Ever since Darwin’s early descriptions of coral reefs, scientists have debated how one of the world’s most productive and diverse ecosystems can thrive in the marine equivalent of a desert. It is an enigma how the flux of dissolved organic matter (DOM), the largest resource produced on reefs, is transferred to higher trophic levels. Here we show that sponges make DOM available to fauna by rapidly expelling filter cells as detritus that is subsequently consumed by reef fauna. This “sponge loop” was confirmed in aquarium and in situ food web experiments, using 13C- and 15N-enriched DOM. The DOM-sponge-fauna pathway explains why biological hot spots such as coral reefs persist in oligotrophic seas—the reef’s paradox—and has implications for reef ecosystem functioning and conservation strategies.
We studied the removal of dissolved organic carbon (DOC) and bacterioplankton by the encrusting sponges Halisarca caerulea, Mycale microsigmatosa and Merlia normani in coral reefs along Curaçao, Netherlands Antilles. Sponge specimens were collected from coral reef cavities and incubations were done on the fore-reef slope at 12 m depth. The concentrations of DOC and bacterioplankton carbon (BC) were monitored in situ, using incubation chambers with sponges and without sponges (incubations with coral rock or ambient reef water only). Average (± SD) DOC removal rates (in μmol C cm -3 sponge h -1 ) amounted to 13.1 ± 2.5, 15.2 ± 0.9 and 13.6 ± 2.4 for H. caerula, M. microsigmatosa and M. normani, respectively. The DOC removal rates by the 3 sponges were on average 2 orders of magnitude higher than BC removal rates and accounted for more than 90% of the total organic carbon removal. Total organic carbon removal rates presented here were the highest ever reported for sponges. In an additional experiment with H. caerulea, the fate of organic carbon was reconstructed by measuring dissolved oxygen (O 2 ) removal and dissolved inorganic carbon (DIC) release in a laminar flow chamber. H. caerulea respired 39 to 45% of the organic carbon removed. The remaining 55 to 61% of carbon is expected to be assimilated. We argue that H. caerulea may have a rapid turnover of matter. All 3 sponge species contained associated bacteria, but it is unclear to what extent the associated bacteria are involved in the nutrition of the sponge. We conclude that the 3 sponge-microbe associations are (related to the availability of dissolved and particulate carbon sources in the ambient water) 'dissolved organic matter (DOM)-feeders' and encrusting sponges are of quantitative importance in the removal of DOC in coral reef cavities.KEY WORDS: DOC · Sponges · Nutrition · Carbon budget · Nutrient cycling · Coral reef · Reef framework cavities · Caribbean · Curaçao Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 357: [139][140][141][142][143][144][145][146][147][148][149][150][151] 2008 organic carbon by sponges (Reiswig 1971) and the vast volumes of water sponges can process over time (Reiswig 1974b). He found a discrepancy between the supply and demand of carbon in benthic suspension feeders, and DOM was proposed to be the missing link (Reiswig 1981). It is generally assumed that only sponges with sponge-associated bacteria, sometimes comprising up to half of the total biomass of the sponge, are capable of utilizing DOM (Frost 1987, Ribes et al. 1999. Sponges have been demonstrated to take up the amino acid glycine (Stephens & Schinske 1961), 0.1 μm beads (Leys & Eerkes-Medrano 2006), as well as virus particles (Hadas et al. 2006) from ambient water. Both viral particles and 0.1 μm beads easily pass a 0.2 μm filter and are therefore operationally defined as 'dissolved '. Yahel et al. (2003) were the first to show extensive removal of bulk dissolved organic carbon (DOC) by the sponge Theone...
Shallow warm-water and deep-sea cold-water corals engineer the coral reef framework and fertilize reef communities by releasing coral mucus, a source of reef dissolved organic matter (DOM). By transforming DOM into particulate detritus, sponges play a key role in transferring the energy and nutrients in DOM to higher trophic levels on Caribbean reefs via the so-called sponge loop. Coral mucus may be a major DOM source for the sponge loop, but mucus uptake by sponges has not been demonstrated. Here we used laboratory stable isotope tracer experiments to show the transfer of coral mucus into the bulk tissue and phospholipid fatty acids of the warm-water sponge Mycale fistulifera and cold-water sponge Hymedesmia coriacea, demonstrating a direct trophic link between corals and reef sponges. Furthermore, 21–40% of the mucus carbon and 32–39% of the nitrogen assimilated by the sponges was subsequently released as detritus, confirming a sponge loop on Red Sea warm-water and north Atlantic cold-water coral reefs. The presence of a sponge loop in two vastly different reef environments suggests it is a ubiquitous feature of reef ecosystems contributing to the high biogeochemical cycling that may enable coral reefs to thrive in nutrient-limited (warm-water) and energy-limited (cold-water) environments.
SUMMARYThis study reveals the peculiar in vivo cell kinetics and cell turnover of the marine sponge Halisarca caerulea under steady-state conditions. The tropical coral reef sponge shows an extremely high proliferation activity, a short cell cycle duration and massive cell shedding. Cell turnover is predominantly confined to a single cell population, i.e. the choanocytes, and in this process apoptosis only plays a minor role. To our knowledge, such fast cell kinetics under steady-state conditions, with high turnover by shedding in the absence of apoptosis, has not been observed previously in any other multicellular organism. The duration of the cell cycle in vivo resembles that of unicellular organisms in culture. Morphological and histochemical studies demonstrate compartmentalization of choanocytes in the sponge tissue, which corresponds well with its remarkable cellular kinetics. Coral reef cavity sponges, like H. caerulea, inhabit low nutrient tropical waters, forcing these organisms to filter large volumes of water and to capture the few nutrients efficiently. Under these oligotrophic conditions, a high cell turnover may be considered as a very useful strategy, preventing permanent damage to the sponge by environmental stress. Halisarca caerulea maintains its body mass and keeps its food uptake system up to date by constantly renewing its filter system. We conclude that studies on cell kinetics and functional morphology provide new and essential information on the growth characteristics and the regulation of sponge growth in vivo as well as in vitro and the role of choanocytes in tissue homeostasis.
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