Skip to main content

Advertisement

Log in

Trophodynamics of the sclerosponge Ceratoporella nicholsoni along a shallow to mesophotic depth gradient

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

The sclerosponge Ceratoporella nicholsoni is a hyper-calcifying high microbial abundance sponge. This sponge has been observed at high densities throughout the Caribbean in the mesophotic zone (30–150 m), as well as cryptic environments in shallow (< 30 m) depths. Given the densities of this sponge, it could play an important role in the cycling of inorganic and organic sources of carbon and nitrogen at mesophotic depths. Additionally, there is broad interest in this sponge as a tool for paleobiology, paleoclimatology and paleoceanography. As a result, it is increasingly important to understand the ecology of these unique sponges in the underexplored Caribbean mesophotic zone. Here we show that this sponge increases in abundance from shallow depths into the mesophotic zone of Grand Cayman Island. We observed no significant differences in the stable isotope signatures of δ15N and δ13C of sponge tissue between depths. A predictive model of sponge diet with increasing depth shows that these sponges consume dissolved organic matter of algal and coral origin, as well as the consumption of particulate organic matter consistent with the interpretation of the stable isotope data. The taxonomic composition of the sclerosponge microbiome was invariant across the shallow to mesophotic depth range but did contain the Phylum Chloroflexi, known to degrade a variety of dissolved organic carbon sources. These data suggest that the depth distribution of this sponge may not be driven by changes in trophic strategy and is potentially regulated by other biotic or abiotic factors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

taken from Morrow et al. (2016), data for A. tubulata was taken from Slattery et al. (2011) and data for H. caerulea was taken from Lesser et al. (2020)

Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Apprill A, McNally S, Parsons R, Weber L (2015) Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat Microb Ecol 75:129–137

    Article  Google Scholar 

  • Barbera P, Kozlov AM, Czech L, Morel B, Darriba D, Flouri T, Stamatakis A (2019) EPA-ng: massively parallel evolutionary placement of genetic sequences. Syst Biol 68:365–369

    Article  PubMed  Google Scholar 

  • Bayer K, Jahn MT, Slaby BM, Moitinho-Silva L, Hentschel U (2018) Marine sponges as Chloroflexi hot spots: genomic insights and high-resolution visualization of an abundant and diverse symbiotic clade. mSystems 3:1–19

    Article  Google Scholar 

  • Benavides LM, Druffel ERM (1986) Sclerosponge growth rate as determined by 210Pb and Δ14C chronologies. Coral Reefs 4:221–224

    Article  Google Scholar 

  • Böhm F, Joachimski MM, Lehnert H, Morgenroth G, Kretschmer W, Vacelet J, Dullo WC (1996) Carbon isotope records from extant Caribbean and South Pacific sponges: Evolution of δ13C in surface water DIC. Earth Planet Sci Lett 139:291–303

    Article  Google Scholar 

  • Callahan BJ, Sankaran K, Fukuyama JA, McMurdie PJ, Holmes SP (2016) Bioconductor workflow for microbiome data analysis: from raw reads to community analyses. F1000Research 5:1492

    Article  PubMed  PubMed Central  Google Scholar 

  • Cleary DFR, de Voogd NJ, Polónia ARM, Freitas R, Gomes NCM (2015) composition and predictive functional analysis of bacterial communities in seawater, sediment and sponges in the Spermonde Archipelago, Indonesia. Microb Ecol 70:889–903

    Article  CAS  PubMed  Google Scholar 

  • de Goeij JM, van Duyl FC (2007) Coral cavities are sinks of dissolved organic carbon (DOC). Limnol Oceanogr 52:2608–2617

    Article  Google Scholar 

  • de Goeij JM, Lesser MP, Pawlik JR (2017) Nutrient Fluxes and Ecological Functions of Coral Reef Sponges in a Changing Ocean. Climate Change, Ocean Acidification and Sponges. Springer International Publishing, pp 373–410

  • de Goeij JM, van Oevelen D, Vermeij MJA, Osinga R, Middelburg JJ, de Goeij AFPM, Admiraal W (2013) Surviving in a Marine Desert: The Sponge Loop Retains Resources Within Coral Reefs. Science 342:108–110

    Article  PubMed  CAS  Google Scholar 

  • Eddy SR (2008) A Probabilistic Model of Local Sequence Alignment That Simplifies Statistical Significance Estimation. PLoS Comput Biol 4:e1000069

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Engelberts JP, Robbins SJ, de Goeij JM, Webster NS, Aranda M, Bell SC, Webster NS (2020) Characterization of a sponge microbiome using an integrative genome-centric approach. ISME J 14:1100–1110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fiore CL, Baker DM, Lesser MP (2013) Nitrogen Biogeochemistry in the Caribbean Sponge, Xestospongia muta: A Source or Sink of Dissolved Inorganic Nitrogen? PLoS ONE 8:e72961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fiore CL, Jessica KJ, Steinert G, Lesser MP (2020) Trait-based comparison of coral and sponge microbiomes. Sci Rep 10:2340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fiore CL, Labrie M, Jarett JK, Lesser MP (2015) Transcriptional activity of the giant barrel sponge, Xestospongia muta Holobiont: molecular evidence for metabolic interchange. Front Microbiol 6:364

    Article  PubMed  PubMed Central  Google Scholar 

  • Freeman CJ, Thacker RW (2011) Complex interactions between marine sponges and their symbiotic microbial communities. Limnol Oceanogr 56:1577–1586

    Article  Google Scholar 

  • Fry B (2006) Stable isotope ecology. Springer, New York

    Book  Google Scholar 

  • Garate L, Sureda J, Agell G, Uriz MJ (2017) Endosymbiotic calcifying bacteria across sponge species and oceans. Sci Rep 7:43674

    Article  PubMed  PubMed Central  Google Scholar 

  • Germer J, Cerveau N, Jackson DJ (2017) The holo-transcriptome of a calcified early branching metazoan. Front Mar Sci 4:81

    Article  Google Scholar 

  • Ginsburg RN (1983) Geological and biological roles of cavities in coral reefs. In: Barnes DJ (ed) Perspectives on Coral Reefs. Australian Institute of Marine Sciences, Townsville, Australia, pp 148–153

    Google Scholar 

  • Gutleben J, Koehorst JJ, McPherson K, Pomponi S, Wijffels RH, Smidt H, Sipkema D (2019) Diversity of tryptophan halogenases in sponges of the genus Aplysina. FEMS Microbiol Ecol 95:fiz108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haase-Schramm A, Böhm F, Eisenhauer A, Dullo W-C, Joachimski MM, Hansen B, Reitner J (2003) Sr/Ca ratios and oxygen isotopes from sclerosponges: temperature history of the Caribbean mixed layer and thermocline during the Little Ice Age. Paleoceanogr Paleoclimat 18:3

    Google Scholar 

  • Hentschel U, Piel J, Degnan SM, Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nat Rev Microbiol 10:641–654

    Article  CAS  PubMed  Google Scholar 

  • Kolasinski J, Rogers K, Frouin P (2008) Effects of acidification on carbon and nitrogen stable isotopes of benthic macrofauna from a tropical coral reef. Rap Comm Mass Spec 22:2955–2960

    Article  CAS  Google Scholar 

  • Lang JC, Hartman WD (1975) Sclerosponges: primary framework constructors on the Jamaican deep fore-reef. J Mar Res 33:223–231

    Google Scholar 

  • Langille MGI (2018) Exploring Linkages between taxonomic and functional profiles of the human microbiome. mSystems 3:e00163-17

    Article  PubMed  PubMed Central  Google Scholar 

  • Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lesser MP (2006) Benthicpelagic coupling on coral reefs: Feeding and growth of Caribbean sponges. J Exp Mar Bio Ecol 328:277–288

    Article  Google Scholar 

  • Lesser MP, Slattery M (2018) Sponge density increases with depth throughout the Caribbean. Ecosphere 9:e02525

    Article  Google Scholar 

  • Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J Exp Mar Bio Ecol 375:1–8

    Article  Google Scholar 

  • Lesser MP, Slattery M, Stat M, Ojimi M, Gates RD, Grottoli A (2010) Photoacclimatization by the coral Montastraea cavernosa in the mesophotic zone: light, food, and genetics. Ecology, 91, 990–1003.Lesser MP, Slattery M, Mobley CD (2018) Biodiversity and functional ecology of mesophotic coral reefs. Ann Rev Ecol Evol Syst 49:49–71

    Article  Google Scholar 

  • Lesser MP, Slattery M, Laverick JH, Macartney KJ, Bridge TC (2019) Global community breaks at 60 m on mesophotic coral reefs. Glob Ecol Biogeogr 28:1403–1416

    Article  Google Scholar 

  • Lesser MP, Mueller B, Pankey MS, Macartney KJ, Slattery M, Goeij JM (2020) Depth-dependent detritus production in the sponge, Halisarca caerulea. Limnol Oceanogr 65:1200–1216

    Article  Google Scholar 

  • Loya Y, Eyal G, Treibitz T, Lesser MP, Appeldoorn R (2016) Theme section on mesophotic coral ecosystems: advances in knowledge and future perspectives. Coral Reefs 35:1–9

    Article  Google Scholar 

  • Mackenzie GJ, Schaffner FC, Swart PK (2015) The stable isotopic composition of carbonate (C and O) and the organic matrix (C and N) in waterbird eggshells from South Florida: insights into feeding ecology, timing of egg formation, and geographic range. Hydrobiologia 743:89–108

    Article  CAS  Google Scholar 

  • McMurdie PJ, Holmes S (2015) Shiny-phyloseq: web application for interactive microbiome analysis with provenance tracking. Bioinformatics 31:282–283

    Article  CAS  PubMed  Google Scholar 

  • McMurray SE, Stubler AD, Erwin PM, Finelli CM, Pawlik JR (2018) A test of the sponge-loop hypothesis for emergent Caribbean reef sponges. Mar Ecol Prog Ser 588:1–14

    Article  CAS  Google Scholar 

  • Morrow KM, Fiore CL, Lesser MP (2016) Environmental drivers of microbial community shifts in the giant barrel sponge, Xestospongia muta, over a shallow to mesophotic depth gradient. Environ Microbiol 18:2025–2038

    Article  CAS  PubMed  Google Scholar 

  • Mueller B, de Goeij JM, Vermeij MJA, Mulders Y, van der Ent E, Ribes M, van Duyl FC (2014) Natural diet of coral-excavating sponges consists mainly of dissolved organic carbon (DOC). PLoS ONE 9:e90152

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Muscatine L, Porter JW, Kaplan IR (1989) Resource partitioning by reef corals as determined from stable isotope composition - I. δ13C of zooxanthellae and animal tissue vs depth. Mar Biol 100:185–193

    Article  Google Scholar 

  • Muscatine L, Kaplan IR (1994) Resource partitioning by reef corals as determined from stable isotope composition II. δ15N of zooxanthellae and animal tissue versus depth. Pac Sci 48:304–312

    Google Scholar 

  • Parada AE, Needham DM, Fuhrman JA (2016) Every base matters: Assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol 18:1403–1414

    Article  CAS  PubMed  Google Scholar 

  • Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5(3):e9672

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pawlik JR (2011) The chemical ecology of sponges on caribbean reefs: natural products shape natural systems. Bioscience 61:888–898

    Article  Google Scholar 

  • Pita L, Rix L, Slaby BM, Franke A, Hentschel U (2018) The sponge holobiont in a changing ocean: from microbes to ecosystems. Microbiome 6:46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren H, Sigman DM, Thunell RC, Prokopenko MG (2012) Nitrogen isotopic composition of planktonic foraminifera from the modern ocean and recent sediments. Limnol Oceanogr 57:1011–1024

    Article  CAS  Google Scholar 

  • Rix L, de Goeij JM, Mueller CE, Struck U, Middelburg JJ, van Duyl FC, Al-Horani FA, Wild C, Naumann MS, van Oevelen D (2016) Coral mucus fuels the sponge loop in warm- and cold-water coral reef ecosystems. Sci Rep 6:18715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santavy DL, Willenz P, Colwell RR (1990) Phenotypic study of bacteria associated with the Caribbean sclerosponge, Ceratoporella nicholsoni. Appl Environ Microbiol 56:1750–1762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schubert CJ, Nielsen B (2000) Effects of decarbonation treatments on δ13C values in marine sediments. Mar Chem 72:55–59

    Article  CAS  Google Scholar 

  • Shih JL, Selph KE, Wall CB, Wallsgrove NJ, Lesser MP, Popp BN (2020) Trophic ecology of the tropical Pacific sponge Mycale grandis inferred from amino acid compound-specific isotopic analyses. Microb Ecol 79:495–510

    Article  CAS  PubMed  Google Scholar 

  • Slaby BM, Hackl T, Horn H, Bayer K, Hentschel U (2017) Metagenomic binning of a marine sponge microbiome reveals unity in defense but metabolic specialization. ISME J 11:2465–2478

    Article  PubMed  PubMed Central  Google Scholar 

  • Slattery M, Lesser MP (2014) Allelopathy in the tropical alga Lobophora variegata (P haeophyceae): mechanistic basis for a phase shift on mesophotic coral reefs? J Phycol 50:493–505

    Article  PubMed  Google Scholar 

  • Slattery M, Lesser MP (2015) Trophic ecology of sponges from shallow to mesophotic depths (3 to 150 m): Comment on Pawlik et al. (2015) Mar Ecol Prog Ser 527:275–279

  • Slattery M, Gochfeld DJ, Easson CG, O’Donahue LRK (2013) Facilitation of coral reef biodiversity and health by cave sponge communities. Mar Ecol Prog Ser 476:71–86

    Article  Google Scholar 

  • Slattery M, Lesser MP, Brazeau D, Stokes MD, Leichter JJ (2011) Connectivity and stability of mesophotic coral reefs. J Exp Mar Bio Ecol 408:32–41

    Article  Google Scholar 

  • Slattery M, Gochfeld DJ, Diaz MC, Thacker RW, Lesser MP (2016) Variability in chemical defense across a shallow to mesophotic depth gradient in the Caribbean sponge Plakortis angulospiculatus. Coral Reefs 35:11–22

    Article  Google Scholar 

  • Swart PK, Greer L, Rosenheim BE, Moses CS, Waite AJ, Winter A, Dodge RE, Helmle K (2010) The 13C Suess effect in scleractinian corals mirror changes in the anthropogenic CO2 inventory of the surface oceans. Geophys Res Lett 37:5

    Article  CAS  Google Scholar 

  • Swart PK, Rubenstone JL, Charles C, Reitner J (1998) Sclerosponges : A new proxy indicator of climate. NOAA Climate and Global Change Program: Special Report 12:19

    Google Scholar 

  • Swart PK, Thorrold S, Rosenheim B, Eisenhauer A, Harrison CGA, Grammer M, Latkoczy C (2002) Intra-annual variation in the stable oxygen and carbon and trace element composition of sclerosponges. Paleoceanogr Paleoclimat 17:1045

    Google Scholar 

  • Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas T, Moitinho-Silva L, Lurgi M, Björk JR, Easson C, Astudillo-García C, Olson JB, Erwin PM, López-Legentil S, Luter H, Chaves-Fonnegra A, Costa R, Schupp PJ, Steindler L, Erpenbeck D, Gilbert J, Knight R, Ackermann G, Victor Lopez J, Taylor MW, Thacker RW, Montoya JM, Hentschel U, Webster NS (2016) Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun 7:1–12

    CAS  Google Scholar 

  • Trindade-Silva AE, Rua CPJ, Andrade BGN, Vicente ACP, Silva GGZ, Berlinck RGS, Thompson FL (2013) Polyketide synthase gene diversity within the microbiome of the sponge Arenosclera brasiliensis, endemic to the southern Atlantic Ocean. Appl Environ Microbiol 79:1598–1605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trussell GC, Lesser MP, Patterson MR, Genovese SJ (2006) Depth-specific differences in growth of the reef sponge Callyspongia vaginalis: role of bottom-up effects. Mar Ecol Prog Ser 323:149–158

    Article  Google Scholar 

  • van Duyl FC, Moodley L, Nieuwland G, van Ijzerloo L, van Soest RWM, Houtekamer M, Meesters EH, Middelburg JJ (2011) Coral cavity sponges depend on reef-derived food resources: stable isotope and fatty acid constraints. Mar Biol 158:1653–1666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Duyl FC, Mueller B, Meesters EH (2018) Spatio-temporal variation in stable isotope signatures (δ13C and δ15N) of sponges on the Saba Bank. PeerJ 2018:1–25

    Google Scholar 

  • Vacelet J, Willenz P, Hartman WD (2015) Living hypercalcified sponges: Treatise on invertebrate palaeontology, part E(revised), Porifera, vol. 4–5, pp. 1–14. Lawrence, KS: The University of Kansas Palaeontological Institute

  • Yahel G, Sharp JH, Marie D, Häse C, Genin A (2003) In situ feeding and element removal in the symbiont-bearing sponge Theonella swinhoei: Bulk DOC is the major source for carbon. Limnol Oceanogr 48:141–149

    Article  Google Scholar 

  • Ye Y, Doak TG (2009) A parsimony approach to biological pathway reconstruction/inference for genomes and metagenomes. PLoS Comput Biol 5:e1000465

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

We thank K. Morrow, E. Kintzing, and D. Gochfeld for field and laboratory support. We thank A. Weinheimer for insightful comments on the manuscript draft and statistical analyses. We thank Dr. Peter Swart for his comments on the manuscript, and for re-running non-acidified sponge tissue samples at the University of Miami’s Rosenstiel School of Marine Geosciences. All sample collections complied with the laws of the Cayman Islands and the United States of America. Support was provided by NSF Biological Oceanography (OCE–1632348/1632333) to MPL and MS respectively, and the University of New Hampshire Marine Biology Small Grants fund to KJM.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Keir J. Macartney.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Topic Editor Alastair Harborne

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 3978 kb)

Supplementary file2 (DOCX 21 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Macartney, K.J., Pankey, M.S., Slattery, M. et al. Trophodynamics of the sclerosponge Ceratoporella nicholsoni along a shallow to mesophotic depth gradient. Coral Reefs 39, 1829–1839 (2020). https://doi.org/10.1007/s00338-020-02008-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-020-02008-3

Keywords

Navigation