A Deep-Sea Sponge Loop? Sponges Transfer Dissolved and Particulate Organic Carbon and Nitrogen to Associated Fauna

Cold-water coral reefs and sponge grounds are deep-sea biological hotspots, equivalent to shallow-water tropical coral reefs. In tropical ecosystems, biodiversity and productivity are maintained through efficient recycling pathways, such as the sponge loop. In this pathway, encrusting sponges recycle dissolved organic matter (DOM) into particulate detritus. Subsequently, the sponge-produced detritus serves as a food source for other organisms on the reef. Alternatively, the DOM stored in massive sponges was recently hypothesized to be transferred to higher trophic levels through predation of these sponges, instead of detritus production. However, for deep-sea sponges, the existence of all prerequisite, consecutive steps of the sponge loop have not yet been established. Here, we tested whether cold-water deep-sea sponges, similar to their tropical shallow-water counterparts, take up DOM and transfer assimilated DOM to associated fauna via either detritus production or predation. We traced the fate of 13carbon (C)- and 15nitrogen (N)-enriched DOM and particulate organic matter (POM) in time using a pulse-chase approach. During the 24-h pulse, the uptake of 13C/15N-enriched DOM and POM by two deep-sea sponge species, the massive species Geodia barretti and the encrusting species Hymedesmia sp., was assessed. During the subsequent 9-day chase in label-free seawater, we investigated the transfer of the consumed food by sponges into brittle stars via two possible scenarios: (1) the production and subsequent consumption of detrital waste or (2) direct feeding on sponge tissue. We found that particulate detritus released by both sponge species contained C from the previously consumed tracer DOM and POM, and, after 9-day exposure to the labeled sponges and detritus, enrichment of 13C and 15N was also detected in the tissue of the brittle stars. These results therefore provide the first evidence of all consecutive steps of a sponge loop pathway via deep-sea sponges. We cannot distinguish at present whether the deep-sea sponge loop is acting through a detrital or predatory pathway, but conclude that both scenarios are feasible. We conclude that sponges could play an important role in the recycling of DOM in the many deep-sea ecosystems where they are abundant, although in situ measurements are needed to confirm this hypothesis.publishedVersio

Reef sponges facilitate the transfer of coral-derived organic matter to their associated fauna via the sponge loop

The high biodiversity of coral reefs results in complex trophic webs where energy and nutrients are transferred between species through a multitude of pathways. Here, we hypothesize that reef sponges convert the dissolved organic matter released by benthic primary producers (e.g. corals) into particulate detritus that is transferred to sponge-associated detritivores via the sponge loop pathway. To test this hypothesis, we conducted stable isotope (13C and15N) tracer experiments to investigate the uptake and transfer of coral-derived organic matter from the sponges Mycale fistulifera and Negombata magnifica to 2 types of detritivores commonly associated with sponges: ophiuroids (Ophiothrix savignyi and Ophiocoma scolopendrina) and polychaetes (Polydorella smurovi). Findings revealed that the organic matter naturally released by the corals was indeed readily assimilated by both sponges and rapidly released again as sponge detritus. This detritus was subsequently consumed by the detritivores, demonstrating transfer of coral-derived organic matter from sponges to their associated fauna and confirming all steps of the sponge loop. Thus, sponges provide a trophic link between corals and higher trophic levels, thereby acting as key players within reef food webs

Heterotrophy in the earliest gut: a single-cell view of heterotrophic carbon and nitrogen assimilation in sponge-microbe symbioses

Sponges are the oldest known extant animal-microbe symbiosis. These ubiquitous benthic animals play an important role in marine ecosystems in the cycling of dissolved organic matter (DOM), the largest source of organic matter on Earth. The conventional view on DOM cycling through microbial processing has been challenged by the interaction between this efficient filter-feeding host and its diverse and abundant microbiome. Here we quantify, for the first time, the role of host cells and microbial symbionts in sponge heterotrophy. We combined stable isotope probing and nanoscale secondary ion mass spectrometry to compare the processing of different sources of DOM (glucose, amino acids, algal-produced) and particulate organic matter (POM) by a high-microbial abundance (HMA) and low-microbial abundance (LMA) sponge with single-cell resolution. Contrary to common notion, we found that both microbial symbionts and host choanocyte (i.e. filter) cells and were active in DOM uptake. Although all DOM sources were assimilated by both sponges, higher microbial biomass in the HMA sponge corresponded to an increased capacity to process a greater variety of dissolved compounds. Nevertheless, in situ feeding data demonstrated that DOM was the primary carbon source for both the LMA and HMA sponge, accounting for ~90% of their heterotrophic diets. Microbes accounted for the majority (65–87%) of DOM assimilated by the HMA sponge (and ~60% of its total heterotrophic diet) but <5% in the LMA sponge. We propose that the evolutionary success of sponges is due to their different strategies to exploit the vast reservoir of DOM in the ocean

An investigation of the relation between the number of children and education in Italy

In this paper we have investigated the impact of the level of education on the number of children in Italy. We have selected 1,490 families from the 1997- 2005 Longitudinal Investigation on Italian Families (ILFI) dataset. Our dependent variable is represented by the number of children ever born to each respondent (and to his partner). Since the number of children ever born (CEB) is a count variable, we have implemented three empirical models: Poisson, Zero-Truncated Poisson and an Instrumental Variable Poisson, where grandparents’ education is exerted as an instrument of parents’ education. In particular, we have considered two stages for each model: in the first stage, we have estimated the impact of female’s education on her number of children, and in the second one, we have used also partner’s education to identify the previous effect. From the empirical results, we may observe a significant negative effect of the level of education on the number of children

The important role of sponges in carbon and nitrogen cycling in a deep-sea biological hotspot

Deep-sea sponge grounds are hotspots of biodiversity, harbouring thriving ecosystems in the otherwise barren deep sea. It remains unknown how these sponge grounds survive in this food-limited environment. Here, we unravel how sponges and their associated fauna sustain themselves by identifying their food sources and food-web interactions using bulk and compound-specific stable isotope analysis of amino and fatty acids. We found that sponges with a high microbial abundance had an isotopic composition resembling organisms at the base of the food web, suggesting that they are able to use dissolved resources that are generally inaccessible to animals. In contrast, low microbial abundance sponges had a bulk isotopic composition that resembles a predator at the top of a food web, which appears to be the result of very efficient recycling pathways that are so far unknown. The compound-specific-isotope analysis, however, positioned low-microbial abundance sponges with other filter-feeding fauna. Furthermore, fatty-acid analysis confirmed transfer of sponge-derived organic material to the otherwise food-limited associated fauna. Through this subsidy, sponges are key to the sustenance of thriving deep-sea ecosystems and might have, due to their ubiquitous abundance, a global impact on biogeochemical cycles.publishedVersio

Cell Turnover and Detritus Production in Marine Sponges from Tropical and Temperate Benthic Ecosystems

Alexander, Brittany E. et. al.-- 11 pages, 5 figures, 2 tables, supporting information http://dx.doi.org/10.1371/journal.pone.0109486.s001 https://doi.org/10.1371/journal.pone.0109486.s002This 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-29-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 16.1615.9% and 19.062.0% choanocyte proliferation (mean6SD) after 6 h and the Mediterranean species, C. reniformis, showed 16.663.2% after 10 h BrdU-labeling. Monanchora arbuscula showed lower choanocyte proliferation (8.163.7%), whereas the mangrove species Mycale microsigmatosa showed relatively higher levels of choanocyte proliferation (70.566.6%). 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 bodyweight21?d21) 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. © 2014 Alexander et al.Porifarma B.V. received funding from the European Union Seventh Framework Programme (FP7/2007–2013) under grant agreement no. KBBE-2010– 266033 to undertake the research leading to these results. Funding was also received from The Innovational Research Incentives Scheme of the Netherlands Organization for Scientific Research (NWO-VENI; 863.10.009; personal grant to JMdG). Mediterranean sampling was partially funded by the grant CGL2010–18466 from the Spanish Government to MR. BEA, RO, and JMdG are affiliated with Porifarma B.V. Porifarma B.V. provided support in the form of salaries for authors BEA, RO, and JMdG, but no employees of Porifarma B.V. other than BEA, RO, and JMdG had any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscriptPeer Reviewe

Thesis_Niklas-Kornder_Supplementary-data_Chapter2

Supplementary data of Chapter 2 of the PhD thesis of Niklas Kornder</p

Thesis_Niklas-Kornder_Chapter4

Supplementary data of Chapter 4 of the PhD thesis of Niklas Kornder</p

Thesis_Niklas-Kornder_Chapter5

Supplementary data of Chapter 5 of the PhD thesis of Niklas Kornder</p

Development of an Integrated Mariculture for the Collagen-Rich Sponge Chondrosia reniformis

In this study, novel methods were tested to culture the collagen-rich sponge Chondrosia reniformis Nardo, 1847 (Demospongiae, Chondrosiida, Chondrosiidae) in the proximity of floating fish cages. In a trial series, survival and growth of cultured explants were monitored near a polluted fish farm and a pristine control site. Attachment methods, plate materials, and plate orientation were compared. In a first trial, chicken wire-covered polyvinyl chloride (PVC) was found to be the most suitable substrate for C. reniformis (100% survival). During a second trial, survival on chicken wire-covered PVC, after six months, was 79% and 63% for polluted and pristine environments, respectively. Net growth was obtained only on culture plates that were oriented away from direct sunlight (39% increase in six months), whereas sponges decreased in size when sun-exposed. Chicken wire caused pressure on explants and it resulted in unwanted epibiont growth and was therefore considered to be unsuitable for long-term culture. In a final trial, sponges were glued to PVC plates and cultured for 13 months oriented away from direct sunlight. Both survival and growth were higher at the polluted site (86% survival and 170% growth) than at the pristine site (39% survival and 79% growth). These results represent a first successful step towards production of sponge collagen in integrated aquacultures.</p