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Fast and efficient sponge engines drive and modulate the food web of reef ecosystems

Periodic Reporting for period 3 - SPONGE ENGINE (Fast and efficient sponge engines drive and modulate the food web of reef ecosystems)

Reporting period: 2020-01-01 to 2021-06-30

Coral reef ecosystems were originally described as enigmatic hotspots of biodiversity, as seemingly paradoxical highly productive ecosystems residing in marine deserts, and from a purely anthropomorphic viewpoint: just marvels of natural beauty (Darwin 1842). In the year 2016, 174 years later, it is crystal clear that coral reef ecosystems around the world are rapidly declining because of the combined effects of human activities (e.g. coastal development, overfishing, and eutrophication), including the most detrimental, longer-term effects of climate change (e.g. ocean acidification, increases in seawater temperature, and the intensity and number of hurricanes and tropical cyclones. While the overall decline of reefs in response to these stressors has received significant attention, our understanding of ecological processes that shaped coral reefs in the first place, and how such processes change with shifting reef states have not received similar attention. Consequently, changing patterns of reef community composition have been well described, but processes shaping these patterns remain poorly understood. In particular the failure to recognize other key ecosystem drivers other than the “big three” (i.e. corals, algae, fish) by coral reef scientists in recent decades have hampered our ability to predict changes on coral reefs. In this ERC project we will recognize a so far largely neglected key ecosystem driver in the cycling of nutrients and energy on coral reef ecosystems: the sponges.

The prevailing view of how highly productive coral reefs maintain such high biomass and biodiversity under oligotrophic conditions was recently challenged with the discovery of the so-called sponge loop pathway (De Goeij et al. 2013, Science), in which sponges efficiently shunt a significant proportion of the ecosystem resources (i.e. carbon and nitrogen) to higher trophic levels in an otherwise low-food environment. This has provided new insight into how sponges are key ecosystem drivers that act like ecosystem 'engines': by efficiently retaining, transforming, and allocating nutrients and energy they drive communities within the food web framework of coral reef ecosystems. As a result, current reef food web models, without the inclusion of sponge-driven resource cycling, are incomplete and need be redeveloped. These models are a much-needed foundation to predict future scenarios for tropical, temperate, and cold-water reef ecosystem ecology. However, mechanisms that determine the capacity of sponge engines, how they are fuelled, and how they drive reef communities within the food web are at present largely unknown. Moreover, the sponge loop sparked significant interest, controversy and discussion in the scientific world. It is therefore time for an integrated approach to tackle the knowledge gaps we are currently facing in order to predict how sponge community structure and biomass change under future scenarios of climate change, but also how sponges change the ecosystems in which they reside, from shallow-water tropical, to cold-water deep-sea coral reefs. We will therefore assess critical knowledge gaps at the organismal and ecosystem level concerning the integration of sponges in present food web frameworks. Ultimately, we will the newly developed food web framework model will lead to a predictive model for future scenarios of shallow and deep reef ecosystem development with sponges as key ecosystem drivers.

In order to achieve the ambitious main goal, SPONGE ENGINE has the following key objectives:

Objective 1: Relate processing of different (coral- and algal-derived) DOM substrates to (A) different sponge functional types (abundance of associated microbes, shape, and pumping rate) and (B) identify which microbial communities are involved in DOM processing.

Objective 2: Elucidate (A) contribution of and (B) possible translocation/exchange between sponge cells and associated bacteria in processing different (coral- and algal-derived) DOM substrates.

Objective 3: Assess at community scale how (A) carbon and nitrogen fluxes though different (massive, encrusting, excavating) sponge communities relate to the composition of coral and algal communities and (B) sponge engines drive productivity and diversity of local micro-faunal communities.

Objective 4: Construct and test the novel sponge-driven food web framework (A) for a Caribbean coral reef ecosystem and (B) generalize the new sponge-driven food web framework on other benthic ecosystems where sponges are abundant.
To study the main 'fuels' of the sponge engine, or in fact different sponge engine types (objective 1 of the project), we developed three stable-isotope-enriched food sources of dissolved organic matter (DOM), of which two natural sources of DOM from coral and algae, and one from planktonic algae. We then assessed the processing (i.e. uptake, assimilation and respiration) of the 3 DOM sources by different sponge types (i.e. morphology, high or low number of associated microbes, high or low pumping rate) to study how different types of sponge engines respond to the different fuels. These processing fluxes will ultimately feed into the newly developed food web framework model. For example: Do sponges drive the ecosystem differently on algal versus coral fuel? As reefs are changing from coral to algal-dominated reefs this is important to know. Algal DOM is generally of better quality and produced at higher quantity as coral DOM. We thereby distinguish between the sponge host processing of these fuels and of their many associated microbes. Additionally, we assessed which types of bacteria were consuming DOM, by looking at the DNA and RNA of both sponges and their symbionts.

The role of microbes that are associated with sponges (their symbionts) is further studied at (sub)cellular scale (objective 2 of the project). With our isotopically-labeled food, we can trace that food into sponge host cells and bacteria and visualise that using a new microscopic technique named NanoSIMS. At very small scale, we can also then look at possible exchange of food between the host and its symbionts. Those beneficial traits in a symbiosis are generally not known for sponges. Remarkable, since sponges are the oldest known (about 700 Million years old!), still living multicellular animal. Basically, we could learn from our oldest ancestor how food is taken up and processed between the animal and its symbionts. In this respect you may consider sponges as the earliest "gut". In addition to the complicated NanoSIMS technique, we also use complementary techniques to study host-symbiont interactions, by dissociating cells and looking at fatty acids inside the tissue of sponges.

After these controlled, laboratory studies, we focus on ecosystem scale processes (objective 3). First, we need to know how many sponges there are on a reef! This is not known at present, because a lot of sponges live under the reef, hidden from sight, or even in the reef framework (boring themselves into the coral reef). We also assessed wether sponges on the reef change their microbial communities when living on reefs that contain mostly corals compared to those living in areas that are mostly surrounded by algae (more degraded reefs). All the processes studies in the first objectives are now combined with the ecosystem scale rates of food uptake and release (respiration) to construct a new food web model for tropical coral reefs (objective 4), now including sponges and microbes! In the Red Sea, we for the first time constructed such a model, which will be soon available to read. Also, we tested how sponges feed in the deep-sea. Only a few people, including our group, now know that sponges are everywhere on Earth and they are probably one of the most dominant multicellular organisms on this planet. On the deep-sea floor, we find extensive fields of sponges (sponge grounds or even sponge reefs) up to 3,000 m water depth! How do they 'drive' the ecosystems of our oceans. We hope to find out more by the end of our project.
The progress of our project goed beyond the state-of-the-art in many ways. We are developing new technologies (untargeted metabolomics of DOM), further developing technologies (NanoSIMS) to new model animals. In terms of results, we anticipate to rock the coral reef world by showing how important the so far largely neglected sponges are to the general ecology and physiology of coral reefs, from shallow water tropical to cold water deep sea reefs. And perhaps even more, since sponge may have a significant global effect on the biogeochemistry of our World's oceans.
The Sponge Engine