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

Periodic Reporting for period 4 - SPONGE ENGINE (Fast and efficient sponge engines drive and modulate the food web of reef ecosystems)

Reporting period: 2021-07-01 to 2021-12-31

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 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 discovery of "sponge loop" pathway (De Goeij et al. 2013, Science), in which sponges efficiently shunt a significant proportion of the reef's food and energy to higher trophic levels in an otherwise low-food environment, has provided new insight into how sponges are key ecosystem drivers that act as ecosystem “engines”: by efficiently retaining, transforming, and allocating food and energy, they drive communities within the food web of coral reefs. Current reef ecology models, without the inclusion of sponge-driven resource cycling, are therefore 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. In this project, we assessed critical knowledge gaps at the organismal and ecosystem level concerning the integration of sponges as ecological drivers of shallow and deep-sea ecosystems.

We conclude that sponges are important ecological drivers of coral reefs and many other ecosystems where they are abundant. On the Caribbean reefs of Curacao, we estimated sponges to be the largest group of benthic reef organisms. More than half of the biomass and diversity on these reefs is usually missed through traditional 2D photosurveys performed around the world, since these organisms largely live under and within the 3D reef framework. Sponges possess different strategies to feed on the largest source of food in marine ecosystems: dissolved organic matter. DOM produced by algae is processed better than coral-DOM, and with a more prominent role by the microbial symbionts. But, sponge cells are very important in the uptake, the “drinking”, of DOM and translocation to their symbiotic microbes. Additionally, algal-DOM causes a higher stress and immune response than coral-DOM and increases local eutrophication. Sponges are very abundant in our oceans, even form sponge reefs in the deep-sea, and likely influence the world’s carbon cycle. But to confirm the global role of sponges, to manage and protect them, we need much more precious data from ocean floor.
As reefs are changing from coral to algal-dominated reefs, it is important to know how sponges respond to different sources of coral and algal “fuel”. Therefore, we developed stable-isotope-enriched food sources of dissolved organic matter (DOM), produced by coral and algae. We found that algal-DOM is better available to sponges than coral-DOM. Microbial symbionts are more involved in processing algal-DOM, whereas the host in coral-DOM. Moreover, algal-DOM causes higher immune and stress responses than coral-DOM. We hypothesize that sponges with high numbers of microbes will benefit on future reefs and will likely induce eutrophication on reefs by increased release of (in)organic nutrients. At (sub)cellular scale we then traced isotope-labelled DOM into sponge host cells and bacteria and visualise that using state-of-the-art NanoSIMS technology. We showed that both sponge cells and microbial symbionts are capable of using DOM as food source, whereas the prevailing view was that only microbes would be able to do so. Moreover, we found that sponge cells “drink” this DOM presumably through micropinocytosis by the sponge filter cells and translocate this important resource to their microbial symbionts. It seems sponges with high (HMA) and low (LMA) numbers of microbes have different life strategies: HMA sponge rely heavily on their symbionts, whereas LMA sponge cells are the most important DOM cyclers.

We then focused on ecosystem scale processes. First, we determined how many sponges and other benthic organisms there are on a reef. Many reef organisms live under, or even inside the reef, hidden from sight. We found a huge difference in the community composition when using traditional 2D photosurveys (relative cover of projected reef surface) compared to 3D biomass estimates, including the cryptic surfaces, usually not “seen” in surveys. Sponges are shown to be the largest group of benthic organisms on the reefs of Curacao, and more than half of these sponges are cryptic! Furthermore, we show that sponges literally “sneeze” their waste into their environment through wonderful and unique time-lapse movies, fertilizing the reef. Ultimately, we constructed a new food web model for tropical coral reefs, now including sponges and microbes! Using state-of-the-art stand-alone metabolic chambers that can operate to 3,000 m depth, we gathered the first data to assess how sponges “drive” the shallow and deep-sea ecosystems of our planet.

The project so far yielded 16 publications (8 more in development) in high-end scientific journals, of which 2 Feature Articles, 1 book chapter, 1 PhD-thesis (3 more in development) and 6 policy briefs on the distribution, ecosystem functions, and threats of deep-sea sponge ground, and 1 policy brief on the state of present-day reefs and challenges to mitigate the loss of these important ecosystems. We have also reached >50.000 school children (age 6–12) through live Youtube "lectures" (Axa Coral Live events), the sponge loop was mentioned in the biology final exam of Dutch high-school students, and is now integrated into general textbooks.
We have developed new technologies (stand-alone metabolic chambers to 3,000 m depth, untargeted metabolomics of DOM), further developing technologies (NanoSIMS, DNA-SIP) to new model animals. We are the first to show the intimate relation between an animal host and microbial symbionts in “drinking” and sharing DOM as food source. 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