Duyl, F.C. van

Student Report 

Areas like the Caribbean reefs are a biodiversity hotspot. Deeper waters are shown to be of importance for the structure and composition of biological marine communities, but until now only a view studies have been performed on mesophotic reefs (30-100m depth). During three exploratory dives in a submarine along the coast of Bonaire, widespread fields of benthic cyanobacterial mats (BCMs) were found from 45m till 90m depth. These mats are dense structures consisting of different microbial organisms, dominated by cyanobacteria. No previous studies are available of such mats at these depths. Therefore the first aim of this study was to map the distribution of deep BCMs along the west coast of Bonaire, including Klein Bonaire, and to gather more bathymetric data. Almost 30% of the Bonairean west coast contained BCMs. Thereof 44% were found in front of Kralendijk or its suburbs along the coast. BCMs were only found on relative flat and sandy bottoms. Therefore it is thought that the presence of flat and sandy bottoms play a key role in the development of BCMs, but pollution associated with populated areas might play an important role as well. More research is needed to investigate how big the effect of pollution on BCMs formation is and if this can be minimized. 

Subsequently a BCMs characterisation study was performed. Hereby, the focus was on the light availability in the mesophotic waters and the light-harvesting pigments of BCMs. At 14.5m depth light of 600nm and higher frequencies was almost completely filtered out and at a depth of 61.4m the 5% light intensity left ranged between 460nm and 500nm. While analyzing the phycobilisome pigments, clear PUB and PEB absorption peaks were found, but no clear PC and APC peaks were found, which is unexpected since these pigments are thought to be always present. Therefore it would be interesting to perform more research on the presence of the phycobilisomes in these BCMs, to find an explanation for these results. Twelve hydrophobic pigments were found, including zeaxanthin, which originates from cyanobacteria. Deep samples contained more pigments than shallow samples (p=0.005). Moreover, deep samples compared to shallow samples contained on average 47% more of the light absorbing pigment chlorophyll c3 (p < 2.20-16) and 62% less of the light protecting pigment zeaxanthin (p = 4.62-8). These results are according to expectations and indicate that these BCMs are adapted to the life on the ‘dark’ mesophotic reefs.

The Caribbean is well known for its tropical islands fringed by beautiful coral reefs. However, reefs nowadays shift from coral dominance to dominance by algae and cyanobacteria, probably due to eutrophication and overfishing. This is known for shallow reefs on the leeward side of islands. The deep (mesophotic, > 30 m deep) reefs are considered to be important as providers of offspring to shallow reef communities that are arguably more affected by climate change, overfishing and unsustainable coastal development. Mesophotic reefs are probably also important on the wind ward side of islands: due to high wave exposure benthic communities are largely confined to the mesophotic region. These mesophotic reefs are still mostly unexplored because of their remoteness or inaccessibility. Incidental deep dives and submarine dives have established sites where well developed reef communities have been found (Curaçao), but also where large areas with cyanobacterial mats (Bonaire) were observed. Cyanobacteria are known to proliferate under eutrophied conditions and to be stimulated by global warming. We hypothesize that submarine groundwater discharge (SGD) is a main and continuous nutrient transport route from land to sea on Caribbean islands and cause proliferation of cyanobacterial mats. Understanding its role in the onshore-offshore hydro(geo)logy of the island is a prerequisite for cost-effective waste (water) management on the island and consequently improved health of the coral reefs.

26 February - 10 March 2018 

St Maarten-St Maarten (NICO expedition leg 6)

Over the past decades numerous studies have reported declines in stony corals and, in many cases, phase shifts to fleshy macroalgae. However, long-term studies documenting changes in other benthic reef organisms are scarce. Here, we studied changes in cover of corals, algal turfs, benthic cyanobacterial mats, macroalgae, sponges and crustose coralline algae at four reef sites of the Caribbean islands of Curaçao and Bonaire over a time span of 40 yr. Permanent 9 m2quadrats at 10, 20, 30 and 40 m depth were photographed at 3- to 6-yr intervals from 1973 to 2013. The temporal and spatial dynamics in the six dominant benthic groups were assessed based on image point-analysis. Our results show consistent patterns of benthic community change with a decrease in the cover of calcifying organisms across all sites and depths from 32.6 (1973) to 9.2% (2013) for corals and from 6.4 to 1% for crustose coralline algae. Initially, coral cover was replaced by algal turfs increasing from 24.5 (1973) to 38% around the early 1990s. Fleshy macroalgae, still absent in 1973, also proliferated covering 12% of the substratum approximately 20 yr later. However, these new dominants largely declined in abundance from 2002 to 2013 (11 and 2%, respectively), marking the rise of benthic cyanobacterial mats. Cyanobacterial mats became the most dominant benthic component increasing from a mere 7.1 (2002) to 22.2% (2013). The observed increase was paralleled by a small but significant increase in sponge cover (0.5 to 2.3%). Strikingly, this pattern of degradation and phase change occurred over the reef slope down to mesophotic depths of 40 m. These findings suggest that reefs dominated by algae may be less stable than previously thought and that the next phase may be the dominance of slimy cyanobacterial mats with some sponges.

The dissolved organic carbon (DOC) pool on tropical coral reefs is mainly fueled by photosynthates released from benthic primary producers (BPP), such as reef algae and scleractinian corals. DOC concentrations near BPP have repeatedly been observed to be elevated compared to those in the surrounding water column. As the DOC release of BPP increases with increasing light availability, elevated DOC concentrations near them will, in part, also depend on light availability. Consequently, DOC concentrations are likely to be higher on the shallow, well-lit reef terrace than in deeper sections on the fore reef slope. We measured in situ DOC concentrations and light intensity in close proximity to the reef alga Dictyota sp. and the scleractinian coral Orbicella faveolata along a depth gradient from 5 to 20 m depth and compared these to background concentrations in the water column. DOC concentrations near Dictyota sp. were significantly higher at 10 m than at 5 and 20 m depth. Furthermore, at 10 m DOC concentrations near Dictyota sp. were elevated by 15 μmol C L-1 compared to background concentrations in the water column, but not at 5 and 20 m. DOC concentrations near O. faveolata and in the water column did not differ between depths and concentrations near O. faveolata were not elevated compared to background concentrations at any of the tested depths. Our results indicate that DOC concentrations near Dictyota sp. can differ along a depth gradient from 5 to 20 m. However, the occurrence of elevated DOC concentrations did not follow a natural light gradient across depth. Instead, a combination of light availability (including a restriction by photoinhibition) and water movement are proposed to interactively determine the DOC concentrations in the close vicinity of BPP across the reef slope. 

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.

Cruise Background

Many islands in the Caribbean sea are fringed by coral reefs and/or coral veneers, which produce CaCO3 for their skeletons. Not only stony corals but also coralline algae and other organisms form CaCO3 skeletons and contribute
to the CaCO3 produc on of these systems. Synchronously forces are at work to mechanis cally and chemically de- struct the CaCO3 structure. Erosion of CaCO3 by organisms such as grazing sea urchins, fishes and by scouring of coral skeleton-derived debris (e.g. rubble, sand, silt) is mainly mechanical. Boring worms and sponges combine mechani- cal and chemical removal of CaCO3. Chemical dissolu on by sponges can be substan al. Up to 75% of the bioerosion (CaCO3 mass loss) by coral excava ng sponges has been reported to be due to dissolu on, but more frequently values between 10%-30% have been found. Endolithic microorganisms bore purely chemically and infest bare CaCO3 sub- strates on reefs.

CaCO3 produc on and dissolu on is influenced by the seawater chemistry of CO2 (Andersson & Gledhill, 2013). The average pCO2 in water is enhanced by ocean acidifica on and by increased benthic mineraliza on of organic ma er due to eutrophica on. There are indica ons that seawater chemistry of CO2 and carbonate effects calcifying as well as decalcifying organisms differently and as such influence the balance between construc on and destruc on. How the balance is influenced in rela on to varia on in the carbonate system over different coral reef communi es and whole reef systems of different trophic status is s ll poorly understood.

Focus of this short NIOZ cruise was on benthic community carbon metabolism and the seawater carbonate system. With different methods we explored the balance between calcifica on and dissolu on of CaCO3. Bo om-water fluxes of the carbonate system were measured in rela on to the cover and composi on of the coral reef bo om commu- nity. This was done by (1) placing a dome tent over 4m2 of a coral reef community (and a small triangle tent as con- trol) and follow the diurnal changes of the chemistry in the tents and (2) by measuring diurnal changes in carbonate chemistry (e.g. pH and DIC in rela on to light) at the reef bo om outside of the tent in conjunc on with physical and hydrodynamic measurements and (3) by determining the benthic community with special focus on cover of calcifying and bioeroding organisms. In addi on depth profiles of conduc vity, temperature, pressure and oxygen were taken, to characterize the water masses over me in the research area.

The Saba Bank site was selected on basis of the purported oligotrophic status of the Bank. The selected site on the bank was at least 20 nau cal miles removed from coastal run-off and/or sewage pollu on of closest islands, the small islands of Saba an St Eusta us. Moreover the Saba Bank is separated from these islands by >800 m deep wa- ters. The selected loca on at Saba was more eutrophic than the Saba Bank site due to run-off from land. Physics and hydrodynamics (see CHAP II) were addressed with the aim to describe characteris cs of water masses flowing over the reef, and water movement profiles from the bo om to the surface. In CHAP III the experiments addressing the C metabolism and the carbonate system in the benthic compartment in and outside incuba on tents (placed in situ over benthic communi es) were elucidated. In Chap IV methods used to survey the benthic community were explained and preliminary results are presented. Chap V comprises a report of the coral species surveys of a site on the Saba Bank and a site in Ladder Bay, Saba. 

Turf algae increasingly dominate benthic communities on coral reefs. Given their abundance and high dissolved organic carbon (DOC) release rates, turf algae are considered important contributors to the DOC pool on modern reefs. The release of photosynthetically fixed carbon as DOC generally, but not always, increases with increased light availability. Nutrient availability was proposed as an additional factor to explain these conflicting observations. To address this proposed but untested hypothesis, we documented the interactive contributions of light and nutrient availability on the release of DOC by turf algae. DOC release rates and oxygen production were quantified in incubation experiments at two light levels (full and reduced light) and two nutrient treatments (natural seawater and enriched seawater). In natural seawater, DOC release at full light was four times higher than at reduced light. When nutrients were added, DOC release rates at both light levels were similar to the natural seawater treatment at full light. Our results therefore show that low light in combination with low nutrient availability reduces the release of DOC by turf algae and that light and nutrient availability interactively determine DOC release rates by this important component of Caribbean reef communities.

Abstract

Benthic cyanobacterial mats (BCMs) are increasing in abundance on coral reefs worldwide. However, their impacts on biogeochemical cycling in the surrounding water and sediment are virtually unknown. By measuring chemical fluxes in benthic chambers placed over sediment covered by BCMs and sediment with BCMs removed on coral reefs in Curaçao, Southern Caribbean, we found that sediment covered by BCMs released 1.4 and 3.5 mmol C m(-2) h(-1) of dissolved organic carbon (DOC) during day and night, respectively. Conversely, sediment with BCMs removed took up DOC, with day and night uptake rates of 0.9 and 0.6 mmol C m(-2) h(-1). DOC release by BCMs was higher than reported rates for benthic algae (turf and macroalgae) and was estimated to represent 79% of the total DOC released over a 24 h diel cycle at our study site. The high nocturnal release of DOC by BCMs is most likely the result of anaerobic metabolism and degradation processes, as shown by high respiration rates at the mat surface during nighttime. We conclude that BCMs are significant sources of DOC. Their increased abundance on coral reefs will lead to increased DOC release into the water column, which is likely to have negative implications for reef health.

Dissolved organic carbon (DOC) release of three algal and two coral species was determined at three light intensities (0, 30–80, and 200–400 μmol photons m−2 s−1) in ex situ incubations to quantify the effect of light availability on DOC release by reef primary producers. DOC release of three additional algal species was quantified at the highest light intensity only to infer inter-specific differences in DOC release. For species tested at different light intensities, highest net release of DOC occurred under full light (200–400 μmol photons m−2 s−1). DOC released by benthic algae under full light differed (up to 16-fold) among species, whereas DOC release by scleractinian corals was minimal (Orbicella annularis Ellis and Solander, 1786) or net uptake occurred (Madracis mirabilis Duchassaing and Michelotti, 1860) independent of light availability. DOC concentrations and light intensities were also measured in situ near seven benthic primary producers, sediment, and in the water column at nine sites evenly distributed along the leeward coast of Curaçao. In situ DOC concentrations increased with light availability, although the magnitude of this positive effect differed among species and bottom types tested. In situ DOC concentrations were on average lower in November–December [87 (SD 45) μmol L−1] compared to May–June [186 (SD 136) μmol L−1], which can, at least partly, be explained by the lower light availability in the latter period. Our results suggest that DOC release by Caribbean benthic primary producers varies considerably among species and depends on light availability in reef algae.