Visser, P.M.

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.

Student Report 

The abundance of CyanoBacterial Mats (CBMs) at a depth of 50-90m was mapped along the west coast of Bonaire. Simultaneously local conditions (i.e. nutrient concentrations, temperature, salinity, pH, and light intensity) were measured and compared with locations where CBMs were absent. Most CBMs were found near Kralendijk. Differences in temperature and salinity levels between sites with and without CBMs were found, but nutrient concentrations were similar. The species composition in samples of the deep water CBMs were compared with samples of CBMs at 15m depth. All CBMs had a rich species consortia of bacteria, averagely consisting out of 7821 different species (OTUs). The composition between shallow and deep CBMs was found to be significantly different. Moreover, a gradient was seen in the abundances of cyanobacterial genera between the different locations of deep CBMs, which suggests that all deep CBMs have a comparable species composition with different abundances adapted to the local conditions. Overall, the presence of the deep CBMs seems to be related to a combination of multiple parameters: sufficient nutrients which are likely caused by eutrophication events, a relatively flat sandy bottom and low wave energy. 

keywords CyanoBacterial Mats, CBM, deep, genera, Illumina sequencing, species composition

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.

Turf algae are multispecies communities of small marine macrophytes that are becoming a dominant component of coral reef communities around the world. To assess the impact of turf algae on corals, we investigated the effects of increased nutrients (eutrophication) on the interaction between the Caribbean coral Montastraea annularis and turf algae at their growth boundary. We also assessed whether herbivores are capable of reducing the abundance of turf algae at coral-algae boundaries. We found that turf algae cause visible (overgrowth) and invisible negative effects (reduced fitness) on neighbouring corals. Corals can overgrow neighbouring turf algae very slowly (at a rate of 0.12 mm 3 wk−1) at ambient nutrient concentrations, but turf algae overgrew corals (at a rate of 0.34 mm 3 wk−1) when nutrients were experimentally increased. Exclusion of herbivores had no measurable effect on the rate turf algae overgrew corals. We also used PAM fluorometry (a common approach for measuring of a colony's “fitness”) to detect the effects of turf algae on the photophysiology of neighboring corals. Turf algae always reduced the effective photochemical efficiency of neighbouring corals, regardless of nutrient and/or herbivore conditions. The findings that herbivores are not capable of controlling the abundance of turf algae and that nutrient enrichment gives turf algae an overall competitive advantage over corals together have serious implications for the health of Caribbean coral reef systems. At ambient nutrient levels, traditional conservation measures aimed at reversing coral-to-algae phase shifts by reducing algal abundance (i.e., increasing herbivore populations by establishing Marine Protected Areas or tightening fishing regulations) will not necessarily reduce the negative impact of turf algae on local coral communities. Because turf algae have become the most abundant benthic group on Curaçao (and likely elsewhere in the Caribbean), new conservation strategies are required to mitigate their negative impact on coral communities.

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

Background: Scleractinian corals and their algal endosymbionts (genus Symbiodinium) exhibit distinct bathymetric distributions on coral reefs. Yet, few studies have assessed the evolutionary context of these ecological distributions by exploring the genetic diversity of closely related coral species and their associated Symbiodinium over large depth ranges. Here we assess the distribution and genetic diversity of five agariciid coral species (Agaricia humilis, A. agaricites, A. lamarcki, A. grahamae, and Helioseris cucullata) and their algal endosymbionts (Symbiodinium) across a large depth gradient (2-60 m) covering shallow to mesophotic depths on a Caribbean reef.

Results: The five agariciid species exhibited distinct depth distributions, and dominant Symbiodinium associations were found to be species-specific, with each of the agariciid species harbouring a distinct ITS2-DGGE profile (except for a shared profile between A. lamarcki and A. grahamae). Only A. lamarcki harboured different Symbiodinium types across its depth distribution (i.e. exhibited symbiont zonation). Phylogenetic analysis (atp6) of the coral hosts demonstrated a division of the Agaricia genus into two major lineages that correspond to their bathymetric distribution (“shallow”: A. humilis / A. agaricites and “deep”: A. lamarcki / A. grahamae), highlighting the role of depth-related factors in the diversification of these congeneric agariciid species. The divergence between “shallow” and “deep” host species was reflected in the relatedness of the associated Symbiodinium (with A. lamarcki and A. grahamae sharing an identical Symbiodinium profile, and A. humilis and A. agaricites harbouring a related ITS2 sequence in their Symbiodinium profiles), corroborating the notion that brooding corals and their Symbiodinium are engaged in coevolutionary processes.

Conclusions: Our findings support the hypothesis that the depth-related environmental gradient on reefs has played an important role in the diversification of the genus Agaricia and their associated Symbiodinium, resulting in a genetic segregation between coral host-symbiont communities at shallow and mesophotic depths. 

Abstract: 

The mechanisms by which algae disperse across space on coral reefs are poorly known. We inves- tigated the ability of four common Caribbean herbivorous fish species to disperse viable algal fragments through consumption of macroalgae and subsequent defecation. Fragments of all major algal taxa (Phaeophyta, Rhodophyta, and Chlorophyta) were found in 98.7 % of the fecal droppings of all fish species; however, the ability to survive gut passage and reattach to a substrate differed between algal taxa. While survival and reattachment approached zero for Phaeophyta and Chlorophyta, 76.4 % of the fragments belonging to the group Rhodophyta (mostly species in the order Gelidiaceae) survived gut passage, and were able to grow and reattach to the substrate by forming new rhizoids. Our results thus show that Gelidid algal species are dispersed by swimming herbivores. While the relative contribution of this mechanism to overall algal dispersal and recruitment in a wider ecological context remains unknown, our findings illustrate a previously undescribed mechanism of algal dispersal on coral reefs which is analogous to the dispersal of terrestrial plants, plant fragments, and seeds via herbivore ingestion and defecation. 

Abstract:

Background: Rapid determination of which nutrients limit the primary production of macroalgae and seagrasses is vital for understanding the impacts of eutrophication on marine and freshwater ecosystems. However, current methods to assess nutrient limitation are often cumbersome and time consuming. For phytoplankton, a rapid method has been described based on short-term changes in chlorophyll fluorescence upon nutrient addition, also known as Nutrient-Induced Fluorescence Transients (NIFTs). Thus far, though, the NIFT technique was not well suited for macroalgae and seagrasses.

Methodology & Principal Findings: We developed a new experimental setup so that the NIFT technique can be used to assess nutrient limitation of benthic macroalgae and seagrasses. We first tested the applicability of the technique on sea lettuce (Ulva lactuca) cultured in the laboratory on nutrient-enriched medium without either nitrogen or phosphorus. Addition of the limiting nutrient resulted in a characteristic change in the fluorescence signal, whereas addition of non- limiting nutrients did not yield a response. Next, we applied the NIFT technique to field samples of the encrusting fan-leaf alga Lobophora variegata, one of the key algal species often involved in the degradation of coral reef ecosystems. The results pointed at co-limitation of L. variegata by phosphorus and nitrogen, although it responded more strongly to phosphate than to nitrate and ammonium addition. For turtle grass (Thalassia testudinum) we found the opposite result, with a stronger NIFT response to nitrate and ammonium than to phosphate.

Conclusions & Significance: Our extension of the NIFT technique offers an easy and fast method (30–60 min per sample) to determine nutrient limitation of macroalgae and seagrasses. We successfully applied this technique to macroalgae on coral reef ecosystems and to seagrass in a tropical inner bay, and foresee wider application to other aquatic plants, and to other marine and freshwater ecosystems.