A number of factors have recently caused mass coral mortality events in all of the world's tropical oceans. However, little is known about the timing, rate or spatial variability of the loss of reef-building corals, especially in the Indo-Pacific, which contains 75% of the world's coral reefs.
We compiled and analyzed a coral cover database of 6001 quantitative surveys of 2667 Indo-Pacific coral reefs performed between 1968 and 2004. Surveys conducted during 2003 indicated that coral cover averaged only 22.1% (95% CI: 20.7, 23.4) and just 7 of 390 reefs surveyed that year had coral cover >60%. Estimated yearly coral cover loss based on annually pooled survey data was approximately 1% over the last twenty years and 2% between 1997 and 2003 (or 3,168 km2 per year). The annual loss based on repeated measures regression analysis of a subset of reefs that were monitored for multiple years from 1997 to 2004 was 0.72 % (n = 476 reefs, 95% CI: 0.36, 1.08).
The rate and extent of coral loss in the Indo-Pacific are greater than expected. Coral cover was also surprisingly uniform among subregions and declined decades earlier than previously assumed, even on some of the Pacific's most intensely managed reefs. These results have significant implications for policy makers and resource managers as they search for successful models to reverse coral loss.
Citation: Bruno JF, Selig ER (2007) Regional Decline of Coral Cover in the Indo-Pacific: Timing, Extent, and Subregional Comparisons. PLoS ONE2(8): e711. https://doi.org/10.1371/journal.pone.0000711
Academic Editor: Rob Freckleton, University of Sheffield, United Kingdom
Received: January 30, 2007; Accepted: May 29, 2007; Published: August 8, 2007
Copyright: © 2007 Bruno, Selig. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This research was funded in part by the National Science Foundation (OCE-0326983 to J.F.B.), an EPA Star Fellowship to E.R.S, and the University of North Carolina at Chapel Hill.
Competing interests: The authors have declared that no competing interests exist.
There is growing scientific and public awareness of the widespread depletion of marine habitat-forming species, such as mangroves, seagrasses, oysters, and corals [e.g., 1,2,3]. This loss inevitably leads to the decline of the plants and animals that live in the biogenic structures created by such foundation species, and contributes to the overall degradation of marine ecosystems . For example, the reduction of coral cover on tropical coral reefs directly and rapidly causes a decline in the abundance and diversity of reef fish through the loss of structural heterogeneity , .
Scientists have recognized the ecological and economic value of coral reefs and the threats to reef-building corals for decades - and there is broad scientific consensus that coral reef ecosystems are being rapidly degraded , . Yet there is little published empirical information on regional and global patterns of coral loss  or the current state of reefs in the Indo-Pacific (Fig. 1). This region encompasses approximately 75% of the world's coral reefs (Text S1) and includes the center of global marine diversity for several major taxa including corals, fish, and crustaceans . Many previous studies have documented mass coral mortality events and ecologically significant reductions in coral cover on particular reefs -, throughout the Caribbean , and across the Great Barrier Reef , . However, the inference that this decline is a general, global phenomenon is based largely on qualitative assessments [e.g., 22,23]. The absence of regional-scale quantitative analyses of reef health in general and coral cover in particular has led to substantial confusion and disagreement about the patterns and causes of coral decline , . This shortcoming has also greatly limited our ability to measure the efficacy of different management practices designed to mitigate and reverse reef degradation , .
Here we describe a comprehensive analysis of the timing, rate, and geographic extent of the loss of coral cover across the Indo-Pacific (Fig. 1). For the purposes of this study, the Indo-Pacific region is defined by the Indonesian island of Sumatra in the west (95°E) and by French Polynesia in the east (145.5°W) (Fig. 1). We compiled a coral cover database that included 6001 quantitative surveys of 2667 subtidal coral reefs (Fig. 1, Map S1, Tables S1 and S2, Text S2) performed between 1968 and 2004. The surveys were performed by scientists or trained volunteers using either in situ or photographic/video-based measurements. Because corals facilitate so many reef inhabitants , , , living coral cover is a key measure of reef habitat quality and quantity, analogous to the coverage of trees as a measure of tropical forest loss.
This study provides the first regional scale and long-term analysis of coral cover in the Indo-Pacific. Our results indicate that the loss of coral cover began earlier than assumed and that coral cover is currently very similar across the Indo-Pacific, suggesting that coral decline is a general global phenomenon.
Our analyses were based on quantitative surveys that measured the percentage of the bottom covered by living scleractinian corals on subtidal coral reefs (1–15 m depth, mean survey depth was 6.2 m) within ten subregions of the Indo-Pacific (Fig. 1, Table S1). We included data from several sources including the published results of academic, governmental, and non-governmental organization (NGO) scientists and, for one source (Reef Check), volunteers trained and supervised by professional scientists (Table S2). We used a number of online literature search tools (e.g., ISI Web of Science and Google Scholar) to find published peer review and gray literature sources of coral cover data (Text S2) using search terms including “coral” and “cover”, “reef” and “health”. We also browsed all available issues of several relevant journals including Atoll Research Bulletin, Coral Reefs, Marine Pollution Bulletin, and the Proceedings of the International Coral Reef Symposium and similar regional symposia on reef ecology and conservation. All of the data collected before 1984 are from such published sources or ReefBase.
Coral cover data from the Australian Institute of Marine Science's (AIMS) Long Term Monitoring Program (LTMP)  were available for 1986–2004 and NGOs only began intensive reef monitoring a decade ago (Table S2). Therefore, there is a shift in the dominant data sources over time as well as a standardization of survey techniques. All reef monitoring databases that we obtained coral cover data from are publicly accessible. Portions of the coral cover data from these sources including AIMS, the National Oceanic and Atmospheric Administration (NOAA), the Hawaii Coral Reef Assessment and Monitoring Program (CRAMP), and Reef Check (Table S2) have been published independently , , , . However, they have not previously been analyzed collectively or combined with other data sources or published as a comprehensive evaluation of regional coral cover change and status.
Most surveys were based on the line transect technique or some variant to estimate coral cover. A transect (typically 10–30 m in length and usually a tape measure or chain) is placed on the reef, oriented either along a depth contour or down the reef slope. Coral cover is then estimated either in situ by recording the number of points along each transect (at either set intervals or random locations) that overlay a living hard coral (the point intercept technique) or by taking digital or film images of the bottom at these points within quadrats (usually 0.25 m2 or 1.0 m2). In most surveys, multiple transects or quadrats were used to estimate cover at a given reef, producing more than one cover value. We always pooled such replicate cover measurements from one depth/zone into a single mean estimate.
We also included data from manta tow surveys of coral cover  performed by the AIMS LTMP (1231 surveys performed at 136 reefs between 1986 and 2003). AIMS uses extensive training  and quality control procedures  to verify the validity of their manta tow surveys, which are unbiased and highly comparable to surveys based on video transects . The manta tow technique is frequently used to perform broadscale reef surveys [e.g., 34]. Because we were not able to verify the validity and reproducibility of manta tow surveys performed by other organizations, we only included AIMS manta tow data in our analyses.
Reef monitoring data
Most of the reefs in the database were surveyed only once, but a subset of 651 reefs were surveyed two or more times (Table S3). In most cases, transects or manta tow paths on these monitoring sites were permanently marked or recorded using GPS so that the exact same location on each reef could be resurveyed in subsequent years. There are more monitoring sites on the GBR than within other subregions, especially from 1984 to 1996. However, 67% of the monitoring sites were within the other nine subregions, and some other subregions including the Philippines and mainland Asia also had a relatively large number of monitoring sites (Table S3).
Linear repeated measures regression analysis was used to test the null hypothesis that there was no relationship between coral cover and time from 1968 to 2004. We were unable to perform a formal meta-analysis because several critical components (e.g., variance estimates, sample size, repeated sampling of each reef, etc.) were not available for all data sets. We used Stata (version 9.1, STATA Corp.) and performed two sets of analyses: (1) on the annual subregional means based on all 6001 surveys, and (2) on the data from the 651 monitoring sites. In both analyses, time (year) and coral cover were treated as continuous variables. Because locations were repeatedly sampled over time, coral cover estimates of a given subregion or reef in different years were not independent. This longitudinal structure was incorporated into the statistical model by using repeated measures of subregions or reefs. Thus, statistical estimates of the absolute net decline in coral cover were based on the individual trajectories of subregions or reefs and were not derived by pooling all the data for each year. For these and all other analyses, data were transformed when necessary to meet basic statistical assumptions.
In the subregion analysis, we used the mean cover in each subregion for each year as the dependent variable, rather than the individual reef means, in part because the sample size varied greatly among years, periods, and subregions. Performing this analysis on yearly subregional averages equalizes the influence of each subregion and prevents the results from being driven primarily by especially well-sampled subregions like the GBR and the Philippines (Table S3). However, this procedure did not remove the influence of either intentionally or unintentionally biased sampling within subregions that could have caused the estimated coral cover means to differ from the true subregional population means.
For the analysis of the reef monitoring data, we performed four repeated measures regression analyses to test the null hypothesis and estimate the slope of significant linear functions during the entire 36 year range and for each of the three periods: 1970–1983, 1984–1996, and 1997–2004. The period delineations were based on the timing of major disturbance events and expected and observed trends in coral cover in the Indo-Pacific. For example, the beginning of the third period (1997–2004) coincides with a major global mass-bleaching event in 1998 and 1999 , , fairly rapid declines in coral cover in several subregions between 1996 and 1998 (Fig. S1), and the beginning of an eight year decline of mean regional coral cover. We also repeated the analysis of the last two time periods without the GBR monitoring sites to assess their influence.
Estimates of the rate of coral loss could be influenced by year-to-year and period-to-period changes in the location of reef surveys. For example, if surveys initially focused on high cover reefs or subregions and then shifted focus to low cover reefs, the estimated rate of regional or subregional coral loss could be exaggerated. Alternatively, an initial overrepresentation of low cover reefs or subregions could underestimate the true rate of net coral loss. This problem is diminished in the monitoring sites analysis because individual reefs are monitored through time and reef identity is far less variable. Nevertheless, the identity of monitored reefs did change over time (e.g., when new reefs and subregions were added), so this potential source of bias was not entirely eliminated. A second potential bias in the analyses is the overrepresentation of the best-sampled subregions, mainly the Philippines and the GBR. Therefore, the regression results are not necessarily representative of all ten subregions, especially those that were not well monitored.
Because the effects of a variety of disturbances on coral cover are depth-dependent –, , spatial and temporal variability of the depth of reef surveys could complicate our analyses. Therefore we conducted an extensive analysis of the potential confounding effects of depth on our subregional comparisons and rate estimations (Text S3, Table S4).
Results and Discussion
Our results indicate that coral cover on Indo-Pacific reefs is currently lower and far more uniform than expected (Fig. 2A). The region-wide average was only 22.1% in 2003 (95% CI: 20.7, 23.4, n = 390 reefs) and did not vary significantly among subregions (Kruskal-Wallis p = 0.19, ANOVA p = 0.40, Power = 0.91 when δ = 3)(Fig. 2A). A number of factors thought to influence coral reef resilience including management resources and enforcement, coral diversity, and human population density and social structure, vary substantially among the ten subregions , . Therefore, the observed uniformity of the average coral cover in 2003 across the entire region is one of the most surprising results of our analysis.
(a) Cover (means ± 1 SE) in ten subregions of the Indo-Pacific. Data are from 2003 for seven subregions and from 2002 for three subregions not adequately sampled after 2002 (Hawaiian Islands, Taiwan & Japan, and Western Pacific). Values above the bars are the number of reefs surveyed in each subregion. (b-i) Histograms illustrating percent coral cover in the Indo-Pacific and selected subregions during different periods. (d) is based on .
The general absence of quantitative data on reef health has led to several misconceptions about the causes, patterns, and best remedies for global coral decline. For example, in 2003, coral cover on the Great Barrier Reef (GBR), considered the “best-managed”  and “one of the most ‘pristine’ coral reefs in the world” , was not significantly greater than on reefs in the Philippines and other subregions that are often thought to be highly threatened and poorly managed . Additionally, based on the impression that Hawaiian reefs were “far further down the trajectory of decline” [than reefs in the Caribbean and Australia] a recent essay  argued for a total overhaul of U.S. coral reef management policy. But our analysis suggests that coral cover in the main Hawaiian islands, including frequently visited reefs close to urban and tourism centers, appears to have been as high as GBR cover over the last two decades (Fig. 2A; also see Fig. S5). However, we necessarily combined data from surveys using different techniques and protocols for site selection which could have exaggerated or obscured differences in coral cover among subregions (Text S4).
Additionally, there are other important measures of reef degradation, in particular the abundance and diversity of reef inhabitants . It is possible that there is currently greater variance in metrics such as fish biomass among subregions of the Indo-Pacific. However, for these metrics there is far less available information, substantial natural variance across the region due to differences in local productivity and reef connectivity, and greater uncertainty about historical baselines. Thus direct geographic comparisons would be more difficult. The focus of this investigation was coral cover; given the key role that corals play in facilitating the entire reef ecosystem, coral cover is a critical measure of habitat loss and degradation. Nonetheless, there is an urgent need for similar regional-scale comparative studies of the health of populations of commercially and ecologically important reef inhabitants.
Historically, i.e., 100–1000 y.b.p., average coral cover in the Indo-Pacific was probably approximately 50% . Generating natural baselines to estimate the long-term impact of human activities on species and ecosystems is always difficult, particularly in the ocean since records are rarely kept until a resource is already significantly depleted . Humans have affected fringing reefs close to inhabited islands for hundreds of years via overfishing and land use practices that lead to increased sedimentation , . But these effects were localized and it is doubtful that humans significantly influenced regional or subregional average coral cover before the twentieth century. Some of the earliest quantitative Indo-Pacific reef surveys reported local coral cover of nearly 90% . However, it is unlikely that such values represented regional or even subregional averages, even when the Indo-Pacific was pristine. Coral reefs have always been affected by a variety of natural disturbances including severe storms that can drastically reduce coral cover , , . Even in a pristine, pre-human state, some proportion of reefs within a subregion would be in a state of recovery from a recent disturbance, thereby reducing subregional coral cover averages.
We may never know the precise Indo-Pacific coral cover baseline, but we now know that regionally, cover is currently at least 20% below the best historical reference points. Our results suggest that average Indo-Pacific coral cover declined from 42.5% during the early 1980s (95% CI: 39.3, 45.6, n = 154 reefs surveyed between 1980 and 1982) to 22.1% by 2003 (Fig. 3A); an average annual cover loss of approximately 1% or 1,500 km2. However, coral cover fluctuated somewhat throughout the 1980s and the regional average was still 36.1% in 1995 (95% CI: 34.2, 38.0, n = 487), subsequently declining by 14% in just seven years (or 3,168 km2 year−1). We used repeated measures regression analysis based on the individual trajectories of subregions or reefs (for the analysis of the reef monitoring data) to quantitatively estimate the absolute net decline of coral cover. Estimates based on subregional means and the reef monitoring data (a subset of the entire database) for similar periods were nearly identical (Table 1) and were slightly lower than estimates based on annual pooling (described above).
(a) White bars represent Indo-Pacific coral cover and open symbols (right axis) are the number of reefs surveyed each year. (b) Coral cover in ten Indo-Pacific subregions in each of three periods. Plotted values are means±1 SE and values above each bar are the subregional sample sizes. * = no data were available
The estimated annual rate of coral cover loss in the Caribbean between 1977 and 2001 was approximately 1.5%, with the greatest decline occurring during the 1980s . In contrast, the estimated net annual loss of global humid tropical rainforest was only 0.4 % from 1990–1997 . Additionally, the spatial patterns of coral reef degradation are very different from rainforest loss in that nearly all reefs have been affected; there are virtually no remaining pristine reefs and very few with coral cover close to the historical average (Fig. 2C). Remarkably, in 2003, only 4% of the 390 surveyed Indo-Pacific reefs had coral cover >50% and only 2% had cover >60%. In contrast, cover was ≥50% on nearly a third of the reefs surveyed between 1980 and 1983 (Fig. 2B). This striking shift in the distribution of coral cover is apparent in several subregions (Figs. 2B–H). For example, a landmark study of Philippine reef health in 1981  found that coral cover was greater than 25% on 68% of 559 surveyed reefs. Twenty years later, only 26% of reefs in the Philippines had cover greater than 25% (Figs. 2D & E).
Regional and subregional trends in coral cover during the 1970s are less clear than for more recent periods because fewer surveys were performed, few subregions were adequately sampled, and 77% of surveyed reefs prior to 1973 were on the GBR. Therefore, it is unlikely that the regional cover average of 30% between 1968 and 1972 (95% CI: 23.5, 35.5, n = 70) is representative of all subregions, particularly those that did not experience outbreaks of Acanthaster plancii, a corallivorous sea star that substantially reduced cover on many GBR reefs . Acanthaster predation had similar effects in Guam, Fiji, Palau and other locations over the last forty years and is a principle cause of coral loss in several subregions , . But many Indo-Pacific reefs affected by Acanthaster in the 1960s and 1970s partially or wholly recovered by the early 1980s , , . Our analysis of coral cover data from the 651 reef monitoring sites reflects this recovery (Table 1). Cover on 110 reefs monitored between 1970 and 1983 increased significantly, which is concordant with documented cases of local increases in coral cover following major disturbances prior to this period [e.g., 48,47]. Coral cover on the reef monitoring sites did not change significantly between 1984 and 1996 but has declined substantially since 1997 (0.72% per year, 95% CI: 0.36, 1.08).
Our analysis suggests that the regional-scale coral decline in the Indo-Pacific began several decades earlier than often assumed. For example, Pandolfi et al.  and others ,  have argued that due to greater coral diversity, superior management practices, and a variety of historical socio-economic factors, coral cover on Indo-Pacific reefs in general and on the GBR in particular declined much more recently than in the Caribbean. However, our results indicate Indo-Pacific coral cover was already quite low, and in some subregions substantially declining during the 1960s and 1970s (Fig. 3 and Fig. S1). This finding is consistent with often overlooked published studies over the last forty years that documented localized coral decline in the Indo-Pacific, particularly after Acanthaster outbreaks. For example, Endean and Stablum  quantified the collapse of coral cover on 19 reefs on the GBR to 16.8±5.6 % (mean±1 SE) by 1970, fifteen years before similar broad scale coral mortality was observed in the Caribbean , .
Comparing the timing and rate of coral decline among Indo-Pacific subregions is difficult because many were not adequately sampled until the early 1980s. Furthermore, historic baseline coral cover may have varied among subregions due to differences in disturbance frequency or the morphology of dominant species. For example, reefs dominated by plating acroporiid corals probably had higher baseline cover than reefs dominated by branching corals. Thus, similar current cover among subregions could actually reflect variability in the degree of coral loss. Additionally, the dependence of facilitation and other ecosystem functions on coral cover could vary among subregions (e.g., 20% cover might not be universally functionally equivalent).
Between 1984 and 1996, coral cover was slightly lower in east Indonesia than on the GBR (Fig. 3B). However, cover in several other subregions was substantially higher during this period, particularly in mainland Asia, Taiwan and Japan, and west Indonesia (Fig. 3B & S2). Absolute coral cover in these subregions declined by 10–20% between 1996 and 1998, possibly due in part to El Niño-related bleaching , . Well-documented mass coral bleaching events driven by elevated seawater temperatures have caused coral mortality throughout the Indo-Pacific, particularly in 1998, 1999, and 2002 , , , .
Major storms, though not novel disturbances, are considered primary causes of recent coral loss in several locations including Hawaii and Moorea , . Infectious coral disease epidemics are not thought to be as prevalent or important in the Pacific as they are in the Caribbean , although this could be largely due to limited Indo-Pacific disease research . In fact, recent surveys of coral diseases on the GBR indicate that disease frequency increased dramatically over the last five years, particularly on the outer GBR  and following periods when water temperature was anomalously high , . In addition to these regional-scale stressors, more localized human impacts have also caused coral losses. Examples include sedimentation from urban development and agriculture in Hong Kong and Papua New Guinea, respectively , , , and destructive fishing practices such as blast fishing and muro-ami (a form of destructive net fishing) in Indonesia and the Philippines .
Despite the well-documented effects of several causes of mass coral mortality, there is substantial evidence that coral communities remain resilient, often recovering in ten to thirty years after major disturbances , , , , . However, such “recovery,” loosely defined as a return to pre-disturbance coral cover, often does not mean a return to original coral species composition because the recovery of slow-growing species can take centuries. Such compositional shifts can influence reef geomorphology, the structure of associated invertebrate and fish communities, and resilience to future disturbances.
Average GBR coral cover has been consistently below 27% since 1986 (Fig. S1). But this subregional stability, also apparent in most other subregions over the last ten years (Fig. S1), masks complex within-subregion dynamics (Figs. 4A & B). The cover and trajectories of individual reefs, in many cases separated by only a few kilometers, remains surprisingly unpredictable. This small scale spatial asynchrony in coral cover is likely caused in part by the highly localized effects of even regional scale disturbances, including predator and disease outbreaks and thermal anomalies that cause coral bleaching , . The frequency and spatial variability of these disturbances have prevented recovery at subregional and regional scales despite significant local increases in coral cover on many reefs. Such asynchrony also increases intra-annual variability, reducing the amount of variance explained by time in the regression analyses.
The results of our analysis of 6001 quantitative reef surveys indicate that the degree, geographic extent, and duration of the Indo-Pacific coral decline have been significantly underestimated. Many coral reef scientists know of exceptions to the general pattern of reef degradation: there are currently many, perhaps hundreds or even thousands of high coral cover (i.e., >60%) reefs in the Indo-Pacific and Caribbean that resemble the presumed historical coral baseline [e.g.,59]. But our results indicate that such observations are anomalies and currently represent less than 2% of reefs in the Indo-Pacific. This study also highlights the urgent need for conservation policies to restore coral reefs and the ecosystem services they provide, estimated to be worth $23,100–$270,000 km−2 year−1 . Halting and reversing coral loss will require actions across a range of scales including local restoration and conservation of herbivores that facilitate coral recruitment ,  and the reduction of fishing practices that directly kill corals , the implementation of regional land use practices that reduce sedimentation and nutrient pollution , and the institution of global policies to reduce anthropogenic ocean warming and acidification , .
The loss of coral cover represents both an absolute loss and a reduction in the quality of reef habitat . Coral reefs, like nearly all aquatic and terrestrial habitats, are hierarchically organized and are wholly dependent on the presence of the foundation species that generate the physical reef framework . Ecosystem management should also be hierarchical and begin with the preservation of foundation species. Unfortunately, most marine conservation policies focus on the commercially harvested occupants of these habitats. Such remedies will fail unless we gather the scientific knowledge and political will needed to effectively reduce the stressors degrading corals and other marine foundation species.
Calculation of Indo-Pacific reef area
(0.03 MB DOC)
Analysis of potential effects of depth on coral cover estimates
(0.05 MB DOC)
Potential biases in survey techniques and site selection
(0.05 MB DOC)
The number of surveyed reefs in the ten Indo-Pacific subregions.
(0.05 MB DOC)
Characteristics of the eight basic sources of coral cover data.
(0.05 MB DOC)
Number of monitoring sites in the ten Indo-Pacific subregions during each of three periods (note most monitoring sites were surveyed for more than one period).
(0.05 MB DOC)
Results of linear repeated measures regression analyses on the relationship between coral cover and time in the Indo-Pacific. Unlike the results presented in Table 1, these analyses include survey depth as a covariate. The effect of depth was non-significant (Subregional analysis p = 0.90, Monitoring sites p = 0.60). Results presented in the table are for the time effect. n = total number of observations
(0.04 MB DOC)
Patterns of coral cover decline in ten Indo-Pacific subregions. Black bars are mean coral cover ± 1 SE for each year (missing bars are years in which no data are available). Open symbols (right axis) are the number reefs surveyed in each subregion during each year (note changes in scale).
(0.73 MB EPS)
We thank R. Aronson, K. France, W. Precht and P. Reynolds for helpful comments on the manuscript, A. Melendy for assistance with statistical analysis, and K. France, R. Katz, L. Ladwig, S. Lee, M. O'Connor, C. Shields, G. Smelick and I. Vu for assistance with data collection. We are especially grateful to the many organizations that shared their published and unpublished data with us, including the Australian Institute of Marine Science, the Great Barrier Reef Marine Park Authority, the Hawaii Coral Reef Assessment and Monitoring Program, the National Oceanic and Atmospheric Administration, the Nature Conservancy, ReefBase, Reef Check, the World Resources Institute, and the thousands of divers who collected the data.
Conceived and designed the experiments: JB ES. Performed the experiments: JB ES. Analyzed the data: JB ES. Contributed reagents/materials/analysis tools: JB ES. Wrote the paper: JB ES.
- 1. Silliman BR, van de Koppel J, Bertness MD, Stanton LE, Mendelssohn IA (2005) Drought, snails, and large-scale die-off of southern U.S. salt marshes. Science 310: 1803–1806.BR SillimanJ. van de KoppelMD BertnessLE StantonIA Mendelssohn2005Drought, snails, and large-scale die-off of southern U.S. salt marshes.Science31018031806
- 2. Lotze HK, Lenihan HS, Bourque BJ, Bradbury RH, Cooke RG, et al. (2006) Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312: 1806–1809.HK LotzeHS LenihanBJ BourqueRH BradburyRG Cooke2006Depletion, degradation, and recovery potential of estuaries and coastal seas.Science31218061809
- 3. Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, et al. (2006) A global crisis for seagrass ecosystems. Bioscience 56: 987–996.RJ OrthTJB CarruthersWC DennisonCM DuarteJW Fourqurean2006A global crisis for seagrass ecosystems.Bioscience56987996
- 4. Bruno JF, Bertness MD (2001) Habitat modification and facilitation in benthic marine communities. In: Bertness MD, Gaines SD, Hay ME, editors. Marine Community Ecology. Sunderland, MA: Sinauer. pp. 201–218.JF BrunoMD Bertness2001Habitat modification and facilitation in benthic marine communities.MD BertnessSD GainesME HayMarine Community EcologySunderland, MASinauer201218
- 5. Jones GP, McCormick MI, Srinivasan M, Eagle JV (2004) Coral decline threatens fish biodiversity in marine reserves. Proc Natl Acad Sci USA 101: 8251–8253.GP JonesMI McCormickM. SrinivasanJV Eagle2004Coral decline threatens fish biodiversity in marine reserves.Proc Natl Acad Sci USA10182518253
- 6. Graham NAJ, Wilson SK, Jennings S, Polunin NVC, Bijoux JP, et al. (2006) Dynamic fragility of oceanic coral reef ecosystems. Proc Natl Acad Sci USA 103: 8425–8429.NAJ GrahamSK WilsonS. JenningsNVC PoluninJP Bijoux2006Dynamic fragility of oceanic coral reef ecosystems.Proc Natl Acad Sci USA10384258429
- 7. Grigg RW, Dollar SJ (1990) Natural and anthropogenic disturbance on coral reefs. In: Dubinski Z, editor. Ecosystems of the world: coral reefs. Amsterdam: Elsevier. pp. 439–452.RW GriggSJ Dollar1990Natural and anthropogenic disturbance on coral reefs.Z. DubinskiEcosystems of the world: coral reefsAmsterdamElsevier439452
- 8. Wilkinson CR (1993) Coral reefs of the world are facing widespread devastation: can we prevent this through sustainable management practices? Proceedings of the Seventh International Coral Reef Symposium 1: 11–21.CR Wilkinson1993Coral reefs of the world are facing widespread devastation: can we prevent this through sustainable management practices?Proceedings of the Seventh International Coral Reef Symposium11121
- 9. Sebens KP (1994) Biodiversity of coral reefs: what are we losing and why? American Zoologist 34: 115–133.KP Sebens1994Biodiversity of coral reefs: what are we losing and why?American Zoologist34115133
- 10. Knowlton N (2001) The future of coral reefs. Proc Natl Acad Sci USA 98: 5419–5425.N. Knowlton2001The future of coral reefs.Proc Natl Acad Sci USA9854195425
- 11. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, et al. (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301: 929–933.TP HughesAH BairdDR BellwoodM. CardSR Connolly2003Climate change, human impacts, and the resilience of coral reefs.Science301929933
- 12. Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301: 958–960.TA GardnerIM CôtéJA GillA. GrantAR Watkinson2003Long-term region-wide declines in Caribbean corals.Science301958960
- 13. Burke L, Selig E, Spalding M (2002) Reefs at risk in Southeast Asia. Washington, DC: World Resources Institute. L. BurkeE. SeligM. Spalding2002Reefs at risk in Southeast Asia.Washington, DCWorld Resources Institute72
- 14. Roberts CM, McClean CJ, Veron JEN, Hawkins JP, Allen GR, et al. (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295: 1280–1284.CM RobertsCJ McCleanJEN VeronJP HawkinsGR Allen2002Marine biodiversity hotspots and conservation priorities for tropical reefs.Science29512801284
- 15. Done T (1992) Constancy and change in some Great Barrier Reef coral communities: 1980–1990. American Zoologist 32: 655–662.T. Done1992Constancy and change in some Great Barrier Reef coral communities: 1980–1990.American Zoologist32655662
- 16. Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265: 1547–1551.TP Hughes1994Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef.Science26515471551
- 17. Aronson RB, Precht WF, Macintyre IG, Murdoch TJT (2000) Coral bleach-out in Belize. Nature 405: 36.RB AronsonWF PrechtIG MacintyreTJT Murdoch2000Coral bleach-out in Belize.Nature40536
- 18. Bruno JF, Siddon CE, Witman JD, Colin PL, Toscano MA (2001) El Niño related coral bleaching in Palau, Western Caroline Islands. Coral Reefs 20: 127–136.JF BrunoCE SiddonJD WitmanPL ColinMA Toscano2001El Niño related coral bleaching in Palau, Western Caroline Islands.Coral Reefs20127136
- 19. Edmunds PJ, Elahi R (2007) The demographics of a 15-year decline in cover of the Caribbean reef coral Montastraea annularis. Ecological Monographs 77: 3–18.PJ EdmundsR. Elahi2007The demographics of a 15-year decline in cover of the Caribbean reef coral Montastraea annularis.Ecological Monographs77318
- 20. Ninio R, Meekan M, Done T, Sweatman H (2000) Temporal patterns in coral assemblages on the Great Barrier Reef from local to large spatial scales. Marine Ecology Progress Series 194: 65–74.R. NinioM. MeekanT. DoneH. Sweatman2000Temporal patterns in coral assemblages on the Great Barrier Reef from local to large spatial scales.Marine Ecology Progress Series1946574
- 21. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429: 827–833.DR BellwoodTP HughesC. FolkeM. Nyström2004Confronting the coral reef crisis.Nature429827833
- 22. Wilkinson C, editor. (2002) Status of coral reefs of the world: 2002. Townsville, Australia: Australian Institute of Marine Science. C. Wilkinson2002Status of coral reefs of the world: 2002.Townsville, AustraliaAustralian Institute of Marine Science378
- 23. Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, et al. (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301: 955–958.JM PandolfiRH BradburyE. SalaTP HughesKA Bjorndal2003Global trajectories of the long-term decline of coral reef ecosystems.Science301955958
- 24. Grigg RW, Dollar SJ (2005) Reassessing U.S. coral reefs. Science 308: 1740.RW GriggSJ Dollar2005Reassessing U.S. coral reefs.Science3081740
- 25. Pandolfi JM, Jackson JBC, Baron N, Bradbury RH, Guzman HM, et al. (2005) Are U.S. coral reefs on the slippery slope to slime? Science 307: 1725–1726.JM PandolfiJBC JacksonN. BaronRH BradburyHM Guzman2005Are U.S. coral reefs on the slippery slope to slime?Science30717251726
- 26. Aronson RB, Precht WF (2006) Conservation, precaution, and Caribbean reefs. Coral Reefs 25: 441–450.RB AronsonWF Precht2006Conservation, precaution, and Caribbean reefs.Coral Reefs25441450
- 27. Idjadi JA, Edmunds PJ (2006) Scleractinian corals act as facilitators for other invertebrates on a Caribbean reef. Marine Ecology Progress Series 319: 117–127.JA IdjadiPJ Edmunds2006Scleractinian corals act as facilitators for other invertebrates on a Caribbean reef.Marine Ecology Progress Series319117127
- 28. Sweatman H, Abdo D, Burgess S, Cheal A, Coleman G, et al. (2003) Long-Term Monitoring of the Great Barrier Reef: Status Report Number 6. Townsville: Australian Institute of Marine Science. H. SweatmanD. AbdoS. BurgessA. ChealG. Coleman2003Long-Term Monitoring of the Great Barrier Reef: Status Report Number 6.TownsvilleAustralian Institute of Marine Science
- 29. Hodgson G (1999) A global assessment of human effects on coral reefs. Marine Pollution Bulletin 38: 345–355.G. Hodgson1999A global assessment of human effects on coral reefs.Marine Pollution Bulletin38345355
- 30. Jokiel PL, Brown EK, Friedlander A, Ku'ulei Rogers S, Smith WR (2004) Hawai'i coral reef assessment and monitoring program: spatial patterns and temporal dynamics in reef coral communities. Pacific Science 58: 159–174.PL JokielEK BrownA. FriedlanderS. Ku'ulei RogersWR Smith2004Hawai'i coral reef assessment and monitoring program: spatial patterns and temporal dynamics in reef coral communities.Pacific Science58159174
- 31. Miller I, Müller R (1997) A quality control procedure for observer agreement of manta tow benthic cover estimates. Proc 8th Int Coral Reef Symp 2: 1475–1478.I. MillerR. Müller1997A quality control procedure for observer agreement of manta tow benthic cover estimates.Proc 8th Int Coral Reef Symp214751478
- 32. Miller IR, De'ath G (1996) Efects of training on observers' performance in assessing benthic cover by means of the manta tow technique. Mar Freshwater Res 47: 19–26.IR MillerG. De'ath1996Efects of training on observers' performance in assessing benthic cover by means of the manta tow technique.Mar Freshwater Res471926
- 33. Miller I, Müller R (1999) Validity and reproducibility of benthic cover estimates made during broadscale surveys of coral reefs by manta tow. Coral Reefs 18: 353–356.I. MillerR. Müller1999Validity and reproducibility of benthic cover estimates made during broadscale surveys of coral reefs by manta tow.Coral Reefs18353356
- 34. Montebon ARF (1997) Status of coral reefs in Negros Oriental, Central Philippines. Proc 8th Int Coral Reef Symp 1: 295–300.ARF Montebon1997Status of coral reefs in Negros Oriental, Central Philippines.Proc 8th Int Coral Reef Symp1295300
- 35. Berkelmans R, De'ath G, Kininmonth S, Skirving WJ (2004) A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions. Coral Reefs 23: 74–83.R. BerkelmansG. De'athS. KininmonthWJ Skirving2004A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions.Coral Reefs237483
- 36. Endean R, Stablum W (1973) The apparent extent of recovery of reefs of Australia's Great Barrier Reef devastated by the crown-of-thorns starfish. Atoll Research Bulletin 168: 1–41.R. EndeanW. Stablum1973The apparent extent of recovery of reefs of Australia's Great Barrier Reef devastated by the crown-of-thorns starfish.Atoll Research Bulletin168141
- 37. Connell JH (1997) Disturbance and recovery of coral assemblages. Coral Reefs 16, suppl.s101–s113.JH Connell1997Disturbance and recovery of coral assemblages.Coral Reefs16, suppl.s101s113
- 38. Connell JH, Hughes TP, Wallace CC (1997) A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecological Monographs 67: 461–488.JH ConnellTP HughesCC Wallace1997A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time.Ecological Monographs67461488
- 39. Salvat B (2002) Status of southeast and central Pacific coral reefs ‘Polynesia Mana Node’: Cook Islands, French Polynesia, Kiribati, Niue, Tokelau, Tonga, Wallis and Futuna. In: Wilkinson C, editor. Status of coral reefs of the world: 2002. Townsville, Australia: Australian Institute of Marine Science. pp. 203–215.B. Salvat2002Status of southeast and central Pacific coral reefs ‘Polynesia Mana Node’: Cook Islands, French Polynesia, Kiribati, Niue, Tokelau, Tonga, Wallis and Futuna.C. WilkinsonStatus of coral reefs of the world: 2002Townsville, AustraliaAustralian Institute of Marine Science203215
- 40. Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423: 280–283.RA MyersB. Worm2003Rapid worldwide depletion of predatory fish communities.Nature423280283
- 41. Wing SR, Wing ES (2001) Prehistoric fisheries in the Caribbean. Coral Reefs 20: 1–8.SR WingES Wing2001Prehistoric fisheries in the Caribbean.Coral Reefs2018
- 42. Dana TF (1979) Species-numbers relationships in an assemblage of reef-building corals: McKean Island, Phoenix Islands. Atoll Research Bulletin 228: 1–42.TF Dana1979Species-numbers relationships in an assemblage of reef-building corals: McKean Island, Phoenix Islands.Atoll Research Bulletin228142
- 43. Stoddart DR (1974) Post-hurricane changes on the British Honduras reefs: re-survey of 1972. Proceedings of the Second International Coral Reef Symposium 2: 473–483.DR Stoddart1974Post-hurricane changes on the British Honduras reefs: re-survey of 1972.Proceedings of the Second International Coral Reef Symposium2473483
- 44. Achard F, Eva HD, Stibig H-J, Mayaux P, Gallego J, et al. (2002) Determination of deforestation rates of the world's humid tropical forests. Science 297: 999–1002.F. AchardHD EvaH-J StibigP. MayauxJ. Gallego2002Determination of deforestation rates of the world's humid tropical forests.Science2979991002
- 45. Gomez ED, Alcala AC, San Diego AC (1981) Status of the Philippine coral reefs – 1981. Proceedings of the Fourth International Coral Reef Symposium, Manila 1: 275–282.ED GomezAC AlcalaAC San Diego1981Status of the Philippine coral reefs – 1981.Proceedings of the Fourth International Coral Reef Symposium, Manila1275282
- 46. Chesher RH (1969) Destruction of Pacific corals by the sea star Acanthaster planci. Science 165: 280–283.RH Chesher1969Destruction of Pacific corals by the sea star Acanthaster planci.Science165280283
- 47. Lourey MJ, Ryan DAJ, Miller IR (2000) Rates of decline and recovery of coral cover on reefs impacted by, recovering from and unaffected by crown-of-thorns starfish Acanthaster planci: a regional perspective of the Great Barrier Reef. Marine Ecology Progress Series 196: 179–186.MJ LoureyDAJ RyanIR Miller2000Rates of decline and recovery of coral cover on reefs impacted by, recovering from and unaffected by crown-of-thorns starfish Acanthaster planci: a regional perspective of the Great Barrier Reef.Marine Ecology Progress Series196179186
- 48. Colgan MW (1987) Coral reef recovery on Guam (Micronesia) after catastrophic predation by Acanthaster planci. Ecology 68: 1592–1605.MW Colgan1987Coral reef recovery on Guam (Micronesia) after catastrophic predation by Acanthaster planci.Ecology6815921605
- 49. Berkelmans R, Oliver JK (1999) Large-scale bleaching of corals on the Great Barrier Reef. Coral Reefs 18: 55–60.R. BerkelmansJK Oliver1999Large-scale bleaching of corals on the Great Barrier Reef.Coral Reefs185560
- 50. Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12: 1–17.PW Glynn1993Coral reef bleaching: ecological perspectives.Coral Reefs12117
- 51. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research 50: 839–866.O. Hoegh-Guldberg1999Climate change, coral bleaching and the future of the world's coral reefs.Marine and Freshwater Research50839866
- 52. Harmelin-Vivien ML, Laboute P (1986) Catastrophic impact of hurricanes on atoll outer reef slopes in the Tuamotu (French Polynesia). Coral Reefs 5: 55–62.ML Harmelin-VivienP. Laboute1986Catastrophic impact of hurricanes on atoll outer reef slopes in the Tuamotu (French Polynesia).Coral Reefs55562
- 53. Aronson RB, Precht WF (2001) White-band disease and the changing face of Caribbean coral reefs. Hydrobiologia 460: 25–38.RB AronsonWF Precht2001White-band disease and the changing face of Caribbean coral reefs.Hydrobiologia4602538
- 54. Willis BL, Page CA, Dinsdale EA (2004) Coral disease on the Great Barrier Reef. In: Rosenberg E, Loya Y, editors. Coral Health and Disease. Berlin: Springer-Verlag. pp. 69–104.BL WillisCA PageEA Dinsdale2004Coral disease on the Great Barrier Reef.E. RosenbergY. LoyaCoral Health and DiseaseBerlinSpringer-Verlag69104
- 55. Selig ER, Harvell CD, Bruno JF, Willis BL, Page CA, et al. (2006) Analyzing the relationship between ocean temperature anomalies and coral disease outbreaks at broad spatial scales. In: Phinney J, Hoegh-Guldberg O, Kleypas J, Skirving W, Strong A, editors. Coral reefs and climate change: science and management. Washington, DC: American Geophysical Union. pp. 111–128.ER SeligCD HarvellJF BrunoBL WillisCA Page2006Analyzing the relationship between ocean temperature anomalies and coral disease outbreaks at broad spatial scales.J. PhinneyO. Hoegh-GuldbergJ. KleypasW. SkirvingA. StrongCoral reefs and climate change: science and managementWashington, DCAmerican Geophysical Union111128
- 56. Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, et al. (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biology 5: e124.JF BrunoER SeligKS CaseyCA PageBL Willis2007Thermal stress and coral cover as drivers of coral disease outbreaks.PLoS Biology5e124
- 57. ISRS (2004) The effects of terrestrial runoff of sediments, nutrients and other pollutants on coral reefs. Briefing Paper 3: International Society for Reef Studies. ISRS2004The effects of terrestrial runoff of sediments, nutrients and other pollutants on coral reefs. Briefing Paper 3: International Society for Reef Studies.18
- 58. McManus JW, Reyes RB Jr, Nañola CL Jr (1997) Effects of some destructive fishing methods on coral cover and potential rates of recovery. Environmental Management 21: 69–78.JW McManusRB Reyes JrCL Nañola Jr1997Effects of some destructive fishing methods on coral cover and potential rates of recovery.Environmental Management216978
- 59. Idjadi JA, Lee SC, Bruno JF, Precht WF, Allen-Requa L, et al. (2006) Rapid phase-shift reversal on a Jamaican coral reef. Coral Reefs 25: 209–211.JA IdjadiSC LeeJF BrunoWF PrechtL. Allen-Requa2006Rapid phase-shift reversal on a Jamaican coral reef.Coral Reefs25209211
- 60. Edmunds PJ, Carpenter RC (2001) Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef. Proc Natl Acad Sci USA 98: 5067–5071.PJ EdmundsRC Carpenter2001Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef.Proc Natl Acad Sci USA9850675071
- 61. Mumby PJ, Harborne AR, Williams J, Kappel CV, Brumbaugh DR, et al. (2007) Trophic cascade facilitates coral recruitment in a marine reserve. Proc Natl Acad Sci USA 104: 8362–8367.PJ MumbyAR HarborneJ. WilliamsCV KappelDR Brumbaugh2007Trophic cascade facilitates coral recruitment in a marine reserve.Proc Natl Acad Sci USA10483628367
- 62. Guinotte JM, Buddemeier RW, Kleypas JA (2003) Future coral reef habitat marginality: temporal and spatial effects of climate change in the Pacific basin. Coral Reefs 22: 551–558.JM GuinotteRW BuddemeierJA Kleypas2003Future coral reef habitat marginality: temporal and spatial effects of climate change in the Pacific basin.Coral Reefs22551558
- 63. Côté IM, Gill JA, Gardner TA, Watkinson AR (2005) Measuring coral reef decline through meta-analyses. Philosophical Transactions of the Royal Society B-Biological Sciences 360: 385–395.IM CôtéJA GillTA GardnerAR Watkinson2005Measuring coral reef decline through meta-analyses.Philosophical Transactions of the Royal Society B-Biological Sciences360385395