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.     

Phase shifts and the stability of macroalgal communities on Caribbean coral reefs

Caribbean coral reefs are widely thought to exhibit two alternate stable states with one being dominated by coral and the other by macroalgae. However, the observation of linear empirical relationships among grazing, algal cover and coral recruitment has led the existence of alternate stable states to be questioned; are reefs simply exhibiting a continuous phase shift in response to grazing or are the alternate states robust to certain changes in grazing? Here, a model of a Caribbean forereef is used to reconcile the existence of two stable community states with common empirical observations. Coral-depauperate and coral-dominated reef states are predicted to be stable on equilibrial time scales of decades to centuries and their emergence depends on the presence or absence of a bottleneck in coral recruitment, which is determined by threshold levels of grazing intensity and other process variables. Under certain physical and biological conditions, corals can be persistently depleted even while increases in grazing reduce macroalgal cover and enhance coral recruitment; only once levels of recruitment becomes sufficient to overwhelm the population bottleneck will the coral-dominated state begin to emerge. Therefore, modest increases in grazing will not necessarily allow coral populations to recover, whereas large increases, such as those associated with recovery of the urchin Diadema antillarum, are likely to exceed threshold levels of grazing intensity and set a trajectory of coral recovery. The postulated existence of alternate stable states is consistent with field observations of linear relationships between grazing, algal cover and coral recruitment when coral cover is low and algal exclusion when coral cover is high. The term ‘macroalgal dominated’ is potentially misleading because the coral-depauperate state can be associated with various levels of macroalgal cover. The term ‘coral depauperate’ is preferable to ‘macroalgal dominated’ when describing alternate states of Caribbean reefs.     

Data-driven models for regional coral-reef dynamics

Coral reefs have been affected by natural and anthropogenic disturbances. Coral cover has declined on many reefs, and macroalgae have increased on some. The existence of alternative stable states with high or low coral cover has been widely debated, but not clearly established. We evaluate the evidence for alternative stable states in benthic coral-reef dynamics in the Caribbean, Kenya and Great Barrier Reef (GBR), using stochastic semi-parametric models based on large numbers of time series of cover of hard corals, macroalgae and other components. Only the GBR showed a consistent short-term regional decline in coral cover. There was no evidence for regional increases in macroalgae. The equilibrium distributions of our models were close to recently observed distributions, and differed among regions. In all three regions, the equilibrium distributions were unimodal rather than bimodal, and thus did not suggest the existence of alternative stable states on a regional scale, under current conditions.     

Habitat complexity and consumer-mediated positive feedbacks on a Caribbean coral reef

Theoretical and empirical evidence suggest that positive feedbacks can increase resilience in ecological communities. On Caribbean coral reefs, there have been striking shifts from physically complex communities with high coral cover to relatively homogenous communities dominated by macroalgae, which have persisted for decades. However, little is known about positive feedbacks that may maintain coral reef community states. Here, I explore a potential consumer-mediated feedback on a Jamaican reef by examining how grazing by a keystone herbivore ( Diadema antillarum ) is enhanced by physical structure, which offer refugia from predation. Surveys revealed that habitat complexity and Diadema density were positively related. Increasing habitat complexity by adding physical structure significantly decreased macroalgal cover and increased the proportion of urchins in algal habitats in field manipulations. Experimental increases in urchin density also decreased macroalgal cover, but did not affect the proportion of urchins in algal habitats. These results suggest that the low habitat complexity of macroalgal-dominated reefs may inhibit an urchin-mediated shift to coral dominance and that positive feedbacks must be considered in reef restoration efforts.     

Markov chain analysis of sessile community dynamics in a degraded Philippine reef to support restoration of coral populations

Quantitative approaches are needed for assessing assisted recovery potential in degraded coral reefs. A lagoonal community (Bolinao, Philippines) that has experienced severe disturbances (overfishing, blast fishing and coral bleaching) in the past was observed for 26 months. Benthic state sequences in 4 × 4 cm patches were used to quantify monthly probabilities of transitions between reef states. Benthic cover distribution was consistent with a spatially heterogeneous Markov process, with high variability in transition probabilities within a subset of four states: crustose algae with cropped turf, the codominant sponge Callyspongia samarensis, articulated coralline algae and fleshy macroalgae (MA). Once a patch is dominated by any of these states, there is high likelihood of cycling within the set before escaping to the rarer invertebrate groups. The assemblage is unlikely to recover naturally given prevailing conditions. Patches dominated by juvenile and adult corals have mean turnover times of about 3 and 5 months, respectively, due to (partial) mortality and competition. Asymmetry was detected for coral–macroalgal competition, despite low fleshy algal cover (9.5%), that was more adverse for coral juveniles than adults. While competition between coral and the mat-forming C. samarensis was symmetrical, loss of coral cover through this path is relatively higher as a result of the higher interaction frequency. Articulated coralline algae do not appear as a constraint. Complementary strategies for assisted recovery were inferred from successional indices as well as the sensitivity of stationary coral cover to changes in transition probabilities. Results demonstrate that short-term, fine-scale observations of state variables can be used to resolve biotic constraints to inform restoration initiatives.     

Herbivory facilitates growth of a key reef‐building Caribbean coral

The decline of reef‐building corals in conjunction with shifts to short‐lived opportunistic species has prompted concerns that Caribbean reef framework‐building capacity has substantially diminished. Restoring herbivore populations may be a potential driver of coral recovery; however, the impact of herbivores on coral calcification has been little studied. We performed an exclusion experiment to evaluate the impact of herbivory on Orbicella faveolata coral growth over 14 months. The experiment consisted of three treatments: full exclusion cages; half cage procedural controls; and uncaged control plates, each with small O. faveolata colonies. We found that herbivorous fish exclusion had a substantial impact on both macroalgal cover and coral growth. Fleshy macroalgae reached 50% cover within some exclusion cages, but were almost absent from uncaged control plates. Critically, O. faveolata calcification rates were suppressed by almost half within exclusion cages, with monthly coral growth negatively related to overgrowth by fleshy macroalgae. These findings highlight the importance of herbivorous fishes for coral growth and the detrimental impact of macroalgal proliferation in the Caribbean. Policy makers and local managers should consider measures to protect herbivorous fishes and reduce macroalgal proliferation to enable coral communities to continue to grow and function.     

Effects of herbivory,nutrients, and reef protection on algal proliferation and coral growth on a tropical reef

Maintaining coral reef resilience against increasing anthropogenic disturbance is critical for effective reef management. Resilience is partially determined by how processes, such as herbivory and nutrient supply, affect coral recovery versus macroalgal proliferation following disturbances. However, the relative effects of herbivory versus nutrient enrichment on algal proliferation remain debated. Here, we manipulated herbivory and nutrients on a coral-dominated reef protected from fishing, and on an adjacent macroalgal-dominated reef subject to fishing and riverine discharge, over 152 days. On both reefs, herbivore exclusion increased total and upright macroalgal cover by 9-46 times, upright macroalgal biomass by 23-84 times, and cyanobacteria cover by 0-27 times, but decreased cover of encrusting coralline algae by 46-100% and short turf algae by 14-39%. In contrast, nutrient enrichment had no effect on algal proliferation, but suppressed cover of total macroalgae (by 33-42%) and cyanobacteria (by 71% on the protected reef) when herbivores were excluded. Herbivore exclusion, but not nutrient enrichment, also increased sediment accumulation, suggesting a strong link between herbivory, macroalgal growth, and sediment retention. Growth rates of the corals Porites cylindrica and Acropora millepora were 30-35% greater on the protected versus fished reef, but nutrient and herbivore manipulations within a site did not affect coral growth. Cumulatively, these data suggest that herbivory rather than eutrophication plays the dominant role in mediating macroalgal proliferation, that macroalgae trap sediments that may further suppress herbivory and enhance macroalgal dominance, and that corals are relatively resistant to damage from some macroalgae but are significantly impacted by ambient reef condition.     

Linking Demographic Processes of Juvenile Corals to Benthic Recovery Trajectories in Two Common Reef Habitats

Tropical reefs are dynamic ecosystems that host diverse coral assemblages with different life-history strategies. Here, we quantified how juvenile (<50 mm) coral demographics influenced benthic coral structure in reef flat and reef slope habitats on the southern Great Barrier Reef, Australia. Permanent plots and settlement tiles were monitored every six months for three years in each habitat. These environments exhibited profound differences: the reef slope was characterised by 95% less macroalgal cover, and twice the amount of available settlement substrata and rates of coral settlement than the reef flat. Consequently, post-settlement coral survival in the reef slope was substantially higher than that of the reef flat, and resulted in a rapid increase in coral cover from 7 to 31% in 2.5 years. In contrast, coral cover on the reef flat remained low (~10%), whereas macroalgal cover increased from 23 to 45%. A positive stock-recruitment relationship was found in brooding corals in both habitats; however, brooding corals were not directly responsible for the observed changes in coral cover. Rather, the rapid increase on the reef slope resulted from high abundances of broadcast spawning Acropora recruits. Incorporating our results into transition matrix models demonstrated that most corals escape mortality once they exceed 50 mm, but for smaller corals mortality in brooders was double those of spawners (i.e. acroporids and massive corals). For corals on the reef flat, sensitivity analysis demonstrated that growth and mortality of larger juveniles (21–50 mm) highly influenced population dynamics; whereas the recruitment, growth and mortality of smaller corals (<20 mm) had the highest influence on reef slope population dynamics. Our results provide insight into the population dynamics and recovery trajectories in disparate reef habitats, and highlight the importance of acroporid recruitment in driving rapid increases in coral cover following large-scale perturbation in reef slope environments.     

The status of coral reef ecology research in the Red Sea

The Red Sea has long been recognized as a region of high biodiversity and endemism. Despite this diversity and early history of scientific work, our understanding of the ecology of coral reefs in the Red Sea has lagged behind that of other large coral reef systems. We carried out a quantitative assessment of ISI-listed research published from the Red Sea in eight specific topics (apex predators, connectivity, coral bleaching, coral reproductive biology, herbivory, marine protected areas, non-coral invertebrates and reef-associated bacteria) and compared the amount of research conducted in the Red Sea to that from Australia’s Great Barrier Reef (GBR) and the Caribbean. On average, for these eight topics, the Red Sea had 1/6th the amount of research compared to the GBR and about 1/8th the amount of the Caribbean. Further, more than 50 % of the published research from the Red Sea originated from the Gulf of Aqaba, a small area (<2 % of the area of the Red Sea) in the far northern Red Sea. We summarize the general state of knowledge in these eight topics and highlight the areas of future research priorities for the Red Sea region. Notably, data that could inform science-based management approaches are badly lacking in most Red Sea countries. The Red Sea, as a geologically “young” sea located in one of the warmest regions of the world, has the potential to provide insight into pressing topics such as speciation processes as well as the capacity of reef systems and organisms to adapt to global climate change. As one of the world’s most biodiverse coral reef regions, the Red Sea may yet have a significant role to play in our understanding of coral reef ecology at a global scale.     

Interpreting coral reef monitoring data: A guide for improved management decisions

Coral reef monitoring programmes exist in all regions of the world, recording reef attributes such as coral cover, fish biomass and macroalgal cover. Given the cost of such monitoring programs, and the degraded state of many of the world’s reefs, understanding how reef monitoring data can be used to shape management decisions for coral reefs is a high priority. However, there is no general guide to understanding the ecological implications of the data in a format that can trigger a management response. We attempt to provide such a guide for interpreting the temporal trends in 41 coral reef monitoring attributes, recorded by seven of the largest reef monitoring programmes. We show that only a small subset of these attributes is required to identify the stressors that have impacted a reef (i.e. provide a diagnosis), as well as to estimate the likely recovery potential (prognosis). Two of the most useful indicators, turf algal canopy height and coral colony growth rate are not commonly measured, and we strongly recommend their inclusion in reef monitoring. The diagnosis and prognosis system that we have developed may help guide management actions and provides a foundation for further development as biological and ecological insights continue to grow.     

Episodic heterogeneous decline and recovery of coral cover in the Indian Ocean

Long-term changes in coral cover for the Caribbean and the Pacific/Southeast Asia regions (PSEA) have proven extremely useful in assessing the main drivers, magnitude and timescales of change. The one major coral reef region where such assessments have not been made is the Indian Ocean (IO). Here, we compiled coral cover survey data from across the IO into a database of ~2,000 surveys from 366 coral reef sites collected between 1977 and 2005. The compilation shows that the 1998 mass coral bleaching event was the single most important and widespread factor influencing the change in coral cover across the region. The trend in coral cover followed a step-type function driven by the 1998 period, which differs from findings in the Caribbean and the PSEA regions where declines have been more continuous and mostly began in the 1980s. Significant regional variation was observed, with most heterogeneity occurring during and after 1998. There was a significant relationship between cover and longitude for all periods, but the relationship became stronger in the period immediately after 1998. Before 1998, highest coral cover was observed in the central IO region, while this changed to the eastern region after 1998. Coral cover and latitude displayed a significant U-shaped relationship immediately after 1998, due to a large decrease in cover in the northern-central regions. Post-1998 coral cover was directly correlated to the impact of the disturbance; areas with the lowest mortality having the highest cover with India–Sri Lanka being an outlier due to its exceptionally high recovery. In 1998, reefs within Marine Protected Areas (MPAs) were more heavily impacted than unmanaged reefs, losing significantly greater total cover. MPA recovery was greater such that no differences were observed by 2001–2005. This study indicates that the regional patterns in coral cover distribution in the IO are driven mainly by episodic and acute environmental stress.     

Temporal clustering of tropical cyclones on the Great Barrier Reef and its ecological importance

Tropical cyclones have been a major cause of reef coral decline during recent decades, including on the Great Barrier Reef (GBR). While cyclones are a natural element of the disturbance regime of coral reefs, the role of temporal clustering has previously been overlooked. Here, we examine the consequences of different types of cyclone temporal distributions (clustered, stochastic or regular) on reef ecosystems. We subdivided the GBR into 14 adjoining regions, each spanning roughly 300 km, and quantified both the rate and clustering of cyclones using dispersion statistics. To interpret the consequences of such cyclone variability for coral reef health, we used a model of observed coral population dynamics. Results showed that clustering occurs on the margins of the cyclone belt, being strongest in the southern reefs and the far northern GBR, which also has the lowest cyclone rate. In the central GBR, where rates were greatest, cyclones had a relatively regular temporal pattern. Modelled dynamics of the dominant coral genus, Acropora, suggest that the long-term average cover might be more than 13 % greater (in absolute cover units) under a clustered cyclone regime compared to stochastic or regular regimes. Thus, not only does cyclone clustering vary significantly along the GBR but such clustering is predicted to have a marked, and management-relevant, impact on the status of coral populations. Additionally, we use our regional clustering and rate results to sample from a library of over 7000 synthetic cyclone tracks for the GBR. This allowed us to provide robust reef-scale maps of annual cyclone frequency and cyclone impacts on Acropora. We conclude that assessments of coral reef vulnerability need to account for both spatial and temporal cyclone distributions.

     

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.     

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.     

Local variation in herbivore feeding activity on an inshore reef of the Great Barrier Reef

Threats to coral reefs may be manifested through an increase in macroalgae. Across the globe, phase-shifts from coral to macroalgal dominance have been reported from the Caribbean, Indian and Pacific Oceans. While the Great Barrier Reef (GBR) is in relatively good condition, inshore reefs may exhibit over 50% macroalgal cover. However, our understanding of the processes preventing the macroalgal expansion remains uncertain. Using a remote video bioassay approach, this study quantified herbivory in three bays along the leeward margin of Orpheus Island. Despite significant with-in bay variation in herbivory there was no detectable statistical difference in the rates of herbivory among bays. Furthermore, of the 45 herbivore species recorded from the island, only three played a significant role in bioassay removal, Siganus canaliculatus, Siganus javus and Kyphosus vaigiensis, with only one species predominating in each bay. Reefs of the GBR may therefore be more vulnerable than previously thought, with the removal of macroalgae depending on just a few species, which exhibit considerable spatial variability in their feeding behaviour.     

Large-scale associations between macroalgal cover and grazer biomass on mid-depth reefs in the Caribbean

Since the 1970s, macroalgae have become considerably more abundant on many Caribbean reefs and overfishing of grazing fishes has been implicated as a contributory factor. We explored relationships between algal cover and grazers (biomass of herbivorous fishes and abundance of the sea-urchin Diadema antillarum) on mid-depth reefs (12-15 m) in 19 areas at seven locations in Jamaica, Barbados, Belize, Grand Cayman and Cuba, between April 1997 and April 1998. Diadema antillarum density was never >0.01 m^-2, while herbivorous fish biomass (acanthurids and scarids ⁸ cm total length) varied from 2-5 g m^-2 in Jamaica to 17.1 g m^-2 in Barbados, and was strongly correlated, negatively with macroalgal cover and positively with 'cropped' substratum (sum of 'bare', turf and crustose-coralline substrata) cover. However, overfishing of herbivorous fishes alone cannot explain the widespread abundance of macroalgae, as even on lightly fished reefs, macroalgal cover was mostly >20%. Herbivorous fish populations on those reefs were apparently only able to maintain approximately 40-60% of reef substratum in cropped states, but due to low space-occupation by coral and other invertebrates, 70-90% of substratum was available to algae. The abundance of macroalgae on lightly fished reefs may therefore be a symptom of low coral cover in combination with the continuing absence of Diadema antillarum.     

Changing dynamics of Caribbean reef carbonate budgets: emergence of reef bioeroders as critical controls on present and future reef growth potential

Coral cover has declined rapidly on Caribbean reefs since the early 1980s, reducing carbonate production and reef growth. Using a cross-regional dataset, we show that widespread reductions in bioerosion rates—a key carbonate cycling process—have accompanied carbonate production declines. Bioerosion by parrotfish, urchins, endolithic sponges and microendoliths collectively averages 2 G (where G = kg CaCO₃ m⁻² yr⁻¹) (range 0.96–3.67 G). This rate is at least 75% lower than that reported from Caribbean reefs prior to their shift towards their present degraded state. Despite chronic overfishing, parrotfish are the dominant bioeroders, but erosion rates are reduced from averages of approximately 4 to 1.6 G. Urchin erosion rates have declined further and are functionally irrelevant to bioerosion on most reefs. These changes demonstrate a fundamental shift in Caribbean reef carbonate budget dynamics. To-date, reduced bioerosion rates have partially offset carbonate production declines, limiting the extent to which more widespread transitions to negative budget states have occurred. However, given the poor prognosis for coral recovery in the Caribbean and reported shifts to coral community states dominated by slower calcifying taxa, a continued transition from production to bioerosion-controlled budget states, which will increasingly threaten reef growth, is predicted.     

Disturbance and the dynamics of coral cover on the Great Barrier Reef (1995-2009)

Coral reef ecosystems worldwide are under pressure from chronic and acute stressors that threaten their continued existence. Most obvious among changes to reefs is loss of hard coral cover, but a precise multi-scale estimate of coral cover dynamics for the Great Barrier Reef (GBR) is currently lacking. Monitoring data collected annually from fixed sites at 47 reefs across 1300 km of the GBR indicate that overall regional coral cover was stable (averaging 29% and ranging from 23% to 33% cover across years) with no net decline between 1995 and 2009. Subregional trends (10-100 km) in hard coral were diverse with some being very dynamic and others changing little. Coral cover increased in six subregions and decreased in seven subregions. Persistent decline of corals occurred in one subregion for hard coral and Acroporidae and in four subregions in non-Acroporidae families. Change in Acroporidae accounted for 68% of change in hard coral. Crown-of-thorns starfish (Acanthaster planci) outbreaks and storm damage were responsible for more coral loss during this period than either bleaching or disease despite two mass bleaching events and an increase in the incidence of coral disease. While the limited data for the GBR prior to the 1980's suggests that coral cover was higher than in our survey, we found no evidence of consistent, system-wide decline in coral cover since 1995. Instead, fluctuations in coral cover at subregional scales (10-100 km), driven mostly by changes in fast-growing Acroporidae, occurred as a result of localized disturbance events and subsequent recovery.     

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