Steneck, R.S.

The “resilience” of coral reef ecosystems has been an important goal of managers and policy makers for decades. At its most basic level, resilience means that if coral reefs suffer damage from say a hurricane or bleaching mortality event, they will recover to their previous state. Remarkably, this has never been documented for any coral reef ecosystem in the Caribbean.

In a highly cited scientific study entitled: “Disturbance and recovery of coral assemblages” (Connell 1997) all existing data on trends of coral reefs world-wide were reviewed but no examples of coral reefs recovering from disturbance in the Caribbean were found (Fig. 1).

Several important studies have documented the decline of coral reef ecosystems in the Caribbean (Gardiner et al. 2003, Jackson et al. 2014) and in the tropical Pacific (Bruno and Selig 2007). The global decline of coral reefs was the impetus for very high impact scientific papers with titles such as “Confronting the coral reef crisis” (Bellwood et al. 2004) and “Rising to the challenge of sustaining coral reef resilience” (Hughes et al. 2010) or specifically asking the shocking question: “Are U.S. coral reefs on the slippery slope to slime?” (Pandolfi et al. 2005). These alarming titles and the associated press coverage caught the attention of managers and policy makers but to date there has been little progress operationalizing coral reef management for resilience. Nevertheless, some studies gave clear advice to managers such as, “Capturing the cornerstones of coral reef resilience, linking theory to practice” (Nyström et al 2008). In that paper, the authors proposed that research identify:

“...empirical indicators of the cornerstones of coral reef resilience. These indicators include functional group approaches” ... “identifying ‘good’ and ‘bad’ colonizers of space, measurements of spatial heterogeneity, and estimates of potential space availability against grazing capacity. The essence of these operational indicators of resilience is to use them as predictive tools to recognize vulnerability before disturbance occurs that may lead to abrupt phase shifts [of coral loss and seaweed increase]. Moving toward operationalizing resilience theory is imperative to the successful management of coral reefs in an increasingly disturbed and human-dominated environment.”

The Nyström et al. 2008 quote describes precisely the approach we have taken since our reef monitoring began in Bonaire in 2003. In 2005, the Bonaire National Marine Park asked for advice on developing a monitoring program, to which we advocated three points: 1) keep monitoring data simple, 2) focus on known drivers and indicators of reef health and 3) monitor trends among those drivers.

Although coral reefs are complex ecosystems, relatively few “drivers” control much of their structure and how they function. “Drivers” are key processes that control critically important aspects of coral reefs. Several processes can interact with one another (Fig. 2). For example seaweed (also called “macroalgae”) are known to poison corals (Rasher and Hay 2010) and reduce or halt the settlement and survival of juvenile corals (Arnold et al. 2010, Steneck et al. 2014). It has also been shown that herbivorous fishes are capable of reducing or eliminating macroalgae from coral reefs (Lewis 1986, Williams and Polunin 2001). Thus herbivores such as parrotfish enable the recruitment of reef corals, reduce toxic seaweed and facilitate the growth of complex coral habitats into which juvenile reef fish recruit (Caselle and Warner 1996). These drivers and their interactions have been viewed as integral to a complex system of feedbacks that maintain healthy coral reefs (Fig. 2: Mumby and Steneck 2008); they are the “cornerstones” advocated by Nystrom et al. (2008).

Evaluating key drivers of coral reef health and resilience identified in Fig. 2 is complicated because all components interact. Therefore, it is difficult or impossible to define a specific level as being particularly healthy or unhealthy for any given coral reef. Instead, our monitoring protocol measures components to determine changes through time. This is because there is a consensus on trends that constitute healthy trajectories in reef condition. For example, trends of increasing live coral cover or decreasing macroalgal abundance are both moving towards improved conditions (Fig. 3). This allows us to create a very simple means of reporting condition and monitoring trends in key drivers. Importantly, this approach was developed explicitly in the 2005 Bonaire report and has been applied semiannually ever since. All semiannual Bonaire Reports beginning in 2003 are available via STINAPA’s website (http://stinapabonaire.org/nature/coral-reefs-adjacent-waters/).

Managing for coral reef resilience in Bonaire National Marine Park

First, it is important to acknowledge there are several unique biophysical and social factors that play a role in the health of Bonaire reefs. The island is sufficiently far south that hurricane frequency is very low compared to elsewhere in the Caribbean. It is a relatively dry island with very little agriculture, generally low runoff and no rivers that can carry harmful sediment, nutrients and chemicals to coral reefs. In 1971, the island banned the use of spearfishing and there was traditionally very little use of fish traps that are so common throughout the Caribbean. We know of no other coral reef system in the Caribbean with those restrictions but those two factors alone protect herbivorous parrotfish that are easy to shoot with spears and readily enter fish traps. The consequences of these factors are that Bonaire’s coral reefs have relatively intact habitat architecture and an abundance of herbivorous parrotfish that keep seaweed cropped short (Steneck, personal observation, 1990, Kramer 2003).

With the quality of Bonaire’s reefs attracting divers from around the globe, a diver fee was instated to fund a non-governmental organization (STINAPA Bonaire) that manages the Bonaire National Marine Park (BNMP) (Solofa, Chapter 10). Without this NGO, the management of Bonaire’s reefs may have been impossible.

We began monitoring reef sites in Bonaire in 2003. The six initial sites (Fig. 4) were designated by Ms. Kalli DeMeyer who was the first Manager of the Bonaire National Marine Park (BNMP). In 2008 enforcement of the Fish Protected Areas (FPAs) began so in 2009, Mr. Ramón de León the then Manager of BNMP suggested the addition of three sites to balance sampling around the FPAs. In 2010 one additional site (free of divers) was added making the total of 11 monitored sites (Fig. 4).

Stratification of sampling design and repeated sampling at fixed locations is necessary for precision and statistical power. Accordingly, we have repeatedly visited the same sites (adding sites when FPA’s were established), at 10 m depths, employing identical methods for the past 14 years (Fig. 4). These sites are physically similar in terms of wave action and sediment effects so they can be combined to assess long-term trends.

Coral reef ecosystems are created by, and require, live coral for their structure and function. Bonaire’s reefs remain among the healthiest in the Caribbean in that corals occupy more space than any other group (specifically seaweed: Fig. 5; Steneck, Chapter 1). In contrast, most formerly coral-dominated reefs are now seaweed-dominated reefs throughout the Caribbean. Nevertheless, static measures of coral or algal cover are not as telling as are the trends.

Unusually warm ocean temperatures surrounding Bonaire during the late summer and fall of 2010 caused 10 to 20 % of corals to bleach (Fig. 1). Bleaching persisted long enough to kill about 10 % of the corals within six months of the event (Steneck, Phillips and Jekielek Chapters 2A – C). That mortality event resulted in the first significant decline in live coral at sites monitored since 1999 (Fig. 2). Live coral declined from a consistent average of 48 % (from 1999 to 2009) to 38 % in 2011 (Steneck Chapter 1). This increase in non-coral substrate increased the area algae can colonize and the area parrotfish must keep cropped short (Mumby and Steneck 2008). For there to be no change in seaweed abundance would require herbivorous fish biomass and population densities to increase, but they have been steadily declining in recent years. This decline in parrotfish continues despite the establishment of no-take areas (called Fish Protection Areas – FPAs) and the recent law that completely bans the harvesting of parrotfish. The other major herbivore throughout the Caribbean is the black spined sea urchin, Diadema antillarum. However, since 2005 Diadema abundance has steadily declined. Damselfishes continue to increase in abundance (except in FPAs) and their aggressive territoriality reduces herbivory where they are present. These declines in herbivory resulted in a marked increase in macroalgae (Steneck Chapter 1). Although patchily distributed, algae on some of Bonaire’s reefs are approaching the Caribbean average (Kramer 2003). All research to date indicates that coral health and recruitment declines directly with increases in algal abundance (e.g., Arnold et al 2010).
On the bright side, predatory fishes are increasing in abundance in general but increasing most strongly in FPAs. Typically, responses to closed areas take 3 - 5 years to begin to manifest themselves. Predators of damselfishes have increased significantly in FPA sites and there, damselfish abundances are trending downward. These trends are the first signs of changes in the FPAs, and they are encouraging.
Overall, Bonaire’s coral reefs today are more seriously threatened with collapse than at any time since monitoring began in 1999.
 
Monitoring Results
The abundance of live coral at the monitoring sites has been remarkably constant since 1999. However, the bleaching related mortality event (Fig. 1) resulted in the first marked decline in live coral.
Seaweed abundance (“macroalgae”) increased sharply in 2011. While the greatest increase in algae occurred at the 18th Palm site where effluent could have increased nutrient levels, most of the other sites showed marked increases in algal abundance (see Steneck Chapter 1). Coralline algae, which has been shown to facilitate coral recruitment, remains at or near unprecedentedly low levels (Fig 2). Herbivory from parrotfishes and the grazing sea urchin Diadema antillarum remains at or near the lowest levels recorded since monitoring began in 1999 (Fig. 3 and see Cleaver Chapter 5). Herbivory from parrotfish is widely thought to be most important (e.g., Steneck and Mumby 2008) but territorial damselfishes can negate parrotfishes’ positive effects by attacking grazing herbivores and preventing them from effectively grazing (Arnold et al 2010). Damselfish abundances have trended upward in recent years (Fig. 3). However, there is a hint of a reversal to this trend in the FPAs (see Arnold Chapter 3). This reversal is consistent with the possibility that areas without fishing have elevated abundances of damselfish predators such as species of groupers and snappers (Randall 1965)  
Predatory fishes including snappers, groupers, barracuda, grunts and others increased in abundance at our monitored sites (Fig. 4 and see DeBey Chapter 6a). Specific predators known to eat damselfishes (see Preziosi Chapter 6b) show variable population densities with only a hint of an increase in 2011.   
Predatory fishes increased in abundance in both biomass (most striking) and population densities (Fig. 5). While biomass of predators in FPA and control sites is identical, the population density of predators is slightly greater at FPA sites
Coral recruitment remained lower than recorded in 2003 and 2005 (Fig. 6). However, the abundance of juvenile corals was higher in 2011 than was quantified in 2009

Bonaire’s reefs remain among the best in the Caribbean. However, our monitoring has revealed some potentially troubling trends that may require management action. In 2005, we reported to the Bonaire Marine National Park on the status of Bonaire’s coral reefs, and we suggested a strategy for monitoring trends among four key reef attributes we believe track the health and resilience of Bonaire’s reefs (Steneck and McClanahan 2005). Here we report the results of monitoring studies conducted 2003, 2005 and now 2007 at each site. Where appropriate, we drew from Bonaire’s first AGRRA assessment conducted in February 1999 (Kramer and Bischof 2003) to extend temporal trends over a period of eight years. 
Troubling trends
We see three troubling trends of increased macroalgae, declining herbivory from parrotfish, and increases in damselfish populations. Of these, the first two are most serious (see Chapters 1, 2 and 3). Secondary trends of concern, increases in damselfish populations (Chapter 4) and declines in coralline algae (Chapter 1), could lead to reduced recruitment of reef corals (Chapter 7), but to date this is not evident (Chapter 7). Importantly, coral cover remains relatively high (Chapter 1). The monitored group of carnivorous fishes, the lutjanid snappers, are holding constant but we remain concerned about the past (Steneck and McClanahan 2003) and continued loss of other larger bodied reef carnivores such as groupers and barracuda. The positive ecological role of parrotfish is well documented (e.g. Mumby et al. 2006) so their decline is troubling. It is unclear exactly why their population densities are declining. While parrotfish are not currently a widely sought group of reef fish (Chapter 8), fishing pressure on them is growing. It is possible they are vulnerable to even modest fishing pressure, particularly from fish traps. Accordingly, we recommend that the capture and killing of parrotfish be stopped because of their key ecological role on Bonaire’s coral reefs. Further, other groups of grazing herbivores such as the longspined sea urchin (Diadema antillarum) are increasing but too slowly to effectively replace the functional role of parrotfish (Chapter 1). We suggest continued monitoring of key drivers of reef health (coral cover, algal abundance, herbivory and coral recruitment). Some standard protocols such as the Atlantic and Gulf Rapid Reef Assessment (AGRRA) are entirely commensurable with the data presented in our reports in 2003, 2005 and 2007 (this report). A streamlined monitoring protocol is likely to be most useful to managers to alert them as a potential problem is growing and, perhaps more importantly, to show improvement when it occurs.
 
 

Bonaire has long been considered to have amongst the healthiest reefs of the Caribbean. However, at the 2002 Annual Meeting of Pew Fellows for Marine Conservation in Bonaire, several scientists with a long history of research on Bonaire’s coral reefs, expressed concern over the future of the island’s reefs. Specifically, they identified the decline in large predatory fish such as groupers as a noticeable change during the past decade. They suspected that this change resulted from increased fishing pressure on Bonaire’s reefs. They also suggested the Bonaire authorities take action to protect the reef-fish stocks. In response to those concerns, officials of the Bonaire Marine Park consulted with scientists and fishermen on Bonaire to explore the possibility of establishing fish protected areas (FPAs), as a way to protect the reef fish stocks. If FPAs improve both fish stocks and the condition of the coral reef, all stakeholders will profit. If fish stocks increased significantly in FPAs, a “spill over” of these fish to adjacent fished areas would be expected. Also, fish that perform important ecological functions could improve the quality of the coral reef ecosystem. Therefore, areas protected from fishing should have healthier coral reefs, which would also improve the island’s valuable ecotourism businesses. The Pew Fellows program funded a research project designed to identify potential FPAs. The Bonaire Marine Park authority, in consultation with the local fishing community would determine the location and size of the FPAs. To monitor the effects of fish protection areas so fishing impacts can be isolated from other factors (such as natural changes, shore-based impacts or effects of scuba divers), an equal number of similar reef sites were selected for study, with half closed to fishing while half remaining open (as “control” reefs). This report reviews the status and recent trends of coral reefs in the Caribbean and Bonaire. It identifies the key features of healthy reefs and how Bonaire’s reefs compares with those elsewhere in the Caribbean. The seven chapters go into scientific detail on factors contributing to the condition of Bonaire’s reefs as of March and April 2003. Special focus will be on factors that threaten reef health or are critical to reef resilience such as seaweed overgrowth, nutrient inputs from land and the ecology of juvenile corals. The report concludes with chapters on the socioeconomic effects of Bonaire’s coral reefs on the fishing and diving industries that depend on them.
Summary Results 2003: The Biological Status of the Coral Reefs of Bonaire & Socioeconomic Implications
 In March and April of 2003, teams of researchers studied the coral reefs of Bonaire to establish the baseline conditions that currently exist and against which trends can be determined and future changes from fish protection areas be assessed. Six study sites were chosen with advice from the Bonaire Marine Park. They represent a range of comparable reefs minimally affected by the 1999 Hurricane Lenny. The sites selected for this study were: Windsock, Plaza, Forest on Klein Bonaire, Scientifico, Barcadera and Karpata (Fig. 0.4). When feasible, parallel studies were conducted at 5 and 10 m depths, however, only the latter depth had fully developed reefs at all sites. The study was designed to quantify the patterns of abundance of the dominant reef organisms as well as to study the processes that control their abundances or threaten their stability. This was done to establish a baseline and to determine if significant differences exist among any of the study sites that would make them a poor choice as a FPA. We also examined some socioeconomic factors related to fishing and scuba diving activities if FPAs are established in Bonaire.

Abstract

Coral cover on Caribbean reefs has declined rapidly since the early 1980's. Diseases have been a major driver, decimating communities of framework building Acropora and Orbicella coral species, and reportedly leading to the emergence of novel coral assemblages often dominated by domed and plating species of the genera Agaricia, Porites and Siderastrea. These corals were not historically important Caribbean framework builders, and typically have much smaller stature and lower calcification rates, fuelling concerns over reef carbonate production and growth potential. Using data from 75 reefs from across the Caribbean we quantify: (i) the magnitude of non-framework building coral dominance throughout the region and (ii) the contribution of these corals to contemporary carbonate production. Our data show that live coral cover averages 18.2% across our sites and coral carbonate production 4.1 kg CaCO3 m−2 yr−1. However, non-framework building coral species dominate and are major carbonate producers at a high proportion of sites; they are more abundant than Acropora and Orbicella at 73% of sites; contribute an average 68% of the carbonate produced; and produce more than half the carbonate at 79% of sites. Coral cover and carbonate production rate are strongly correlated but, as relative abundance of non-framework building corals increases, average carbonate production rates decline. Consequently, the use of coral cover as a predictor of carbonate budget status, without species level production rate data, needs to be treated with caution. Our findings provide compelling evidence for the Caribbean-wide dominance of non-framework building coral taxa, and that these species are now major regional carbonate producers. However, because these species typically have lower calcification rates, continued transitions to states dominated by non-framework building coral species will further reduce carbonate production rates below ‘predecline’ levels, resulting in shifts towards negative carbonate budget states and reducing reef growth potential.

Bonaire’s coral reefs remain among the healthiest in the Caribbean. Although the island’s reefs have suffered bleaching disturbances similar to those plaguing reefs throughout the Caribbean, they uniquely show signs of recovery. Here we highlight key findings from our March 2015 biennial coral reef monitoring expedition. We put the findings in the context of both the trends recorded since 2003 when we began our regular monitoring and the most recent research related to the factors controlling the structure and functioning of healthy coral reef ecosystems. 

Abstract Distribution and abundance of coral diseases have been well documented, but only a few studies con- sidered diseases affecting crustose coralline algae (CCA), particularly at the species level. We investigated the spa- tiotemporal dynamics of diseases affecting CCA along the south coast of Curac ̧ao, southern Caribbean. Two syn- dromes were detected: the Coralline White Band Syndrome (CWBS) previously described and the Coralline White Patch Disease (CWPD) reported here for the first time. Diseases were present at all six study sites, and our results did not reveal a relationship between disease occurrence and human influence. Both diseases were more prevalent on the shallower reef flat than on the deeper reef slope, and during the warm/rainy season than during the cold/dry season. The patterns observed were consistent with a positive link between temperature and disease occurrence. Reef flat communities were dominated by Neogoniolithon mamillare and Paragoniolithon solubile, whereas deeper habitats were dominated by Hydrolithon boergesenii. Dis- eases affected all the species encountered, and no prefer- able host was detected. There was a significant relationship between both disease occurrences and CCA cover. Moni- toring of affected patches revealed that 90 % of lesions in CWBS increased in size, whereas 88 % of CWPD lesions regenerated over time. CWBS linear progression rate did not vary between seasons or species and ranged from 0.15 to 0.36 cm month-1, which is in the same order of mag- nitude as rates previously documented. We conclude that diseases have the potential to cause major loss in CCA cover, particularly in shallow waters. As CCA play a key role in reef ecosystems, our study suggests that the emer- gence of diseases affecting these algae may pose a real threat to coral reef ecosystems. The levels of disease reported here will provide a much-needed local baseline allowing future comparisons. 

TABLE OF CONTENTS:

• Chapter 1: Patterns and trends in corals, seaweeds
• Chapter 2: Trends in Bonaire’s herbivorous fish: change over time 
• Chapter 3: Fish bite rates of herbivorous fishes
• Chapter 4: Status and trends in sea urchins Diadema and Echinometra 
• Chapter 5: Patterns of distribution, abundance and temporal trends of the sea urchins Diadema antillarum and Echinometra lucunter in the shallow reef zones of Bonaire
• Chapter 6: Damselfish density and abundance: distribution and predator impacts 
• Chapter 7: Patterns of predatory fish biomass and density within and around Fish Protection Areas of the Bonaire Marine Park
• Chapter 8: Juvenile Corals

Global-scale deteriorations in coral reef health have caused major shifts in species composition. One projected consequence is a lowering of reef carbonate production rates, potentially impairing reef growth, compromising ecosystem functionality and ultimately leading to net reef erosion. Here, using measures of gross and net carbonate production and erosion from 19 Caribbean reefs, we show that contemporary carbonate production rates are now substantially below historical (mid- to late-Holocene) values. On average, current production rates are reduced by at least 50%, and 37% of surveyed sites were net erosional. Calculated accretion rates (mm/year) for shallow fore-reef habitats are also close to an order of magnitude lower than Holocene averages. A live coral cover threshold of around 10% appears critical to maintaining positive production states. Below this ecological threshold carbonate budgets typically become net negative and threaten reef accretion. Collectively, these data suggest that recent ecological declines are now suppressing Caribbean reef growth potential.