ISRN Oceanography

Volume 2013 (2013), Article ID 739034, 18 pages

http://dx.doi.org/10.5402/2013/739034

Review Article

Coral Reef Resilience through Biodiversity

Caroline S. Rogers

US Geological Survey, Southeast Ecological Science Center, Caribbean Field Station, St. John, VI 00830, USA

Received 12 September 2012; Accepted 18 October 2012

Academic Editors: D. Alongi and C. Grenz

Copyright © 2013 Caroline S. Rogers. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract.

Irrefutable evidence of coral reef degradation worldwide and increasing pressure from rising seawater temperatures and ocean acidification associated with climate change have led to a focus on reef resilience and a call to “manage” coral reefs for resilience. Ideally, global action to reduce emission of carbon dioxide and other greenhouse gases will be accompanied by local action. Effective management requires reduction of local stressors, identification of the characteristics of resilient reefs, and design of marine protected area networks that include potentially resilient reefs. Future research is needed on how stressors interact, on how climate change will affect corals, fish, and other reef organisms as well as overall biodiversity, and on basic ecological processes such as connectivity. Not all reef species and reefs will respond similarly to local and global stressors. Because reef-building corals and other organisms have some potential to adapt to environmental changes, coral reefs will likely persist in spite of the unprecedented combination of stressors currently affecting them. The biodiversity of coral reefs is the basis for their remarkable beauty and for the benefits they provide to society. The extraordinary complexity of these ecosystems makes it both more difficult to predict their future and more likely they will have a future.

1. Introduction

Increasing concern over worldwide deterioration of coral reefs and the likelihood that global climate change will cause further degradation has led to a focus on the concept of reef resilience. Local, regional, and global stressors have the potential to cause irreversible losses of biodiversity in some reefs and consequently of the ecosystem services they provide [1–9]. Even the physical structure of some coral reefs may be in jeopardy. Can these reefs recover and persist? Can they be managed for resilience? The future of many reefs will depend on whether fundamental processes like photosynthesis, calcification, and recruitment can continue in the face of a multitude of local and global stressors. Reefs that previously could recover after a disturbance may not be able to survive the assaults of global climate change, especially when combined with local pressures.

The limits of our current knowledge of the biodiversity of coral reefs, of the potential for corals and other reef species to adapt to climate change, and of the effects of increasing sea water temperatures, ocean acidification, and other components of climate change on reef organisms make it challenging to predict what the future holds for coral reefs. As Vitousek et al. [10, page 498] observed, “we are changing Earth more rapidly than we are understanding it.” Ten years ago, Walther et al. [11] noted that marine and terrestrial ecosystems were already being affected by human-driven changes in the climate.

This paper reviews and synthesizes scientific literature that provides insights into the future for coral reefs in the face of climate change and explores the concept that biodiversity could help confer resilience. It evaluates the potential for management to reverse degradation, identifies some key research priorities, and explores the possibility that coral reefs will prove to be resilient primarily because of their inherent complexity and biodiversity.

2. What Is Resilience?

Resilience is not a new concept. In 1973, Holling [12, page 14] defined it as “a measure of the persistence of systems and of their ability to absorb change and disturbance and still maintain the same relationships between populations or state variables.” He differentiated it from stability which he defined as “the ability of a system to return to an equilibrium state after a temporary disturbance—the more rapidly it returns and the less it fluctuates, the more stable it would be.” Holling noted that the spruce budworm forest community in eastern Canada, which experiences budworm outbreaks and shifts in dominance of different tree species, is highly unstable but the instability confers high resilience. Holling did not discuss any marine examples. It is possible that coral reefs are relatively stable ecological systems which are less likely to be resilient than other ecosystems when disturbed. Reef scientists still debate the relative stability of coral reefs with some suggesting that some reefs are stable while others are not [13–15]. At least some of the disagreement comes from the consideration and interpretation of reef response over different spatial and temporal scales (see [16]). For example, some might conclude that a reef that recovered to its initial coral cover 100 years after a major disturbance was stable while others would disagree.

Although the word resilience is sometimes used to encompass resistance, greater clarity is achieved by making a distinction between the two [14, 17]. Resilience commonly refers to the ability to rebound, while resistance refers to the quality of opposing or withstanding. When applied to coral reefs, resistance can refer to the ability of the entire reef or of individual corals and other organisms to remain unaffected by a stress. For example, fragile, branching corals are more likely to be damaged by storm waves than massive corals which could be thought of as more resistant.

In essence, coral reef resilience can be thought of as the capacity for the reef to recover after disturbance or stress. The term recovery has been used in many ways. In his review of 65 quantitative studies of coral abundance worldwide, Connell [18] defined recovery as an increase in coral abundance (cover) but he noted that such recovery did not necessarily imply a return to the reef’s former structure and function, including colony size structure, species composition, and diversity of functional aspects such as growth and reproduction. However, as Done [19, p. 128] noted, the most stringent definition of the point in time when recovery can be considered complete, in ecological and geological terms, “would be the restitution of prior diversity, mix of colony growth forms (if not species), colony size, frequency distributions, and structural extent and complexity of reef framework (after Johannes [20]).” Although the concept of resilience is based on the capacity to recover, it broadens the perspective to include the consideration of factors (such as connectivity) that contribute to resilience beyond the boundaries of the specific disturbed location (see [21]).

3. Signs of Coral Reef Stress

The most recent International Coral Reef Symposium (July 2012) produced a Consensus Statement that was signed by hundreds of scientists and managers recognizing the severity of climate change and calling for global action to reduce emission of carbon dioxide and other greenhouse gases. The previous symposium, in 2008, issued a Call to Action, noting that coral reefs are on the brink of collapse, primarily because of the actions of humans. Major concerns include increasing levels of carbon dioxide, overfishing, and coastal development ([22–24]).

Disturbances (also referred to as stressors or stresses) can vary greatly. Lugo and Snedaker [25, page 56] state “The term stress is used—to describe any action or influence which retards or restricts the normal functioning or development of living biological units (species, populations, communities, or whole systems). Stress can be construed as a drain of potential energy that would otherwise be available for other ecological purposes.”

Stressors can be acute or chronic, natural or anthropogenic, direct or indirect. Some are far harder to evaluate and manage than others. Damage from anchors is easier to understand than the effects of overfishing, and the effects of greenhouse gas emissions and ocean acidification are particularly difficult to comprehend and address [2, 26, 27]. Some stressors, like hurricanes, are clearly natural and impossible to control and some, like sewage input, are clearly associated with human actions and therefore possible to manage. Diseases of corals and other reef organisms, which are becoming of increasing concern, are poorly understood, and currently not possible to classify exclusively as natural or anthropogenic.

Some reefs have changed so much in terms of their dominant organisms that they have been described as undergoing a phase shift, usually involving the replacement of corals with macroalgae as the dominant benthic component. There has not been consensus on what constitutes dominance by corals, meaning that it is not possible to state just when major shifts have occurred [28, 29]. Although there is discussion of communities shifting from dominance by corals to dominance by macroalgae above a certain threshold, that threshold has not been rigorously or consistently defined. Furthermore, there has been insufficient discussion of the temporal aspect of phase shifts—in other words, how long must the change persist to be considered a shift? Another complicating factor is that macroalgal abundance varies greatly, and single values for macroalgal cover recorded during annual surveys may or may not accurately reflect the influence of macroalgae on the reef for the entire year. After an extensive analysis of reef studies from 1996 to 2006, Bruno et al. [29] concluded that the replacement of corals by macroalgae as a dominant benthic component has been less extensive and common than many have assumed. Phase shifts were less common in the Indo-Pacific than in the Caribbean (see also [30]). They acknowledge that major shifts may have occurred before most reef surveys began.

In many cases, there have been significant losses of living coral and increases in algae (e.g., [19, 31–33]). In one of the best examples, Jamaican reef zones over a depth range of 7 m to 35 m exhibited a phase shift (by any definition) from a combination of natural and human stressors with significant declines in coral cover (from over 50% down to less than 5%) and increases in macroalgal cover to over 90% [33]. A loss of herbivorous fish and urchins decreased the resilience of these reefs, and little recovery has occurred [21].

Some argue that phase shifts are reversible while alternate stable states are not, and they conclude that coral reefs for the most part have exhibited reversible phase shifts, leading to the hope that the degradation can be reversed [34] Several recent papers have debated the applicability of the terms phase shift and alternate stable states/regime shifts [28, 34, 35].

Regardless of the terms used to characterize changes on reefs, and whether or not all would agree that shifts have occurred, the focus needs to be on whether or not the coral reef can recover to its former condition and composition following disturbance, in particular anthropogenic disturbance. Decreases in coral cover may be large enough to warrant concern and action even in cases where no shifts are apparent.

3.1. Global Stressors

Recently global climate change (GCC) has been described as the single greatest threat to coral reefs (e.g., [23, 36]). However, it is important to keep in mind that GCC is not a single threat. It encompasses higher temperatures, sea level rise, ocean acidification, and changes in major storm patterns (e.g., [27, 37, 38]). The various, inherently different components of GCC need to be differentiated as they will have varying effects on reefs and closely linked ecosystems such as seagrass beds and mangroves, which have received much less attention than reefs. This review focuses particularly on warming and acidification because they are potentially the most damaging.

It is now clear that human actions are affecting the earth’s atmosphere and that CO₂ and other gases will increase within the next 50 years [27, 39–42]. In less than four decades, by the middle of this century, mean atmospheric CO₂ over 500 ppm is expected, along with an increase of 2°C or more in mean global temperature and an increase in mean overall acidity of over 60% ([43, 44]). There are constraints on our ability to predict how this changing climate will affect coral reefs, particularly how they will respond to warmer, more acidic oceans [27, 37, 45, 46]. The most conspicuous effects of climate-driven change on reefs are the bleaching episodes that have been increasing in frequency in association with higher seawater temperatures [47–50], (Figure 1).

Figure 1: Coral bleaching in the Keppel Islands, Australia, 2006. (photo by R. Berkelmans).

Bleaching reflects the loss of zooxanthellae pigments after disintegration and expulsion of zooxanthellae [51, 52]. Both the visible and ultraviolet components of solar radiation can act alone or together to increase the likelihood of bleaching by decreasing the temperature threshold above which it occurs [51, 53–55]. The host coral and zooxanthellae are both affected by the production of reactive oxygen species associated with thermal stress [51]. High seawater temperatures do not always result in extensive bleaching of corals and other reef organisms, as rainfall and overcast conditions (not currently accounted for in most climate models) can reduce the stress contributed by concomitant high irradiance [56, 57]. Sometimes bleaching is very widespread as in 1998 when reefs were affected globally, but it can be regional as in the Caribbean in 2005 or very localized, as local current patterns can reduce the stress from high temperatures [58].

Global climate change, according to a model developed by Bender et al. [59], is expected to decrease the overall frequency of tropical cyclones but double the frequency of the most powerful storms (categories 4 and 5) by the end of this century. Hurricanes can be very destructive (e.g., [60, 61]), however reef damage is often patchy, varying from zone to zone, over a gradient of depths, and even within zones [62]. Swells from huge storms can alter light and current patterns by rearranging the physical structure and local topography [61]. Predicted decreases in the aragonite saturation state of reef waters from GCC could make corals more fragile and vulnerable to storms [19]. In addition, physical damage might lead to more coral disease [63, 64]. A decrease in the structural complexity of reefs could affect fish recruitment and survival [65]. However, these intense storms also can have positive effects—they can move sediments off of reefs into deeper water [62] and lower water temperature, decreasing the likelihood of coral bleaching events [66]. Florida reefs had less bleaching in 2005 than reefs in the northeastern Caribbean, partly because several hurricanes tracked over or close to the reefs in Florida but not those in Puerto Rico and the US Virgin Islands.

Calcification is obviously fundamental to the development and survival of coral reefs. Erez et al. [67] noted “the existence of these wave resistant structures in spite of chemical, biological, and physical erosion depends on their exceedingly high rates of calcification.” Ocean acidification associated with elevated CO₂ (and lower pH levels) could have particularly severe consequences for coral reefs because of its effects on calcification, the process responsible for overall reef architecture [27, 67–71]. Reefs may collapse into rubble and dissolve, possibly as early as 2050 when CO₂ concentrations reach 560 ppm [67, 72, 73]. However, Pandolfi et al. [46] suggest that these predictions are too dire. Although some scientists have suggested that corals could move poleward to escape warming temperatures, other constraints such as lower light regimes and reduced aragonite saturation could prevent reefs from forming in these higher latitudes [45, 74].

We need to know more about the links among different stressors, for example among high seawater temperatures, bleaching, and coral disease [75–81]. (Bleaching is a disease but it is differentiated here from diseases associated with initial tissue loss (see [82]).) Disease prevalence often is correlated with higher seawater temperatures [83]. It seems logical that thermally stressed corals would be more likely to become diseased [84], but not many studies conclusively demonstrate this connection. In one of the few studies of multiple diseases over a wide geographic area, Cróquer and Weil [78, 79] explored the link between bleaching severity in 2005 and disease prevalence a year later on reefs from Bermuda, Puerto Rico, Grand Cayman, Panama, Curacao, and Grenada. Although they found a significant correlation between the percent of bleached corals and disease prevalence, some sites with intense bleaching did not have increase in disease. Based on six years of data from 48 sites on the Great Barrier Reef, Selig et al. [75] and Bruno et al. [76] found a high correlation between high temperatures and disease. However thermal stress was not correlated with the severity of bleaching [85].

Bleaching is sometimes, although not always, followed by an outbreak of coral disease involving tissue loss (mortality), and disease outbreaks are not always preceded by bleaching [76, 80, 86–88]. Diseased corals can be more susceptible to bleaching [77]. We also need to determine the relationship between diseases and excessive nutrients or other effects of human mismanagement [89–91].

Interestingly, two comprehensive review papers [49, 74] barely mention coral diseases, perhaps because many reports of significant outbreaks and of new diseases have been quite recent, since these reviews were published. Several recent papers on reef resilience have failed to even mention coral diseases or have not addressed them sufficiently. Coral diseases have caused significant levels of mortality in the Caribbean [87, 92, 93], and they are of increasing concern in the Indian and Pacific Oceans (e.g., [76, 94, 95]). It is possible that in some studies based on insufficiently frequent monitoring at least some coral mortality attributed to bleaching was actually from disease. Coral diseases are complex, involving corals, the environment, and associated microbial communities [96–98]. New research approaches using genetics and molecular biology could help demonstrate the shifts in the microbiota that occur when a coral becomes diseased and help reveal how the coral holobiont responds to particular stresses [99, 100].

4. Where, in the World, Have Reefs Recovered?

An examination of reefs that have recovered or are recovering would help identify the characteristics that confer resistance and resilience. Unfortunately, there are remarkably few examples of reefs recovering significantly after disturbances, and even fewer after the removal of anthropogenic stressors. Most reports of recovery have been for relatively short periods of time and over small spatial scales (in the Caribbean: [101–104]; in the Eastern Pacific: [105]; in the Great Barrier Reef, Australia, [106], but see [107]). In Kaneohe Bay, Hawaii, diversion of sewage resulted in an increase in coral cover [108, 109], although cover by the invasive algae increased a few years later and then decreased once again [110].

To date no one has documented a persistent reversal of a phase shift (or a severely degraded reef) back to initial coral cover and coral community composition over a large spatial scale on a Caribbean reef [28]. Increases in the density of the grazing sea urchin Diadema antillarum, following its epidemic die-off in the 1980s, have been associated with greater coral recruitment in Jamaica [111, 112]. After mortality from bleaching in 2005 reversed some of these gains [104, 113], coral cover is once again increasing [104].

Pacific reefs may recover more easily than Caribbean reefs [18, 114], but there are too few examples of significant reef recovery to allow a rigorous evaluation of this concept. Fifteen years ago, Connell [18] reviewed studies that had been conducted for a minimum of four years and found declines in coral cover without significant recovery in 57% of the sites from the Western Atlantic and only 29% of sites in the Indo-Pacific. All sites that recovered in terms of coral cover (29% of the total) were in the Indo-Pacific. He attributed the greater likelihood of recovery in the Indo-Pacific to the greater frequency of acute disturbances (e.g., Acanthaster predation, hurricanes) in the Indo-Pacific and chronic disturbances in the Western Atlantic (e.g., overfishing, decreases in herbivory, coastal construction). Halford et al. [107] found complete recovery of corals and nearly total recovery of fish assemblages over 80 km of the Great Barrier Reef about a decade after major storm damage. Monitoring of sites across 1300 km of the Great Barrier Reef (1995 to 2009) indicated increases in coral cover for some reefs but decreases for others [115]. Recently, De’ath et al. [9] reported a loss of over 50% coral cover along the Great Barrier Reef from 1985 to 2012 based on surveys of 214 reefs, attributing the decline to cyclones (48%), Crown-of Thorns starfish (42%), and bleaching (10%).

Roff and Mumby [30] identify a number of factors that could result in Caribbean reefs potentially having less resilience than reefs in the Indo-Pacific, including lower biomass and diversity of herbivores, lack of acroporid corals, and faster rates of macroalgal growth. They note the significant role that disease has played, particularly in causing the loss of acroporid populations in the Caribbean. The higher levels of disease in the Caribbean, affecting almost all of the coral species, not just Acropora palmata and A. cervicornis, should also be considered [93].

Some examples of reef resistance to, or resilience after, bleaching can be found. Diaz-Pulido et al. [106] noted rapid recovery of Acropora spp. colonies on reefs in the Great Barrier Reef that had been almost completely killed by bleaching and subsequent colonization by macroalgae. Coral recruitment, regrowth of corals, and seasonal die-off of the algae contributed to the increased coral cover within just one year of the disturbances. In Moorea, the abundance of butterflyfishes and corals returned to former levels after an outbreak of the crown-of-thorns starfish, bleaching, and hurricanes, but the species composition of the corals and fish differed greatly [116].

In Jamaica, bleaching in 2005 led to a decrease in the size classes of most of the coral species at fringing reef study sites with some but not all species showing an increase in mean size class by 2008 [104]. Colonies of all species increased in abundance by 2008. However, in the US Virgin Islands, widespread bleaching in 2005 was followed by a disease outbreak that led to an average decrease in coral cover of c. 60% [87], and little increase in coral cover has been observed since then (J. Miller, National Park Service (NPS), unpublished data). In the summer/fall of 2010, moderate to severe bleaching occurred again on these reefs, but diseases caused less mortality (J. Miller, NPS, unpublished data.). The less severe bleaching in 2010 does not necessarily demonstrate increased resistance of the corals that survived the 2005 episode to bleaching as the temperature patterns preceding each of the two events differed in terms of number of days above a threshold of 29.5°C and the rates of temperature increase in the preceding spring and summer (J. Miller, pers. obs., NPS and C. Rogers, US Geological Survey (USGS), unpublished data).

In the Caribbean both Acropora palmata and A. cervicornis declined significantly beginning in the late 1970s [13, 117, 118]. A few studies document some recovery of these species (listed as threatened under the US Endangered Species Act in 2006), but there are currently insufficient data to know if they will ever return to their former abundance and size frequency distributions, (Figure 2).

(a)

(b)

Figure 2: Some Acropora palmata zones in the Caribbean have recovered while others have not. Photos from St. John, US Virgin Islands. (photos by C. Rogers).

Recently, Graham et al. [119] used a meta-analysis to explore reef recovery based on 22 publications with data from a total of 48 sites in the Pacific and Atlantic. They included only studies where there had been a decrease of at least 10% in coral cover after a pulse disturbance—most after bleaching. They considered recovery any increase in coral cover after disturbance, no matter how small. It is not clear if any of the reef areas returned to the initial level of coral cover present before the disturbance. Graham et al. [119] noted that none of the studies included sufficient information on ecological characteristics that could potentially play a role in promoting recovery such as structural complexity, fish diversity, and algal cover. Only two were found from the Caribbean (in Belize and St. John, US Virgin Islands). However, the report from St. John [120] was from a reef where coral cover later declined dramatically [87]. Miller et al. [87] reported an increase in coral cover at two out of four long-term monitoring sites in St. John and St. Croix from 2000 to 2004 but then, as noted above, quantified an average decline of about 60% of coral cover following bleaching and disease in 2005/2006.

More research is needed to identify the characteristics of resistant and resilient reefs in the face of all components of global climate change. Resilience will vary depending on the stressor. To date, most of the focus has been on increasing seawater temperatures. Limited evidence suggests that reefs are more likely to resist or to recover from thermal stress if they have experienced high temperature variability over prolonged periods, have corals with thermally tolerant symbionts, are protected from high irradiance, are found where currents are strong (and perhaps where upwelling occurs), have high abundance of herbivorous fishes, and are connected to sources of larvae to replenish degraded populations.

5. Management of Coral Reefs under a Changing Climate

The year 2010 was the International Year of Biodiversity. A recent assessment shows that the 1992 Convention on Biological Diversity failed to meet its goal of substantially reducing the loss of global biodiversity by 2010 [121]. In addition, the IUCN Red List Index for corals declined dramatically indicating increased risk of extinction for corals (see also [122]). Only about 0.5% of the ocean is currently protected [121]. Coral reefs comprise less than 0.1% of the ocean, and only about 4.9% of them are inside no-take areas (less that 1% outside of Australia). Only 6% of the total tropical coral reef area (estimated as 250,000 sq km) is in marine protected areas (MPAs) that are considered effective, with 13% partially effective [23].

Besides reducing the loss of biodiversity and maintaining ecosystem services, scientists have stated other goals for coral reefs, including preventing or reversing phase shifts, and “managing coral reefs for resilience” [35, 123]. Does it matter what the goal is? Would management be different for biodiversity conservation than for resistance to bleaching or to conserve areas that can seed “down current” areas?

Although management priorities can sometimes be contradictory, most would agree that the overall goal is to maintain biodiversity and ecosystem services, and that there are limited management options beyond control of local stressors associated with human actions, such as coastal development (e.g., [17]), establishment of effective networks of marine reserves [58, 124], and increasing protection of reefs that are likely to be more resistant and resilient [125–127].

Managing a coral reef means to do whatever feasible to reduce the stressors affecting the reef. Reef managers can only attempt to control what humans are doing on a local basis—they cannot lower seawater temperature and stop bleaching from occurring. The goal is not to manage for reefs with fewer species that may be better able to cope with storms or thermal stress associated with GCC but rather to attempt to manage whatever stressors we can control in order to reverse the degradation ultimately leading back to original reef structure and function.

Côté and Darling [128] state that “management that controls local stressors to reverse degradation and recover original species assemblages will actually increase the proportion of sensitive taxa within the assemblage and may effectively decrease ecosystem resilience to climate change." However, many scientists would agree that the goal is not maintenance of a resilient reef of low biodiversity but rather the recovery of a reef with the highest biodiversity and coral cover possible for the given location. The concept of sensitive taxa is misleading, as shifts in relative abundance of coral species are much more likely than elimination of coral species. In the US Virgin Islands, after severe bleaching and disease in 2005/2006, species in the Montastraea annularis complex declined significantly but remained the most abundant. Almost all species were affected, and even the most sensitive (Agaricia agaricites) survived [87]. Côté and Darling [128] seem to assume that species will respond the same way each time they are stressed, for example during a bleaching event. However, this is not the case (e.g., [129]). We know that species vary in their responses to these events and that individual coral colonies within a species can show a variety of responses ranging from complete recovery to total mortality (e.g., [130]). Species that are very susceptible to increased temperatures in one location may bleach less in another [129]. In addition, coral species may be more susceptible to some disturbances, including different aspects of climate change, than others. For example, the Caribbean branching species Acropora cervicornis is more vulnerable to storm damage than massive coral species but less likely to be affected by increases in sedimentation [60, 131].

In contrast to the recommendation by Côté and Darling [128] that more protection be given to less diverse reefs with more resistant coral species, the models developed by Baskett et al. [125] indicate that “protecting diverse coral communities is critical, and protecting communities with higher abundances of more thermally tolerant coral species and symbiont types secondary, to the long-term maintenance of coral cover.” We need to conserve species (and their interactions) because we do not know which ones are most critical to ecosystem functioning and which ones might provide resilience [132]. Neither Côté and Darling [128] nor Baskett et al. [125] explicitly address coral mortality from storms, and increased storm frequency and intensity is predicted with GCC.

Some studies have attempted to identify reefs that have the highest likelihood of persisting under climate change, using both empirical data and models [126, 127]. McClanahan et al. [126, 127] sought to identify reefs that were likely to be resilient and which also had moderate to high diversity and low to moderate exposure to high temperatures and other factors associated with climate change. They found some potential refugia within the West Indian Ocean but acknowledged it was difficult to clearly identify locations that would meet all the necessary criteria. Berkelmans [133] examined the history of bleaching at several reefs on the Great Barrier Reef (Australia) and suggested that corals on some of the reefs had become acclimatized to high seawater temperature, perhaps through zooxanthellae shuffling [134–136] or selection of more resistant holobionts, leading to an increase in bleaching thresholds.

It only makes sense to control local stressors to increase the chances that reefs can withstand the onslaught of global climate change. Different human-related stressors differentially affect processes like coral growth, recruitment, mortality, and competition with macroalgae, and therefore, possible responses to and recovery after thermal stress or other disturbances. Consequently, local management priorities could change given specific, local conditions [125, 130]. Wooldridge and Done [137] showed that improving water quality at Great Barrier Reef sites, specifically reducing excess nutrients, could effectively increase the upper thermal threshold for coral bleaching—providing a concrete example of how control of local stressors could increase reef resistance. Carilli et al. [138] examined cores of Montastraea faveolata from four sites off Belize, and found that the 1998 bleaching event reduced extension (growth) rates at all locations. The growth rates of corals from sites stressed by sedimentation, nutrients, high human population, and fishing pressure had not recovered eight years later, but growth rates of corals from less stressed sites were back to prebleaching rates in three years.

Entire reef zones could respond differently to management actions. Mumby and Hastings [139] used a model based on empirical data to explore the consequences of increased grazing by parrotfish and found that the higher grazing pressure would lead to greater coral recovery on deeper zones (7–15 m) than on shallow zones (3–6 m deep). Although the increase in grazing was higher in the shallower reefs, the effects on coral were negligible because grazing intensity was already high enough to move the modeled reefs towards a coral rather than a macroalgal state.

5.1. Marine Reserves: One of the Most Promising Tools

Establishment of marine protected areas (MPAs), specifically marine reserves, is one of the most promising tools for reef conservation [140]. Marine reserves are defined here as “no take zones” where fishing and most or all other extractive activities are prohibited. Marine reserves can be very effective in reversing the effects of overfishing (e.g., [141]), but it is not clear if reefs within marine reserves would be better able to cope with the disturbances associated with climate change. Although we might intuitively think that reefs within marine reserves would be more resistant to disturbance or resilient after disturbance, there is much uncertainty and little evidence to date. Establishment of marine reserves often leads to an increase in formerly harvested species and could result in increases in coral cover if the intensity of grazing increases, allowing more coral recruitment [142]. In an experimental study that confirms the role of herbivory in reef resilience, Hughes et al. [143] used exclusion cages to manipulate the density of herbivorous fishes on reef areas that bleached in 1998. They found that coral cover increased in control areas but not in caged areas where macroalgae increased.

McCook et al. [144] point out that the potential benefits for reef-building corals are even more important than those documented for fishes, because the whole ecosystem depends on these corals. The marine reserves they examined on the Great Barrier Reef had fewer outbreaks of the starfish Acanthaster planci and, consequently, higher coral cover. However, they acknowledge that our understanding of how reserves can benefit corals is still limited. Mumby and Harborne [145] found increased coral cover within reserves in the Bahamas attributable to higher grazing by parrotfishes. Kramer and Heck [146] compared herbivorous fishes, coral cover, and species richness between small marine reserves (called Special Protected Areas, or SPAs) and nearby unprotected areas in the Florida Keys Marine Sanctuary. Outside the reserves, they found higher coral cover and number of coral species and a lower abundance of the larger herbivorous fish species. However, they did not examine trends over time in these parameters from the establishment of the SPAs several years before their study began, and no data are available for initial coral cover. No difference in coral or macroalgal cover was detected after 10 years of protection (no-take) at Glover’s Reef, Belize [147]. It is not surprising that some papers have reported no difference for reefs inside and outside MPAs, given that these studies were not restricted to areas that were marine reserves with effective enforcement (see [148]).

Some studies have shown significant coral declines even within no-take zones, attributable to bleaching [149]. The 2005 bleaching episode in the Caribbean, which was at least partly associated with climate change [40], was followed by a disease outbreak which led to substantial losses in coral cover within and outside of a marine protected area [87].

In the Philippines, Raymundo et al. [150] found lower coral disease prevalence inside MPAs (no-take) with more diverse reef-fish communities than in unprotected areas. The density of coral-feeding butterflyfishes (Chaetodontidae) was significantly related to the prevalence of disease for sites with ≥50% coral cover. They hypothesized that these fishes are vectors of disease and more abundant outside reserves because fishing removes their predators. This would not necessarily be true in the Caribbean, where there are fewer Chaetodontid species feeding directly on corals and coral cover is typically less than 50%.

Large declines in coral cover from bleaching, sedimentation, and Crown-of-Thorns starfish in both marine reserves and unprotected areas in Papua New Guinea resulted in a surprising decrease in abundance of over 75% of reef fish species including many that are not obligate associates of living coral [151]. Species that depended on living coral for juvenile recruitment were the most affected. This study showed a close link between fish biodiversity and the condition of the coral habitat.

In general, Caribbean coral reefs have not only lost coral cover but have become structurally less complex over the last several decades primarily because of coral diseases and hurricanes [152]. Further research is needed on how reef structure is related to biodiversity. Preliminary studies of reefs in three marine parks (Bonaire, Puerto Rico, and St. Vincent and the Grenadines) revealed that overall species richness (including not only corals, but also fish and many other groups) was highest on reefs with the highest topographical (structural) complexity at Bonaire and Puerto Rico [153]. Coral cover and complexity tended to be correlated, but highest coral species richness was not always associated with the highest topographical complexity.

McClanahan et al. [126] noted a possible surprising disadvantage to the creation of marine reserves in the West Indian Ocean, the promotion of faster-growing but more bleaching-susceptible coral species. In this case, a management strategy could lead to differential coral mortality. However, it is not clear that such protected areas (fisheries closures) would lead to more coral species that are more susceptible to thermal stress in other geographic areas. Bleaching susceptibility among Caribbean corals is not always quantifiable or consistent.

Models can help to identify the best locations for establishing MPAs or a network of MPAs to provide protection to reefs from climate change. For example, Mumby et al. [58] used a model to suggest placement of protected areas where thermal stress has been relatively low. They note that integrating connectivity into the design of marine reserves is challenging partly because of the “bewildering number of connections within the system.” Ideally, MPAs would be a source of larvae to replenish degraded, unprotected areas. Baskett et al. [125] used models to show that corals on reefs linked to reefs with lower seawater temperatures, and less thermal stress, could more effectively withstand climate change. However, reefs are subject to many stressors and it is unlikely that they can be protected from all aspects of climate change. In addition, hurricanes, expected to increase in frequency, can actually benefit reefs by lowering seawater temperatures. In 2005, reefs in Florida suffered more physical damage from storms than those in the USVI and Puerto Rico, but they did not experience such severe bleaching or subsequent disease outbreaks [87, 154].

In designing reserves and networks of reserves, it is important to identify sinks and sources of marine larvae ([155, 156]) and to consider the entire, integrated seascape of habitats, particularly mangroves, seagrass beds, and coral reefs [157]. However, even the best-designed networks of marine protected areas could be ineffective if global warming changes the characteristics of connectivity [158]. Ideally, connectivity should be included in the design of these networks.

6. Connectivity: A Prerequisite for Resilience

Recovery of degraded coral reefs depends to a large extent on connectivity with sources of larvae of corals, fish, and other reef organisms and on their successful settlement and growth ([159, 160]). Climate change is likely to change existing connectivity dynamics [158]. Much more information is needed on localized current patterns and duration of larval viability. We also need to understand how climate change will affect coral reefs, mangroves, and seagrass beds, and the biological and physical connections among these ecosystems. They are linked because of the movement of fishes at all life stages and the transport of nutrients ([157, 160, 161]). Seagrass beds and mangroves are critical nurseries, providing food and shelter, for larvae of fish and invertebrates that later move to coral reefs. Reefs buffer shoreward seagrass beds and mangroves from destructive ocean waves, and seagrass beds and mangroves reduce harmful runoff of freshwater and sediments from land that could affect reefs.

Recovery of reefs requires larvae to replenish depleted populations of corals, fish, and other organisms. Complex water current patterns combine with the life histories of key organisms to determine if larvae will be available to help reefs recover. Global warming could affect current patterns with consequences for larval transport; higher water temperatures could shorten pelagic fish larval duration effectively reducing the spatial scale of connectivity [158]. Models are not only helpful but essential in showing connections among coral reefs (inside and outside marine reserves) as well as among reefs, seagrass beds, and mangroves. In some locations, these ecosystems are closely linked; if reefs collapse, seagrass beds and mangroves could also collapse. Reefs that are closely connected to mangroves and seagrass beds might be more resilient, less vulnerable to climate change, than those that are not, or those that are remote [162]. For example, although more research is needed, it is possible that mangroves and seagrass beds would be a source of herbivorous fishes that would influence grazing pressure on reefs affected by bleaching, keeping algae in check while corals recover. Many fish depend on two or more of these habitats for daily movements to find shelter and food or at different stages of their development. In a study in Puerto Rico, the highest mean number of species and density for fishes in mangroves were found where the surrounding seascape (within 100 m of mangroves) was most heterogeneous and provided shelter and settlement sites—with high cover of seagrasses, proximity to coral reefs, and deeper water [157]. Because juveniles of many fish species use shallow seagrass, coral reef, and mangrove habitats, if one habitat declines, others might remain available [157, 163].

Mumby and Hastings [139] used models of Caribbean reefs to show that deeper reefs (7–15 m) near mangroves were better able to recover from intense storms than those that were not linked to mangroves because the mangroves supported a high abundance of parrotfish that reduced cover of macroalgae that compete with corals. Mangroves have suffered even greater degradation and destruction than coral reefs [164].

Reefs, mangroves, and seagrass beds will vary in their response to individual components of climate change—for example, in general mangroves are less likely to be affected by GCC, but rising sea level has been identified as possibly the greatest threat to these systems (e.g., [165]). In contrast, rising sea level could benefit some reef zones and would probably not affect seagrass beds significantly. Growth of seagrasses (and other noncalcifying organisms) could actually increase [166]. All of these tropical ecosystems have already been affected greatly by human activities [167].

7. Biodiversity and Resilience

We currently lack some very basic information, particularly on the biodiversity of coral reefs. It is likely that over 90% of the estimated number of coral reef species in the world (estimates range from one to two million) have not even been discovered yet [169–171]. We are no doubt losing species that we have not even identified. The 2010 Census of Marine Life [171] reports discovery of at least 6, 000 new species, some associated with coral reefs. As Knowlton [3] points out, we know very little about how human activities affect coral reef biodiversity. For many species we even lack sufficient information on ecological functions and life histories, and on distribution of their habitats [15, 167]. We also do not fully understand how species richness affects ecosystem processes and how biodiversity affects ecosystem function and services [5, 7, 132, 172].

Willis and Bhagwat [173] examined models that predict how climate change will affect terrestrial biodiversity. They showed that more refined models that considered local topography and what they termed “microclimate buffering” predicted different (usually lower) rates of extinction for many systems. It is likely that their cautionary comments would apply to models for coral reefs and climate change as well.

Further research on how different reef species will respond to global stressors (combined with local ones) is of the highest priority [65, 158]. Little is known of how different species are reacting to the various stressors and how they will react to the increasing effects of climate change [27, 174]. Coral species vary in their susceptibility to bleaching [175, 176], (Figure 3).

Figure 3: A bleached colony of Diploria labyrinthiformis, near unbleached colonies of Colpophyllia natans, Porites porites, Porites astreoides, and Millepora alcicornis, St. John, US Virgin Islands (from [168]).

We need to have a better understanding of the molecular and physiological mechanisms that determine the tolerance of coral hosts and zooxanthellae to different stressors [99, 177]. Although some corals may be able to adapt to higher seawater temperatures (see [178, 179]), we do not know how much or how quickly. Recent studies of corals in the shallow lagoon in Ofu Island (American Samoa) show that corals that were exposed to more variable temperatures were more tolerant to high temperatures under experimental conditions [81]. Likewise, the high diversity and abundance of corals found in shallow mangrove areas in St. John, US Virgin Islands, may persist in spite of high temperatures because of a combination of acclimatization to variable temperatures and shading by mangrove trees [168]. Van Woesik et al. [180] observed that corals growing in more turbid waters in Palau bleached less in 2010 than those in clearer, offshore waters, although they experienced the highest temperatures. In Southeast Asia, reefs that bleached in 1998 and had higher temperature variability bleached less in 2010, showing the role that thermal history can play [129]. Grottoli et al. [181] found that experimentally bleached colonies of Montipora capitata were able to replenish their energy reserves and biomass by increasing their feeding rates on zooplankton, while colonies of Porites compressa and Porites lobata were not. They suggest that corals with the ability to increase heterotrophy will have a better chance to survive prolonged bleaching events. Experiments involving feeding of two species of corals under elevated temperatures indicated that heterotrophy decreased their susceptibility to bleaching [182].

Even different populations within the same coral species may react differently to climate change [67, 174, 183]. Further information is needed on the ability of different corals within a population to resist stressors and/or recover following stress. Vollmer and Kline [184] showed that 3 out of 69 colonies of Acropora cervicornis were naturally resistant to white band disease suggesting that different genotypes might have more resistance to disease—a promising area for future research. Coral colonies with more photoprotective fluorescent pigments will be less susceptible to bleaching than others of the same or different species [185]. If major reef-builders (here defined as corals that reach a larger size and contribute more to the overall framework of reefs) adapt but other coral species do not, the coral diversity would decrease but the reef could persist. The diversity of the fish and other organisms also might decrease. For corals, fish, and other reef organisms, rates of recovery could differ depending on the type of disturbance, notably those that affect coral cover and those that reduce structural complexity. Coral species richness and architectural complexity will not always be correlated because some species, such as A. palmata and M. annularis in the Caribbean, contribute far more to the complexity than others and can be dominant. The loss of some coral species will be more disruptive than the loss of others. The declines in Acropora palmata from disease and hurricanes in the 1980s and 1990s changed the shallow seascape in the Caribbean. The full ramifications of losing this species, (for which there is no ecological equivalent), including the effects on fish and other reef organisms, were not well documented.

We focus on corals as the architects of the reef, but we need more information on how fish and other reef organisms will be affected by climate change, and we need to learn more about the functional role of different organisms and their ecological equivalency [36, 65, 186–188]. Many studies of resilience emphasize the role of herbivory in reef recovery following disturbances. It is becoming clear that different herbivorous fish species (e.g., Scaridae and Acanthuridae) can vary in their ability to control algal cover and open up new space for coral recruitment [189, 190]. We need to know which fish species are indicators of reef regeneration and which other groups besides herbivores can play a role in making reefs more resilient [65].

Several studies show that bleaching, particularly when followed by mortality and/or subsequent loss of reef structure when corals collapse, can lead to changes in fish assemblages [188, 191–193]. At One Tree Island, Great Barrier Reef, major bleaching led to a decrease in fish recruitment [194]. Loss of corals, both cover and physical structure, can lead to declines in abundance and/or diversity of fish [151, 193]. Extensive mortality following the 1998 bleaching of Chagos Reefs (Indian Ocean) led to severe erosion, with decreases in abundance and diversity of fish that depend on corals [191].

Few studies of the effects of elevated CO₂ on coral reef organisms are available [195]. De’ath et al. [196] examined colonies of Porites from 69 reefs along the Great Barrier Reef and detected declines in linear growth (13.3%) and calcification (14.2%) since 1990. Bak et al. [197] suggested that a decrease in Acropora palmata growth rates in Curacao over 30 years might be related to a decrease in pH. Both growth and recruitment of crustose coralline algae, important for coral recruitment and for cementing reef framework, were reduced by elevated seawater carbon dioxide concentrations in experimental mesocosms [69]. In other experiments in which carbon dioxide levels were increased, the calcification rates of crustose coralline algae were more sensitive than those of corals [198].

Corals and other reef species also vary in their response to acidification [46]. Key species and functional groups (e.g., urchin and fish grazers, bioeroding sponges) could be affected very differently by changes in seawater chemistry, thereby affecting critical reef processes. Some noncalcifying organisms could actually benefit. For example, growth of seagrasses could increase [166]. Kleypas and Yates [195] also point out that algae that bore into coral skeletons dissolve more calcium carbonate at higher CO₂ concentrations [199], possibly tipping the balance from reef accretion to reef dissolution. The threshold above which reefs shift from net accretion to net dissolution will vary substantially on different reefs, reflecting differences in community composition, geographic location, mixing rates of water masses, and other factors [195].

Biodiversity resides not only within coral reefs at the scale of individual reefs, but also within individual coral colonies that contain zooxanthellae as well as a diverse array of other organisms such as bacteria, fungi, and Archaea ([200–202]). There is limited knowledge not only about zooxanthellae but also about these other members of the diverse microbial communities within corals themselves and the degree to which they might be able to adapt to ocean acidification (e.g., [70, 200, 201]). The diversity of these different microorganisms, which interact in complex ways with the coral host [201], could confer resilience to some coral species.

Corals may be able to acclimatize or eventually adapt to warmer temperatures because of the diversity of their symbiotic dinoflagellates (zooxanthellae) and a variety of physiological mechanisms [136, 203–206]. Some symbionts appear to confer resistance to thermal stress [207]. In addition, experiments have shown that some bleached corals can acquire new zooxanthellae from the water column to replace suboptimal ones [178, 179]. Baird et al. [208] argue that research should focus on the holobiont—not just on the zooxanthellae but also on the coral host and its potential to adapt to increasing temperatures (see also [47]). Coral species with the same symbiotic microalgae clades respond differently to thermal stress. Sammarco and Strychar [209] point out our lack of understanding of how corals and their symbionts respond to stressors other than increasing seawater temperatures. Van Oppen and Gates [99] note that hybridization of coral species, while evidently rare, could, over evolutionary time scales, make corals more capable of responding to environmental changes “providing the potential for adaptive evolution.”

It is not just different reef species that will respond differently. Reef zones may respond dissimilarly to the variety of stressors. Although disease appears to have been the cause of much of the mortality of Acropora palmata (typically less than 5 m deep) and A. cervicornis in the late 1970s and 1980s [117, 210], and of the die-off of the important sea urchin grazer Diadema antillarum [211], at least some of the shallow reef zones with these coral species have not been carpeted with macroscopic algae that can radically reduce recruitment [212, 213]. Perhaps there has not been a shift to macroalgal dominance in some of these locations because grazing is more intense in shallow water or heavy wave action periodically removes the macroalgae from the reef.

Deep reefs, farther from the influence of humans, have been considered as possible refugia for organisms that could become sources of larvae that could replenish degraded reefs closer to shore. However, some deep reefs have had extensive coral mortality and increases in algal cover from undetermined causes [214–216]. The severe mass bleaching in 1997-1998 affected corals at depths over 30 m [217]. In addition, although few studies exist, corals growing in deeper water may not be as fecund as those in shallower water [218], and not all coral species inhabit deep reefs.

8. Conclusion

At a conference in 1993, participants concluded that the most serious threats to reefs were associated with human activities: shoreline development, overfishing, degraded water quality from sediments and sewage [219]. Then, with severe bleaching episodes beginning in 1998, the focus shifted more to global stressors and climate change [74]. In some ways we are back to where we started with an emphasis on managing human activities at a local level while still hoping that international efforts to control greenhouse emissions will become more effective [4, 23, 38, 142, 220, 221]. Managing local stressors is far more feasible than trying to control global stressors, but even this has not proven to be easy. In spite of all of the uncertainties, it only makes sense to move forward with controlling those stressors that we can control [23, 71]. Where it is feasible to design networks of marine reserves, every effort should be made to protect areas that are likely to survive future climate-driven changes, although this is very challenging [23].

Coral reefs are at a crossroads, and the situation is urgent [23, 71]. Humans are clearly reducing the resilience of reefs [21]. Over 15 years ago, Walker [186] noted “the loss of species and ecosystems is proceeding faster than research aimed at identifying priorities.” Soon after, Vitousek et al. [10] stated “we can accelerate our efforts to understand Earth’s ecosystems and how they interact with the numerous components of human-caused global change.”

The biodiversity of these complex ecosystems, one of their defining characteristics, offers some hope that they will have a future. Conserving biodiversity increases the chance that marine ecosystems, including reefs, can adapt or recover after disturbances [7]. A loss of biodiversity could reduce resilience [6, 132], but we still have most of the “pieces.” Carpenter et al. [122] highlighted an elevated risk of extinction for reef corals in just 10 years (1998 to 2008) from local and global stressors. However, to date, the observed changes on coral reefs reflect shifts in relative abundance of corals rather than losses of species. To date, no coral species has become extinct throughout its range [50]. However, many are at risk [122], and Knowlton [3] noted that some of the most important framework-building corals, on which so many other species depend, have declined the most. In addition, some models predict that because of a delayed response, even species that are the best competitors can become extinct long after habitat fragmentation and degradation [222]. Hoegh-Guldberg [71] notes little evidence that corals will be able to adapt to all of the changes and concludes that reefs could become rare globally by the middle of this century.

There are some encouraging signs. Even threatened species, such as the Caribbean acroporids, that declined significantly from disease and hurricanes, have persisted and are increasing in some locations [142]. Likewise, the herbivorous sea urchin Diadema antillarum is becoming more abundant in some places in the Caribbean [223]. Corals in some areas show evidence of acclimatizing to warmer sea water temperatures [129, 174]. Some reefs have recovered well after major bleaching episodes. Although there have been few success stories [123], and restoration efforts will at best have very localized benefits, the future does not look entirely bleak.

The high biodiversity of coral reefs means that a high diversity of responses to local and global stressors (including increasing temperatures) is anticipated. Coral species and other reef organisms will differ in their ability to deal with local stresses and the different aspects of climate change (e.g., [224]). Responses will vary even within populations [174]. Some coral species that are more susceptible to bleaching may recover faster and evolve faster than less vulnerable species [46]. In addition, the effects of local and global stressors will vary substantially within different regions [11, 137, 138, 225], and on different reefs and even within different reef zones—not all will suffer equally from high temps, ocean acidification, and increasingly powerful storms. To add to the complexity, many of the possible changes to environmental factors, such as ocean currents, are unpredictable [158].

None of us can predict what reefs will look like in 100 years, or even two decades from now. Ocean acidification and temperature increases are occurring along with changes in other global and local stressors [4, 11, 46]. Changes in climate can push already stressed ecosystems beyond their limits for recovery, but many reefs could have the ability to resist and/or recover after disturbance. Walther et al. [11] point out that linking oceanic and atmospheric processes to the responses of communities and populations is complex. The fossil record provides evidence that at least some coral reefs may be able to persist in spite of global climate change [46].

Additional research and long-term monitoring are essential to improve our predictions of the future for coral reefs and to guide management of reefs and associated ecosystems. Models can be helpful, partly by illustrating areas we need to know more about, or by indicating the best placement for marine reserves. However, by necessity, models are oversimplified. Recent models have not adequately taken coral diseases into consideration, and disease outbreaks not only have already caused severe and widespread mortality of corals but also may well increase in the future.

Many have noted the urgent need for international cooperation to reduce atmospheric concentrations of greenhouse gases [23, 226]. Given the challenges of curbing emissions on a global scale, local efforts to reduce the more tractable stresses to coral reefs and to protect marine areas that show signs of greater resistance and resilience should be emphasized [23]. Rau et al. [227] suggest that more proactive options should be considered—for example, selective breeding of more resilient species, artificial shading of some portions of reefs during thermal stress, and artificial upwelling.

There is no simple answer to the question of how climate change will affect tropical ecosystems, and the connections among them, because of the complexity and unpredictability of the stressors associated with climate change. Reefs that are linked to mangroves and seagrass beds might be more resilient than those that are not or those that are remote. Connectivity to sources of larvae is the basis for resilience. High levels of herbivory, high structural complexity, and presence of fast-growing, resistant corals will contribute to reef resilience.

The remarkable complexity of coral reefs, one of their essential core characteristics, makes it both more difficult to predict their future and more likely that they will have a future. Managers may be able to increase the chances that reefs will persist but the greatest hope may reside in the reefs themselves in the form of biodiversity at all scales.

Over the spatial scale from coral colonies, with their microbial communities, to coral species to reefs across the globe, essentially from genetic diversity within populations to the diversity of ecosystems across the seascape, the different response to the array of stressors makes it likely that at least some reefs will prove to be resilient and persist in spite of local and global pressures. Although there is a great deal of uncertainty as to how the environment will change, there is certainty that large changes will occur.

Acknowledgments

Sincere thanks to Simon Pittman, Judy Lang, Ilsa Kuffner, an anonymous reviewer with the US Geological Survey and two reviewers with ISRN Oceanography for helpful comments on earlier versions of this paper.

References

F. Moberg and C. Folke, “Ecological goods and services of coral reef ecosystems,” Ecological Economics, vol. 29, no. 2, pp. 215–233, 1999.

J. B. C. Jackson, M. X. Kirby, W. H. Berger et al., “Historical overfishing and the recent collapse of coastal ecosystems,” Science, vol. 293, no. 5530, pp. 629–637, 2001.

N. Knowlton, “The future of coral reefs,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 10, pp. 5419–5425, 2001.

T. P. Hughes, A. H. Baird, D. R. Bellwood et al., “Climate change, human impacts, and the resilience of coral reefs,” Science, vol. 301, no. 5635, pp. 929–933, 2003.

E. Sala and N. Knowlton, “Global marine biodiversity trends,” Annual Review of Environment and Resources, vol. 31, pp. 93–122, 2006.

B. Worm, E. B. Barbier, N. Beaumont et al., “Impacts of biodiversity loss on ocean ecosystem services,” Science, vol. 314, no. 5800, pp. 787–790, 2006.

S. R. Palumbi, P. A. Sandifer, J. D. Allan et al., “Managing for ocean biodiversity to sustain marine ecosystem services,” Frontiers in Ecology and the Environment, vol. 7, no. 4, pp. 204–211, 2009.

C. Wild, O. Hoegh-Guldberg, M. S. Naumann et al., “Climate change impedes scleractinian corals as primary reef ecosystem engineers,” Marine and Freshwater Research, vol. 62, no. 2, pp. 205–215, 2011.

G. De'ath, K. E. Fabricius, H. Sweatman, and M. Puotinen, “The 27-yr decline of coral cover on the Great Barrier Reef and its causes,” Proceedings of the National Academy of Sciences, vol. 109, no. 44, pp. 17734–17735, 2012.

P. M. Vitousek, H. A. Mooney, J. Lubchenco, and J. M. Melillo, “Human domination of Earth's ecosystems,” Science, vol. 277, no. 5325, pp. 494–499, 1997.

G. R. Walther, E. Post, P. Convey et al., “Ecological responses to recent climate change,” Nature, vol. 416, no. 6879, pp. 389–395, 2002.

C. S. Holling, “Resilience and stability of ecological systems,” Annual Review of Ecology, Evolution, and Systematics, vol. 4, pp. 1–23, 1973.

R. B. Aronson and W. F. Precht, “Evolutionary paleoecology of Caribbean coral reefs,” in Evolutionary Paleoecology: The Ecological Context of Macroevolutionary Change, W. D. Allmon and D. J. Bottjer, Eds., pp. 171–233, Columbia University Press, New York, NY, USA, 2001.

C. Tang, “Stability in ecological and paleoecological systems: variability at both short and long timescales,” in Evolutionary Paleoecology: The Ecological Context of Macroevolutionary Change, W. Allmon and D. Bottjer, Eds., Chapter 5, pp. 63–81, Columbia University Press, New York, NY, USA, 2001.

P. J. Mumby and R. S. Steneck, “The resilience of coral reefs and its implications for reef management,” in Coral Reefs: An Ecosystem in Transition, Z. Dubinsky and N. Stambler, Eds., pp. 465–491, Springer, Dordrecht, The Netherlands, 2011.

J. H. Connell and W. P. Sousa, “On the evidence needed to judge ecological stability or persistence,” American Naturalist, vol. 121, no. 6, pp. 789–824, 1983.

J. M. West and R. V. Salm, “Resistance and Resilience to Coral Bleaching: implications for Coral Reef Conservation and Management,” Conservation Biology, vol. 17, no. 4, pp. 956–967, 2003.

J. H. Connell, “Disturbance and recovery of coral assemblages,” Coral Reefs, vol. 16, no. 1, pp. S101–S113, 1997.

T. J. Done, “Phase shifts in coral reef communities and their ecological significance,” Hydrobiologia, vol. 247, no. 1-3, pp. 121–132, 1992.

R. E. Johannes, Ed., Pollution and Degradation of Coral Reef Communities, Elsevier Scientific, New York, NY, USA, 1975.

M. Nyström, C. Folke, and F. Moberg, “Coral reef disturbance and resilience in a human-dominated environment,” Trends in Ecology and Evolution, vol. 15, no. 10, pp. 413–417, 2000.

C. Wilkinson, “Status of coral reefs of the world: summary of threats and remedial action,” in Coral Reef Conservation, I. M. Côté and J. D. Reynolds, Eds., pp. 3–39, Cambridge University Press, 2006.

L. Burke, K. Reytar, M. D. Spalding, and A. Perry, Reefs at Risk Revisited, World Resources Institute, Washington, DC, USA, 2011.

B. M. Riegl and R. E. Dodge, Eds., Coral Reefs of the World 1: Coral Reefs of the USA, Springer, Dordrecht, The Netherlands, 2008.

A. E. Lugo and S. C. Snedaker, “The ecology of mangroves,” Annual Review of Ecology and Systematics, vol. 5, pp. 39–64, 1974.

D. R. Bellwood, T. P. Hughes, C. Folke, and M. Nyström, “Confronting the coral reef crisis,” Nature, vol. 429, no. 6994, pp. 827–833, 2004.

J. A. Kleypas, “Constraints on predicting coral reef response to climate change,” in Geological Approaches to Coral Reef Ecology. Ecological Studies, R. B. Aronson, Ed., vol. 192, pp. 386–424, Springer, New York, NY, USA, 2007.

C. S. Rogers and J. Miller, “Permanent “phase shifts” or reversible declines in coral cover? Lack of recovery of two coral reefs in St. John, US Virgin Islands,” Marine Ecology Progress Series, vol. 306, pp. 103–114, 2006.

J. F. Bruno, H. Sweatman, W. F. Precht, E. R. Selig, and V. G. W. Schutte, “Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs,” Ecology, vol. 90, no. 6, pp. 1478–1484, 2009.

G. Roff and P. J. Mumby, “Global disparity in the resilience of coral reefs,” TREE, vol. 27, no. 7, pp. 404–413, 2012.

R. G. Lighty, I. G. Macintyre, and R. Stuckenrath, “Acropora palmata reef framework: a reliable indicator of sea level in the Western Atlantic for the past 10,000 years,” Coral Reefs, vol. 1, no. 2, pp. 125–130, 1982.

B. G. Hatcher, “A maritime accident provides evidence for alternate stable states in benthic communities on coral reefs,” Coral Reefs, vol. 3, no. 4, pp. 199–204, 1984.

T. P. Hughes, “Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef,” Science, vol. 265, no. 5178, pp. 1547–1551, 1994.

S. R. Dudgeon, R. B. Aronson, J. F. Bruno, and W. F. Precht, “Phase shifts and stable states on coral reefs,” Marine Ecology Progress Series, vol. 413, pp. 201–216, 2010.

M. Nyström, N. A. J. Graham, J. Lokrantz, and A. V. Norström, “Capturing the cornerstones of coral reef resilience: linking theory to practice,” Coral Reefs, vol. 27, no. 4, pp. 795–809, 2008.

M. S. Pratchett, S. K. Wilson, N. A. J. Graham, P. L. Munday, G. P. Jones, and N. V. C. Polunin, “Coral bleaching and consequences for motile reef organisms: past, present and uncertain future effects,” in Coral Bleaching, M. J. H. van Oppen and J. M. Lough, Eds., Chapter 9, pp. 139–158, Springer, Berlin, Germany, 2009.

A. B. Pittock, “Coral reefs and environmental change: adapatation to what?” American Zoologist, vol. 39, pp. 10–29, 1999.

O. Hoegh-Guldberg, P. J. Mumby, A. J. Hooten et al., “Coral reefs under rapid climate change and ocean acidification,” Science, vol. 318, no. 5857, pp. 1737–1742, 2007.

J. T. Houghton, Y. Ding, D. J. Griggs, M. Noguer, P. J. van der Linden, and D. Xiaosu, Eds., IPCC Third Assessment Report: Climate Change 2001: The Scientific Basis, Cambridge University Press, 2001.

S. D. Donner, T. R. Knutson, and M. Oppenheimer, “Model-based assessment of the role of human-induced climate change in the 2005 Caribbean coral bleaching event,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 13, pp. 5483–5488, 2007.

M. P. Lesser, “Coral reef bleaching and global climate change: can corals survive the next century?” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 13, pp. 5259–5260, 2007.

G. C. Hegerl, F. W. Zwiers, P. Braconnot et al., “Understanding and attributing climate change,” in Climate Change: The Physical Science Basis. Contribution of Working Group I to the 4th Assessment Report of the Intergovernmental Panel on Climate Change, S. Solomon, D. Qin, M. Manning et al., Eds., Cambridge University Press, Cambridge, UK, 2007.

R. A. Feely, C. L. Sabine, K. Lee et al., “Impact of anthropogenic CO₂ on the CaCO₃ system in the oceans,” Science, vol. 305, no. 5682, pp. 362–366, 2004.

IPCC, Climate Change 2007: The Physical Science Basis. Contribution of the Working Group I to the 4th Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge, UK, 2007.

J. A. Kleypas, J. W. McManus, and L. A. B. Menez, “Environmental limits to coral reef development: where do we draw the line?” American Zoologist, vol. 39, no. 1, pp. 146–159, 1999.

J. M. Pandolfi, S. R. Connolly, D. J. Marshall, and A. L. Cohen, “Projecting coral reef futures under global warming and ocean acidification,” Science, vol. 333, no. 6041, pp. 418–422, 2011.

P. W. Glynn, “Coral reef bleaching: ecological perspectives,” Coral Reefs, vol. 12, no. 1, pp. 1–17, 1993.

B. E. Brown, “Coral bleaching: causes and consequences,” Coral Reefs, vol. 16, suppement 1, pp. S129–S138, 1997.

O. Hoegh-Guldberg, “Climate change, coral bleaching and the future of the world's coral reefs,” Marine and Freshwater Research, vol. 50, no. 8, pp. 839–866, 1999.

A. C. Baker, P. W. Glynn, and B. Riegl, “Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook,” Estuarine, Coastal and Shelf Science, vol. 80, no. 4, pp. 435–471, 2008.

M. P. Lesser, “Coral bleaching: causes and mechanisms,” in Coral Reefs: An Ecosystem in Transition, Z. Dubinsky and N. Stambler, Eds., pp. 405–419, Springer, Dordrecht, The Netherlands, 2011.

N. Stambler, “Zooxanthellae: the yellow symbionts inside animals,” in Coral Reefs: An Ecosystem in Transition, Z. Dubinsky and N. Stambler, Eds., pp. 87–106, Springer, Dordrecht, The Netherlands, 2011.

J. M. Shick, M. P. Lesser, and P. L. Jokiel, “Effects of ultraviolet radiation on corals and other coral reef organisms,” Global Change Biology, vol. 2, no. 6, pp. 527–545, 1996.

M. P. Lesser, “Experimental biology of coral reef ecosystems,” Journal of Experimental Marine Biology and Ecology, vol. 300, no. 1-2, pp. 217–252, 2004.

M. P. Lesser, “Oxidative stress in marine environments: biochemistry and physiological ecology,” Annual Review of Physiology, vol. 68, pp. 253–278, 2006.

P. J. Mumby, J. R. M. Chisholm, A. J. Edwards, S. Andrefouet, and J. Jaubert, “Cloudy weather may have saved Society Island reef corals during the 1998 ENSO event,” Marine Ecology Progress Series, vol. 222, pp. 209–216, 2001.

S. Leahy, M. Kingsford, and C. Steinberg, “Do clouds save the Great Barrier Reef?” in Proceedings of the 12th International Coral Reef Symposium, p. 190, Cairns, Australia, 2012.

P. J. Mumby, I. A. Elliott, C. M. Eakin et al., “Reserve design for uncertain responses of coral reefs to climate change,” Ecology Letters, vol. 14, no. 2, pp. 132–140, 2011.

M. A. Bender, T. R. Knutson, R. E. Tuleya et al., “Modeled impact of anthropogenic warming on the frequency of intense Atlantic hurricanes,” Science, vol. 327, no. 5964, pp. 454–458, 2010.

J. D. Woodley, E. A. Chornesky, P. A. Clifford et al., “Hurricane Allen's impact on Jamaican coral reefs,” Science, vol. 214, no. 4522, pp. 749–755, 1981.

A. E. Lugo, C. S. Rogers, and S. W. Nixon, “Hurricanes, coral reefs and rainforests: resistance, ruin and recovery in the Caribbean,” Ambio, vol. 29, no. 2, pp. 106–114, 2000.

D. K. Hubbard, K. M. Parsons, J. C. Bythell, and N. D. Walker, “The effects of Hurricane Hugo on the reefs and associated environments of St. Croix, US Virgin Islands—a preliminary assessment,” Journal of Coastal Research, Special Issue, vol. 8, pp. 33–48, 1992.

N. Knowlton, J. C. Lang, and B. D. Keller, Case Study of Natural Population Collapse: Post-Hurricane Predation on Jamaican Staghorn Corals, vol. 31 of Smithsonian Contribution, 1990.

A. J. Bright, The effect of swell-generated physical damage on disease prevalence and asexual reproduction in the coral, Acropora palmata (Lamarck) [M.S. thesis], University of the Virgin Islands, St. Thomas, United States Virgin Islands, 2009.

S. K. Wilson, M. Adjeroud, D. R. Bellwood et al., “Crucial knowledge gaps in current understanding of climate change impacts on coral reef fishes,” Journal of Experimental Biology, vol. 213, no. 6, pp. 894–900, 2010.

D. P. Manzello, M. Brandt, T. B. Smith, D. Lirman, J. C. Hendee, and R. S. Nemeth, “Hurricanes benefit bleached corals,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 29, pp. 12035–12039, 2007.

J. Erez, S. Reynaud, J. Silverman, K. Schneider, and D. Allemand, “Coral calcification under ocean acidification and global change,” in Coral Reefs: An Ecosystem in Transition, Z. Dubinsky and N. Stambler, Eds., pp. 151–176, Springer, Dordrecht, The Netherlands, 2011.

J. P. Gattuso, D. Allemand, and M. Frankignoulle, “Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry,” American Zoologist, vol. 39, no. 1, pp. 160–183, 1999.

I. B. Kuffner, A. J. Andersson, P. L. Jokiel, K. S. Rodgers, and F. T. MacKenzie, “Decreased abundance of crustose coralline algae due to ocean acidification,” Nature Geoscience, vol. 1, no. 2, pp. 114–117, 2008.

G. E. Hofmann, J. P. Barry, P. J. Edmunds et al., “The effect of ocean acidification on calcifying organisms in marine ecosystems: an organism-to-ecosystem perspective,” Annual Review of Ecology, Evolution, and Systematics, vol. 41, pp. 127–147, 2010.

O. Hoegh-Guldberg, “The impact of climate change on coral reef ecosystems,” in Coral Reefs: An Ecosystem in Transition, Z. Dubinsky and N. Stambler, Eds., pp. 391–403, Springer, Dordrecht, The Netherlands, 2011.

K. K. Yates and R. B. Halley, “ concentration and pCO₂ thresholds for calcification and dissolution on the Molokai reef flat, Hawaii,” Biogeosciences, vol. 3, pp. 1–13, 2006.

J. Silverman, B. Lazar, L. Cao, K. Caldeira, and J. Erez, “Coral reefs may start dissolving when atmospheric CO₂ doubles,” Geophysical Research Letters, vol. 36, no. 5, Article ID L05606, 2009.

C. R. Wilkinson, “Global and local threats to coral reef functioning and existence: review and predictions,” Marine and Freshwater Research, vol. 50, no. 8, pp. 867–878, 1999.

E. R. Selig, C. D. Harvell, J. F. Bruno et al., “Analyzing the relationship between ocean temperature anomalies and coral disease outbreaks at broad spatial scales,” in Coral Reefs and Climate Change: Science and Management, J. Phinney, O. Hoegh-Guldberg, J. Kleypas, W. Skirving, and A. Strong, Eds., pp. 111–128, American Geophysical Union, Washington, DC, USA, 2006.

J. F. Bruno, E. R. Selig, K. S. Casey et al., “Thermal stress and coral cover as drivers of coral disease outbreaks,” PLoS Biology, vol. 5, no. 6, Article ID e124, 2007.

M. E. Brandt and J. W. McManus, “Disease incidence is related to bleaching extent in reef-building corals,” Ecology, vol. 90, no. 10, pp. 2859–2867, 2009.

A. Cróquer and E. Weil, “Spatial variability in distribution and prevalence of Caribbean scleractinian coral and octocoral diseases. II. Genera-level analysis,” Diseases of Aquatic Organisms, vol. 83, no. 3, pp. 209–222, 2009.

A. Cróquer and E. Weil, “Changes in Caribbean coral disease prevalence after the 2005 bleaching event,” Diseases of Aquatic Organisms, vol. 87, no. 1-2, pp. 33–43, 2009.

C. S. Rogers, E. Muller, T. Spitzack, and J. Miller, “Extensive coral mortality in the US Virgin Islands in 2005/2006: a review of the evidence for synergy among thermal stress, coral bleaching and disease,” Caribbean Journal of Science, vol. 45, no. 2-3, pp. 204–214, 2009.

T. A. Oliver and S. R. Palumbi, “Do fluctuating temperature environments elevate coral thermal tolerance?” Coral Reefs, vol. 30, no. 2, pp. 429–440, 2011.

C. S. Rogers, “Words matter: recommendations for clarifying coral disease nomenclature and terminology,” Diseases of Aquatic Organisms, vol. 91, no. 2, pp. 167–175, 2010.

E. M. Muller, C. S. Rogers, A. S. Spitzack, and R. van Woesik, “Bleaching increases likelihood of disease on Acropora palmata (Lamarck) in Hawksnest Bay, St John, US Virgin Islands,” Coral Reefs, vol. 27, no. 1, pp. 191–195, 2008.

D. Harvell, S. Altizer, I. M. Cattadori, L. Harrington, and E. Weil, “Climate change and wildlife diseases: when does the host matter the most?” Ecology, vol. 90, no. 4, pp. 912–920, 2009.

R. Berkelmans, G. De'ath, S. Kininmonth, and W. J. Skirving, “A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions,” Coral Reefs, vol. 23, no. 1, pp. 74–83, 2004.

H. A. Oxenford, R. Roach, A. Brathwaite et al., “Quantitative observations of a major coral bleaching event in Barbados, Southeastern Caribbean,” Climatic Change, vol. 87, no. 3-4, pp. 435–449, 2008.

J. Miller, E. Muller, C. Rogers et al., “Coral disease following massive bleaching in 2005 causes 60% decline in coral cover on reefs in the US Virgin Islands,” Coral Reefs, vol. 28, no. 4, pp. 925–937, 2009.

S. S. Ban, N. A. J. Graham, and S. R. Connolly, “Relationships between temperature, bleaching and white syndrome on the Great Barrier Reef,” Coral Reefs, 2012.

J. F. Bruno, L. E. Petes, C. D. Harvell, and A. Hettinger, “Nutrient enrichment can increase the severity of coral diseases,” Ecology Letters, vol. 6, no. 12, pp. 1056–1061, 2003.

K. P. Sutherland, J. W. Porter, J. W. Turner et al., “Human sewage identified as likely source of white pox disease of the threatened Caribbean elkhorn coral, Acropora palmata,” Environmental Microbiology, vol. 12, no. 5, pp. 1122–1131, 2010.

J. Haapkylä, R. K. F. Unsworth, M. Flavell, D. G. Bourne, B. Schaffelke, and B. L. Willis, “Seasonal rainfall and runoff promote coral disease on an inshore reef,” PloS ONE, vol. 6, no. 2, Article ID e16893, 2011.

E. Weil, A. Croquer, and I. Urreiztieta, “Temporal variability and impact of coral diseases and bleaching in La Parguera, Puerto Rico from 2003–2007,” Caribbean Journal of Science, vol. 45, no. 2-3, pp. 221–246, 2009.

E. Weil and C. S. Rogers, “Coral reef diseases in the Atlantic-Caribbean,” in Coral Reefs: An Ecosystem in Transition, Z. Dubinsky and N. Stambler, Eds., pp. 465–491, Springer, Dordrecht, The Netherlands, 2011.

B. L. Willis, C. A. Page, and E. A. Dinsdale, “Coral disease on the Great Barrier Reef,” in Coral Health and Disease, E. Rosenberg and L. Loya, Eds., Chapter 3, pp. 69–104, Springer, Berlin, Germany, 2004.

T. McClanahan, “Coral bleaching, diseases and mortality in the Western Indian Ocean,” in Coral Health and Disease, E. Rosenberg and Y. Loya, Eds., Chapter 7, pp. 157–176, Springer, Berlin, Germany, 2004.

L. L. Richardson, G. W. Smith, K. B. Ritchie, and R. G. Carlton, “Integrating microbiological, microsensor, molecular, and physiologic techniques in the study of coral disease pathogenesis,” Hydrobiologia, vol. 460, pp. 71–89, 2001.

D. Harvell, E. Jordán-Dahlgren, S. Merkel, et al., “Coral disease, environmental drivers, and the balance between coral and microbial associates,” Oceanography, vol. 20, no. 1, pp. 172–195, 2007.

T. M. Work, L. L. Richardson, T. L. Reynolds, and B. L. Willis, “Biomedical and veterinary science can increase our understanding of coral disease,” Journal of Experimental Marine Biology and Ecology, vol. 362, no. 2, pp. 63–70, 2008.

M. J. H. van Oppen and R. D. Gates, “Conservation genetics and the resilience of reef-building corals,” Molecular Ecology, vol. 15, no. 13, pp. 3863–3883, 2006.

R. V. Thurber, D. Willner-Hall, B. Rodriguez-Mueller et al., “Metagenomic analysis of stressed coral holobionts,” Environmental Microbiology, vol. 11, no. 8, pp. 2148–2163, 2009.

P. J. Edmunds and R. C. Carpenter, “Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 9, pp. 5067–5071, 2001.

R. C. Carpenter and P. J. Edmunds, “Local and regional scale recovery of Diadema promotes recruitment of scleractinian corals,” Ecology letters, vol. 9, no. 3, pp. 271–280, 2006.

A. L. Zubillaga, L. M. Márquez, A. Cróquer, and C. Bastidas, “Ecological and genetic data indicate recovery of the endangered coral Acropora palmata in Los Roques, Southern Caribbean,” Coral Reefs, vol. 27, no. 1, pp. 63–72, 2008.

M. J. C. Crabbe, “Scleractinian coral population size structures and growth rates indicate coral resilience on the fringing reefs of North Jamaica,” Marine Environmental Research, vol. 67, no. 4-5, pp. 189–198, 2009.

H. M. Guzman and J. Cortés, “Reef recovery 20 years after the 1982–1983 El Niño massive mortality,” Marine Biology, vol. 151, no. 2, pp. 401–411, 2007.

G. Diaz-Pulido, L. J. McCook, S. Dove et al., “Doom and boom on a resilient reef: climate change, algal overgrowth and coral recovery,” PloS ONE, vol. 4, no. 4, Article ID e5239, 2009.

A. Halford, A. J. Cheal, D. Ryan, and D. M. Williams, “Resilience to large-scale disturbance in coral and fish assemblages on the Great Barrier Reef,” Ecology, vol. 85, no. 7, pp. 1892–1905, 2004.

S. V. Smith, W. J. Kimmerer, E. A. Laws, R. E. Brock, and T. W. Walsh, “Kaneohe Bay sewage diversion experiment: perspectives on ecosystem responses to nutritional perturbation,” Pacific Science, vol. 35, no. 4, pp. 279–395, 1981.

C. L. Hunter and C. W. Evans, “Reefs in Kaneohe Bay, Hawaii: two centuries of western influence and two decades of data,” Proceedings of the Colloquium on Global Aspects of Coral Reefs Miami 1993, pp. 339–345, 1994.

J. Stimson and E. Conklin, “Potential reversal of a phase shift: the rapid decrease in the cover of the invasive green macroalga Dictyosphaeria cavernosa Forsskål on coral reefs in Kāne'ohe Bay, Oahu, Hawai'i,” Coral Reefs, vol. 27, no. 4, pp. 717–726, 2008.

J. A. Idjadi, S. C. Lee, J. F. Bruno, W. F. Precht, L. Allen-Requa, and P. J. Edmunds, “Rapid phase-shift reversal on a Jamaican coral reef,” Coral Reefs, vol. 25, no. 2, pp. 209–211, 2006.

J. A. Idjadi, R. N. Haring, and W. F. Precht, “Recovery of the sea urchin Diadema antillarum promotes scleractinian coral growth and survivorship on shallow Jamaican reefs,” Marine Ecology Progress Series, vol. 403, pp. 91–100, 2010.

N. J. Quinn and B. L. Kojis, “The recent collapse of a rapid phase-shift reversal on a Jamaican north coast coral reef after the 2005 bleaching event,” Revista de Biologia Tropical, vol. 56, supplement 1, pp. 149–159, 2008.

A. J. Cheal, M. A. MacNeil, E. Cripps et al., “Coral-macroalgal phase shifts or reef resilience: links with diversity and functional roles of herbivorous fishes on the Great Barrier Reef,” Coral Reefs, vol. 29, no. 4, pp. 1005–1015, 2010.

K. Osborne, A. M. Dolman, S. C. Burgess, and K. A. Johns, “Disturbance and the dynamics of coral cover on the Great Barrier Reef (1995–2009),” PloS ONE, vol. 6, no. 3, Article ID e17516, 2011.

M. L. Berumen and M. S. Pratchett, “Recovery without resilience: persistent disturbance and long-term shifts in the structure of fish and coral communities at Tiahura Reef, Moorea,” Coral Reefs, vol. 25, no. 4, pp. 647–653, 2006.

W. B. Gladfelter, “White-band disease in Acropora palmata: implications for the structure and growth of shallow reefs,” Bulletin of Marine Science, vol. 32, pp. 639–643, 1982.

A. W. Bruckner, “Proceedings of the Caribbean Acropora workshop: potential application of the U.S. Endangered Species Act as a conservation strategy,” NOAA Tech Memo NMFS-OPR-24, Silver Spring, 2003.

N. A. J. Graham, K. L. Nash, and J. T. Kool, “Coral reef recovery dynamics in a changing world,” Coral Reefs, vol. 30, no. 2, pp. 283–294, 2011.

P. J. Edmunds, “Long-term dynamics of coral reefs in St. John, US Virgin Islands,” Coral Reefs, vol. 21, no. 4, pp. 357–367, 2002.

E. Stokstad, “Despite progress, biodiversity declines,” Science, vol. 329, no. 5997, pp. 1272–1273, 2010.

K. E. Carpenter, M. Abrar, G. Aeby et al., “One-third of reef-building corals face elevated extinction risk from climate change and local impacts,” Science, vol. 321, no. 5888, pp. 560–563, 2008.

T. P. Hughes, N. A. J. Graham, J. B. C. Jackson, P. J. Mumby, and R. S. Steneck, “Rising to the challenge of sustaining coral reef resilience,” Trends in Ecology and Evolution, vol. 25, no. 11, pp. 633–642, 2010.

E. McLeod, R. Salm, A. Green, and J. Almany, “Designing marine protected area networks to address the impacts of climate change,” Frontiers in Ecology and the Environment, vol. 7, no. 7, pp. 362–370, 2009.

M. L. Baskett, R. M. Nisbet, C. V. Kappel, P. J. Mumby, and S. D. Gaines, “Conservation management approaches to protecting the capacity for corals to respond to climate change: a theoretical comparison,” Global Change Biology, vol. 16, no. 4, pp. 1229–1246, 2010.

T. McClanahan, A. Baker, and M. Ateweberhan, Preparing for Climate Change in the Western Indian Ocean—Identifying Climate Refugia, Biodiversity Responses, and Preferred Management, WIOMSA Book Series 12, 2011.

T. R. McClanahan, J. M. Maina, and N. A. Muthiga, “Associations between climate stress and coral reef diversity in the western Indian Ocean,” Global Change Biology, vol. 17, no. 6, pp. 2023–2032, 2011.

I. M. Côté and E. S. Darling, “Rethinking ecosystem resilience in the face of climate change,” PLoS Biology, vol. 8, no. 7, Article ID e1000438, 2010.

J. R. Guest, A. H. Baird, A. J. Maynard, et al., “Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress,” PloS ONE, vol. 7, no. 3, Article ID e33343, 2012.

P. Marshall and H. Schuttenberg, Reef Manager's Guide to Coral Bleaching. Great Barrier Reef Marine Park Authority, Townsville, Australia, 2006.

C. S. Rogers, “Sublethal and lethal effects of sediments applied to common Caribbean reef corals in the field,” Marine Pollution Bulletin, vol. 14, no. 10, pp. 378–382, 1983.

F. S. Chapin, E. S. Zavaleta, V. T. Eviner et al., “Consequences of changing biodiversity,” Nature, vol. 405, no. 6783, pp. 234–242, 2000.

R. Berkelmans, “Bleaching and mortality thresholds: how much is too much?” in Coral Bleaching, M. van Oppen and J. M. Lough, Eds., Chapter 7, pp. 103–119, Springer, 2009.

A. C. Baker, C. J. Starger, T. R. McClanahan, and P. W. Glynn, “Coral reefs: corals' adaptive response to climate change,” Nature, vol. 430, no. 7001, article 741, 2004.

R. Rowan, “Thermal adaptation in reef coral symbionts,” Nature, vol. 430, no. 7001, article 742, 2004.

R. Berkelmans and M. J. H. van Oppen, “The role of zooxanthellae in the thermal tolerance of corals: a “nugget of hope” for coral reefs in an era of climate change,” Proceedings of the Royal Society B, vol. 273, no. 1599, pp. 2305–2312, 2006.

S. A. Wooldridge and T. J. Done, “Improved water quality can ameliorate effects of climate change on corals,” Ecological Applications, vol. 19, no. 6, pp. 1492–1499, 2009.

J. E. Carilli, R. D. Norris, B. A. Black, S. M. Walsh, and M. McField, “Local stressors reduce coral resilience to bleaching,” PloS ONE, vol. 4, no. 7, Article ID e6324, 2009.

P. J. Mumby and A. Hastings, “The impact of ecosystem connectivity on coral reef resilience,” Journal of Applied Ecology, vol. 45, no. 3, pp. 854–862, 2008.

J. Sobel and C. Dahlgren, Marine Reserves: A Guide to Science, Design and Use, Island Press, Washington, DC, USA, 2004.

B. S. Halpern and R. R. Warner, “Marine reserves have rapid and lasting effects,” Ecology Letters, vol. 5, no. 3, pp. 361–366, 2002.

R. B. Aronson and W. F. Precht, “Conservation, precaution, and Caribbean reefs,” Coral Reefs, vol. 25, no. 3, pp. 441–450, 2006.

T. P. Hughes, M. J. Rodrigues, D. R. Bellwood et al., “Phase Shifts, Herbivory, and the Resilience of Coral Reefs to Climate Change,” Current Biology, vol. 17, no. 4, pp. 360–365, 2007.

L. J. McCook, T. Ayling, M. Cappo et al., “Adaptive management of the Great Barrier Reef: a globally significant demonstration of the benefits of networks of marine reserves,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 43, pp. 18278–18285, 2010.

P. J. Mumby and A. R. Harborne, “Marine reserves enhance the recovery of corals on Caribbean reefs,” PloS ONE, vol. 5, no. 1, Article ID e8657, 2010.

K. L. Kramer and K. L. Heck, “Top-down trophic shifts in Florida Keys patch reef marine protected areas,” Marine Ecology Progress Series, vol. 349, pp. 111–123, 2007.

B. E. Huntington, M. Karnauskas, and D. Lirman, “Corals fail to recover at a Caribbean marine reserve despite ten years of reserve designation,” Coral Reefs, vol. 30, no. 4, pp. 1077–1085, 2011.

J. Claudet and P. Guidetti, “Improving assessments of marine protected areas,” Aquatic Conservation, vol. 20, no. 2, pp. 239–242, 2010.

V. R. Coelho and C. Manfrino, “Coral community decline at a remote Caribbean island: marine no-take reserves are not enough,” Aquatic Conservation, vol. 17, no. 7, pp. 666–685, 2007.

L. J. Raymundo, A. R. Halford, A. P. Maypa, and A. M. Kerr, “Functionally diverse reef-fish communities ameliorate coral disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 40, pp. 17067–17070, 2009.

G. P. Jones, M. I. McCormick, M. Srinivasan, and J. V. Eagle, “Coral decline threatens fish biodiversity in marine reserves,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 21, pp. 8251–8253, 2004.

L. Alvarez-Filip, N. K. Dulvy, J. A. Gill, I. M. Côté, and A. R. Watkinson, “Flattening of Caribbean coral reefs: region-wide declines in architectural complexity,” Proceedings of the Royal Society B, vol. 276, no. 1669, pp. 3019–3025, 2009.

C. Dryden, J. Cortes, S. Newman, C. Sanchez, S. Williams, and N. Polunin, “Future of reefs in a changing environment: an ecosystem approach to managing Caribbean coral reefs in the face of climate change. Preliminary report on the relationship between architectural complexity and reef biodiversity,” 7th Framework Programme, Force Project. (10 pp), 2012

D. L. Ballantine, R. S. Appeldoorn, P. Yoshioka, et al., “Biology and ecology of Puerto Rican coral reefs,” in Coral Reefs of the USA, B. Riegl and R. E. Dodge, Eds., Chapter 9, pp. 375–406, Springer, Dordrecht, The Netherlands, 2008.

J. C. Ogden, “Marine managers look upstream for connections,” Science, vol. 278, no. 5342, pp. 1414–1415, 1997.

C. M. Roberts, “Connectivity and management of Caribbean coral reefs,” Science, vol. 278, no. 5342, pp. 1454–1457, 1997.

S. J. Pittman, C. Caldow, S. D. Hile, and M. E. Monaco, “Using seascape types to explain the spatial patterns of fish in the mangroves of SW Puerto Rico,” Marine Ecology Progress Series, vol. 348, pp. 273–284, 2007.

P. L. Munday, J. M. Leis, J. M. Lough et al., “Climate change and coral reef connectivity,” Coral Reefs, vol. 28, no. 2, pp. 379–395, 2009.

R. K. Cowen, C. B. Paris, and A. Srinivasan, “Scaling of connectivity in marine populations,” Science, vol. 311, no. 5760, pp. 522–527, 2006.

J. C. Ogden, “Ecosystem interactions in the tropical coastal seascape,” in Life and Death of Coral Reefs, C. Birkeland, Ed., Chapman and Hall, New York, NY, USA, 1997.

J. C. Ogden and E. H. Gladfelter, Eds., Coral Reefs, Seagrass Beds, and Mangroves: Their Interaction in the Coastal Zones of the Caribbean: Report of a Workshop Held at West Indies Laboratory, May 1982, vol. 23 of Reports in Marine Science, UNESCO, 1983.

P. J. Mumby, A. J. Edwards, J. E. Arias-González et al., “Mangroves enhance the biomass of coral reef fish communities in the Caribbean,” Nature, vol. 427, no. 6974, pp. 533–536, 2004.

I. Nagelkerken, G. van der Velde, M. W. Gorissen, G. J. Meijer, T. Van't Hof, and C. Den Hartog, “Importance of mangroves, seagrass beds and the shallow coral reef as a nursery for important coral reef fishes, using a visual census technique,” Estuarine, Coastal and Shelf Science, vol. 51, no. 1, pp. 31–44, 2000.

I. Valiela, J. L. Bowen, and J. K. York, “Mangrove forests: one of the world's threatened major tropical environments,” Bioscience, vol. 51, no. 10, pp. 807–815, 2001.

E. L. Gilman, J. Ellison, N. C. Duke, and C. Field, “Threats to mangroves from climate change and adaptation options: a review,” Aquatic Botany, vol. 89, no. 2, pp. 237–250, 2008.

S. L. Palacios and R. C. Zimmerman, “Response of eelgrass Zostera marina to CO₂ enrichment: possible impacts of climate change and potential for remediation of coastal habitats,” Marine Ecology Progress Series, vol. 344, pp. 1–13, 2007.

B. S. Halpern, S. Walbridge, K. A. Selkoe et al., “A global map of human impact on marine ecosystems,” Science, vol. 319, no. 5865, pp. 948–952, 2008.

C. S. Rogers and J. J. Herlan, “Life on the edge: corals in mangroves and climate change,” in Proceedings of the 12th International Coral Reef Symposium, p. 5, Cairns, Australia, July 2012.

M. Reaka-Kudla, “The global biodiversity of coral reefs: a comparison with rain forests,” in Biodiversity II: Understanding and Protecting our Biological Resources, M. Reaka-Kudla, D. Wilson, and E. Wilson, Eds., Chapter 7, pp. 83–108, Joseph Henry Press, Washington, DC, USA, 1997.

N. Knowlton, “Ecology: coral reef biodiversity—habitat size matters,” Science, vol. 292, no. 5521, pp. 1493–1495, 2001.

J. H. Ausubel, D. T. Crist, and P. E. Waggoner, Eds., First Census of Marine Life 2010: Highlights of a decade of discovery. Census of Marine Life, Washington, DC, USA, 2010.

G. Paulay, “Diversity and distribution of reef organisms,” in Life and Death of Coral Reefs, C. Birkeland, Ed., Chapter 14, pp. 298–353, Chapman and Hall, New York, NY, USA, 1997.

K. J. Willis and S. A. Bhagwat, “Biodiversity and climate change,” Science, vol. 326, no. 5954, pp. 806–807, 2009.

B. E. Brown and A. R. Cossins, “The potential for temperature acclimatisation of reef corals in the face of climate change,” in Coral Reefs: An Ecosystem in Transition, Z. Dubinsky and N. Stambler, Eds., pp. 421–433, Springer, Dordrecht, The Netherlands, 2011.

P. A. Marshall and A. H. Baird, “Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa,” Coral Reefs, vol. 19, no. 2, pp. 155–163, 2000.

T. McClanahan, E. Weil, J. Cortes, A. H. Baird, and M. Ateweberhan, “Consequences of coral bleaching for sessile reef organisms,” in Ecological Studies: Coral Bleaching: Patterns, Processes, Causes and Consequences, M. H. van Oppen and J. M. Lough, Eds., Springer, 2009.

S. L. Coles and B. E. Brown, “Coral bleaching—capacity for acclimatization and adaptation,” Advances in Marine Biology, vol. 46, pp. 183–223, 2003.

A. C. Baker, “Reef corals bleach to survive change,” Nature, vol. 411, no. 6839, pp. 765–766, 2001.

R. A. Kinzie III, M. Takayama, S. R. Santos, and M. A. Coffroth, “The adaptive bleaching hypothesis: experimental tests of critical assumptions,” Biological Bulletin, vol. 200, no. 1, pp. 51–58, 2001.

R. van Woesik, P. Houk, A. L. Isechal, J. W. Idechong, S. Victor, and Y. Golbuu, “Climate-change refugia in the sheltered bays of Palau: analogs of future reefs,” Ecology and Evolution, vol. 2, no. 10, pp. 2474–2484, 2012.

A. G. Grottoli, L. J. Rodrigues, and J. E. Palardy, “Heterotrophic plasticity and resilience in bleached corals,” Nature, vol. 440, no. 7088, pp. 1186–1189, 2006.

E. M. Borell, A. R. Yuliantri, K. Bischof, and C. Richter, “The effect of heterotrophy on photosynthesis and tissue composition of two scleractinian corals under elevated temperature,” Journal of Experimental Marine Biology and Ecology, vol. 364, no. 2, pp. 116–123, 2008.

I. B. Baums, M. W. Miller, and M. E. Hellberg, “Geographic variation in clonal structure in a reef-building Caribbean coral, Acropora palmata,” Ecological Monographs, vol. 76, no. 4, pp. 503–519, 2006.

S. V. Vollmer and D. I. Kline, “Natural disease resistance in threatened staghorn corals,” PloS ONE, vol. 3, no. 11, Article ID e3718, 2008.

A. Salih, A. Larkum, G. Cox, M. Kühl, and O. Hoegh-Guldberg, “Fluorescent pigments in corals are photoprotective,” Nature, vol. 408, no. 6814, pp. 850–853, 2000.

B. Walker, “Conserving biological diversity through ecosystem resilience,” Conservation Biology, vol. 9, no. 4, pp. 747–752, 1995.

M. Nyström, “Redundancy and response diversity of functional groups: implications for the resilience of coral reefs,” Ambio, vol. 35, no. 1, pp. 30–35, 2006.

N. A. J. Graham, S. K. Wilson, S. Jennings et al., “Lag effects in the impacts of mass coral bleaching on coral reef fish, fisheries, and ecosystems,” Conservation Biology, vol. 21, no. 5, pp. 1291–1300, 2007.

S. C. Cardoso, M. C. Soares, H. A. Oxenford, and I. M. Côté, “Interspecific differences in foraging behaviour and functional role of Caribbean parrotfish,” Marine Biodiversity Records, vol. 2, pp. 1–6, 2009.

D. E. Burkepile and M. E. Hay, “Feeding complementarity versus redundancy among herbivorous fishes on a Caribbean reef,” Coral Reefs, vol. 30, no. 2, pp. 351–362, 2011.

C. R. C. Sheppard, M. Spalding, C. Bradshaw, and S. Wilson, “Erosion vs. recovery of coral reefs after 1998 El Niño: Chagos reefs, Indian Ocean,” Ambio, vol. 31, no. 1, pp. 40–48, 2002.

N. A. J. Graham, S. K. Wilson, S. Jennings, N. V. C. Polunin, J. P. Bijoux, and J. Robinson, “Dynamic fragility of oceanic coral reef ecosystems,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 22, pp. 8425–8429, 2006.

S. K. Wilson, N. A. J. Graham, M. S. Pratchett, G. P. Jones, and N. V. C. Polunin, “Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient?” Global Change Biology, vol. 12, no. 11, pp. 2220–2234, 2006.

D. J. Booth and G. A. Beretta, “Changes in a fish assemblage after a coral bleaching event,” Marine Ecology Progress Series, vol. 245, pp. 205–212, 2002.

J. A. Kleypas and K. K. Yates, “Coral reefs and ocean acidification,” Oceanography, vol. 22, no. 4, pp. 108–117, 2009.

G. De'ath, J. M. Lough, and K. E. Fabricius, “Declining coral calcification on the Great Barrier Reef,” Science, vol. 323, no. 5910, pp. 116–119, 2009.

R. P. M. Bak, G. Nieuwland, and E. H. Meesters, “Coral growth rates revisited after 31 years: what is causing lower extension rates in Acropora palmata?” Bulletin of Marine Science, vol. 84, no. 3, pp. 287–294, 2009.

K. R. N. Anthony, D. I. Kline, G. Diaz-Pulido, S. Dove, and O. Hoegh-Guldberg, “Ocean acidification causes bleaching and productivity loss in coral reef builders,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 45, pp. 17442–17446, 2008.

A. Tribollet, C. Godinot, M. J. Atkinson, and C. Langdon, “Seawater carbonate chemistry and dissolution rates by boring microflora during ex situ experiments with dead corals (Porites lobata),” 2009.

F. Rohwer, V. Seguritan, F. Azam, and N. Knowlton, “Diversity and distribution of coral-associated bacteria,” Marine Ecology Progress Series, vol. 243, pp. 1–10, 2002.

T. D. Ainsworth, R. V. Thurber, and R. D. Gates, “The future of coral reefs: a microbial perspective,” Trends in Ecology and Evolution, vol. 25, no. 4, pp. 233–240, 2010.

C. A. Kellogg, “Tropical Archaea: diversity associated with the surface microlayer of corals,” Marine Ecology Progress Series, vol. 273, pp. 81–88, 2004.

R. W. Buddemeier and D. G. Fautin, “Coral bleaching as an adaptive mechanism—a testable hypothesis,” Bioscience, vol. 43, pp. 320–326, 1993.

R. D. Gates and P. J. Edmunds, “The physiological mechanisms of acclimatization in tropical reef corals,” American Zoologist, vol. 39, no. 1, pp. 30–43, 1999.

D. G. Fautin and R. W. Buddemeier, “Adaptive bleaching: a general phenomenon,” Hydrobiologia, vol. 530-531, pp. 459–467, 2004.

M. L. Baskett, S. D. Gaines, and R. M. Nisbet, “Symbiont diversity may help coral reefs survive moderate climate change,” Ecological Applications, vol. 19, no. 1, pp. 3–17, 2009.

M. Stat and R. D. Gates, “Clade D Symbiodinium in scleractinian corals: a, “nugget” of hope, a selfish opportunist, an ominous sign, or all of the above?” Journal of Marine Biology, vol. 2011, Article ID 730715, 9 pages, 2011.

A. H. Baird, R. Bhagooli, P. J. Ralph, and S. Takahashi, “Coral bleaching: the role of the host,” Trends in Ecology and Evolution, vol. 24, no. 1, pp. 16–20, 2009.

P. W. Sammarco and K. B. Strychar, “Effects of climate change/global warming on coral reefs: adaptation/exaptation in corals, evolution in zooxanthellae, and biogeographic shifts,” Environmental Bioindicators, vol. 4, no. 1, pp. 9–45, 2009.

R. B. Aronson and W. F. Precht, “White-band disease and the changing face of Caribbean coral reefs,” Hydrobiologia, vol. 460, pp. 25–38, 2001.

H. A. Lessios, “Mass mortality of Diadema antillarum in the Caribbean: what have we learned?” Annual Review of Ecology and Systematics, vol. 19, pp. 371–393, 1988.

M. Anderson, H. Lund, E. H. Gladfelter, and M. Davis, “Ecological community type maps and biological community descriptions for Buck Island Reef National Monument and proposed marine park sites in the British Virgin Islands,” Biosphere Reserve Research Report 4 VIRMC/NPS, 1986.

J. C. Bythell, Z. M. Hillis-Starr, and C. S. Rogers, “Local variability but landscape stability in coral reef communities following repeated hurricane impacts,” Marine Ecology Progress Series, vol. 204, pp. 93–100, 2000.

C. Menza, M. Kendall, C. Rogers, and J. Miller, “A deep reef in deep trouble,” Continental Shelf Research, vol. 27, no. 17, pp. 2224–2230, 2007.

P. Bongaerts, T. Ridgway, E. M. Sampayo, and O. Hoegh-Guldberg, “Assessing the “deep reef refugia” hypothesis: focus on Caribbean reefs,” Coral Reefs, vol. 29, no. 2, pp. 1–19, 2010.

T. B. Smith, J. Blondeau, R. S. Nemeth et al., “Benthic structure and cryptic mortality in a Caribbean mesophotic coral reef bank system, the Hind Bank Marine Conservation District, U.S. Virgin Islands,” Coral Reefs, vol. 29, no. 2, pp. 289–308, 2010.

C. Wilkinson, Status of Coral Reefs of the World: 1998, Australian Institute of Marine Science, Townsville, Australia, 1998.

B. L. Kojis and N. J. Quinn, “Seasonal and depth variation in fecundity of Acropora palifera at two reefs in Papua New Guinea,” Coral Reefs, vol. 3, no. 3, pp. 165–172, 1984.

R. N. Ginsburg and F. G. W. Smith, “Proceedings of the colloquium on global aspects of coral reefs: health, hazards and history, June 1993,” 1994.

J. A. Maynard, A. H. Baird, and M. S. Pratchett, “Revisiting the Cassandra syndrome; the changing climate of coral reef research,” Coral Reefs, vol. 27, no. 4, pp. 745–749, 2008.

R. P. Kelly, M. M. Foley, W. S. Fisher et al., “Mitigating local causes of ocean acidification with existing laws,” Science, vol. 332, no. 6033, pp. 1036–1037, 2011.

D. Tilman, R. M. May, C. L. Lehman, and M. A. Nowak, “Habitat destruction and the extinction debt,” Nature, vol. 371, no. 6492, pp. 65–66, 1994.

R. J. Miller, A. J. Adams, N. B. Ogden, J. C. Ogden, and J. P. Ebersole, “Diadema antillarum 17 years after mass mortality: is recovery beginning on St. Croix?” Coral Reefs, vol. 22, no. 2, pp. 181–187, 2003.

Y. Loya, K. Sakai, K. Yamazato, Y. Nakano, H. Sambali, and R. van Woesik, “Coral bleaching: the winners and the losers,” Ecology Letters, vol. 4, no. 2, pp. 122–131, 2001.

D. M. Thompson and R. van Woesik, “Corals escape bleaching in regions that recently and historically experienced frequent thermal stress,” Proceedings of the Royal Society B, vol. 276, no. 1669, pp. 2893–2901, 2009.

B. Walker, S. Barrett, S. Polasky et al., “Looming global-scale failures and missing institutions,” Science, vol. 325, no. 5946, pp. 1345–1346, 2009.

G. H. Rau, E. L. McLeod, and O. Hoegh-Guldberg, “The need for new ocean conservation strategies in a high-carbon dioxide world,” Nature Climate Change, vol. 2, pp. 720–724, 2012.