Natural diet of coral-excavating sponges consists mainly of dissolved organic carbon (DOC)

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Mueller, Benjamin ^a,b,c   De Goeij, Jasper M ^b,d   Vermeij, Mark J A ^b,d   Mulders, Yannick ^c   Van Der Ent, Esther ^c   Ribes, Marta ^e   Van Duyl, Fleur C ^a,b  

^a ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^b CARMABI ^*  (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

^e INSTITUT DE CIÈNCIES DEL MAR   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; DISSOLVED ORGANIC MATTER; ORGANIC CARBON;

ARTICLE; BACTERIUM; CLIONA DELITRIX; CONTROLLED STUDY; CORAL EXCAVATING SPONGE; CORAL REEF; FOOD AVAILABILITY; FOOD COMPOSITION; NONHUMAN; NUTRIENT UPTAKE; PARTICULATE MATTER; PHYTOPLANKTON; SAMPLER; SIPHONODICTYON; SPECIES COMPARISON; SPONGE (PORIFERA); WATER SAMPLING;

ANIMALS; ANTHOZOA; BACTERIA; BIOLOGICAL TRANSPORT; CARBON; DIET; ORGANIC CHEMICALS; PORIFERA;

EID: 84896387677     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0090152     Document Type: Article

References (66)

1. Hein JF, Risk MJ (1975) Bioerosion of coral heads: inner patch reefs, Florida reef tract. Bull Mar Sci 25: 133-138.
2. Gonzalez-Rivero M, Yakob L, Mumby PJ (2011) The role of sponge competition on coral reef alternative steady states. Ecological Modelling 222: 1847-1853.
3. Risk MJ, Sammarco PW, Edinger EN (1995) Bioerosion in Acropora across the continental shelf of the Great Barrier Reef. Coral Reefs 14: 79-86. (Pubitemid 26452052)
4. Mallela J, Perry CT (2007) Calcium carbonate budget for two coral reefs affected by different terrestrial runoff regimes, Rio Bueno, Jamaica. Coral Reefs 26: 129-145. (Pubitemid 46491130)
5. Calcinai B, Azzini F, Bavestrello G, Gaggero L, Cerrano C (2007) Excavating rates and boring pattern of Cliona albimarginata (Porifera: Clionaidae) in different substrata. In: Custódio MR, Hajdu E, Lôbo-Hajdu G, Muricy G (eds) Porifera research: biodiversity, innovation and sustainability. Proc 7th Int Sponge Symp: 255-263.
6. Andersson AJ, Gledhill D (2013) Ocean acidification and coral reefs: Effects on breakdown, dissolution, and net ecosystem calcification. Annu Rev Mar Sci 5: 321-48.
7. Glynn PW (1997) Bioerosion and coral reef growth: a dynamic balance. In: Birkeland C editor. Life and Death of Coral Reefs. New York: Chapman and Hall. pp. 68-95.
8. Holmes KE (2000) Effects of eutrophication on bioeroding sponge communities with the description of new West Indian sponges, Cliona spp. (Porifera: Hadromerida: Clionidae). Invert Biol 119: 125-138.
9. Ward-Paige CA, Risk MJ, Sherwood OA, Jaap WC (2005) Clionid sponge surveys on the Florida Reef Tract suggest land-based nutrient inputs. Mar Pollut Bull 51: 570-570.
10. Chaves-Fonnegra A, Zea S, Gómez ML (2007) Abundance of the excavating sponge Cliona delitrix in relation to sewage discharge at San Andrés Island, SW Caribbean, Colombia. Bol Investig Mar Costeras 36: 63-78.
11. Hoegh-Guldberg O, Mumby PJ, Steneck RS, Greenfield P, Gomez E, et al. (2007) Coral reefs under rapid climate change and ocean acidification. Science 318: 1737-1742.
12. Cantin NE, Cohen AL, Karnauskas KB, Tarrant AM, McCorkle DC (2010) Ocean warming slows coral growth in the central Red Sea. Science 329: 322-325.
13. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333: 418.
14. Duckworth AR, Petersen BJ (2012) Effects of seawater temperature and pH on the boring rates of the sponge Cliona celata in scallop shells. Mar Biol 160: 27-35.
15. Fang JKH, Mello-Athayde MA, Schönberg CHL, Kline DI, Hoegh-Guldberg O, et al. (2013) Sponge biomass and bioerosion rates increase under ocean warming and acidification. Glob Change Biol 19: 3581-3591.
16. Wisshak M, Schönberg CHL, Form A, Freiwald A (2012) Ocean acidification accelerates reef bioerosion. PLoS ONE 7(9): e45124. doi:10.1371/journal.pone. 0045124.
17. Wisshak M, Schönberg CHL, Form A, Freiwald A (2013) Effects of ocean acidification and global warming on reef bioerosion - lessons from a clionaid sponge. Aquat Biol 19: 11-127.
18. Schönberg CHL (2008) A history of sponge erosion: from past myths and hypotheses to recent approaches. In Wisshak M, Tapanila L (eds) Current developments in bioerosion. Springer-Verlag Berlin: 165-202.
19. Schönberg CHL, Wisshak M (2012) The perks of being endolithic. Aquat Biol 17: 1-5.
20. Hill MS (1996) Symbiotic zooxanthellae enhance boring and growth rates of the tropical sponge Anthosigmella varians forma varians. Mar Biol 125: 649-654.
21. Weisz JB, Massaro AJ, Ramsby BD, Hill MS (2010) Zooxanthellar symbionts shape host sponge trophic status through translocation of carbon. Biol Bull 219: 189-97.
22. Reiswig HM (1971) Particle feeding in natural populations of three marine demosponges. Biol Bull 141: 568-591.
23. Reiswig HM (1975) Bacteria as food for temperate-water marine sponges. Can J Zool 533: 582-589.
24. 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. (Pubitemid 27422623)
25. 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. (Pubitemid 29107456)
26. Perea-Blázquez A, Davy SK, Bell JJ (2012) Estimates of particulate organic carbon flowing from the pelagic environment to the benthos through sponge assemblages. PlosOne 7(1): e29569. doi:10.1371/journal.pone.0029569.
27. Vacelet J, Boury-Esnault N (1995) Carnivorous sponges. Nature 373: 333-335.
28. Reiswig HM (1974) Water transport, respiration and energetics of three tropical marine sponges. J Exp Mar Biol Ecol 14: 231-249.
29. Yahel G, Sharp JH, Marie D, Haese 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. (Pubitemid 36144745)
30. De Goeij JM, Van den Berg H, Van Oostveen MM, Epping EHG, Van Van Duyl FC (2008) Major bulk dissolved organic carbon (DOC) removal by encrusting coral reef cavity sponges. Mar Ecol Prog Ser 357: 139-151. (Pubitemid 351655948)
31. De Goeij JM, Van Oevelen D, Vermeij MJA, Osinga R, Middelburg JJ, et al. (2013) Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342: 108-110.
32. Ribes M, Jimenez E, Yahel G, Lopez-Sendino P, Diez B, et al. (2012) Functional convergence of microbes associated with temperate marine sponges. Environ Microbiol 14: 1224-1239.
33. Van Duyl FC (1985) Atlas of the living reefs of Curaçao and Bonaire (Netherlands Antilles). Studies of the flora and fauna of Surinam and the Netherlands Antilles Vol 117, Utrecht.
34. Yahel G, Whitney F, Reiswig HM, Eerkes-Medrano DI, Leys SP (2007) In situ feeding and metabolism of glass sponges (Hexactinellida, Porifera) studied in a deep temperate fjord with a remotely operated submersible. Limnol Oceanogr 52: 428-440. (Pubitemid 46972152)
35. 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. (Pubitemid 43723675)
36. Fukuda R, Ogawa H, Nagata T, Koike I (1998) Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments. Appl Environ Microbiol 64: 3352-3358. (Pubitemid 28411458)
37. Ayukai T (1995) Retention of phytoplankton and planktonic microbes on coral reefs within the Great Barrier Reef, Australia. Coral Reefs 14: 141-147.
38. Yahel G, Post AF, Fabricius K, Marie D, Vaulot D, et al. (1998) Phytoplankton distribution and grazing near coral reefs. Limnol Oceanogr 43: 551-563. (Pubitemid 28382165)
39. Van Duyl FC, Gast GJ, Steinhoff W, Kloff S, Veldhuis MJW, et al. (2002) Factors influencing the short-term variation in phytoplankton composition and biomass in coral reef waters. Coral Reefs 21: 293-306. (Pubitemid 36053187)
40. Richter C, Wunsch M, Rasheed M, Kötter I, Badran MI (2001) Endoscopic exploration of Red Sea coral reefs reveals dense populations of cavity-dwelling sponges. Nature 413: 726-730. (Pubitemid 33009949)
41. Kötter I (2003) Feeding ecology of coral reef sponges. PhD thesis, Universität Bremen.
42. Rützler K (2002) Impact of crustose clionid sponges in Caribbean coral reefs. Acta Geol Hisp 37: 61-72.
43. Coma R, Ribes M, Gili JM, Hughes RN (2001) The ultimate opportunists: consumers of seston. 44. Mar Ecol Prog Ser 219: 305-308.
44. Van Duyl FC, Hegeman J, Hoogstraten A, Maier C (2008) Dissolved carbon fixation by sponge-microbe consortia of deep water coral mounds in the northeastern Atlantic Ocean. Mar Ecol Prog Ser 358: 137-150. (Pubitemid 351723932)
45. Gerrodette T, Flechsig AO (1979) Sediment-induced reduction in the pumping rate of the tropical sponge Verongia lacunosa. Mar Biol 55: 103-110.
46. Tompkins-Mac Donald GJ, Leys SP (2008) Glass sponges arrest pumping in response to 48. sediment: implications for physiology of the hexactinellid conduction system. Mar Biol 154: 973-984.
47. Rose CS, Risk MJ (1985) Increase in Cliona delitrix infestation of Montastraea cavernosa heads on an organically polluted portion of the Grand Cayman. P.S.Z.N.I: Mar Ecol 6: 345-363. (Pubitemid 17248200)
48. Rützler K (1971) Bredin-Archbold-Smithsonian biological survey of Dominica: burrowing sponges, genus Siphonodictyon Bergquist, from the Caribbean. Smithson Contrib Zool 77: 37.
49. 13C-enriched dissolved and particulate carbon in Halisarca caerulea, a coral reef sponge with associated bacteria: evidence for DOM-feeding. Limnol Oceanogr 53: 1376-1386.
50. Maliao RJ, Turingan RG, Lin J (2008) Phase-shift in coral reef communities in the Florida Keys National Marine Sanctuary (FKNMS), USA. Mar Biol 154: 841-853.
51. Wild C, Haas AF, Naumann MS, Mayr C, el-Zidbah M (2008) Phase shifts in coral reefs - comparative investigation of corals and benthic algae as ecosystem engineers. Proc 11th Int Coral Reef Symp Ft. Lauderdale, pp. 1319-1323.
52. Haas AF, Nelson CE, Rohwer F, Wegley-Kelly L, Quistad SD, et al. (2013) Influence of coral and algal exudates on microbially mediated reef metabolism. PeerJ 1: e108; DOI 565 10.7717/peerj.108.
53. Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265(5178): 1547.
54. McCook LJ, Jompa J, Diaz-Pulido G (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19: 400- 417.
55. Kennedy EV, Perry CT, Halloran PR, Iglesias-Prieto R, Schönberg CHL, et al. (2013) Avoiding coral reef functional collapse requires local and global action. Curr Biol 23: 912-918.
56. 2 availability. Mar Ecol Prog Ser 409: 27-39.
57. Haas AF, Naumann MS, Struck U, Mayr C, el-Zidah M, et al. (2010b) Organic matter release by coral reef associated benthic algae in the Northern Red Sea. J Exp Mar Biol Ecol 389: 53-60.
58. Naumann MS, Haas AF, Struck U, Mayr C, el-Zibdah M, et al. (2010) Organic matter release by dominant scleractinian corals of the Northern Red Sea. Coral Reefs 29: 649-659.
59. Haas AF, Nelson CE, Wegley Kelly L, Carlson CA, Rohwer F, et al. (2011) Effects of coral reef benthic primary producers on dissolved organic carbon and microbial activity. PLoS ONE 6(11): e27973. doi:10.1371/journal.pone. 0027973.
60. Nelson CE, Goldberg SJ, Wegley Kelly L, Haas AF, Smith JE, et al. (2013) Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages. ISME J 7: 962-979.
61. Cebrian E, Uriz MJ (2006) Grazing on fleshy seaweeds by sea urchins facilitates sponge Cliona viridis growth. Mar Ecol Prog Ser 323: 83-89. (Pubitemid 44689617)
62. Cebrian E (2010) Grazing on coral reefs facilitates growth of the excavating sponge Cliona orientalis (Clionaidae, Hadromerida). Mar Ecol 31: 533-538.
63. González-Rivero M, Ferrari R, Schönberg CHL, Mumby PJ (2012) Impacts of macroalgal competition and parrotfish predation on the growth of a common bioeroding sponge. Mar Ecol Prog Ser 444: 133-142.
64. López-Victoria M, Zea S, Weil E (2006) Competition for space between encrusting excavating Caribbean sponges and other coral reef organisms. Mar Ecol Prog Ser 312: 1132121.
65. Colvard NB, Edmunds PJ (2010) Decadal-scale changes in abundance of non-scleractinian invertebrates on a Caribbean coral reef. J Exp Mar Biol Ecol 397: 153-160.
66. Bell JJ, Davy SK, Jones T, Taylor MW, Webster NS (2013) Could some coral reefs become sponge reefs as our climate changes? Glob Change Biol 19: 2613-2624.