40 years of change on the coral reefs of Curaçao and Bonaire

Summary

Tropical coral reefs are among the most species-rich and productive ecosystems on earth. They cover only 0.1-0.5% of the ocean floor, but provide a home to almost a third of all fish species and other marine biota. Just like with tropical rainforests, the terrestrial counterpart of these reefs, 3-dimensional complexity underlies this unique biodiversity. On coral reefs, such structural complexity is mainly provided by scleractinian corals. In the interest of growth and protection, these organisms deposit large amounts of limestone, which provides the rigid foundation for the reef. In this way, corals facilitate complex ecosystem functioning and offer shelter and substratum to an exceptional diversity of species. In addition, millions of people depend on these coral reefs, for goods and services such as nourishment (fishing), coastal protection, tourism and recreation. In spite of this, coral reefs are at present under substantial pressure as a consequence of increased human activities. Large-scale global processes such as climate change have a severe impact on these delicate systems, while at the same time a variety of stressors including overfishing, coastal development and pollution substantially reduce reef resilience on a local scale. In this thesis I describe various aspects of the ecological degradation that coral reefs in the Caribbean have undergone since the early 1970s, as a result of factors associated with continuous human population growth (e.g. pollution, overfishing, climate change). The focus of the presented work lies on the coral reefs surrounding Curaçao and Bonaire (southern Caribbean).

Chapter I

This chapter serves as an introduction explaining the importance of coral reefs and focusses on the main threats that these delicate ecosystems face today. Specifically, it emphases the history and current status of coral reefs in the wider Caribbean region. The main research topics of this thesis are presented, which revolve around the spatio-temporal dynamics of benthic sessile reef communities and the impact that reef degradation and shifts in community composition have on the carbonate budget of the studied reefs.

Chapter II

Chapter II describes changes in the composition of benthic sessile coral communities on the basis of a 40-year time series. In 1973, Prof. dr. Rolf Bak photographed 16 sections of coral reef on the reef slopes of Curaçao and Bonaire, each measuring 9 m2. Since then, these sections were photographed almost annually. To date, this is the longest running time series on coral reefs in the world, dating from before the mass-mortality of the branched Acropora corals and the Diadema antillarum sea urchins in the 1980s and the major bleaching events in 1998, 2005 and 2010. Quadrats were positioned at four locations along a depth gradient at 10, 20, 30 and 40 meters, respectively. Where the pre-1980 reef configurations are still characterized by exceptionally high cover of scleractinian corals we subsequently see a shift towards a dominance of fleshy macroalgae and algal turf assemblages. These fast-growing opportunistic organisms appear to thrive in the altered reef environment. Reduced herbivory and increased nutrient loads have rapidly provided these algae a competitive advantage over the already weakened corals and calcifying algae. The observed gradual decline in coral to an average cover of less than 10% inherently means a substantial loss of the fundament that underpins the striking biodiversity on these reefs. The rigidity provided by corals can by no means be accommodated by soft-bodied algae. Notably, this chapter describes the manifestation of a novel player that, since the early 2000s, is gaining a foothold on these reefs: benthic cyanobacterial mats. These thick red-brown bacterial assemblages are dominated by cyanobacteria and have become one of the prominent components on these reef. They are comparable to the toxic planktonic cyanobacteria that bloom in freshwater lakes during summertime. Similar to these assemblages, cyanobacterial mats on reefs are known to have a wide variety of negative effects on reef communities including the inhibition of larval settlement, acting as pathogens, smothering other organisms, and creating an anoxic environment. A striking conclusion of this chapter is that the observed path of reef degradation occurs at least down to 40 m depth. Considering the ongoing increase of anthropogenic impact on the coral reef environment, the rise of cyanobacterial mats in combination with algae and sponges is hypothesized to represent the next alarming step in the degradation of coral reefs.

Chapter III

In this chapter, shifts in the composition of coral species assemblages are described on the basis of the same time series as presented in the previous chapter. Whereas Chapter II described the trajectories of change of the various sessile organisms, this chapter focusses specifically on the different types of scleractinian corals. Although virtually all coral species declined in cover and abundance over the course of the studied period, a community shift was observed towards dominance of opportunistic species. While the historically prominent framework-building species of the Orbicella and Acropora genera have largely been diminished in the quadrats, species such as Madracis mirabilis, Porites astreoides, Pseudodiploria strigosa (formerly Diploria strigosa), and Agaricia lamarcki appear to possess life-history traits that allow them to better cope with the increasingly more hostile marine environment. Their persistence might make these opportunistic species modest ‘winners’ in the present-day coral assemblage. Yet, their overall cover declined over the past decades as well. A major concern is that these ‘weedy’ corals cannot equal the calcification rates of Orbicella and Acropora species, neither can they produce comparable architectural relief. Indeed, the gross calcium carbonate production of these reefs decline, on average, by 67% over the studied time period.

Chapter IV

On a healthy reef there is a subtle balance between calcification and erosion, which results in the deposition of calcium carbonate and ultimately net reef accretion. Current global and local disturbance, however, is affecting this balance at increasingly more sites, often pushing it towards net destruction of the limestone structures that form the foundation of these reefs. In addition to a general decline in the abundance of carbonate producing organisms (corals, calcifying algae) (Chapter II and Chapter III), we also see that various bioeroding organisms appear to thrive under the current reef conditions. On many reefs in the Caribbean, excavating sponges are the dominant organisms to bore into the coral skeleton. They do this by chemically dissolving limestone in combination with the mechanical removal of limestone fragments (chips). These sponges are found to increase in both abundance and eroding capacity as a result of pollution, ocean acidification and surface water heating. Nonetheless, to date relatively little is known about these organisms. In this chapter various methods, including a flow-through incubation method are presented to quantify erosion rates of the six most prominent bioeroding sponges existing on the reefs of Curaçao. Markedly, the flow-through incubation methodology prevented the accumulation of waste and the depletion of oxygen, resulting in more accurate estimates for chemical erosion. Considerable interspecific variation was observed in the capacity of the various sponges to mechanically remove CaCO3 chips and chemically dissolve coral substrate. This observed interspecific variability could evidently be related to specific life-history traits such as the adopted boring strategy (i.e. gallery-forming, cavity-forming or network-working) and presence or absence of symbiotic zooxanthellae. Similarly, a distinct diurnal pattern was observed, where species that have high zooxanthellae densities have higher erosion rates at daytime. Such a pattern was absent in species with a low abundance or complete absence of zooxanthellae.

Chapter V

Chapter V describes the effect that decreasing calcification and increasing erosion have on the net production of calcium carbonate on the reefs of Bonaire. Net production and maximum reef accretion potential were determined on the basis of the ReefBudget approach for 115 locations on the shallow reef on the leeward side of Bonaire and Klein Bonaire. The balance is drawn up between the gross biogenic calcification and the gross biogenic erosion, which ultimately yields an estimate for the net carbonate production. For each site, the ReefBudget method was applied to the terrace zone (~ 5 m depth) and to the shallowest area of the reef slope (~ 10 m depth). The striking results indicate that many shallow reef sites display marginal growth or even net loss of carbonate substrate. The maximum reef accretion potential of the vast majority of the studied reef sites will, in their current configurations, not match the most optimistic projections for of future sea level rise (IPCC 2018: RCP2.6 scenario). Alarmingly, reefs with the lowest vertical accretion potential are found in regions characterized by a low coastline (often < 1 m above sea level), and include the coastal areas with highest human activity and development around Kralendijk (capital). The current absence of well-developed, rapidly accreting shallow reefs that would otherwise aid in reducing wave energy at the shoreline makes these regions more susceptible to inundation. The risk of flooding will be aggravated especially by the increased frequency and intensity of tropical storms, hurricanes and extreme swell events.

Chapter VI

In Chapter VI, the new time series described in the previous chapter is used to address both the recent developments within the coral and fish community and the current status of the coral reefs and on the leeward side of Bonaire at remarkably high spatial resolution. A novel classification of present-day benthic reef habitats is proposed for reefs in the lower-terrace and drop-off zones. Four distinct benthic communities are classified within each zone, characterized by distinct configurations of both biotic and abiotic (e.g. sand, rubble) constituents. The majority of the eight newly described communities show little resemblance to pre-1980 configurations. Similarly, a thorough description of reef fish communities is provided for the two zones. Within fish communities, the focus lies on the current population status of herbivorous (parrotfish, surgeonfish and damselfish) and commercially important fish species (groupers and snappers). Their abundance and total biomass declined ubiquitously across the shallow reef of Bonaire. Both Chapters V and Chapter VI demonstrate that spatially a distinct gradient of ecological degradation exists on a fine spatial scale (the leeward fringing reef of Bonaire), from nearly pristine reefs in the north to reefs that are at the tipping point of full functional collapse (in front of Kralendijk). The data presented in these chapters further emphasize the negative anthropogenic impacts that locally threaten ecological functioning of coral reefs, but also hints towards stabilization of degradation and possible recovery when local conditions are favourable. The currently existing near-pristine reefs and the reefs to which the latter findings apply should be the ones we learn from to implement adequate management of local stressors.

Chapter VII

In the final chapter the overall gloomy findings of this thesis are discussed thoroughly. The chapter ends with a positive note, namely that the coral reefs are not lost yet. Mainly the findings described in Chapter V and Chapter VI give a modest reason for hope, at least for the shallower reef zones. The presented work shows that nowadays, under the harsh global environment, it is still possible to maintain reefs that exist in relatively good conditions. The latter appears to be strongly correlated to favourable local conditions (both natural and anthropogenic) (see also Chapter II). These reefs should be studied in detail to reveal the processes underlying their notable ecological success. Furthermore, it is tentatively hypothesized that adequate local management at least in part, facilitated an apparent stabilizing trend observed on the shallow coral reefs around Bonaire. The observation that some of the least degraded reefs are found in marine reserves, where entrance for humans is prohibited, suggests that proper local nature policies indeed aid in making reefs more resilient to the large-scale global disturbance. The main message presented here is that Caribbean coral reefs have been heavily impacted over the past decades but that these reefs and the essential services they provide are not yet lost. Nonetheless, we will have to act now and intervene, on a global and local scale, in order to maintain relatively healthy reefs and improve the condition of severely impacted reefs!