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

Marine Ecology Progress Series, Journal Year: 2017, Volume and Issue: 589, P. 85 - 96

Published: Dec. 13, 2017

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout JournalEditorsTheme Sections 589:85-96 (2018) - DOI: https://doi.org/10.3354/meps12443 Reef sponges facilitate transfer of coral-derived organic matter their associated fauna sponge loop Laura Rix1,*, Jasper M. de Goeij2, Dick van Oevelen3, Ulrich Struck4, Fuad A. Al-Horani5, Christian Wild6,**, Malik S. Naumann6,7,** 1GEOMAR Helmholtz Centre for Ocean Research Kiel, RD3 Microbiology, Düsternbrooker Weg 20, 24105 Germany 2Department Freshwater and Ecology, Institute Biodiversity Ecosystem Dynamics, University Amsterdam, PO Box 94248, 1090 GE The Netherlands 3Department Estuarine Delta Systems, NIOZ Royal Sea Research, Utrecht University, 140, 4400 AC Yerseke, 4Museum für Naturkunde, Leibniz Evolution Science, Invalidenstr. 43, 10115 Berlin, 5The Jordan Aqaba Science Station, 2595, 77110, 6Faculty Biology Chemistry (FB 2), Bremen, UFT, Leobener Str. 6, 28359 7Coral Group, Center Tropical (ZMT), Fahrenheitstr. *Corresponding author: [email protected]**These authors contributed equally this work ABSTRACT: high biodiversity coral reefs results in complex trophic webs where energy nutrients are transferred between species through a multitude pathways. Here, we hypothesize that reef convert dissolved released by benthic primary producers (e.g. corals) into particulate detritus is sponge-associated detritivores pathway. To test hypothesis, conducted stable isotope (13C 15N) tracer experiments investigate uptake from Mycale fistulifera Negombata magnifica 2 types commonly with sponges: ophiuroids (Ophiothrix savignyi Ophiocoma scolopendrina) polychaetes (Polydorella smurovi). Findings revealed naturally corals was indeed readily assimilated both rapidly again as detritus. This subsequently consumed detritivores, demonstrating confirming all steps loop. Thus, provide link higher levels, thereby acting key players within food webs. KEY WORDS: Coral mucus · web Detritus Sponge Detritivore Trophic interactions Interspecific associations Full text pdf format PreviousNextCite article as: Rix L, Goeij JMd, Oevelen Dv, Struck U, Al-Horani FA, Wild C, Naumann MS Mar Ecol Prog Ser 589:85-96. Export citation Tweet linkedIn Cited Published Vol. 589. Online publication date: February 23, 2018 Print ISSN: 0171-8630; 1616-1599 Copyright © Inter-Research.

Language: Английский

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A test of the sponge-loop hypothesis for emergent Caribbean reef sponges

Marine Ecology Progress Series, Journal Year: 2018, Volume and Issue: 588, P. 1 - 14

Published: Jan. 2, 2018

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout JournalEditorsTheme Sections 588:1-14 (2018) - DOI: https://doi.org/10.3354/meps12466 FEATURE ARTICLE A test of sponge-loop hypothesis for emergent Caribbean reef sponges Steven E. McMurray1,*, Amber D. Stubler1,2, Patrick M. Erwin1, Christopher Finelli1, Joseph R. Pawlik1 1Department Biology and Biology, University North Carolina Wilmington, Carolina, USA 2Biology Department, Occidental College, 1600 Campus Road, Los Angeles, California, *Corresponding author: [email protected] ABSTRACT: The proposes that coral convert dissolved organic matter (DOM) released by benthic primary producers into particulate detritus available higher trophic levels. was developed subsequently supported from studies cryptic, encrusting sponges; however, has yet be considered massive, sponge species dominate surface reefs represent a large proportion community biomass. We tested generality fauna using direct In-Ex methods combined with acoustic Doppler velocimetry volume calculations quantify carbon flux 9 representing variety functional types. diet 5 hosting abundant symbiotic microbes (HMA) primarily consisted (DOC), while 4 low microbial abundances (LMA) consumed picoplankton. None studied were found produce significant quantities detritus. conclude that, instead releasing assimilated in form detritus, as originally proposed encrusting, cryptic sponges, likely retain Given high rates DOC uptake observed HMA species, we propose an additional pathway which fuels levels predation fish, turtle, invertebrate spongivores. KEY WORDS: Benthic-pelagic coupling · Suspension feeding Dissolved Particulate POC Porifera Detritus Full text pdf format Information about this Feature Article NextCite article as: McMurray SE, Stubler AD, Erwin PM, Finelli CM, Pawlik JR sponges. Mar Ecol Prog Ser 588:1-14. Export citation Tweet linkedIn Cited Published Vol. 588. Online publication date: February 08, 2018 Print ISSN: 0171-8630; 1616-1599 Copyright © Inter-Research.

Language: Английский

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Nutrient Fluxes and Ecological Functions of Coral Reef Sponges in a Changing Ocean

Springer eBooks, Journal Year: 2017, Volume and Issue: unknown, P. 373 - 410

Published: Jan. 1, 2017

Language: Английский

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A genomic view of the microbiome of coral reef demosponges

The ISME Journal, Journal Year: 2021, Volume and Issue: 15(6), P. 1641 - 1654

Published: Jan. 19, 2021

Abstract Sponges underpin the productivity of coral reefs, yet few their microbial symbionts have been functionally characterised. Here we present an analysis ~1200 metagenome-assembled genomes (MAGs) spanning seven sponge species and 25 phyla. Compared to MAGs derived from reef seawater, sponge-associated were enriched in glycosyl hydrolases targeting components tissue, mucus macroalgae, revealing a critical role for cycling organic matter. Further, visualisation distribution these genes amongst symbiont taxa uncovered functional guilds matter degradation. Genes utilisation sialic acids glycosaminoglycans tissue found specific lineages that also encoded attachment sponge-derived fibronectins cadherins, suggesting can utilise structural elements tissue. encoding CRISPR restriction-modification systems used defence against mobile genetic symbionts, along with eukaryote-like gene motifs thought be involved maintaining host association. Finally, provide evidence many sponge-enriched are laterally transferred between taxa, they confer selective advantage within niche therefore play ecology evolution.

Language: Английский

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

The ISME Journal, Journal Year: 2020, Volume and Issue: 14(10), P. 2554 - 2567

Published: June 29, 2020

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

Language: Английский

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Size Is the Major Determinant of Pumping Rates in Marine Sponges

Frontiers in Physiology, Journal Year: 2019, Volume and Issue: 10

Published: Dec. 10, 2019

Sponges play an important ecological function in many benthic habitats. They filter large volumes of water, retain suspended particles with high efficiency, and process dissolved compounds. Nevertheless, the factors that regulate sponge pumping rate its relation to environmental have been rarely studied. We examined, situ, variation rates for five Mediterranean species relationship temperature, particulate food abundance size over two annual cycles. Surprisingly, temperature concentration had only a small effect on rates, seasonal was (1.9-2.5 folds). Sponge main determinant specific (pumping normalized volume or mass). Within natural distribution each species, volume-specific [PR V , ml min-1 (cm sponge)-3] decreased (up 33 folds) increase (V, cm3), conforming allometric power (PR = aVb ) negative exponents. The strong dependence size-specific suggests simplistic use this value categorize predict their activity may be misleading. For example, specimens, low-microbial-abundance (LMA) (allometric exponent b -0.2 -0.3) were similar those high-microbial-abundance (HMA) (b -0.5 -0.7). However, larger markedly different. Our results suggest sponges we studied can approximated using measured constants alone conjunction surveys distribution. This information is essential quantification situ feeding respiration estimates magnitude sponge-mediated energy nutrient fluxes at community level. Further work required establish if what extent low dependency generalized other

Language: Английский

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

Frontiers in Marine Science, Journal Year: 2021, Volume and Issue: 8

Published: March 19, 2021

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

Language: Английский

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Microbial processes driving coral reef organic carbon flow

FEMS Microbiology Reviews, Journal Year: 2017, Volume and Issue: 41(4), P. 575 - 595

Published: April 10, 2017

Coral reefs are one of the most productive ecosystems on planet, with primary production rates compared to that rain forests. Benthic organisms release 10-50% their gross organic as mucus stimulates heterotrophic microbial metabolism in water column. As a result, coral reef microbes grow up 50 times faster than open ocean communities. Anthropogenic disturbances cause once coral-dominated become dominated by fleshy organisms, several outcomes for trophic relationships. Here we review processes implicated carbon flux displaying species phase shifts. The first section presents players and interactions within holobiont contribute flow. In second section, identify four ecosystem-level features directly respond benthic shifts: community composition, biomass, viral predation. third discusses significance consumption matter fourth propose 'microbial shifts' discussed here conducive lower resilience, facilitating transition new degradation states reefs.

Language: Английский

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Interactive effects of temperature and p CO ₂ on sponges: from the cradle to the grave

Global Change Biology, Journal Year: 2016, Volume and Issue: 23(5), P. 2031 - 2046

Published: Aug. 23, 2016

As atmospheric CO2 concentrations rise, associated ocean warming (OW) and acidification (OA) are predicted to cause declines in reef-building corals globally, shifting reefs from coral-dominated systems those dominated by less sensitive species. Sponges important structural functional components of coral reef ecosystems, but despite increasing field-based evidence that sponges may be 'winners' response environmental degradation, our understanding how they respond the combined effects OW OA is limited. To determine tolerance adult climate change, four abundant Great Barrier Reef species were experimentally exposed levels for 2100, under two Representative Concentration Pathways (RCPs). The impact on early life-history stages was also assessed one these provide a more holistic view impacts. All generally unaffected conditions RCP6.0, although projected RCP8.5 caused significant adverse effects: with elevated temperature decreasing survival all species, tissue necrosis bleaching, elevating respiration rates photosynthetic rates. alone had little effect, even concentrations. Importantly, interactive effect varied between different nutritional modes, pCO2 exacerbating stress heterotrophic mitigating phototrophic This antagonistic interaction reflected reduced mortality, bleaching highest OW/OA treatment. Survival settlement success Carteriospongia foliascens larvae experimental treatments, juvenile exhibited greater than their counterparts. With providing protection temperature, across life stages, change ultimately drive shift composition sponge assemblages towards dominance

Language: Английский

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Consumption of dissolved organic carbon by Caribbean reef sponges

Limnology and Oceanography, Journal Year: 2017, Volume and Issue: 63(1), P. 337 - 351

Published: Aug. 1, 2017

Abstract Sponges are conspicuous and abundant within the benthic fauna on Caribbean reefs. The ability of these organisms to efficiently capture carbon from particulate sources is well known importance dissolved organic (DOC) uptake has been recognized for several species. We surveyed DOC ingestion by seven sponge species common Florida Keys reefs using nondisruptive sampling methods undisturbed individuals. Three exhibited significant removal ranging 13% 24% ambient concentrations. tested that removed host large microbial consortia their tissues, while converse was observed those did not. This divergent behavior may suggest an important role associated microbes in utilization feeding behaviors individuals Xestospongia muta were then monitored over time investigate its respiratory consumption DOC. rates oxygen (DO) two revealed represented 96% C, approximately equal quantities C DO. demonstrates X. largely satisfies respiration demands through consumption, likely represents dominant source biomass production cell overturn this These results further illustrate metabolic sponges, pathway remineralizing matter

Language: Английский

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