Accelerated nitrogen cycling on Mediterranean seagrass leaves at volcanic CO2 vents.

Seagrass meadows form highly productive and diverse ecosystems in coastal areas worldwide, where they are increasingly exposed to ocean acidification (OA). Efficient nitrogen (N) cycling and uptake are essential to maintain plant productivity, but the effects of OA on N transformations in these systems are poorly understood. Here we show that complete N cycling occurs on leaves of the Mediterranean seagrass Posidonia oceanica at a volcanic CO2 vent near Ischia Island (Italy), with OA affecting both N gain and loss while the epiphytic microbial community structure remains largely unaffected. Daily leaf-associated N2 fixation contributes to 35% of the plant's N demand under ambient pH, while it contributes to 45% under OA. Nitrification potential is only detected under OA, and N-loss via N2 production increases, although the balance remains decisively in favor of enhanced N gain. Our work highlights the role of the N-cycling microbiome in seagrass adaptation to OA, with key N transformations accelerating towards increased N gain.

Microbial associates of an endemic Mediterranean seagrass enhance the access of the host and the surrounding seawater to inorganic nitrogen under ocean acidification.

Seagrasses are important primary producers in oceans worldwide. They live in shallow coastal waters that are experiencing carbon dioxide enrichment and ocean acidification. Posidonia oceanica, an endemic seagrass species that dominates the Mediterranean Sea, achieves high abundances in seawater with relatively low concentrations of dissolved inorganic nitrogen. Here we tested whether microbial metabolisms associated with P. oceanica and surrounding seawater enhance seagrass access to nitrogen. Using stable isotope enrichments of intact seagrass with amino acids, we showed that ammonification by free-living and seagrass-associated microbes produce ammonium that is likely used by seagrass and surrounding particulate organic matter. Metagenomic analysis of the epiphytic biofilm on the blades and rhizomes support the ubiquity of microbial ammonification genes in this system. Further, we leveraged the presence of natural carbon dioxide vents and show that the presence of P. oceanica enhanced the uptake of nitrogen by water column particulate organic matter, increasing carbon fixation by a factor of 8.6-17.4 with the greatest effect at CO2 vent sites. However, microbial ammonification was reduced at lower pH, suggesting that future ocean climate change will compromise this microbial process. Thus, the seagrass holobiont enhances water column productivity, even in the context of ocean acidification.

Nested interactions between chemosynthetic lucinid bivalves and seagrass promote ecosystem functioning in contaminated sediments.

In seagrass sediments, lucinid bivalves and their chemoautotrophic bacterial symbionts consume H2S, relying indirectly on the plant productivity for the presence of the reduced chemical. Additionally, the role of lucinid bivalves in N provisioning to the plant (through N2 fixation by the symbionts) was hypothesized. Thus, lucinids may contribute to sediment detoxification and plant fitness. Seagrasses are subject to ever-increasing human pressure in coastal environments. Here, disentangling nested interactions between chemosynthetic lucinid bivalves and seagrass exposed to pollution may help to understand seagrass ecosystem dynamics and to develop successful seagrass restoration programs that consider the roles of animal-microbe symbioses. We evaluated the capacity of lucinid bivalves (Loripes orbiculatus) to promote nutrient cycling and seagrass (Cymodocea nodosa) growth during a 6-week mesocosm experiment. A fully crossed design was used to test for the effect of sediment contamination (metals, nutrients, and hydrocarbons) on plant and bivalve (alone or interacting) fitness, assessed by mortality, growth, and photosynthetic efficiency, and for the effect of their nested interaction on sediment biogeochemistry. Plants performed better in the contaminated sediment, where a larger pool of dissolved nitrogen combined with the presence of other trace elements allowed for an improved photosynthetic efficiency. In fact, pore water nitrogen accumulated during the experiment in the controls, while it was consumed in the contaminated sediment. This trend was accentuated when lucinids were present. Concurrently, the interaction between clams and plants benefitted both organisms and promoted plant growth irrespective of the sediment type. In particular, the interaction with lucinid clams resulted in higher aboveground biomass of C. nodosa in terms of leaf growth, leaf surface, and leaf biomass. Our results consolidate the notion that nested interactions involving animal-microbe associations promote ecosystem functioning, and potentially help designing unconventional seagrass restoration strategies that exploit chemosynthetic symbioses.

A photographic data set of reef and coral communities across Venezuela.

This dataset contains 2850 photographs of the seafloor in coral communities from Venezuela that were taken during 2017 and 2018. We used a hierarchical experimental design with four random factors representing four different spatial scales: (1) region (hundreds of kilometers), (2) localities (tens of kilometers), (2) reef sites (hundreds of meters) and (3) transects (a couple meters) across the Venezuelan coast. At each site, four 30-m transects were deployed parallel to the coastline, and 15 pictures were taken every other meter at each transect, containing an area of at least 80 × 90cm with enough resolution to identify benthic groups. This dataset covers spatial scales from a few meters to hundreds of kilometers; marine protected areas, and non-protected areas; coastal zones, continental and oceanic islands. These images have the potential to be further used for training researchers in benthic organisms identification, and training artificial intelligence classification algorithms. Also, they represent and updated baseline to perform spatial and temporal comparisons in Venezuela or further studies involving multiple spatial scales in the region.

On the importance of spatial scales on beta diversity of coral assemblages: a study from Venezuelan coral reefs.

Estimating variability across spatial scales has been a major issue in ecology because the description of patterns in space is extremely valuable to propose specific hypotheses to unveil key processes behind these patterns. This paper aims to estimate the variability of the coral assemblage structure at different spatial scales in order to determine which scales explain the largest variability on ß-diversity. For this, a fully-nested design including a series of hierarchical-random factors encompassing three spatial scales: (1) regions, (2) localities and (3) reefs sites across the Venezuelan territory. The variability among spatial scales was tested with a permutation-based analysis of variance (Permanova) based on Bray-Curtis index. Dispersion in species presence/absence across scales (i.e., ß-diversity) was tested with a PermDisp analysis based on Jaccard's index. We found the highest variability in the coral assemblage structure between sites within localities (Pseudo-F = 5.34; p-value = 0.001, CV = 35.10%). We also found that longitude (Canonical corr = 0.867, p = 0.001) is a better predictor of the coral assemblage structure in Venezuela, than latitude (Canonical corr = 0.552, p = 0.021). Largest changes in ß-diversity of corals occurred within sites (F = 2.764, df1= 35, df2 = 107, p = 0.045) and within localities (F = 4.438, df1= 6, df2 = 29, p = 0.026). Our results suggest that processes operating at spatial scales of hundreds of meters and hundreds of kilometers might both be critical to shape coral assemblage structure in Venezuela, whereas smaller scales (i.e., hundreds of meters) showed to be highly- important for the species turnover component of ß-diversity. This result highlights the importance of creating scale-adapted management actions in Venezuela and likely across the Caribbean region.

The use of pseudo-multivariate standard error to improve the sampling design of coral monitoring programs.

The characteristics of coral reef sampling and monitoring are highly variable, with numbers of units and sampling effort varying from one study to another. Numerous works have been carried out to determine an appropriate effect size through statistical power; however, these were always from a univariate perspective. In this work, we used the pseudo multivariate dissimilarity-based standard error (MultSE) approach to assess the precision of sampling scleractinian coral assemblages in reefs of Venezuela between 2017 and 2018 when using different combinations of number of transects, quadrats and points. For this, the MultSE of 36 sites previously sampled was estimated, using four 30m-transects with 15 photo-quadrats each and 25 random points per quadrat. We obtained that the MultSE was highly variable between sites and is not correlated with the univariate standard error nor with the richness of species. Then, a subset of sites was re-annotated using 100 uniformly distributed points, which allowed the simulation of different numbers of transects per site, quadrats per transect and points per quadrat using resampling techniques. The magnitude of the MultSE stabilized by adding more transects, however, adding more quadrats or points does not improve the estimate. For this case study, the error was reduced by half when using 10 transects, 10 quadrats per transect and 25 points per quadrat. We recommend the use of MultSE in reef monitoring programs, in particular when conducting pilot surveys to optimize the estimation of the community structure.

Systematic review and meta-analysis of 50 years of coral disease research visualized through the scope of network theory.

Coral disease research encompasses five decades of undeniable progress. Since the first descriptions of anomalous signs, we have come to understand multiple processes and environmental drivers that interact with coral pathologies. In order to gain a better insight into the knowledge we already have, we explored how key topics in coral disease research have been related to each other using network analysis. We reviewed 719 papers and conference proceedings published from 1965 to 2017. From each study, four elements determined our network nodes: (1) studied disease(s); (2) host genus; (3) marine ecoregion(s) associated with the study site; and (4) research objectives. Basic properties of this network confirmed that there is a set of specific topics comprising the majority of research. The top five diseases, genera, and ecoregions studied accounted for over 48% of the research effort in all cases. The community structure analysis identified 15 clusters of topics with different degrees of overlap among them. These clusters represent the typical sets of elements that appear together for a given study. Our results show that while some coral diseases have been studied considering multiple aspects, the overall trend is for most diseases to be understood under a limited range of approaches, e.g., bacterial assemblages have been considerably studied in Yellow and Black band diseases while immune response has been better examined for the aspergillosis-Gorgonia system. Thus, our challenge in the near future is to identify and resolve potential gaps in order to achieve a more comprehensive progress on coral disease research.