Arnold, S.N.

Coral reefs are among the world’s most endangered ecosystems. Coral mortality can result from ocean warming or other climate-related events such as coral bleaching and intense hurricanes. While resilient coral reefs can recover from these impacts as has been documented in coral reefs throughout the tropical Indo-Pacific, no similar reef-wide recovery has ever been reported for the Caribbean. Climate change-related coral mortality is unavoidable, but local management actions can improve conditions for regrowth and for the establishment of juvenile corals thereby enhancing the recovery resilience of these ecosystems. Previous research has determined that coral reefs with sufficient herbivory limit macroalgae and improve conditions for coral recruitment and regrowth. Management that reduces algal abundance increases the recovery potential for both juvenile and adult corals on reefs. Every other year on the island of Bonaire, Dutch Caribbean, we quantified patterns of distribution and abundance of reef fish, coral, algae, and juvenile corals along replicate fixed transects at 10 m depth at multiple sites from 2003 to 2017. Beginning with our first exploratory study in 2002 until 2007 coral was abundant (45% cover) and macroalgae were rare (6% cover). Consecutive disturbances, beginning with Hurricane Omar in October 2008 and a coral bleaching event in October 2010, resulted in a 22% decline in coral cover and a sharp threefold increase in macroalgal cover to 18%. Juvenile coral densities declined to about half of their previous abundance. Herbivorous parrotfishes had been declining in abundance but stabilized around 2010, the year fish traps were phased out and fishing for parrotfish was banned. The average parrotfish biomass from 2010 to 2017 was more than twice that reported for coral reefs of the Eastern Caribbean. During this same period, macroalgae declined and both juvenile coral density and total adult coral cover returned to pre-hurricane and bleaching levels. To our knowledge, this is the first example of a resilient Caribbean coral reef ecosystem that fully recovered from severe climate-related mortality events.

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

This report characterizes the state of Bonaire’s reefs as of March 2005. We pay particular attention to structural and functional attributes of reefs that have changed in so many other Caribbean reefs. We characterize coral reefs by their resident organisms and the forces regulating their distribution and abundance. Thus, corals, algae and fish define the “structure” of coral reefs but climate changes, diseases, hurricanes, overfishing, sedimentation and excess nutrients may affect how they “function”. Recent unfavorable changes in the structural and functional attributes of reefs have caused “the coral reef crisis” (Bellwood et al. 2004). In Caribbean coral reefs the most alarming changes have been the declines in the abundance of corals, sea urchins and reef fishes and the accompanying increases in large harmful seaweeds (called “macroalgae”). The decline in coral and increase in macroalgae, called a “phase shift”, represents a significant change in the structure of coral reef ecosystems that could lower its resilience.

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In March of 2005, a team of graduate students from the University of Maine revisited six study reefs on Bonaire to determine the status of those reefs and to detect if any change has occurred since March of 2003 when the last such survey was conducted. The study sites established in 2003 from north to south are: Karpata, Barcadera, Reef Scientifico, Forest on Klein Bonaire, Plaza and Windsock. Bonaire’s shallow (10 m) reefs remain in good condition. Coral cover averaged 47% in 2005 compared to 46% in 2003 (no change). Turf algae have increased and coralline algae have declined slightly over the past two years. Harmful seaweed “macroalgae” abundance remains low (2% in 2005 and 5% in 2003; see Steneck in this report) at the 10 m depth we studied. At depths below 20 m, macroalgae are now and have been (for at least the past 30 years) much more abundant (e.g. Van den Hoek et al. 1975) The absence of macroalgae in Bonaire most likely relates to the abundance of seaweedeating species or “herbivores”. Caribbean-wide, harmful macroalgal seaweed abundance corresponds inversely with the abundance of grazing fish such as parrotfish and tangs (Fig. 1). No comparable plot exists for seaweed abundance and any other measured factor on reefs.

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Changes over the past two decades
Comparisons between the status of reefs over a few years tell us little about long-term changes. For example, today there is a distinct demarcation between where Bonaire’s fringing reefs begin at 5 to 10 m depth and the shore. This region today is largely coralfree and dominated by rubble and sediment laden turf algae. However, this may not have always been the case. Prior to whiteband disease that killed nearly 90% of the elkhorn and staghorn corals in the Caribbean (i.e. Acropora palmata and A. cervicornis) (Aronson et al. 1998, Aronson and Precht 2001), most of the near shore zone was coral-dominated.
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Coral cover in the near shore zone surrounding Bonaire has declined dramatically and is now dominated by dead coral rubble where once elkhorn and staghorn corals had formed near monocultures prior to white band disease. Five of our six study sites have changed dramatically over the past 20 years except for Karpata. The decline of the Acropora species may have allowed competitively inferior species such as lettuce, pencil, finger and fire corals (Agaricia spp, Madracis spp, Porites porities and Millepora complanata) to expand since all have increased in abundance since the Van Duyl study (1985). Corals are not the only group to have changed dramatically since the 1980s. Diadema antillarum, the dominant grazing sea urchins was abundant in the near shore zone until it succumbed to the mass mortality of the mid 1980s. Today, more than 20 years later it remains below detectable levels at most of the sites we studied (Smith and Malek this report, Steneck this report). These changes, along with the significant declines in large predator finfish (see Bonaire Report 2003) indicate that several key players for the resilience of coral reefs (e.g. Fig. 3) have declined in abundance.

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. 

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

Abstract:

Although Bonaire’s coral reefs remain among the healthiest and most resilient in the Caribbean, this IUCN report based on the IUCN Resilience Assessment of Coral Reefs highlights some of the threats that exist to Bonaire’s coral reefs, and which could have serious implications for resilience to future climate change and other threats. The report identified recommendations for addressing the current threats, as well as high and low resilience sites.

The threats and recommendations identified include:

Coastal development and artificial beaches.
Recommendation: All coastal construction on Bonaire should be strictly regulated and follow the construction guidelines. The guidelines should become law in order to be enforced appropriately.

Leaching from septic tanks.
Recommendation: It is strongly recommended that Bonaire invest in appropriate sewage treatment facilities to improve water quality and increase the resilience of its valuable coral reefs. It is also recommended that a water quality monitoring program be set up and sustained.

Increasing damselfish populations.
Recommendation: It is recommended that the fishing of predatory fish species on Bonaire’s coral reefs be controlled and managed to a sustainable level to prevent population explosions of prey fish capable of modifying the reef habitat.

Trididemnum and Lobophora.
Recommendation: It is recommended that the populations of Trididemnum and Lobophora are closely monitored and the factors contributing to the unnatural abun- dance of these coral-overgrowing organisms should be studied and then eliminated.

Due to a variety of factors affecting resilience which were assessed using the IUCN methodology, sites were also ranked according to their overall resilience: 

It is noteworthy that sites with lowest resilience ratings (e.g. Chachácha) are those most impacted by coastal development, while sites with highest resilience ratings (e.g. Marine Reserve North, Playa Frans, Karpata, Margate Bay, Vista Blue and South Bay) are those furthest away and least impacted by coastal development.