Relationships between Meiofaunal Biodiversity and Prokaryotic Heterotrophic Production in Different Tropical Habitats and Oceanic Regions

Tropical marine ecosystems are among the most diverse of the world oceans, so that assessing the linkages between biodiversity and ecosystem functions (BEF) is a crucial step to predict consequences of biodiversity loss. Most BEF studies in marine ecosystems have been carried out on macrobenthic diversity, whereas the influence of the meiofauna on ecosystem functioning has received much less attention. We compared meiofaunal and nematode biodiversity and prokaryotic heterotrophic production across seagrass, mangrove and reef sediments in the Caribbean, Celebes and Red Seas. For all variables we report the presence of differences among habitats within the same region, and among regions within the same habitat. In all regions, the richness of meiofaunal taxa in reef and seagrass sediments is higher than in mangrove sediments. The sediments of the Celebes Sea show the highest meiofaunal biodiversity. The composition of meiofaunal assemblages varies significantly among habitats in the same region. The nematode beta diversity among habitats within the same region is higher than the beta diversity among regions. Although one site per habitat was considered in each region, these results suggest that the composition of meiofaunal assemblages varies primarily among biogeographic regions, whereas the composition of nematode assemblages varies more considerably among habitats. Meiofauna and nematode biodiversity and prokaryotic heterotrophic production, even after the removal of covariate effects linked with longitude and the quantity and nutritional quality of organic matter, are positively and linearly linked both across regions and within each habitat type. Our results confirm that meiofauna and nematode biodiversity may influence benthic prokaryotic activity, which, in turn, implies that diversity loss could have negative impacts on ecosystem functioning in these systems

Composición de la materia orgánica particulada en un sistema periantártico semi-cerrado: el Estrecho de Magallanes

The elemental and biochemical composition of particulate organic matter (POM) was investigated in the Straits of Magellan during February-March 1991. Twenty-two stations were selected in order to identify different areas of the Magellan ecosystem from a trophic point of view. The Strait of Magellan can be divided into three subsystems characterized by different hydrological and geomorphological conditions. Seston concentrations were mostly constrained by physical events, particularly the influence of oceanic and land run-off water inputs and the strong vertical mixing and resuspension events. POM composition displayed quali-quantitative differences between the three areas. In the first subsystem, influenced by Pacific waters, the low seston and POM concentrations and the high POC/Chl-a ratio values indicated the general predominance of the detrital and heterotrophic fractions. In the second subsystem, characterized by superficial stratification, higher seston and organic matter concentrations and lower values of POC/Chl-a ratio were found, indicating that this subsystem was influenced by an active autotrophic component. Shallow waters with intense tidal regime and strong vertical mixing characterized the third subsystem, connected to the Atlantic Ocean, which displayed an increasing importance of the inorganic fraction (values of the POC/TSM ratio lower than in the other systems). Moreover, the third subsystem showed higher values of the RNA/DNA ratio, possibly indicating that resuspension events may enhance the metabolic state of the organic particles mainly dominated by heterotrophic components.Se estudió la composición elemental y bioquímica de la POM (materia orgánica particulada) en el Estrecho de Magallanes durante el periodo febrero-marzo de 1991. Se eligieron 22 estaciones a fin de identificar diferentes áreas del ecosistema magallánico desde un punto de vista trófico. De acuerdo con las características hidrológicas y geomorfológicas dicho Estrecho se puede dividir en 3 subsistemas. Las concentraciones de seston estuvieron condicionadas, principalmente, por los fenómenos físicos y, en particular, por los aportes oceánicos y terrestres, por la mezcla vertical y por los fenómenos de resuspensión. La composición de la materia orgánica particulada (POM) mostró diferencias cualitativas y cuantitativas en las tres áreas. En el primer subsistema, influenciado por las aguas del Océano Pacífico, las bajas concentraciones de seston y POM y los altos valores de la relación POC/clorofila a indicaron una predominancia general de las fracciones detrítica y heterótrofa. En el segundo subsistema, caracterizado por una estratificación superficial, se encontraron altas concentraciones de seston y de materia orgánica y bajos valores de la relación POC/clorofila a, señalando una influencia de la componente autótrofa activa. El tercer subsistema, conectado con el Océano Atlántico y caracterizado por aguas poco profundas y por un régimen mareal intenso y una fuerte mezcla vertical, mostró un importante aumento de la fracción inorgánica (valores de la relación POC/TSM más bajos que en los otros dos subsistemas). Por otra parte, el tercer subsistema mostró altos valores de la relación RNA/DNA, indicando que posiblemente el estado metabólico de las partículas orgánicas (dominadas principalmente por componentes heterótrofas) estaría influenciado por fenómenos de resuspensión

Red coral extinction risk enhanced by ocean acidification

The red coral Corallium rubrum is a habitat-forming species with a prominent and structural role in mesophotic habitats, which sustains biodiversity hotspots. This precious coral is threatened by both over-exploitation and temperature driven mass mortality events. We report here that biocalcification, growth rates and polyps’ (feeding) activity of Corallium rubrum are significantly reduced at pCO2 scenarios predicted for the end of this century (0.2 pH decrease). Since C. rubrum is a long-living species (.200 years), our results suggest that ocean acidification predicted for 2100 will significantly increases the risk of extinction of present populations. Given the functional role of these corals in the mesophotic zone, we predict that ocean acidification might have cascading effects on the functioning of these habitats worldwid

Nematode diversity patterns at different spatial scales in bathyal sediments of the Mediterranean Sea

Understanding biodiversity patterns and how they are driven at different spatial scales is a crucial issue in eco- logical studies. This is particularly evident for the deep sea, the largest biome of the biosphere, where information on the scales of spatial variation is very scant. Here, we investigated deep-sea nematodes species richness, turnover and func- tional diversity, and life strategies at different spatial scales (from local to macro-regional) to identify the factors that shape regional (γ) and macro-regional (ε) deep-sea diver- sity. This study was conducted in several deep-sea habitats (canyons, open slopes, deep-water corals, and bathyal plains) over > 2000 km across the whole Mediterranean Basin, at a bathymetric range comprised between ca. 600 and 1300 m. Our results indicate that the patterns of local (α) diversity across the deep Mediterranean follow the gradients of the trophic conditions, which decrease from the western to the eastern basins. For all of the sites and habitats, the α diversity is generally low. Conversely, the turnover diversity changes significantly among habitats (β diversity) and between re- gions (δ diversity), showing values of dissimilarity (based on species presence/absence matrixes) between 59 and 90 % for β diversity and between 81 and 89 % for δ diversity. This suggests that patterns and values of γ and ε diversities in the deep Mediterranean Sea are related to turnover diversity among habitats and between regions (β and δ diversities), rather than to the local biodiversity (α diversity). These re- sults indicate also that the differences in β and δ diversi- ties are even more important than those in α diversity for the comprehension of the drivers of biodiversity in the deep Mediterranean Sea. We conclude that the presence of differ- ent habitats and gradients in environmental conditions, by promoting a high turnover diversity across the Mediterranean Sea, may play a crucial role in the levels of γ diversity of deep-sea nematodes

Unveiling the biodiversity of deep-sea nematodes through metabarcoding: Are we ready to bypass the classical taxonomy?

Nematodes inhabiting benthic deep-sea ecosystems account for >90% of the total metazoan abundances and they have been hypothesised to be hyper-diverse, but their biodiversity is still largely unknown. Metabarcoding could facilitate the census of biodiversity, especially for those tiny metazoans for which morphological identification is difficult. We compared, for the first time, different DNA extraction procedures based on the use of two commercial kits and a previously published laboratory protocol and tested their suitability for sequencing analyses of 18S rDNA of marine nematodes. We also investigated the reliability of Roche 454 sequencing analyses for assessing the biodiversity of deep-sea nematode assemblages previously morphologically identified. Finally, intra-genomic variation in 18S rRNA gene repeats was investigated by Illumina MiSeq in different deep-sea nematode morphospecies to assess the influence of polymorphisms on nematode biodiversity estimates. Our results indicate that the two commercial kits should be preferred for the molecular analysis of biodiversity of deep-sea nematodes since they consistently provide amplifiable DNA suitable for sequencing. We report that the morphological identification of deep-sea nematodes matches the results obtained by metabarcoding analysis only at the order-family level and that a large portion of Operational Clustered Taxonomic Units (OCTUs) was not assigned. We also show that independently from the cut-off criteria and bioinformatic pipelines used, the number of OCTUs largely exceeds the number of individuals and that 18S rRNA gene of different morpho-species of nematodes displayed intragenomic polymorphisms. Our results indicate that metabarcoding is an important tool to explore the diversity of deep-sea nematodes, but still fails in identifying most of the species due to limited number of sequences deposited in the public databases, and in providing quantitative data on the species encountered. These aspects should be carefully taken into account before using metabarcoding in quantitative ecological research and monitoring programmes of marine biodiversity

The first metazoa living in permanently anoxic conditions

Background: Several unicellular organisms (prokaryotes and protozoa) can live under permanently anoxic conditions. Although a few metazoans can survive temporarily in the absence of oxygen, it is believed that multi-cellular organisms cannot spend their entire life cycle without free oxygen. Deep seas include some of the most extreme ecosystems on Earth, such as the deep hypersaline anoxic basins of the Mediterranean Sea. These are permanently anoxic systems inhabited by a huge and partly unexplored microbial biodiversity.Results: During the last ten years three oceanographic expeditions were conducted to search for the presence of living fauna in the sediments of the deep anoxic hypersaline L'Atalante basin (Mediterranean Sea). We report here that the sediments of the L'Atalante basin are inhabited by three species of the animal phylum Loricifera (Spinoloricus nov. sp., Rugiloricus nov. sp. and Pliciloricus nov. sp.) new to science. Using radioactive tracers, biochemical analyses, quantitative X-ray microanalysis and infrared spectroscopy, scanning and transmission electron microscopy observations on ultra-sections, we provide evidence that these organisms are metabolically active and show specific adaptations to the extreme conditions of the deep basin, such as the lack of mitochondria, and a large number of hydrogenosome-like organelles, associated with endosymbiotic prokaryotes.Conclusions: This is the first evidence of a metazoan life cycle that is spent entirely in permanently anoxic sediments. Our findings allow us also to conclude that these metazoans live under anoxic conditions through an obligate anaerobic metabolism that is similar to that demonstrated so far only for unicellular eukaryotes. The discovery of these life forms opens new perspectives for the study of metazoan life in habitats lacking molecular oxygen

Exploring benthic biodiversity patterns and hotspots on European margin slopes

There is increasing evidence that continental slope ecosystems represent one of the major repositories of benthic marine biodiversity. The enhanced levels of biodiversity along slopes are hypothesized to be a source of biodiversity for continental shelves and deeper basins. Continental margins are increasingly altered by human activities, but the consequences of these anthropogenic impacts on benthic biodiversity and ecosystem functioning are almost completely unknown. Thus, there is an urgent need to gather sufficient information to enable us to understand patterns and drivers of deep sea biodiversity along continental margins. Although the local diversity of some deep open slope ecosystems is moderately well documented, very little is known about the biodiversity of these systems at greater spatial scales. Topographic setting, hydrodynamic forcing, and the biogeochemical characteristics of the deep-sea floor may play key roles in promoting and sustaining high biodiversity along the open slopes of continental margins. HERMES provided the opportunity to acquire a significant volume of information on the biodiversity, trophic conditions, and topographic characteristics of open slopes across European margins, increasing our knowledge of the latitudinal, longitudinal, and bathymetric patterns of benthic biodiversity, and extending our comprehension of the mechanisms driving deep-sea biodiversity and its potential loss. Improved knowledge of these processes is needed to inform policy decisions for promoting sustainable management of open slopes and deep-sea ecosystems along continental margins

Trophic state of benthic deep-sea ecosystems from two different continental margins off Iberia

The bioavailability of organic matter in benthic deep-sea ecosystems, commonly used to define their trophic state, can greatly influence key ecological processes such as biomass production and nutrient cycling. Here, we assess the trophic state of deep-sea sediments from open slopes and canyons of the Catalan (NW Mediterranean) and Portuguese (NE Atlantic) continental margins, offshore east and west Iberia, respectively, by using a biomimetic approach based on enzymatic digestion of protein and carbohydrate pools. Patterns of sediment trophic state were analyzed in relation to increasing water depth, including repeated samplings over a 3 yr period in the Catalan margin. Two out of the three sam- pling periods occurred a few months after dense shelf water cascading events. The benthic deep-sea ecosystems investi- gated in this study were characterized by high amounts of bioavailable organic matter when compared to other deep- sea sediments. Bioavailable organic matter and its nutritional value were significantly higher in the Portuguese margin than in the Catalan margin, thus reflecting differences in pri- mary productivity of surface waters reported for the two re- gions. Similarly, sediments of the Catalan margin were char- acterized by significantly higher food quantity and quality in spring, when the phytoplankton bloom occurs in surface wa- ters, than in summer and autumn. Differences in the benthic trophic state of canyons against open slopes were more ev- ident in the Portuguese than in the Catalan margin. In both continental margins, bioavailable organic C concentrations did not vary or increase with increasing water depth. Overall our findings suggest that the intensity of primary production processes along with the lateral transfer of organic particles, even amplified by episodic events, can have a role in controlling the quantity and distribution of bioavailable organic detritus and its nutritional value along these continental margin ecosystems

Technical Note: Determination of the metabolically active fraction of benthic foraminifera by means of Fluorescent In Situ Hybridization (FISH)

Benthic foraminifera are an important component of the marine biota, but protocols for investigating their viability and metabolism are still extremely limited. Classical studies on benthic foraminifera have been based on direct counting under light microscopy. Typically, these organisms are stained with Rose Bengal, which binds proteins and other macromolecules, but does not allow discrimination between viable and recently dead organisms. The fluorescent in situ hybridization technique (FISH) represents a new and useful approach to identify living cells possessing an active metabolism. Our work is the first test of the suitability of the FISH technique, based on fluorescent probes targeting the 18S rRNA, to detect live benthic foraminifera. The protocol was applied on <I>Ammonia</I> group and Miliolids, as well as on agglutinated polythalamous (i.e., <I>Leptohalysis scottii</I> and <I>Eggerella scabra</I>) and soft-shelled monothalamous (i.e., <I>Psammophaga</I> sp. and saccamminid morphotypes) taxa. The results from FISH analyses were compared with those obtained, on the same specimens assayed with FISH, from microscopic analysis of the cytoplasm colour, presence of pigments and pseudopodial activity. Our results indicate that FISH targets only metabolically active foraminifera, and allows discerning from low to high cellular activity, validating the hypothesis that the intensity of the fluorescent signal emitted by the probe is dependent upon the physiological status of cells. These findings support the usefulness of this molecular approach as a key tool for obtaining information on the physiology of living foraminifera, both in field and experimental settings

Bridging the gap between policy and science in assessing the health status of marine ecosystems

Human activities, both established and emerging, increasingly affect the provision of marine ecosystem services that deliver societal and economic benefits. Monitoring the status of marine ecosystems and determining how human activities change their capacity to sustain benefits for society requires an evidence-based Integrated Ecosystem Assessment approach that incorporates knowledge of ecosystem functioning and services). Although, there are diverse methods to assess the status of individual ecosystem components, none assesses the health of marine ecosystems holistically, integrating information from multiple ecosystem components. Similarly, while acknowledging the availability of several methods to measure single pressures and assess their impacts, evaluation of cumulative effects of multiple pressures remains scarce. Therefore, an integrative assessment requires us to first understand the response of marine ecosystems to human activities and their pressures and then develop innovative, cost-effective monitoring tools that enable collection of data to assess the health status of large marine areas. Conceptually, combining this knowledge of effective monitoring methods with cost-benefit analyses will help identify appropriate management measures to improve environmental status economically and efficiently. The European project DEVOTES (DEVelopment Of innovative Tools for understanding marine biodiversity and assessing good Environmental Status) specifically addressed t hese topics in order to support policy makers and managers in implementing the European Marine Strategy Framework Directive. Here, we synthesize our main innovative findings, placing these within the context of recent wider research, and identifying gaps and the major future challenges