Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-26T17:13:10.737Z Has data issue: false hasContentIssue false
  • English
  • Français

Niche structure of marine sponges from temperate hard-bottom habitats within Gray's Reef National Marine Sanctuary

Published online by Cambridge University Press:  10 April 2015

Christopher J. Freeman ,
Cole G. Easson  and
David M. Baker
Christopher J. Freeman*
Affiliation:
Smithsonian Marine Station, Fort Pierce, FL, USA
Cole G. Easson
Affiliation:
Department of Biology, University of Alabama at Birmingham, Birmingham, AL, USA
David M. Baker
Affiliation:
The Swire Institute of Marine Science, School of Biological Sciences & Department of Earth Science, University of Hong Kong, Hong Kong, PR China
*
Correspondence should be addressed to:C.J. Freeman, Smithsonian Marine Station, Fort Pierce, FL, USA email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Many species of marine sponges on tropical reefs host abundant and diverse symbiont communities capable of varied metabolic pathways. While such communities may confer a nutritional benefit to some hosts (termed High Microbial Abundance (HMA) sponges), other sympatric species host only sparse symbiont communities (termed Low Microbial Abundance (LMA) sponges) and obtain a majority of their C and N from local sources. Sponge communities are widespread across large latitudinal gradients, however, and recent evidence suggests that these symbioses may also extend beyond the tropics. We investigated the role that symbionts play in the ecology of sponges from the temperate, hard-bottom reefs of Gray's Reef National Marine Sanctuary by calculating the niche size (as standard ellipse area (SEAc)) and assessing the relative placement of five HMA and four LMA sponge species within bivariate (δ13C and δ15N) isotopic space. Although photosymbiont abundance was low across most of these species, sponges were widespread across isotopic niche space, implying that microbial metabolism confers an ecological benefit to temperate sponges by expanding host metabolic capability. To examine how these associations vary across a latitudinal gradient, we also compared the relative placement of temperate and tropical conspecifics within isotopic space. Surprisingly, shifts in sponge δ13C and δ15N values between these regions suggest a reduced reliance on symbiont-derived nutrients in temperate sponges compared with their tropical conspecifics. Despite this, symbiotic sponges in temperate systems likely have a competitive advantage, allowing them to grow and compete for space within these habitats.

Keywords

Gray's Reeflatitudinal gradientisotopic niche spacemicrobesmicrobial abundancePoriferastandard ellipse areastable isotopessymbiosistemperate
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 96 , Issue 2: Proceedings of the 9th World Sponge Conference held in Fremantle Australia in 2013: New Frontiers in Sponge Science , March 2016 , pp. 559 - 565
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Becerro, M.A. (2008) Quantitative trends in sponge ecology research. Marine Ecology 29, 167–177.CrossRefGoogle Scholar
Bell, J.J. (2007) The ecology of sponges in Lough Hyne Marine Nature Reserve (south-west Ireland): past, present and future perspectives. Journal of the Marine Biological Association of the United Kingdom 87, 1655–1668.CrossRefGoogle Scholar
Chollett, I., Stoyle, G. and Box, S. (2014) Honduran Miskito Cays: among the last unexplored reef systems in the Caribbean. Coral Reefs 33, 155.CrossRefGoogle Scholar
Deegan, L.A. and Garritt, R.H. (1997) Evidence for spatial variability in estuarine food webs. Marine Ecology Progress Series 147, 31–47.CrossRefGoogle Scholar
Easson, C.G. and Thacker, R.W. (2014) Phylogenetic signal in the community structure of host-specific microbiomes of tropical marine sponges. Frontiers in Microbiology 5, 1–11.CrossRefGoogle ScholarPubMed
Erwin, P.M., López-Legentil, S. and Turon, X. (2012) Ultrastructure, molecular phylogenetics, and chlorophyll a content of novel cyanobacterial symbionts in temperate sponges. Microbial Ecology 64, 771–783.CrossRefGoogle ScholarPubMed
Erwin, P.M. and Thacker, R.W. (2007) Incidence and identity of photosynthetic symbionts in Caribbean coral reef sponge assemblages. Journal of the Marine Biological Association of the United Kingdom 87, 1683–1692.CrossRefGoogle Scholar
Erwin, P.M. and Thacker, R.W. (2008) Cryptic diversity of the symbiotic cyanobacterium Synechococcus spongiarum among sponge hosts. Molecular Ecology 17, 2937–2947.CrossRefGoogle ScholarPubMed
Freeman, C.J., Easson, C.G. and Baker, D.M. (2014) Metabolic diversity and niche structure in sponges from the Miskito Cays, Honduras. Peer J 2, e695. doi: 10.7717/peerj.695.CrossRefGoogle ScholarPubMed
Freeman, C.J., Gleason, D.F., Ruzicka, R., van Soest, R.W.M., Harvey, A.W. and Mcfall, G. (2007) A biogeographic comparison of sponge fauna from Gray's Reef National Marine Sanctuary and other hard-bottom reefs of coastal Georgia, USA. In Custódio, M.R., Lôbo-Hajdu, G., Hajdu, E. and Muricy, G. (eds) Proceedings of the Seventh International Sponge Symposium, Búzios, Brazil, May 2006. Porifera research: biodiversity, innovation, and sustainability. Série Livros 28. Rio de Janeiro: Museu Nacional, pp. 319–325.Google Scholar
Freeman, C.J. and Thacker, R.W. (2011) Complex interactions between marine sponges and their symbiotic microbial communities. Limnology and Oceanography 56, 1577–1586.CrossRefGoogle Scholar
Freeman, C.J., Thacker, R.W., Baker, D.M. and Fogel, M. (2013) Quality or quantity: is nutrient transfer driven more by symbiont identity and productivity than by symbiont abundance? ISME Journal 7, 1116–1125.CrossRefGoogle ScholarPubMed
Fry, B. (2006) Stable isotope ecology. New York: Springer.CrossRefGoogle Scholar
Gloeckner, V., Wehrl, M., Moitinho-Silva, L., Gernert, C., Schupp, P., Pawlik, J.R., Lindquist, N.L., Erpenbeck, D., Wörheide, G. and Hentschel, U. (2014) The HMA-LMA dichotomy revisited: an electron microscopical survey of 56 sponge species. Biological Bulletin 227, 78–88.CrossRefGoogle ScholarPubMed
Hopkinson, C.S., Fallon, R.D., Jansson, B. and Schubauer, J.P. (1991) Community metabolism and nutrient cycling at Gray's Reef, a hard bottom habitat in the Georgia Bight. Marine Ecology Progress Series 73, 105–120.CrossRefGoogle Scholar
Jackson, A.L., Inger, R., Parnell, A. and Bearhop, S. (2011) Comparing isotopic niche widths among and within communities: SIBER-Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80, 595–602.CrossRefGoogle ScholarPubMed
Knowlton, N. and Jackson, J.B.C. (1994) New taxonomy and niche partitioning on coral reefs: jack of all trades or master of some? Trends in Ecology and Evolution 9, 7–9.CrossRefGoogle ScholarPubMed
Knowlton, N. and Rohwer, F. (2003) Multispecies microbial mutualisms on coral reefs: the host as a habitat. American Naturalist 162, S51–S62.CrossRefGoogle ScholarPubMed
Lamb, K. and Swart, P.K. (2008) The carbon and nitrogen isotopic values of particulate organic material from the Florida Keys: a temporal and spatial study. Coral Reefs 27, 351–362.CrossRefGoogle Scholar
Layman, C.A., Araujo, M.S., Boucek, R., Harrison, E., Jud, Z.R., Matich, P., Hammerschlag-Peyer, C.M., Rosenblatt, A.E., Vaudo, J.J., Yeager, L.A., Post, D. and Bearhop, S. (2012) Applying stable isotopes to examine food web structure: an overview of analytical tools. Biological Reviews 87, 542–562.CrossRefGoogle ScholarPubMed
Layman, C.A., Arrington, D.A., Montaña, C.G. and Post, D.M. (2007) Can stable isotope ratios provide quantitative measures of trophic diversity within food webs? Ecology 88, 42–48.CrossRefGoogle Scholar
Lemloh, M., Fromont, J., Brümmer, F. and Usher, K.M. (2009) Diversity and abundance of photosynthetic sponges in temperate Western Australia. BMC Ecology 9, 4.CrossRefGoogle ScholarPubMed
Maldonado, M., Ribes, M. and van Duyl, F.C. (2012) Nutrient fluxes through sponges: biology, budgets, and ecological implications. Advances in Marine Biology 62, 113–182.CrossRefGoogle ScholarPubMed
Michener, R.H. and Kaufman, L. (2007) Stable isotope ratios as tracers in marine aquatic food webs: an update. In Michener, R.H. and Lajtha, K. (eds) Stable isotopes in ecology and environmental science. 2nd edition. Oxford: Blackwell Publishing, pp. 238–282.CrossRefGoogle Scholar
Mohamed, N.M., Colman, A.S., Tal, Y. and Hill, R.T. (2008) Diversity and expression of nitrogen fixation genes in bacterial symbionts of marine sponges. Environmental Microbiology 10, 2910–2921.CrossRefGoogle ScholarPubMed
Moran, N.A. (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proceedings of the National Academy of Sciences USA 104, 8627–8633.CrossRefGoogle ScholarPubMed
Moya, A., Peretó, J., Gil, R. and Latorre, A. (2008) Learning how to live together: genomic insights into prokaryote-animal symbioses. Nature Review Genetics 9, 218–229.CrossRefGoogle ScholarPubMed
Muller-Parker, G. and Davy, S.K. (2001) Temperate and tropical algal-sea anemone symbioses. Invertebrate Biology 120, 104–123.CrossRefGoogle Scholar
Muscatine, L. and Cernichiari, E. (1969) Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biological Bulletin 137, 506–523.CrossRefGoogle ScholarPubMed
Muscatine, L. and Porter, J.W. (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience 27, 454–460.CrossRefGoogle Scholar
Newsome, S.D., Del Rio, C.M., Bearhop, S. and Phillips, D.L. (2007) A niche for isotopic ecology. Frontiers in Ecology and the Environment 5, 429–436.CrossRefGoogle Scholar
Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O'hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H. and Wagner, H. (2014) Vegan: community ecology package. Available at: http://cran.r-project.org/web/packages/vegan.Google Scholar
Roberts, D.E., Cummins, S.P., Davis, A.R. and Pangway, C. (1999) Evidence for symbiotic algae in sponges from temperate coastal reefs in New South Wales, Australia. Memoirs of the Queensland Museum 44, 493–497.Google Scholar
Ruzicka, R. and Gleason, D.F. (2009) Sponge community structure and anti-predator defenses on temperate reefs of the South Atlantic Bight. Journal of Experimental Marine Biology and Ecology 380, 36–46.CrossRefGoogle Scholar
Southwell, M.W., Popp, B.N. and Martens, C.S. (2008) Nitrification controls on fluxes and isotopic composition of nitrate from Florida Keys sponges. Marine Chemistry 108, 96–108.CrossRefGoogle Scholar
Taylor, M.W., Radax, R., Steger, D. and Wagner, M. (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiology and Molecular Biology Reviews 71, 295–347.CrossRefGoogle ScholarPubMed
Thacker, R.W. and Freeman, C.J. (2012) Sponge-microbe symbioses: recent advances and new directions. Advances in Marine Biology 62, 57–111.CrossRefGoogle ScholarPubMed
Thurber, A.R. (2007) Diets of Antarctic sponges: links between the pelagic microbial loop and benthic metazoan food web. Marine Ecology Progress Series 351, 77–89.CrossRefGoogle Scholar
Turner, T.F., Collyer, M.L. and Krabbenhoft, T.J. (2010) A general hypothesis-testing framework for stable isotope ratios in ecological studies. Ecology 91, 2227–2233.CrossRefGoogle ScholarPubMed
Usher, K.M. (2008) The ecology and phylogeny of cyanobacterial symbionts in sponges. Marine Ecology 29, 178–192.CrossRefGoogle Scholar
van Duyl, F.C., Moodley, L., Nieuwland, G., van Ijzerloo, L., van Soest, R.W.M., Houtekamer, M., Meesters, E.H. and Middelburg, J.J. (2011) Coral cavity sponges depend on reef-derived food resources: stable isotope and fatty acid constraints. Marine Biology 158, 1653–1666.CrossRefGoogle ScholarPubMed
Vrijenhoek, R.C. (2010) Genetics and evolution of deep-sea chemosynthetic bacteria and their invertebrate hosts. In Kiel, S. (ed.) The vent and seep biota, Topics in Geobiology 33. Berlin: Springer, pp. 15–50.CrossRefGoogle Scholar
Webster, N.S., Negri, A.P., Munro, M.M. and Battershill, C.N. (2004) Diverse microbial communities inhabit Antarctic sponges. Environmental Microbiology 6, 288–300.CrossRefGoogle ScholarPubMed
Weisz, J.B. (2006) Measuring impacts of associated microbial communities on Caribbean reef sponges: searching for symbiosis. PhD thesis. University of North Carolina at Chapel Hill, North Carolina, USA.Google Scholar
Weisz, J.B., Hentschel, U., Lindquist, N. and Martens, C.S. (2007) Linking abundance and diversity of sponge-associated microbial communities to metabolic differences in host sponges. Marine Biology 152, 475–483.CrossRefGoogle Scholar
Wilkinson, C.R. (1983) Net primary productivity in coral reef sponges. Science 219, 410–412.CrossRefGoogle ScholarPubMed
Supplementary material: File

Freeman supplementary material

Supplementary Table 1

Download Freeman supplementary material(File)
File 115.9 KB