the central shelf lagoon of Belize. The lettuce coral Agaricia tenuifolia replaced Acropora cervicornis in the early 1990s, but anomalously high water temperatures in 1998 caused severe bleaching and catastrophic mortality of Agaricia tenuifolia. The short-lived transition in dominance from Acropora cervicornis to Agaricia tenuifolia left an unambiguous signature in the fossil record of these uncemented lagoonal reefs. Analysis of 38 cores, extracted from 22 sampling stations in a 375-km2 area of the central lagoon, showed that Acropora cervicornis dominated continuously for at least 3000 years prior to the recent events. Agaricia tenuifolia occasionally grew in small patches, but no coral-to-coral replacement sequence occurred over the entire area until the late 1980s. Within a decade, the scale of species turnover increased from tens of square meters or less to hundreds of square kilometers or more. This unprecedented increase in the scale of turnover events is rooted in the accelerating pace of ecological change on coral reefs at the regional level.

Severe 2010 Cold-Water Event Caused Unprecedented Mortality to Corals of the Florida Reef Tract and Reversed Previous Survivorship Patterns

Background Coral reefs are facing increasing pressure from natural and anthropogenic stressors that have already caused significant worldwide declines. In January 2010, coral reefs of Florida, United States, were impacted by an extreme cold-water anomaly that exposed corals to temperatures well below their reported thresholds (16°C), causing rapid coral mortality unprecedented in spatial extent and severity. Methodology/Principal Findings Reef surveys were conducted from Martin County to the Lower Florida Keys within weeks of the anomaly. The impacts recorded were catastrophic and exceeded those of any previous disturbances in the region. Coral mortality patterns were directly correlated to in-situ and satellite-derived cold-temperature metrics. These impacts rival, in spatial extent and intensity, the impacts of the well-publicized warm-water bleaching events around the globe. The mean percent coral mortality recorded for all species and subregions was 11.5% in the 2010 winter, compared to 0.5% recorded in the previous five summers, including years like 2005 where warm-water bleaching was prevalent. Highest mean mortality (15%–39%) was documented for inshore habitats where temperatures were <11°C for prolonged periods. Increases in mortality from previous years were significant for 21 of 25 coral species, and were 1–2 orders of magnitude higher for most species. Conclusions/Significance The cold-water anomaly of January 2010 caused the worst coral mortality on record for the Florida Reef Tract, highlighting the potential catastrophic impacts that unusual but extreme climatic events can have on the persistence of coral reefs. Moreover, habitats and species most severely affected were those found in high-coral cover, inshore, shallow reef habitats previously considered the “oases” of the region, having escaped declining patterns observed for more offshore habitats. Thus, the 2010 cold-water anomaly not only caused widespread coral mortality but also reversed prior resistance and resilience patterns that will take decades to recover.

Extrinsic control of species replacement on a Holocene reef in Belize: the role of coral disease

Abstract Well-preserved, Holocene coral reefs provide the opportunity to discriminate between models of intrinsically driven succession and extrinsically driven species replacement, especially when paleontological patterns can be combined with ecological observations of the underlying mechanisms. Rhomboid shoals in the central shelf lagoon of the Belizean Barrier Reef experienced a recent and dramatic change in community composition. Agaricia tenuifolia replaced Acropora cervicornis as the dominant coral species at 3–15 m depth along the flanks of the reefs. We tested the hypothesis that shallowing upward caused this shift in dominance. A core extracted from 0.5 m water depth on one of the shoals, Channel Cay, revealed a shallowing-upward shift in dominance from Acropora to Porites divaricata. This successional sequence was quite different from the Acropora-to-Agaricia transition observed in four cores from 6–11 m water depth. Ecological observations showed that Agaricia became the dominant at ≥3 m depth after Acropora populations were decimated by a regional outbreak of white-band disease. The Acropora-to-Agaricia transition was clearly a case of extrinsically driven species replacement rather than an intrinsically driven, successional, shallowing-upward sequence.

Landscape patterns of reef coral diversity: a test of the intermediate disturbance hypothesis

Abstract The intermediate disturbance hypothesis predicts that species diversity within habitats will be maximal at intermediate levels of disturbance, because competitive exclusion will be balanced by destruction of the competitive dominant(s). Previous tests of the hypothesis on coral reefs have produced variable results, in part because they were conducted at the small spatial scale of the quadrat. This study tested the intermediate disturbance hypothesis on a landscape scale, over an area >10 4 m 2 within a single reef habitat. Among replicate shallow reef spurs in Belize, coral species diversity was maximal at intermediate levels of disturbance, as measured by the topographic complexity of the substratum. Increased diversity at intermediate disturbance levels was due primarily to increased evenness rather than to increased species richness. The impacts of storm-generated debris appear to have reduced the cover of the competitively dominant coral, Agaricia tenuifolia Dana, allowing competitively subordinate coral species to increase on some spurs. This landscape-scale analysis provides the first rigorous, quantitative support for the hypothesis in a reef coral assemblage.

Coral bleach-out in Belize

The highest sea surface temperatures ever recorded, related both to the 1997–98 El Niño/Southern Oscillation and to global warming, caused severe bleaching of corals worldwide in 1998 (ref. 2). This thermal anomaly induced mass mortality of scleractinian corals on lagoonal reefs in Belize, the first time that a coral population in the Caribbean has collapsed completely from bleaching. Cores extracted from the Belizean reefs showed that these events were unprecedented over at least the past 3,000 years.