VacuSIP, an Improved InEx Method for <em>In Situ</em> Measurement of Particulate and Dissolved Compounds Processed by Active Suspension Feeders

Benthic suspension feeders play essential roles in the functioning of marine ecosystems. By filtering large volumes of water, removing plankton and ...

Institut de Ciències del Mar (ICM-CSIC)

Summer conditions in the Mediterranean Sea are characterized by high temperatures and low food availability. This leads to "summer dormancy" in many benthic suspension feeders due to energetic constraints. Analysis of the most recent 33-year temperature time series demonstrated enhanced stratification due to global warming, which produced a approximately 40% lengthening of summer conditions. Many biological processes are expected to be affected by this trend, culminating in such events as mass mortality of invertebrates. Climatic anomalies concomitant with the occurrence of these events represent prolonged exposure to warmer summer conditions coupled with reduced food resources. Simulation of the effects of these conditions on a model organism demonstrated a biomass loss of >35%. Losses of this magnitude result in mortality similar to that noted in field observations during mass mortality events. These results indicate that temperature anomalies are the underlying cause of the events, with energetic constraints serving as the main triggering mechanism.

Global warming-enhanced stratification and mass mortality events in the Mediterranean.

Macroalgae is the dominant trophic group on Mediterranean infralittoral rocky bottoms, whereas zooxanthellate corals are extremely rare. However, in recent years, the invasive coral Oculina patagonica appears to be increasing its abundance through unknown means. Here we examine the pattern of variation of this species at a marine reserve between 2002 and 2010 and contribute to the understanding of the mechanisms that allow its current increase. Because indirect interactions between species can play a relevant role in the establishment of species, a parallel assessment of the sea urchin Paracentrotus lividus, the main herbivorous invertebrate in this habitat and thus a key species, was conducted. O. patagonica has shown a 3-fold increase in abundance over the last 8 years and has become the most abundant invertebrate in the shallow waters of the marine reserve, matching some dominant erect macroalgae in abundance. High recruitment played an important role in this increasing coral abundance. The results from this study provide compelling evidence that the increase in sea urchin abundance may be one of the main drivers of the observed increase in coral abundance. Sea urchins overgraze macroalgae and create barren patches in the space-limited macroalgal community that subsequently facilitate coral recruitment. This study indicates that trophic interactions contributed to the success of an invasive coral in the Mediterranean because sea urchins grazing activity indirectly facilitated expansion of the coral. Current coral abundance at the marine reserve has ended the monopolization of algae in rocky infralittoral assemblages, an event that could greatly modify both the underwater seascape and the sources of primary production in the ecosystem.

Sea urchins predation facilitates coral invasion in a marine reserve.

Marine sponges are able to process a variety of carbon (C), nitrogen (N), phosphorous (P), and silicon (Si) dissolved compounds, in addition to the particulate C, N, and P obtained through regular feeding. While Si fluxes through sponges are exclusively related to the elaboration of their skeleton of biogenic silica, C, N, and P fluxes derive from a complex combination of metabolic processes that include feeding, respiration, egestion, excretion, as well as hosting of large microbial populations within the sponge body. Because of the remarkable abundance of sponges in many benthic marine communities, they have the potential to impact the availability of the compounds they take up and release, affecting the benthic-pelagic coupling and cycling rates of chemical elements that are crucial to determine growth of bacterioplankton and primary producers at the ecosystem level. Unfortunately, our knowledge and understanding of the magnitude of the sponge-meditated nutrient fluxes and their ecological implications depends much on the compound type (i.e. C, N, P, or Si). Herein, we review the available knowledge on the subject with emphasis on recent developments.

Nutrient fluxes through sponges: biology, budgets, and ecological implications.

The hermatypic coral Oculina patagonica can drive a compositional shift in shallow water benthic marine communities in the northwestern Mediterranean. Here, we analyze a long-term, large-scale observational dataset to characterize the dynamics of the species' recent northward range shift along the coast of Catalonia and examine the main factors that could have influenced this spread. The variation in the distributional range of Oculina patagonica was examined by monitoring 223 locations including natural and artificial habitats along >400 km of coastline over the last 19 years (1992-2010). Abundance of the species increased from being present in one location in 1992 to occur on 19% of the locations in 2010, and exhibited an acceleration of its spreading over time driven by the join action of neighborhood and long-distance dispersal. However, the pattern of spread diverged between artificial and natural habitats. A short lag phase and a high slope on the exponential phase characterized the temporal pattern of spread on artificial habitats in contrast to that observed on natural ones. Northward expansion has occurred at the fastest rate (22 km year(-1)) reported for a coral species thus far, which is sufficiently fast to cope with certain climate warming predictions. The pattern of spread suggests that this process is mediated by the interplay of (i) the availability of open space provided by artificial habitats, (ii) the seawater temperature increase with the subsequent extension of the growth period, and (iii) the particular biological features of O. patagonica (current high growth rates, early reproduction, and survival to low temperature and in polluted areas). These results are indicative of an ongoing fundamental modification of temperate shallow water assemblages, which is consistent with the predictions indicating that the Mediterranean Sea is one of the most sensitive regions to global change.

Rapid northward spread of a zooxanthellate coral enhanced by artificial structures and sea warming in the western Mediterranean.

Coral-excavating sponges are the most important bioeroders on Caribbean reefs and increase in abundance throughout the region. This increase is commonly attributed to a concomitant increase in food availability due to eutrophication and pollution. We therefore investigated the uptake of organic matter by the two coral-excavating sponges Siphonodictyon sp. and Cliona delitrix and tested whether they are capable of consuming dissolved organic carbon (DOC) as part of their diet. A device for simultaneous sampling of water inhaled and exhaled by the sponges was used to directly measure the removal of DOC and bacteria in situ. During a single passage through their filtration system 14% and 13% respectively of the total organic carbon (TOC) in the inhaled water was removed by the sponges. 82% (Siphonodictyon sp.; mean ± SD; 13 ± 17 μmol L(-1)) and 76% (C. delitrix; 10 ± 12 μmol L(-1)) of the carbon removed was taken up in form of DOC, whereas the remainder was taken up in the form of particulate organic carbon (POC; bacteria and phytoplankton) despite high bacteria retention efficiency (72 ± 15% and 87 ± 10%). Siphonodictyon sp. and C. delitrix removed DOC at a rate of 461 ± 773 and 354 ± 562 μmol C h(-1) respectively. Bacteria removal was 1.8 ± 0.9 × 10(10) and 1.7 ± 0.6 × 10(10) cells h(-1), which equals a carbon uptake of 46.0 ± 21.2 and 42.5 ± 14.0 μmol C h(-1) respectively. Therefore, DOC represents 83 and 81% of the TOC taken up by Siphonodictyon sp. and C. delitrix per hour. These findings suggest that similar to various reef sponges coral-excavating sponges also mainly rely on DOC to meet their carbon demand. We hypothesize that excavating sponges may also benefit from an increasing production of more labile algal-derived DOC (as compared to coral-derived DOC) on reefs as a result of the ongoing coral-algal phase shift.

Natural diet of coral-excavating sponges consists mainly of dissolved organic carbon (DOC).

Microbes are known to form intricate and intimate relationships with most animal and plant taxa. Microbe--host symbiotic associations are poorly explored in comparison with other species interaction networks. The current paradigm on symbiosis research stems from species-poor systems where pairwise and reciprocally specialized interactions between a single microbe and a single host that coevolve are the norm. These symbioses involving just a few species are fascinating in their own right, but more diverse and complex host-associated microbial communities are increasingly found, with new emerging questions that require new paradigms and approaches. Here we adopt an intermediate complexity approach to study the specificity, phylogenetic community structure, and temporal variability of the subset of the most abundant bacteria associated with different sponge host species with diverse eco-evolutionary characteristics. We do so by using a monthly resolved annual temporal series of host-associated and free-living bacteria. Bacteria are very abundant and diverse within marine sponges, and these symbiotic interactions are hypothesized to have a very ancient origin. We show that host-bacteria reciprocal specialization depends on the temporal scale and level of taxonomic aggregation considered. Sponge hosts with similar eco-evolutionary characteristics (e.g., volume of tissue corresponding to microbes, water filtering rates, and microbial transmission type) have similar bacterial phylogenetic community structure when looking at interactions aggregated over time. In general, sponge hosts hypothesized to form more intricate relationships with bacteria show a remarkably persistent bacterial community over time. Other hosts, however, show a large turnover similar to that observed for free-living bacterioplankton. Our study highlights the importance of exploring temporal variability in host--microbe interaction networks if we aim to determine how specific and persistent these poorly explored but extremely common interactions are.

Specificity and temporal dynamics of complex bacteria--sponge symbiotic interactions.

This study describes in vivo cell turnover (the balance between cell proliferation and cell loss) in eight marine sponge species from tropical coral reef, mangrove and temperate Mediterranean reef ecosystems. Cell proliferation was determined through the incorporation of 5-bromo-2'-deoxyuridine (BrdU) and measuring the percentage of BrdU-positive cells after 6 h of continuous labeling (10 h for Chondrosia reniformis). Apoptosis was identified using an antibody against active caspase-3. Cell loss through shedding was studied quantitatively by collecting and weighing sponge-expelled detritus and qualitatively by light microscopy of sponge tissue and detritus. All species investigated displayed substantial cell proliferation, predominantly in the choanoderm, but also in the mesohyl. The majority of coral reef species (five) showed between 16.1±15.9% and 19.0±2.0% choanocyte proliferation (mean±SD) after 6 h and the Mediterranean species, C. reniformis, showed 16.6±3.2% after 10 h BrdU-labeling. Monanchora arbuscula showed lower choanocyte proliferation (8.1±3.7%), whereas the mangrove species Mycale microsigmatosa showed relatively higher levels of choanocyte proliferation (70.5±6.6%). Choanocyte proliferation in Haliclona vansoesti was variable (2.8-73.1%). Apoptosis was negligible and not the primary mechanism of cell loss involved in cell turnover. All species investigated produced significant amounts of detritus (2.5-18% detritus bodyweight(-1)·d(-1)) and cell shedding was observed in seven out of eight species. The amount of shed cells observed in histological sections may be related to differences in residence time of detritus within canals. Detritus production could not be directly linked to cell shedding due to the degraded nature of expelled cellular debris. We have demonstrated that under steady-state conditions, cell turnover through cell proliferation and cell shedding are common processes to maintain tissue homeostasis in a variety of sponge species from different ecosystems. Cell turnover is hypothesized to be the main underlying mechanism producing sponge-derived detritus, a major trophic resource transferred through sponges in benthic ecosystems, such as coral reefs.

Cell turnover and detritus production in marine sponges from tropical and temperate benthic ecosystems.

Microbial communities associated with marine sponges carry out nutrient transformations essential for benthic-pelagic coupling; however, knowledge about their composition and function is still sparse. We evaluated the richness and diversity of prokaryotic assemblages associated with three high-microbial-abundance (HMA) and three low-microbial-abundance (LMA) sympatric Mediterranean sponges to address their stability and uniqueness. Moreover, to examine functionality and because an imbalance between nitrogen ingestion and excretion has been observed for some of these species, we sequenced nitrogenase genes (nifH) and measured N2 fixation. The prokaryotic communities in the two sponge types did not differ in terms of richness, but the highest diversity was found in HMA sponges. Moreover, the discrete composition of the communities in the two sponge types relative to that in the surrounding seawater indicated that horizontal transmission and vertical transmission affect the microbiomes associated with the two sponge categories. nifH genes were found in all LMA species and sporadically in one HMA species, and about half of the nifH gene sequences were common between the different sponge species and were also found in the surrounding water, suggesting horizontal transmission. (15)N2-enriched incubations showed that N2 fixation was measurable in the water but was not associated with the sponges. Also, the analysis of the isotopic ratio of (15)N to (14)N in sponge tissue indicated that N2 fixation is not an important source of nitrogen in these Mediterranean sponges. Overall, our results suggest that compositional and functional features differ between the prokaryotic communities associated with HMA and LMA sponges, which may affect sponge ecology.

Microbial Diversity and Putative Diazotrophy in High- and Low-Microbial-Abundance Mediterranean Sponges.

Marine sponges host bacterial communities with important ecological and economic roles in nature and society, yet these benefits depend largely on the stability of host-symbiont interactions and their susceptibility to changing environmental conditions. Here, we investigated the temporal stability of complex host-microbe symbioses in a temperate, seasonal environment over three years, targeting sponges across a range of symbiont density (high and low microbial abundance, HMA and LMA) and host taxonomy (six orders). Symbiont profiling by terminal restriction fragment length polymorphism analysis of 16S rRNA gene sequences revealed that bacterial communities in all sponges exhibited a high degree of host specificity, low seasonal dynamics and low interannual variability: results that represent an emerging trend in the field of sponge microbiology and contrast sharply with the seasonal dynamics of free-living bacterioplankton. Further, HMA sponges hosted more diverse, even and similar symbiont communities than LMA sponges and these differences in community structure extended to core members of the microbiome. Together, these findings show clear distinctions in symbiont structure between HMA and LMA sponges while resolving notable similarities in their stability over seasonal and inter-annual scales, thus providing insight into the ecological consequences of the HMA-LMA dichotomy and the temporal stability of complex host-microbe symbioses.

Marta Ribes

Department of Marine Biology and Oceanography

Institut de Ciències del Mar (ICM-CSIC)

VacuSIP, an Improved InEx Method for In Situ Measurement of Particulate and Dissolved Compounds Processed by Active Suspension Feeders

Marta Ribes

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Institut de Ciències del Mar (ICM-CSIC)

VacuSIP, an Improved InEx Method for In Situ Measurement of Particulate and Dissolved Compounds Processed by Active Suspension Feeders

Department of Marine Biology and Oceanography