Frontiers in Marine Science

One mechanism giving fleshy algae a competitive advantage over corals during reef degradation is algal-induced and microbially-mediated hypoxia (typically less than 69.5 µmol oxygen L⁻¹). During hypoxic conditions oxygen availability becomes insufficient to sustain aerobic respiration in most metazoans. Algae are more tolerant of low oxygen conditions and may outcompete corals weakened by hypoxia. A key question on the ecological importance of this mechanism remains unanswered: How extensive are local hypoxic zones in highly turbulent aquatic environments, continuously flushed by currents and wave surge? To better understand the concert of biological, chemical, and physical factors that determine the abundance and distribution of oxygen in this environment, we combined 3D imagery, flow measurements, macro- and micro-organismal abundance estimates, and experimentally determined biogenic oxygen and carbon fluxes as input values for a 3D bio-physical model. The model was first developed and verified for controlled flume experiments containing coral and algal colonies in direct interaction. We then developed a three-dimensional numerical model of an existing coral reef plot off the coast of Curaçao where oxygen concentrations for comparison were collected in a small-scale grid using fiberoptic oxygen optodes. Oxygen distribution patterns given by the model were a good predictor for in situ concentrations and indicate widespread localized differences exceeding 50 µmol L^-1 over distances less than a decimeter. This suggests that small-scale hypoxic zones can persist for an extended period of time in the turbulent environment of a wave- and surge- exposed coral reef. This work highlights how the combination of three-dimensional imagery, biogenic fluxes, and fluid dynamic modeling can provide a powerful tool to illustrate and predict the distribution of analytes (e.g., oxygen or other bioactive substances) in a highly complex system.

The massive die-off of the sea urchin Diadema antillarum in 1983–1984 is one the main reasons for low coral recruitment and little coral recovery in the Caribbean. As the natural recovery of D. antillarum is slow to non-existent, multiple restoration studies have been attempted. There are currently three different approaches to obtain individuals for restocking: the translocation of wild-collected juveniles or adults, lab-reared juveniles cultured from wild-collected settlers, or lab-reared juveniles cultured from gametes. All three methods are costly and can only be applied on a relatively small scale. We here propose a fourth, new, approach, which we term assisted natural recovery (ANR) of D. antillarum populations. ANR, a concept already applied in terrestrial restoration to restore forests and grasslands, can accelerate succession by removing barriers to natural recovery. In this study, performed on the Dutch Caribbean island of Saba, suitable settlement substrate was provided in the form of bio ball streamers that were attached to the reef shortly before the settlement season. At the end of the experiment, reefs with streamers had significantly higher D. antillarum recruit densities than control reefs without additional settlement substrate, indicating that the lack of settlement substrate is an important factor constraining natural recovery. However, D. antillarum recruit abundance was low compared to the measured settlement rates, possibly due to low post-settlement survival. The size distribution of recruits showed that recruits almost never became larger than 20 mm, which is likely due to predation. We conclude that, next to low settlement availability, low post-settlement survival and high predation on recruits also constrain the natural recovery of D. antillarum populations on Saba. To improve the survival of settlers till adults, we propose to 1) reduce predation on settlers by using bio balls or other substrates that can provide shelter to larger individuals and 2) optimize the reef habitat by removing macroalgae, either manually or by facilitating other herbivores. To improve the survival of recruits, we suggest to 1) choose sites with a known lower predation density or 2) protect recruits with a corral around the reef underneath the streamers. The combination of these measures could improve prospects for ANR, and we expect this new approach can contribute to the recovery of D. antillarum populations in the future.

A Commentary on
Managing Recovery Resilience in Coral Reefs Against Climate-Induced Bleaching and Hurricanes: A 15 Year Case Study From Bonaire, Dutch Caribbean

by Steneck, R. S., Arnold, S. N., Boenish, R., de León, R., Mumby, P. J., Rasher, D. B., et al. (2019) Front. Mar. Sci. 6:265. doi: 10.3389/fmars.2019.00265

A closer look at the methods of Steneck et al. (2019) reveals two issues of concern in making comparisons between the authors' estimate of coral cover and other published estimates.

• First, their method of estimating coral cover differs from conventional methods.
• Second, contrary to the sites sampled by Steneck and co-workers many of our sites have a coral cover of less than 10 percent and none are above 60%. The sites sampled by Steneck and colleagues appear to be a non-random selection of sites and as such should not have been presented as an average for Bonaire

The deep sloping sides of Saba Bank, the largest submarine atoll in the Atlantic Ocean, show quite different internal wave characteristics. To measure these characteristics, two 350 m long arrays consisting of primary a high-resolution temperature T-sensor string and secondary an acoustic Doppler current profiler were moored around 500 m water depth at the northern and southern flanks of Saba Bank for 23 days. We observed that the surrounding density stratified waters supported large internal tides and episodically large turbulent exchange in up to 50 m tall overturns. However, an inertial subrange was observed at frequencies/wavenumbers smaller than the mean buoyancy scales but not at larger than buoyancy scales, while near-bottom non-linear turbulent bores were absent. The latter reflect more open-ocean than steep sloping topography internal wave turbulence. Both the Banks’ north-side and south-side slopes are locally steeper ‘super-critical’ than internal tide slope angles. However, the three times weaker north-side slope showed quasi-mode-2 semidiurnal internal tides, not high-frequency solitary waves occurring every 12 h, over the range of observations, centered with dominant near-inertial shear around 150 m above the bottom. They generated the largest turbulence when touching the bottom and providing off-bank flowing turbid waters. In contrast, the steeper south-side slope showed quasi-mode-1 internal tides occasionally having excursions > 100 m crest-trough, with weak inertial shear and smallest buoyancy scale turbulence periodicity occurring near the bottom and about half-way the water column, below abundant coral reefs in shallow <20 m deep waters.

 Assessing marine soundscapes provides an understanding of the biological, geological and anthropogenic composition of a habitat, including species diversity, community composition, and human impacts. For this study, nine acoustic recorders were deployed between December 2016 and June 2017 off six Caribbean islands in several Marine Parks: the Dominican Republic (DR), St. Martin (SM), Guadeloupe east and west (GE, GW), Martinique (MA), Aruba (AR), and Bonaire (BO). Humpback whale song was recorded at five sites on four islands (DR, SM, GE, GW, and MA) and occurred on 49–93% of recording days. Song appeared first at the DR site and began 4–6 weeks later at GE, GW, and MA. No song was heard in AR and BO, the southernmost islands. A 2-week period was examined for the hourly presence of vessel noise and the number and duration of ship passages. Hourly vessel presence ranged from low (20% – DR, 30% – SM), medium (52% – MA, 54% – BO, 77% – GE) to near continuous (99% – GW; 100% – AR). Diurnal patterns were observed at BO, GE, and MA with few to no vessels present during night time hours, possibly reflecting the activity of recreational craft and fishing vessels. At the DR and GW sites, vessel traffic was ubiquitous for most of the day, likely reflecting heavy cruise ship and container ship presence. Soundscapes were diverse across islands with persistent fish choruses, sporadic sperm whale (Physeter macrocephalus ) and dolphin (Delphinidae ) presence at BO, minke whales (Balaenoptera acutorostrata ) from late December to late February at MA and an earthquake recorded across all sites. These analyses provide an important first step in characterizing the health and species richness in Caribbean marine parks and demonstrate a surprising high anthropogenic foot print. Vessel traffic in particular contributes adversely to marine soundscapes, masking marine mammal sounds, potentially changing typical animal behavior and raising the risk of ship strike.

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.

Queen conch (Lobatus gigas) is an important food source and export product for Belize, where extraction is regulated by shell length (SL) and market clean weight (MCW) limits. However, lip thickness (LT) limits are used to manage juvenile mortality and reduce risk of growth overfishing in other countries. Empirical studies suggest relationships between LT and sexual maturity vary spatially and need to be determined locally. This study was conducted to determine the most reliable, easily measurable proxy indicator(s) of maturity and associated target size limits in L. gigas that can effectively restrict harvest of juveniles. Morphological measures (SL, LT, lip width, unprocessed meat weight, MCW, operculum dimensions), gonadosomatic index (GSI) and histological evaluations were recorded from L. gigas collected in PHMR before, during, and after the L. gigas closed season. Upon determining Period 2 (during closed season) as the peak reproductive period, relationships between these variables in Period 2 were examined. No relationship was found in males between SL and maturity, and was weak in females, whereas there were significant curvilinear relationships between LT and GSI for both sexes, suggesting urgent need to base size limits on LT not SL. LT at which 50% of the population was mature (LT50) was 15.51 mm for females and 12.33 mm for males, therefore a 16 mm LT limit is recommended. MCW of female L. gigas was also significantly related to GSI, indicating MCW may be an appropriate management tool in conjunction with LT as it can be measured at landing sites whereas shells are usually discarded at sea. However, MCW at which 50% of females were mature (MCW50) was 199 g and many individuals exceeding LT50 had MCW <199 g, suggesting the current 85 g MCW limit is too low to protect juveniles yet 199 g MCW limit would be too high to substitute the recommended LT limit at landing sites. To minimize short-term impacts yet maximize long-term benefits to fishers’ livelihoods, multi-stage adaptive management is recommended that integrates initial catch reductions, followed by introduction of size limits of 16 mm LT, and 150 g MCW. Adjustable LT and MCW limits determined by fishery simulation could later be introduced. 

Health of tropical coral reefs depends largely on the balance between constructive (calcification and cementation) and destructive forces (mechanical-chemical degradation). Gradual increase in dissolved CO2 and the resulting decrease in carbonate ion concentration (“ocean acidification”) in ocean surface water may tip the balance toward net mass loss for many reefs. Enhanced nutrients and organic loading in surface waters (“eutrophication”), may increase the susceptibility of coral reef and near shore environments to ocean acidification. The impacts of these processes on coral calcification have been repeatedly reported, however the synergetic effects on bioerosion rates by sponges are poorly studied. Erosion by excavating sponges is achieved by a combination of chemical dissolution and mechanical chip removal. In this study, Cliona caribbaea, a photosymbiont-bearing excavating sponge widely distributed in Caribbean reef habitats, was exposed to a range of CO2 concentrations, as well as different eutrophication levels. Total bioerosion rates, estimated from changes in buoyant weights over 1 week, increased significantly with pCO2 but not with eutrophication. Observed chemical bioerosion rates were positively affected by both pCO2 and eutrophication but no interaction was revealed. Net photosynthetic activity was enhanced with rising pCO2 but not with increasing eutrophication levels. These results indicate that an increase in organic matter and nutrient renders sponge bioerosion less dependent on autotrophic products. At low and ambient pCO2, day-time chemical rates were ~50% higher than those observed at night-time. A switch was observed in bioerosion under higher pCO2 levels, with night-time chemical bioerosion rates becoming comparable or even higher than day-time rates. We suggest that the difference in rates between day and night at low and ambient pCO2 indicates that the benefit of acquired energy from photosynthetic activity surpasses the positive effect of increased pCO2 levels at night due to holobiont respiration. This implies that excavation must cost cellular energy, by processes, such as ATP usage for active Ca2+ and/or active proton pumping. Additionally, competition for dissolved inorganic carbon species may occur between bioerosion and photosynthetic activity by the symbionts. Either way, the observed changing role of symbionts in bioerosion can be attributed to enhanced photosynthetic activity at high pCO2 levels.

Current trends demonstrate coral reef health in serious decline worldwide. Some of the most well-preserved coral reefs in the Caribbean basin are located in the waters surrounding Bonaire, in the Dutch Caribbean. In many places on the leeward side on islands dominated by trade winds, the shallow reef systems extend into deeper water where they are known as Mesophotic Coral Ecosystems (MCE). Autonomous Underwater Vehicles (AUVs) were used to collect geoacoustic data of these leeward reefs at multiple sites as part of an ocean exploration project. AUV swath bathymetry and side-scan sonar data were analyzed for depth, acoustic backscatter intensity, seafloor slope, and rugosity. These geomorphic metrics were then used as inputs to generate a composite synthetic index of bottom-type to delineate MCE features. A confusion matrix statistical analysis of the acoustic class map showed an overall accuracy of the acoustic classes at 66%, with accuracy of the hard coral class the highest at 83%, and the sandy-bottom class the lowest at 55. The hard coral class was also the statistically most reliable, at over 80%, with the noise class coming in as the least reliable. This morphologic habitat index is a potentially useful new tool in quantifying the extent of MCE located in proximity to Marine Protected Areas (MPAs).

Tropical coral reefs are among the most biologically diverse and economically important ecosystems on earth. Nevertheless, we found dramatic changes in coral communities on the reef slopes of Curaçao and Bonaire since 1973. Cover and abundance declined for virtually all coral species. The data show a shift from communities dominated by framework building species (e.g., Orbicella spp.) to communities consisting of small opportunistic, phenotypically plastic, species, including few remaining structural colonies. Madracis mirabilis, Porites astreoides, Diploria strigosa, and Agaricia lamarcki are at present modest winners in the coral assemblage, although overall cover declined also for these species. Increased frequency and intensity of events inducing coral mortality and ongoing reduction in suitable hard substratum, provided by the remnants of large colony building species, could reduce the chance of these species to remain winners in the longer run. The observed loss in coral cover and the shift from larger structural to smaller opportunistic species reduced reef carbonate production by 67% and therewith, in combination with a trend toward smaller coral colonies, reef complexity. Alarmingly, reefs at upper-mesophotic depths (30–40 m) did not escape the general degradation of the coral community. The negative effects are larger around densely populated areas where local stressors are adding to degradation caused, for instance, by region wide mass bleaching. Without proper conservation and management this already dramatic degradation will continue and turn more and more coral species into losers.