Shifting ecological baselines and the demise of Acropora cervicornis in the western North Atlantic and Caribbean Province: a Pleistocene perspective

 In recent years, marine scientists have become increasingly alarmed over the decline of live coral cover throughout the Caribbean and tropical western Atlantic region. The Holocene and Pleistocene fossil record of coral reefs from this region potentially provides a wealth of long-term ecologic information with which to assess the historical record of changes in shallow water coral reef communities. Before fossil data can be applied to the modern reef system, critical problems involving fossil preservation must be addressed. Moreover, it must be demonstrated that the classic reef coral zonation patterns described in the early days of coral reef ecology, and upon which “healthy” versus “unhealthy” reefs are determined, are themselves representative of reefs that existed prior to any human influence. To address these issues, we have conducted systematic censuses of life and death assemblages on modern “healthy” patch reefs in the Florida reef tract that conform to the classic Caribbean model of reef coral zonation, and a patch reef in the Bahamas that is currently undergoing a transition in coral dominance that is part of a greater Caribbean-wide phenomenon. Results were compared to censuses of ancient reef assemblages preserved in Pleistocene limestones in close proximity to each modern reef. We have determined that the Pleistocene fossil record of coral reefs may be used to calibrate an ecological baseline with which to compare modern reef assemblages, and suggest that the current and rapid decline of Acropora cervicornis observed on a Bahamian patch reef may be a unique event that contrasts with the long-term persistence of this taxon during Pleistocene and Holocene time. Accepted: 19 May 1998     

Persistence of coral assemblages at East and West Flower Garden Banks,Gulf of Mexico

Since 1989 a federally supported long-term coral reef monitoring program has focused on two study sites atop East and West Flower Garden Banks in the northwestern Gulf of Mexico. We examined 25 yr of benthic cover data to provide a multi-decadal baseline and trend analysis of the community structure for this coral reef system. Despite global coral reef decline in recent decades, mean coral cover at East and West Flower Garden Banks was above 50% for the combined 25 yr of continuous monitoring, and represented a stable coral community. However, mean macroalgal cover increased significantly between 1998 and 1999, rising from approximately 3 to 20%, and reaching a maximum above 30% in 2012. In contrast to many other shallow water reefs in the Caribbean region, increases in mean macroalgal cover have not been concomitant with coral cover decline at the Flower Garden Banks.     

Region‐wide temporal and spatial variation in Caribbean reef architecture: is coral cover the whole story?

The architectural complexity of coral reefs is largely generated by reef‐building corals, yet the effects of current regional‐scale declines in coral cover on reef complexity are poorly understood. In particular, both the extent to which declines in coral cover lead to declines in complexity and the length of time it takes for reefs to collapse following coral mortality are unknown. Here we assess the extent of temporal and spatial covariation between coral cover and reef architectural complexity using a Caribbean‐wide dataset of temporally replicated estimates spanning four decades. Both coral cover and architectural complexity have declined rapidly over time, with little evidence of a time‐lag. However, annual rates of change in coral cover and complexity do not covary, and levels of complexity vary greatly among reefs with similar coral cover. These findings suggest that the stressors influencing Caribbean reefs are sufficiently severe and widespread to produce similar regional‐scale declines in coral cover and reef complexity, even though reef architectural complexity is not a direct function of coral cover at local scales. Given that architectural complexity is not a simple function of coral cover, it is important that conservation monitoring and restoration give due consideration to both architecture and coral cover. This will help ensure that the ecosystem services supported by architectural complexity, such as nutrient recycling, dissipation of wave energy, fish production and diversity, are maintained and enhanced.     

Flattening of Caribbean coral reefs: region-wide declines in architectural complexity

Coral reefs are rich in biodiversity, in large part because their highly complex architecture provides shelter and resources for a wide range of organisms. Recent rapid declines in hard coral cover have occurred across the Caribbean region, but the concomitant consequences for reef architecture have not been quantified on a large scale to date. We provide, to our knowledge, the first region-wide analysis of changes in reef architectural complexity, using nearly 500 surveys across 200 reefs, between 1969 and 2008. The architectural complexity of Caribbean reefs has declined nonlinearly with the near disappearance of the most complex reefs over the last 40 years. The flattening of Caribbean reefs was apparent by the early 1980s, followed by a period of stasis between 1985 and 1998 and then a resumption of the decline in complexity to the present. Rates of loss are similar on shallow (<6 m), mid-water (6–20 m) and deep (>20 m) reefs and are consistent across all five subregions. The temporal pattern of declining architecture coincides with key events in recent Caribbean ecological history: the loss of structurally complex Acropora corals, the mass mortality of the grazing urchin Diadema antillarum and the 1998 El Nino Southern Oscillation-induced worldwide coral bleaching event. The consistently low estimates of current architectural complexity suggest regional-scale degradation and homogenization of reef structure. The widespread loss of architectural complexity is likely to have serious consequences for reef biodiversity, ecosystem functioning and associated environmental services.     

Ecological condition of coral reef assemblages in the Cuban Archipelago

The condition of coral reefs in the Cuban Archipelago is poorly known. We aimed to analyse coral assemblages across 199 reef sites belonging to 12 localities. Crest and fore reefs were assessed using six metrics: species richness, density, coral cover, mortality, coral size and reef complexity. The condition of reefs varied across the archipelago from healthy to depleted reefs. The localities with best scores were Cienfuegos, Bahía de Cochinos and Cazones. These reefs have values of living coral cover (>20%) and complexity (>50?cm) similar to the best preserved Caribbean reefs. However, the majority of crest biotopes suffered important deterioration with old mortality of Acropora palmata populations and moderate coral cover (15%); although crest reefs still maintained their structural complexity. Despite moderate levels of coral cover in fore reefs (18%), their condition was alarming because 25% of the sites had cover below the recovery threshold of 10%, accumulated mortality and structural flattening. Compared with the 1980s, the species richness was roughly the same (42) for crest and fore reefs, although dominance has changed to widespread tolerant species. Coral reef assemblages varied at local and regional scales in similar magnitude, suggesting the combined effects of natural and anthropogenic drivers.     

Mass Coral Bleaching in 2010 in the Southern Caribbean

Ocean temperatures are increasing globally and the Caribbean is no exception. An extreme ocean warming event in 2010 placed Tobago''s coral reefs under severe stress resulting in widespread coral bleaching and threatening the livelihoods that rely on them. The bleaching response of four reef building taxa was monitored over a six month period across three major reefs systems in Tobago. By identifying taxa resilient to bleaching we propose to assist local coral reef managers in the decision making process to cope with mass bleaching events. The bleaching signal (length of exposure to high ocean temperatures) varied widely between the Atlantic and Caribbean reefs, but regardless of this variation most taxa bleached. Colpophyllia natans, Montastraea faveolata and Siderastrea siderea were considered the most bleaching vulnerable taxa. Interestingly, reefs with the highest coral cover showed the greatest decline reef building taxa, and conversely, reefs with the lowest coral cover showed the most bleaching but lowest change in coral cover with little algal overgrowth post-bleaching.     

Drivers of region-wide declines in architectural complexity on Caribbean reefs

Severe declines in the cover of live hard coral on reefs have been reported worldwide, and in the Caribbean region, the architectural complexity of coral reefs has also declined markedly. While the drivers of coral cover loss are relatively well understood, little is known about the drivers of regional-scale declines in architectural complexity. We have used a dataset of 49 time series reporting reef architectural complexity to explore the effect of hurricanes, coral bleaching and fishing on Caribbean-wide annual rates of change in reef complexity. Hurricane impacts greatly influence reef complexity, with the most rapid rates of decline in complexity occurring at sites impacted during their survey period, and with lower rates of loss occurring at unimpacted sites. Reef architectural complexity did not change significantly following mass bleaching events (in a time frame of <5 years) or positive thermal anomalies. Although the rates of change in architectural complexity were similar in and out of marine protected areas (MPAs), significant declines in complexity were observed inside but not outside of MPAs, possibly because reductions in fishing can lead to increased bioerosion by herbivores within MPAs. Our findings suggest that major drivers of coral mortality, such as coral bleaching, do not influence reef architectural complexity in the short term (<5 years). Instead, direct physical impacts and reef bioerosion appear to be important drivers of the widespread loss of architecturally complex reefs in the Caribbean.     

Coral reef resilience to thermal stress in the Eastern Tropical Pacific

Coral reefs worldwide are threatened by thermal stress caused by climate change. Especially devastating periods of coral loss frequently occur during El Niño‐Southern Oscillation (ENSO) events originating in the Eastern Tropical Pacific (ETP). El Niño‐induced thermal stress is considered the primary threat to ETP coral reefs. An increase in the frequency and intensity of ENSO events predicted in the coming decades threatens a pan‐tropical collapse of coral reefs. During the 1982–1983 El Niño, most reefs in the Galapagos Islands collapsed, and many more in the region were decimated by massive coral bleaching and mortality. However, after repeated thermal stress disturbances, such as those caused by the 1997–1998 El Niño, ETP corals reefs have demonstrated regional persistence and resiliency. Using a 44 year dataset (1970–2014) of live coral cover from the ETP, we assess whether ETP reefs exhibit the same decline as seen globally for other reefs. Also, we compare the ETP live coral cover rate of change with data from the maximum Degree Heating Weeks experienced by these reefs to assess the role of thermal stress on coral reef survival. We find that during the period 1970–2014, ETP coral cover exhibited temporary reductions following major ENSO events, but no overall decline. Further, we find that ETP reef recovery patterns allow coral to persist under these El Niño‐stressed conditions, often recovering from these events in 10–15 years. Accumulative heat stress explains 31% of the overall annual rate of change of living coral cover in the ETP. This suggests that ETP coral reefs have adapted to thermal extremes to date, and may have the ability to adapt to near‐term future climate‐change thermal anomalies. These findings for ETP reef resilience may provide general insights for the future of coral reef survival and recovery elsewhere under intensifying El Niño scenarios.     

Maintenance of fish diversity on disturbed coral reefs

Habitat perturbations play a major role in shaping community structure; however, the elements of disturbance-related habitat change that affect diversity are not always apparent. This study examined the effects of habitat disturbances on species richness of coral reef fish assemblages using annual surveys of habitat and 210 fish species from 10 reefs on the Great Barrier Reef (GBR). Over a period of 11 years, major disturbances, including localised outbreaks of crown-of-thorns sea star (Acanthaster planci), severe storms or coral bleaching, resulted in coral decline of 46–96% in all the 10 reefs. Despite declines in coral cover, structural complexity of the reef framework was retained on five and species richness of coral reef fishes maintained on nine of the disturbed reefs. Extensive loss of coral resulted in localised declines of highly specialised coral-dependent species, but this loss of diversity was more than compensated for by increases in the number of species that feed on the epilithic algal matrix (EAM). A unimodal relationship between areal coral cover and species richness indicated species richness was greatest at approximately 20% coral cover declining by 3–4 species (6–8% of average richness) at higher and lower coral cover. Results revealed that declines in coral cover on reefs may have limited short-term impact on the diversity of coral reef fishes, though there may be fundamental changes in the community structure of fishes.     

Measuring coral reef decline through meta-analyses

Coral reef ecosystems are in decline worldwide, owing to a variety of anthropogenic and natural causes. One of the most obvious signals of reef degradation is a reduction in live coral cover. Past and current rates of loss of coral are known for many individual reefs; however, until recently, no large-scale estimate was available. In this paper, we show how meta-analysis can be used to integrate existing small-scale estimates of change in coral and macroalgal cover, derived from in situ surveys of reefs, to generate a robust assessment of long-term patterns of large-scale ecological change. Using a large dataset from Caribbean reefs, we examine the possible biases inherent in meta-analytical studies and the sensitivity of the method to patchiness in data availability. Despite the fact that our meta-analysis included studies that used a variety of sampling methods, the regional estimate of change in coral cover we obtained is similar to that generated by a standardized survey programme that was implemented in 1991 in the Caribbean. We argue that for habitat types that are regularly and reasonably well surveyed in the course of ecological or conservation research, meta-analysis offers a cost-effective and rapid method for generating robust estimates of past and current states.     

Empirical models of transitions between coral reef states: effects of region, protection, and environmental change

There has been substantial recent change in coral reef communities. To date, most analyses have focussed on static patterns or changes in single variables such as coral cover. However, little is known about how community-level changes occur at large spatial scales. Here, we develop Markov models of annual changes in coral and macroalgal cover in the Caribbean and Great Barrier Reef (GBR) regions. We analyzed reef surveys from the Caribbean and GBR (1996-2006). We defined a set of reef states distinguished by coral and macroalgal cover, and obtained Bayesian estimates of the annual probabilities of transitions between these states. The Caribbean and GBR had different transition probabilities, and therefore different rates of change in reef condition. This could be due to differences in species composition, management or the nature and extent of disturbances between these regions. We then estimated equilibrium probability distributions for reef states, and coral and macroalgal cover under constant environmental conditions. In both regions, the current distributions are close to equilibrium. In the Caribbean, coral cover is much lower and macroalgal cover is higher at equilibrium than in the GBR. We found no evidence for differences in transition probabilities between the first and second halves of our survey period, or between Caribbean reefs inside and outside marine protected areas. However, our power to detect such differences may have been low. We also examined the effects of altering transition probabilities on the community state equilibrium, along a continuum from unfavourable (e.g., increased sea surface temperature) to favourable (e.g., improved management) conditions. Both regions showed similar qualitative responses, but different patterns of uncertainty. In the Caribbean, uncertainty was greatest about effects of favourable changes, while in the GBR, we are most uncertain about effects of unfavourable changes. Our approach could be extended to provide risk analysis for management decisions.     

The dynamics of architectural complexity on coral reefs under climate change

One striking feature of coral reef ecosystems is the complex benthic architecture which supports diverse and abundant fauna, particularly of reef fish. Reef‐building corals are in decline worldwide, with a corresponding loss of live coral cover resulting in a loss of architectural complexity. Understanding the dynamics of the reef architecture is therefore important to envision the ability of corals to maintain functional habitats in an era of climate change. Here, we develop a mechanistic model of reef topographical complexity for contemporary Caribbean reefs. The model describes the dynamics of corals and other benthic taxa under climate‐driven disturbances (hurricanes and coral bleaching). Corals have a simplified shape with explicit diameter and height, allowing species‐specific calculation of their colony surface and volume. Growth and the mechanical (hurricanes) and biological erosion (parrotfish) of carbonate skeletons are important in driving the pace of extension/reduction in the upper reef surface, the net outcome being quantified by a simple surface roughness index (reef rugosity). The model accurately simulated the decadal changes of coral cover observed in Cozumel (Mexico) between 1984 and 2008, and provided a realistic hindcast of coral colony‐scale (1–10 m) changing rugosity over the same period. We then projected future changes of Caribbean reef rugosity in response to global warming. Under severe and frequent thermal stress, the model predicted a dramatic loss of rugosity over the next two or three decades. Critically, reefs with managed parrotfish populations were able to delay the general loss of architectural complexity, as the benefits of grazing in maintaining living coral outweighed the bioerosion of dead coral skeletons. Overall, this model provides the first explicit projections of reef rugosity in a warming climate, and highlights the need of combining local (protecting and restoring high grazing) to global (mitigation of greenhouse gas emissions) interventions for the persistence of functional reef habitats.     

Severity of the 1998 and 2005 bleaching events in Venezuela, southern Caribbean

This study describes the severity of the 2005 bleaching event at 15 reef sites across Venezuela and compares the 1998 and 2005 bleaching events at one of them. During August and September 2005, bleached corals were first observed on oceanic reefs rather than coastal reefs, affecting 1 to 4% of coral colonies in the community (3 reef sites, n = 736 colonies). At that time, however, no bleached corals were recorded along the eastern coast of Venezuela, an area of seasonal upwelling (3 reefs, n = 181 colonies). On coastal reefs, bleaching started in October but highest levels were reached in November 2005 and January 2006, when 16% of corals were affected among a wide range of taxa (e.g. scleractinians, octocorals, Millepora and zoanthids). In the Acropora habitats of Los Roques (an oceanic reef),no bleached was recorded in 2005 (four sites,n = 643 colonies). At Cayo Sombrero, a coastal reef site, bleaching was less severe in 1998 than in 2005 (9% of the coral colonies involving 2 species vs. 26% involving 23 species, respectively). Our results indicate that bleaching was more severe in 2005 than in 1998 on Venezuelan reefs; however, no mass mortality was observed in either of these two events.     

Competitive interactions between corals and Trididemnum solidum on Mexican Caribbean reefs

The ascidian Trididemnum solidum competes for space on Caribbean reefs and is capable of overgrowing live scleractinian corals. From 2006 to 2009, we monitored over 30,000 coral colonies and quantified competitive interactions with this ascidian at four reef sites along the Mexican Caribbean. The total number of competitive interactions increased in time, but the mean percentage of coral colonies involved in interactions remained lower than 1% in all reefs. Bottom cover by T. solidum was also low (mean < 0.5%) in all reef sites in all sampling years. We conclude that during the temporal scope of our study, the overall potential effect of T. solidum on the dynamics of Mexican Caribbean coral populations was minimal.     

The abundance of herbivorous fish on an inshore Red Sea reef following a mass coral bleaching event

A healthy herbivore community is critical for the ability of a reef to resist and recover from severe disturbances and to regain lost coral cover (i.e., resilience). The densities of the two major herbivorous fish groups (the family Acanthuridae and scarine labrids) were comparatively studied for an inshore reef that was severely impacted by a mass coral bleaching event in 2010 and an unaffected reef within the same region. Densities were found to be significantly higher on the affected reef, most likely due to the high algal densities on that reef. However, densities of herbivores on both reefs were found to be on average about 1–2 orders of magnitude lower than previously published reports from some Pacific reefs and from Red Sea reefs in the Gulf of Aqaba and only slightly higher than Caribbean reefs. Thus, it is predicted that recovery for this reef and similarly affected reefs may be very slow. The protection of herbivores from overfishing and the introduction of other management strategies that maximize reef resilience in Saudi Arabian waters are highly recommended.     

Decadal changes in turbid-water coral communities at Pandora Reef: loss of resilience or too soon to tell?

Coral communities were monitored at Pandora Reef, nearshore Great Barrier Reef from 1981 to 2005 using photography and videography. In the 1980s, regional elevation of land-based nutrients in coastal waters (ca. 2–6 times pre-European levels of early 1800s) did not prevent overall recovery of coral cover and diversity following a sequence of environmental disturbances in the 1970s. However, prospects for a repeat of such resilience following catastrophic mortality from high-temperature bleaching in 1998 and a cyclone in 2000 are not clear. Different coral communities around the reef varied greatly in relation to impacts and recovery. Fore-reef communities dominated by acroporids (fast growing branching and tabular Acropora and foliose Montipora) recovered strongly in the 1980s following apparently severe impacts by cyclone, flood and heat wave disturbances in the 1970s, attaining 60–90% cover by stabilizing rubble and outgrowing macro-algae in <10 years. In the back-reef, by contrast, poritid-dominated communities (massive and finger Porites and columnar Goniopora and Alveopora) had more stable trajectories and smaller impact from recent disturbances: recovery was well underway in 2005. The contrasting trajectories of different parts of the reef reflect differential survival of more persistent versus more ephemeral taxa, notably poritids and acroporids, respectively, both major contributors to framework and cover on reefs globally. A repeat of earlier resilience appears possible in the shallow fore-reef, but unlikely in the deeper fore-reef, which had few viable fragments or recruits in 2005. The main limits on recovery may be (1) reduced supply of coral larvae due to widespread regional losses of coral brood stock and (2) the reduced intervals between disturbances associated with global climate change. The presence of a high abundance of Acroporidae is a major pre-disposing risk factor for climate change impacts.     

Caribbean reefs of the Anthropocene: Variance in ecosystem metrics indicates bright spots on coral depauperate reefs

Dramatic coral loss has significantly altered many Caribbean reefs, with potentially important consequences for the ecological functions and ecosystem services provided by reef systems. Many studies examine coral loss and its causes—and often presume a universal decline of ecosystem services with coral loss—rather than evaluating the range of possible outcomes for a diversity of ecosystem functions and services at reefs varying in coral cover. We evaluate 10 key ecosystem metrics, relating to a variety of different reef ecosystem functions and services, on 328 Caribbean reefs varying in coral cover. We focus on the range and variability of these metrics rather than on mean responses. In contrast to a prevailing paradigm, we document high variability for a variety of metrics, and for many the range of outcomes is not related to coral cover. We find numerous “bright spots,” where herbivorous fish biomass, density of large fishes, fishery value, and/or fish species richness are high, despite low coral cover. Although it remains critical to protect and restore corals, understanding variability in ecosystem metrics among low‐coral reefs can facilitate the maintenance of reefs with sustained functions and services as we work to restore degraded systems. This framework can be applied to other ecosystems in the Anthropocene to better understand variance in ecosystem service outcomes and identify where and why bright spots exist.     

Local and regional scale recovery of Diadema promotes recruitment of scleractinian corals

The phase change from coral to macroalgal dominance on many Caribbean reefs was exacerbated by the mortality of the echinoid Diadema antillarum in 1983–1984, and until recently, this sea urchin has remained rare on reefs throughout the western Atlantic. By the late 1990s, Diadema started to reappear in large numbers on some Jamaican reefs, and by 2000, the high densities were correlated with significantly greater abundances of juvenile corals. Here, we show that dense populations of Diadema now occur over a multi-kilometre-wide scale at six locations scattered along a 4100 km arc across the entire Caribbean. In all cases, these dense populations are found in shallow water (< 6 m depth) on outer reef communities and are associated with reduced macroalgal cover and enhanced coral recruitment. We conclude that population recovery of Diadema is occurring at both local and regional scales, and that grazing by this echinoid is creating conditions favouring the recruitment of corals.     

No Reef Is an Island: Integrating Coral Reef Connectivity Data into the Design of Regional-Scale Marine Protected Area Networks

We integrated coral reef connectivity data for the Caribbean and Gulf of Mexico into a conservation decision-making framework for designing a regional scale marine protected area (MPA) network that provides insight into ecological and political contexts. We used an ocean circulation model and regional coral reef data to simulate eight spawning events from 2008–2011, applying a maximum 30-day pelagic larval duration and 20% mortality rate. Coral larval dispersal patterns were analyzed between coral reefs across jurisdictional marine zones to identify spatial relationships between larval sources and destinations within countries and territories across the region. We applied our results in Marxan, a conservation planning software tool, to identify a regional coral reef MPA network design that meets conservation goals, minimizes underlying threats, and maintains coral reef connectivity. Our results suggest that approximately 77% of coral reefs identified as having a high regional connectivity value are not included in the existing MPA network. This research is unique because we quantify and report coral larval connectivity data by marine ecoregions and Exclusive Economic Zones (EZZ) and use this information to identify gaps in the current Caribbean-wide MPA network by integrating asymmetric connectivity information in Marxan to design a regional MPA network that includes important reef network connections. The identification of important reef connectivity metrics guides the selection of priority conservation areas and supports resilience at the whole system level into the future.