Skip to main content

Advertisement

SpringerLink
Log in

Do associated microbial abundances impact marine demosponge pumping rates and tissue densities?

  • Community Ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The evolution of marine demosponges has led to two basic life strategies: one involving close associations with large and diverse communities of microorganisms, termed high microbial abundance (HMA) species, and one that is essentially devoid of associated microorganisms, termed low microbial abundance (LMA) species. This dichotomy has previously been suggested to correlate with morphological differences, with HMA species having a denser mesohyl and a more complex aquiferous systems composed of longer and narrower water canals that should necessitate slower seawater filtration rates. We measured mesohyl density for a variety of HMA and LMA sponges in the Florida Keys, and seawater pumping rates for a select group of these sponges using an in situ dye technique. HMA sponges were substantially denser than LMA species, and had per unit volume pumping rates 52–94% slower than the LMA sponges. These density and pumping rate differences suggest that evolutionary differences between HMA and LMA species may have resulted in profound morphological and physiological differences between the two groups. The LMA sponge body plan moves large quantities of water through their porous tissues allowing them to rapidly acquire the small particulate organic matter (POM) that supplies the majority of their nutritional needs. In contrast, the HMA sponge body plan is suited to host large and tightly packed communities of microorganisms and has an aquiferous system that increases contact time between seawater and the sponge/microbial consortium that feeds on POM, dissolved organic matter and the raw inorganic materials for chemolithotrophic sponge symbionts. The two evolutionary patterns represent different, but equally successful patterns and illustrate how associated microorganisms can potentially have substantial effects on host evolution.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ahn Y-B, Rhee S-K, Fennell DE, Kerkhof LJ, Hentschel U, Häggblom MM (2003) Reductive dehalogenation of brominated phenolic compounds by microorganisms associated with the marine sponge Aplysina aerophoba. Appl Environ Microbiol 69:4159–4166

    Article  PubMed  CAS  Google Scholar 

  • Bak RPM, Joenje M, de Jong I, Lambrechts DYM, Nieuwland G (1998) Bacterial suspension feeding by coral reef benthic organisms. Mar Ecol Prog Ser 175:285–288

    Article  Google Scholar 

  • Bergquist PR (1978) Sponges. University of California Press, Berkeley, Calif.

    Google Scholar 

  • Boury-Esnault N, De Vos L, Donadey C, Vacelet J (1990) Ultrastructure of choanosome and sponge classification. In: Rützler K (ed) New perspectives in sponge biology. Smithosonian Institution Press, Washington, D.C. pp 237–244

    Google Scholar 

  • Chanas B, Pawlik JR (1995) Defenses of Caribbean sponges against predatory reef fish. 2. Spicules, tissue toughness, and nutritional quality. Mar Ecol Prog Ser 127:195–211

    Article  Google Scholar 

  • Corredor JE, Wilkinson CR, Vicente VP, Morell JM, Otero E (1988) Nitrate release by Caribbean reef sponges. Limnol Oceanogr 33:114–120

    Article  CAS  Google Scholar 

  • Diaz MC, Ward BB (1997) Sponge-mediated nitrification in tropical benthic communities. Mar Ecol Prog Ser 156:97–107

    Article  CAS  Google Scholar 

  • Diaz MC, Rutzler K (2001) Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci 69:535–546

    Google Scholar 

  • Dunlap M, Pawlik JR (1998) Spongivory by parrotfish in Florida mangrove and reef habitats. PSZN Mar Ecol 19:325–337

    Google Scholar 

  • Fieseler L, Horn M, Wagner M, Hentschel U (2004) Discovery of the novel candidate phylum “Poribacteria” in marine sponges. Appl Environ Microbiol 70:3724–3732

    Article  PubMed  CAS  Google Scholar 

  • Gatti S, Brey T, Muller WEG, Heilmayer O, Holst G (2002) Oxygen microoptodes: a new tool for oxygen measurements in aquatic animal ecology. Mar Biol 140:1075–1085

    Article  Google Scholar 

  • Gerrodette T, Flechsig AO (1979) Sediment-induced reduction in the pumping rate of the tropical sponge Verongia lacunosa. Mar Biol 55:103–110

    Article  Google Scholar 

  • Hadas E, Marie D (2006) Virus predation by sponges is a new nutrient-flow pathway in coral reef food webs. Limnol Oceanogr 51:1548–1550

    Google Scholar 

  • Harrison FW, Cowden RR (1976) Aspects of sponge biology. Academic Press, New York

    Google Scholar 

  • Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M, Hacker J, Horn M (2003) Microbial diversity of marine sponges. In: Mueller WEG (ed) Sponge (Porifera). Springer, Berlin Heidelberg New York

  • Hentschel U, Usher KM, Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55:167–177

    Article  PubMed  CAS  Google Scholar 

  • Hill MS, Hill AL (2002) Morphological plasticity in the tropical sponge Anthosigmella varians: responses to predators and wave energy. Biol Bull 202:86–95

    Article  PubMed  Google Scholar 

  • Hoffmann F, Larsen O, Thiel V, Rapp HT, Pape T, Michaelis W, Reitner J (2005) An anaerobic world in sponges. Geomicrobiol J 22:1–10

    Article  Google Scholar 

  • Jorgensen CB (1949) Feeding-rates of sponges, lamellibranches and ascidians. Nature 163:912

    Article  Google Scholar 

  • Jorgensen CB (1955) Quantitative aspects of filter feeding in invertebrates. Biol Rev 30:391–454

    Google Scholar 

  • Kowalke J (2000) Ecology and energetics of two Antarctic sponges. J Exp Mar Biol Ecol 247:85–97

    Article  PubMed  Google Scholar 

  • LaBarbera M, Vogel S (1976) An inexpensive thermistor flowmeter for aquatic biology. Limnol Oceanogr 21:750–756

    Google Scholar 

  • Lynch TC, Phlips EJ (2000) Filtration of the bloom-forming cyanobacteria Synechococcus by three sponge species from Florida Bay, USA. Bull Mar Sci 67:923–936

    Google Scholar 

  • Martens CS, Southwell MW, Lindquist N, Weisz JB, Hench J (2006) Sponge respiration and organic matter recycling on coral reef ecosystems of the Florida Keys. EOS Trans AGU 87:36

    Google Scholar 

  • McDonald JI, Hooper JNA, McGuinness KA (2002) Environmentally influenced variability in the morphology of Cinachyrella australiensis (Carter 1886) (Porifera : Spirophorida : Tetillidae). Mar Freshwater Res 53:79–84

    Article  Google Scholar 

  • McDonald KS, Rios R, Duffy JE (2006) Biodiversity, host specificity, and dominance by eusocial species among sponge-dwelling alpheid shrimp on the Belize Barrier Reef. Divers Distrib 12:165–178

    Article  Google Scholar 

  • Meroz-Fine E, Shefer S, Ilan M (2005) Changes in morphology and physiology of an east Mediterranean sponge in different habitats. Mar Biol 147:243–250

    Article  Google Scholar 

  • Meylan AB (1988) Spongivory in hawksbill turtles—a diet of glass. Science 239:393–395

    Article  PubMed  CAS  Google Scholar 

  • Parker GH (1910) The reactions of sponges, with a consideration of the origins of the nervous system. J Exp Zool 8:1–41

    Article  Google Scholar 

  • Parker GH (1914) On the strength and the volume of the water currents produced by sponges. J Exp Zool 16:443–446

    Article  Google Scholar 

  • Pile AJ (1997) Finding Reiswig’s missing carbon: quantification of sponge feeding using dual-beam flow cytometry. Proc Int Coral Reef Symp 2:1403–1410

    CAS  Google Scholar 

  • Pile AJ (1999) Resource partitioning by Caribbean coral reef sponges: is there enough food for everyone? Mem Queensl Mus 44:457–461

    Google Scholar 

  • Pile AJ, Young CM (2006) The natural diet of a hexactinellid sponge: benthic–pelagic coupling in a deep-sea microbial food web. Deep Sea Res Pt I 53:1148–1156

    Article  Google Scholar 

  • Pile AJ, Patterson MR, Witman JD (1996) In situ grazing on plankton <10 mu m by the boreal sponge Mycale lingua. Mar Ecol Prog Ser 141:95–102

    Article  Google Scholar 

  • Pile AJ, Patterson MR, Savarese M, Chernykh VI, Fialkov VA (1997) Trophic effects of sponge feeding within Lake Baikal’s littoral zone. 2. Sponge abundance, diet, feeding efficiency, and carbon flux. Limnol Oceanogr 42:178–184

    Article  CAS  Google Scholar 

  • Randall JE, Hartman WD (1968) Sponge-feeding fishes of the West Indies. Mar Biol 1:216–225

    Article  Google Scholar 

  • Reiswig HM (1971a) In-situ pumping activities of tropical demospongiae. Mar Biol 9:38–50

    Article  Google Scholar 

  • Reiswig HM (1971b) Particle feeding in natural populations of three marine demosponges. Biol Bull 141:568–591

    Article  Google Scholar 

  • Reiswig HM (1974) Water transport, respiration and energetics of three tropical marine sponges. J Exp Mar Biol Ecol 14:231–249

    Article  Google Scholar 

  • Reiswig HM (1975a) Bacteria as food for temperate-water sponges. Can J Zool 53:582–589

    Google Scholar 

  • Reiswig HM (1975b) The aquiferous systems of three marine Demospongiae. J Morphol 145:493–502

    Article  Google Scholar 

  • Reiswig HM (1981) Partial carbon and energy budgets of the bacteriosponge Verongia fistularis (Porifera: Demospongiae) in Barbados. PSZNI Mar Ecol 2:273–293

    Article  CAS  Google Scholar 

  • Ribes M, Coma R, Gili JM (1999) Natural diet and grazing rate of the temperate sponge Dysidea avara (Demospongiae, Dendroceratida) throughout an annual cycle. Mar Ecol Prog Ser 176:179–190

    Article  Google Scholar 

  • Richelle-Maurer E, De Kluijver MJ, Feio S, Gaudencio S, Gaspar H, Gomez R, Tavares R, Van de Vyver G, Van Soest RWM (2003) Localization and ecological significance of oroidin and sceptrin in the Caribbean sponge Agelas conifera. Biochem Syst Ecol 31:1073–1091

    Article  CAS  Google Scholar 

  • Riisgard HU, Thomassen S, Jakobsen H, Weeks JM, Larsen PS (1993) Suspension-feeding in marine sponges Halichondria-panicea and Haliclona-urceolus—effects of temperature on filtration-rate and energy-cost of pumping. Mar Ecol Prog Ser 96:177–188

    Article  Google Scholar 

  • Rützler K (1990) Associations between Caribbean sponges and photosynthetic organisms. In: Rützler K (ed) New perspectives in sponge biology. Smithosonian Institution Press, Washington, D.C., pp 455–466

    Google Scholar 

  • Savarese M, Patterson MR, Chernykh VI, Fialkov VA (1997) Trophic effects of sponge feeding within Lake Baikal’s littoral zone. 1. In situ pumping rates. Limnol Oceanogr 42:171–178

    Article  Google Scholar 

  • Southwell MW (2007) Sponge impacts on coral reef N cycling, Florida Keys, USA. PhD thesis. University of North Carolina at Chapel Hill, N.C.

  • Southwell MW, Weisz JB, Martens CS, Lindquist N (2008) In situ measurement of dissolved inorganic nitrogen from the sponge community on Conch Reef, Key Largo, Florida. Limnol Oceanogr (in press)

  • Thomassen S, Riisgard HU (1995) Growth and energetics of the sponge Halichondria panicea. Mar Ecol Prog Ser 128:239–246

    Article  Google Scholar 

  • Turon X, Galera J, Uriz MJ (1997) Clearance rates and aquiferous systems in two sponges with contrasting life-history strategies. J Exp Zool 278:22–36

    Article  Google Scholar 

  • Vacelet J, Donadey C (1977) Electron-microscope study of association between some sponges and bacteria. J Exp Mar Biol Ecol 30:301–314

    Article  Google Scholar 

  • Vacelet J, Fiala-Medioni A, Fisher CR, Boury-Esnault N (1996) Symbiosis between methane-oxidizing bacteria and a deep-sea carnivorous cladorhizid sponge. Mar Ecol Progr Ser 145:77–85

    Article  Google Scholar 

  • Vicente VP (1990) Response of sponges with autotrophic endosymbionts during the coral-bleaching episode in Puerto Rico. Coral reefs 8:199–202

    Article  Google Scholar 

  • Vogel S (1974) Current-induced flow through the sponge, Halichondria. Biol Bull 147:443–456

    Article  PubMed  CAS  Google Scholar 

  • Vogel S (1977) Current-induced flow through living sponges in nature. Proc Natl Acad Sci USA 74:2069–2071

    Article  PubMed  CAS  Google Scholar 

  • Vogel S (1994) Life in moving fluids. Princeton University Press, Princeton, N.J., p 467

    Google Scholar 

  • Wehrl M (2001) Masters thesis. University of Wuerzburg, Germany

  • Weisz JB (2006) Measuring impacts of associated microbial communities on Caribbean reef sponges: searching for symbiosis. PhD thesis. University of North Carolina at Chapel Hill, N.C.

  • Weisz JB, Hentschel U, Lindquist N, Martens CS (2007) Linking abundance and diversity of sponge-associated microbial communities to metabolic differences in host sponges. Mar Biol 152: 475–483

    Article  CAS  Google Scholar 

  • Wilkinson CR (1983) Net primary productivity in coral reef sponges. Science 219:410–412

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson CR (1987) Significance of microbial symbionts in sponge evolution and ecology. Symbiosis 4:135–146

    Google Scholar 

  • Wilkinson CR, Evans E (1989) Sponge distribution across Davies Reef, Great Barrier Reef, relative to location, depth, and water movement. Coral Reefs 8:1–7

    Article  Google Scholar 

  • Wilkinson CR, Summons RE, Evans E (1999) Nitrogen fixation in symbiotic marine sponges: ecological significance and difficulties in detection. Mem Queensl Mus 44:667–673

    Google Scholar 

  • Witte U, Brattegard T, Graf G, Springer B (1997) Particle capture and deposition by deep-sea sponges from the Norwegian–Greenland Sea. Mar Ecol Prog Ser 154:241–252

    Article  Google Scholar 

  • Yahel G, Sharp JH, Marie D, Hase 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

    Google Scholar 

  • Yahel G, Marie D, Genin A (2005) InEx—a direct in situ method to measure filtration rates, nutrition, and metabolism of active suspension feeders. Limnol Oceanogr Methods 3:46–58

    CAS  Google Scholar 

Download references

Acknowledgements

Financial support was provided by the NOAA National Undersea Research (NURP) Center at the UNCW under grant number NA03OAR4300088; the National Science Foundation (NSF) Chemical Oceanography Division (OCE 0351893 & OCE 0531422); a NSF graduate fellowship to J. B. W.; and UNC URC grants to C. S. M, and to N. L. This work was greatly facilitated by the exceptional logistical support provided by all of the staff of the UNCW-NURP Center, including the Aquarius, dayboat, and technical diving crews. The manuscript was greatly improved based on the comments of three anonymous reviewers. This research was conducted under National Marine Sanctuary permit FKNMS-2004-036, and these experiments comply with the current laws of the state of Florida and the United States of America in which they were performed.

Author information

Authors and Affiliations

  1. Institute of Marine Sciences, University of North Carolina at Chapel Hill, 3431 Arendell St, Morehead City, NC, 28557, USA

    Jeremy B. Weisz & Niels Lindquist

  2. Department of Marine Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, 27599, USA

    Christopher S. Martens

  3. Department of Biological Sciences, Old Dominion University, Norfolk, VA, 23529, USA

    Jeremy B. Weisz

Authors
  1. Jeremy B. Weisz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Niels Lindquist
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christopher S. Martens
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jeremy B. Weisz.

Additional information

Communicated by Joel Trexler.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM (PDF 560 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weisz, J.B., Lindquist, N. & Martens, C.S. Do associated microbial abundances impact marine demosponge pumping rates and tissue densities?. Oecologia 155, 367–376 (2008). https://doi.org/10.1007/s00442-007-0910-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-007-0910-0

Keywords

Search

Navigation