Maggy M. Nugues

In Situ Oxygen Dynamics in Coral-Algal Interactions

Background Coral reefs degrade globally at an alarming rate, with benthic algae often replacing corals. However, the extent to which benthic algae contribute to coral mortality, and the potential mechanisms involved, remain disputed. Recent laboratory studies suggested that algae kill corals by inducing hypoxia on the coral surface, through stimulated microbial respiration. Methods/Findings We examined the main premise of this hypothesis by measuring in situ oxygen microenvironments at the contact interface between the massive coral Porites spp. and turf algae, and between Porites spp. and crustose coralline algae (CCA). Oxygen levels at the interface were similar to healthy coral tissue and ranged between 300–400 µM during the day. At night, the interface was hypoxic (∼70 µM) in coral-turf interactions and close to anoxic (∼2 µM) in coral-CCA interactions, but these values were not significantly different from healthy tissue. The diffusive boundary layer (DBL) was about three times thicker at the interface than above healthy tissue, due to a depression in the local topography. A numerical model, developed to analyze the oxygen profiles above the irregular interface, revealed strongly reduced net photosynthesis and dark respiration rates at the coral-algal interface compared to unaffected tissue during the day and at night, respectively. Conclusions/Significance Our results showed that hypoxia was not a consistent feature in the microenvironment of the coral-algal interface under in situ conditions. Therefore, hypoxia alone is unlikely to be the cause of coral mortality. Due to the modified topography, the interaction zone is distinguished by a thicker diffusive boundary layer, which limits the local metabolic activity and likely promotes accumulation of potentially harmful metabolic products (e.g., allelochemicals and protons). Our study highlights the importance of mass transfer phenomena and the need for direct in situ measurements of microenvironmental conditions in studies on coral stress.

Algae as reservoirs for coral pathogens.

Benthic algae are associated with coral death in the form of stress and disease. Its been proposed that they release exudates, which facilitate invasion of potentially pathogenic microbes at the coral-algal interface, resulting in coral disease. However, the original source of these pathogens remains unknown. This study examined the ability of benthic algae to act as reservoirs of coral pathogens by characterizing surface associated microbes associated with major Caribbean and Indo-Pacific algal species/types and by comparing them to potential pathogens of two dominant coral diseases: White Syndrome (WS) in the Indo-Pacific and Yellow Band Disease (YBD) in the Caribbean. Coral and algal sampling was conducted simultaneously at the same sites to avoid spatial effects. Potential pathogens were defined as those absent or rare in healthy corals, increasing in abundance in healthy tissues adjacent to a disease lesion, and dominant in disease lesions. Potentially pathogenic bacteria were detected in both WS and YBD and were also present within the majority of algal species/types (54 and 100% for WS and YBD respectively). Pathogenic ciliates were associated only with WS and not YBD lesions and these were also present in 36% of the Indo-Pacific algal species. Although potential pathogens were associated with many algal species, their presence was inconsistent among replicate algal samples and detection rates were relatively low, suggestive of low density and occurrence. At the community level, coral-associated microbes irrespective of the health of their host differed from algal-associated microbes, supporting that algae and corals have distinctive microbial communities associated with their tissue. We conclude that benthic algae are common reservoirs for a variety of different potential coral pathogens. However, algal-associated microbes alone are unlikely to cause coral death. Initial damage or stress to the coral via other competitive mechanisms is most likely a prerequisite to potential transmission of these pathogens.

The curious case of Hermodice carunculata (Annelida: Amphinomidae): evidence for genetic homogeneity throughout the Atlantic Ocean and adjacent basins

Over the last few decades, advances in molecular techniques have led to the detection of strong geographic population structure and cryptic speciation in many benthic marine taxa, even those with long‐lived pelagic larval stages. Polychaete annelids, in particular, generally show a high degree of population divergence, especially in mitochondrial genes. Rarely have molecular studies confirmed the presence of ‘cosmopolitan’ species. The amphinomid polychaete Hermodice carunculata was long considered the sole species within its genus, with a reported distribution throughout the Atlantic and adjacent basins. However, recent studies have indicated morphological differences, primarily in the number of branchial filaments, between the East and West Atlantic populations; these differences were invoked to re‐instate Hermodice nigrolineata, formerly considered a junior synonym of H. carunculata. We utilized sequence data from two mitochondrial (cytochrome c oxidase subunit I, 16S rDNA) markers and one nuclear (internal transcribed spacer) marker to examine the genetic diversity of Hermodice throughout its distribution range in the Atlantic Ocean, including the Mediterranean Sea, the Caribbean Sea, the Gulf of Mexico and the Gulf of Guinea. Our analyses revealed generally low genetic divergences among collecting localities and between the East and West Atlantic, although phylogenetic trees based on mitochondrial data indicate the presence of a private lineage in the Mediterranean Sea. A re‐evaluation of the number of branchial filaments confirmed differences between East and West Atlantic populations; however, the differences were not diagnostic and did not reflect the observed genetic population structure. Rather, we suspect that the number of branchial filaments is a function of oxygen saturation in the environment. Our results do not support the distinction between H. carunculata in the West Atlantic and H. nigrolineata in the East Atlantic. Instead, they re‐affirm the older notion that H. carunculata is a cohesive species with a broad distribution across the Atlantic Ocean.

High dissolved organic carbon release by benthic cyanobacterial mats in a Caribbean reef ecosystem

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.

Organic matter degradation drives benthic cyanobacterial mat abundance on Caribbean coral reefs.

Benthic cyanobacterial mats (BCMs) are impacting coral reefs worldwide. However, the factors and mechanisms driving their proliferation are unclear. We conducted a multi-year survey around the Caribbean island of Curaçao, which revealed highest BCM abundance on sheltered reefs close to urbanised areas. Reefs with high BCM abundance were also characterised by high benthic cover of macroalgae and low cover of corals. Nutrient concentrations in the water-column were consistently low, but markedly increased just above substrata (both sandy and hard) covered with BCMs. This was true for sites with both high and low BCM coverage, suggesting that BCM growth is stimulated by a localised, substrate-linked release of nutrients from the microbial degradation of organic matter. This hypothesis was supported by a higher organic content in sediments on reefs with high BCM coverage, and by an in situ experiment which showed that BCMs grew within days on sediments enriched with organic matter (Spirulina). We propose that nutrient runoff from urbanised areas stimulates phototrophic blooms and enhances organic matter concentrations on the reef. This organic matter is transported by currents and settles on the seabed at sites with low hydrodynamics. Subsequently, nutrients released from the organic matter degradation fuel the growth of BCMs. Improved management of nutrients generated on land should lower organic loading of sediments and other benthos (e.g. turf and macroalgae) to reduce BCM proliferation on coral reefs.

Synergistic effects of algal overgrowth and corallivory on Caribbean reef-building corals

Indirect biotic interactions play a crucial role in structuring ecological communities, but many of these interactions have not been explored. Algal competition and corallivory are two major stressors contributing to the decline of coral reefs. Here, we provide the first evidence of algal-induced corallivory and synergistic effects between the two stressors on corals. When corals (Montastraeafaveolata) were placed in contact with algae (Halimeda opuntia) together with corallivorous fireworms (Hermodice carunculata) in aquaria, corals suffered high tissue mortality. This mortality was reduced in the presence of algae only, and no mortality occurred in the presence of fireworms only or when excluding both algae and fireworms. These findings were supported by field observations showing a predominance of fireworms inside algae contacting live corals, and by an in situ experiment demonstrating higher coral mortality in contact with algae left undisturbed than with algae from which all mobile epifauna were periodically removed. Among the main contributing mechanisms, we suggest that algal contact produces decaying coral tissue that attracts the corallivore and enhances its aggregation behavior. Our study demonstrates an indirect effect pathway by which algae can impact corals, which shares similarities with the classic models of apparent competition and habitat facilitation.

Evidence for water-mediated mechanisms in coral–algal interactions

Although many coral reefs have shifted from coral-to-algal dominance, the consequence of such a transition for coral–algal interactions and their underlying mechanisms remain poorly understood. At the microscale, it is unclear how diffusive boundary layers (DBLs) and surface oxygen concentrations at the coral–algal interface vary with algal competitors and competitiveness. Using field observations and microsensor measurements in a flow chamber, we show that coral (massive Porites) interfaces with thick turf algae, macroalgae, and cyanobacteria, which are successful competitors against coral in the field, are characterized by a thick DBL and hypoxia at night. In contrast, coral interfaces with crustose coralline algae, conspecifics, and thin turf algae, which are poorer competitors, have a thin DBL and low hypoxia at night. Furthermore, DBL thickness and hypoxia at the interface with turf decreased with increasing flow speed, but not when thick turf was upstream. Our results support the importance of water-mediated transport mechanisms in coral–algal interactions. Shifts towards algal dominance, particularly dense assemblages, may lead to thicker DBLs, higher hypoxia, and higher concentrations of harmful metabolites and pathogens along coral borders, which in turn may facilitate algal overgrowth of live corals. These effects may be mediated by flow speed and orientation.

Effects of protection and sediment stress on coral reefs in Saint Lucia

The extent to which Marine Protected Areas (MPAs) benefit corals is contentious. On one hand, MPAs could enhance coral growth and survival through increases in herbivory within their borders; on the other, they are unlikely to prevent disturbances, such as terrestrial runoff, that originate outside their boundaries. We examined the effect of spatial protection and terrestrial sediment on the benthic composition of coral reefs in Saint Lucia. In 2011 (10 to 16 years after MPAs were created), we resurveyed 21 reefs that had been surveyed in 2001 and analyzed current benthic assemblages as well as changes in benthic cover over that decade in relation to protection status, terrestrial sediment influence (measured as the proportion of terrigenous material in reef-associated sediment) and depth. The cover of all benthic biotic components has changed significantly over the decade, including a decline in coral and increase in macroalgae. Protection status was not a significant predictor of either current benthic composition or changes in composition, but current cover and change in cover of several components were related to terrigenous content of sediment deposited recently. Sites with a higher proportion of terrigenous sediment had lower current coral cover, higher macroalgal cover and greater coral declines. Our results suggest that terrestrial sediment is an important factor in the recent degradation of coral reefs in Saint Lucia and that the current MPA network should be complemented by measures to reduce runoff from land.

Coralline algae disease reduces survival and settlement success of coral planulae in laboratory experiments

Disease outbreaks have been involved in the deterioration of coral reefs worldwide and have been particularly striking among crustose coralline algae (CCA). Although CCA represent important cues for coral settlement, the impact of CCA diseases on the survival and settlement of coral planulae is unknown. Exposing coral larvae to healthy, diseased, and recently dead crusts from three important CCA species, we show a negative effect of disease in the inductive CCA species Hydrolithon boergesenii on larval survivorship of Orbicella faveolata and settlement of O. faveolata and Diploria labyrinthiformis on the CCA surface. No effect was found with the less inductive CCA species Neogoniolithon mamillare and Paragoniolithon accretum. Additionally, a majority of planulae that settled on top of diseased H. boergesenii crusts were on healthy rather than diseased/dying tissue. Our experiments suggest that CCA diseases have the potential to reduce the survivorship and settlement of coral planulae on coral reefs.

Caribbean free-living coral species co-occurring deep off the windward coast of Curaçao

We document the co-occurrence of two Caribbean species of free-living zooxanthellate corals, Meandrina danae (Milne-Edwards and Haime 1848) (Fig. 1a) and Manicina areolata (Linnaeus 1758) (Fig. 1b), in a previously not well-documented environment. The two species were encountered at three locations (ranging from 30 to 50 m depth) on the windward side of the island of Curaçao, southern Caribbean. Corals are present beyond the reef base on substrate consisting of coarse coral sand, small rubble, and fragments of shells and calcareous algae (Fig. 1c). Colony sizes (mean length) were 58 mm (SD 18, n = 133) for M. areolata and 67 mm (SD 19, n = 32) for M. danae. Maximum colony density of both species together was 30 individuals per m 2 with M. areolata colonies being 9 times as abundant. None of these species has been reported from such a deep habitat. M. danae has never previously been recorded on the island while M. areolata has been described in shallow sandy areas in Curaçao by Roos (1971). It was reported in seagrass beds and on sandy and rubble areas on the reef down to 20 m in Jamaica (Goreau and Goreau 1960) and in seagrass flats and mangrove-associated communities in the San Blas Archipelago, northern Panama (Johnson 1992). Furthermore, free-living scleractinian corals can form dense and species-rich assemblages on sandy habitats of Indo-Pacific reef systems (Hoeksema 2012). To our knowledge, this is the first documented multi-species assemblage of free-living zooxanthellate corals in the Caribbean.