Ecology of caribbean sponges: Are top-down or bottom-up processes more important?

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Lesser, Michael P ^a   Slattery, Marc ^b  

^a UNIVERSITY OF NEW HAMPSHIRE   (United States)

^b UNIVERSITY OF MISSISSIPPI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BODY GROWTH; BODY SIZE; BOTTOM UP PROCESS; CALLYSPONGIA; CALLYSPONGIA VAGINALIS; CENTRAL AMERICA; COMMUNITY ECOLOGY; COMMUNITY STRUCTURE; CONTROLLED STUDY; FOOD AVAILABILITY; NONHUMAN; POPULATION ABUNDANCE; PREDATION; TOP DOWN PROCESS;

ANIMALS; BIODIVERSITY; BIOMASS; CARIBBEAN REGION; CORAL REEFS; ECOSYSTEM; FEEDING BEHAVIOR; FOOD CHAIN; PORIFERA; PREDATORY BEHAVIOR;

EID: 84893162081     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079799     Document Type: Article

References (87)

1. Wilkinson CR (1983) Net primary productivity in coral reef sponges. Science 219: 410-412.
2. Wilkinson CR (1987) Interocean differences in size and nutrition of coral reef sponge populations. Science 236: 1654-1657.
3. Wilkinson CR, Cheshire AC (1990) Comparisons of sponge populations across the Barrier Reefs of Australia and Belize: evidence for higher productivity in the Caribbean. Mar Ecol Prog Ser 67: 285-294.
4. Bell JJ (2008) The functional biology of sponges. Est Coast Shelf Sci 79: 341-353.
5. Wulff JL (2006) Rapid diversity and abundance decline in a Caribbean coral reef sponge community. Biol Cons 127: 167-176.
6. Wulff JL (2012) Ecological interactions and the distribution, abundance, and diversity of sponges. Adv Mar Biol 61: 273-344.
7. Schmahl GP (1990) Community structure and ecology of sponges associated with four Southern Florida coral reefs. In: New Perspectives in Sponge Biology. Rützler K, editor. Smithsonian Institution Press, Washington, D.C, pp. 384-390.
8. Reed JK, Pomponi SA (1997) Biodiversity and distribution of deep and shallow water sponges in the Bahamas. Proc of the 8th Int Coral reef Symp 2: 1387-1392.
9. Reiswig HM (1974) Water transport, respiration and energetics of three tropical marine sponges. J Exp Mar Biol Ecol 14: 231-249.
10. Pile AJ (1997) Finding Reiswig's missing carbon: quantification of sponge feeding using dual-beam flow cytometry. Proc 8th Int Coral Reef Symp 2: 1403-1410.
11. Lesser MP (2006) Benthic-pelagic coupling on coral reefs: feeding and growth of Caribbean sponges. J Exp Mar Biol Ecol 328: 277-288.
12. Diaz MC, Rützler K (2001) Sponges: An essential component of Caribbean coral reefs. Bull Mar Sci 69: 535-546. (Pubitemid 34049784)
13. Fiore CL, Jutte PC (2010) Characterization of macrofaunal assemblages associated with sponges and tunicates collected off of the southeastern United States. Invert Biol 129: 105-120.
14. Gili JF, Coma R (1998) Benthic suspension feeders: their paramount role in littoral marine food webs. Trends Ecol Evol 13: 316-321.
15. Trussell GC, Lesser MP, Patterson MR, Genovese SJ (2006) Depth-specific differences in growth of the reef sponge Callyspongi vaginalis: role of bottom-up effects. Mar Ecol Prog Ser 323: 149-158. (Pubitemid 44689622)
16. Perea-Blázquez A, Davy SK, Bell JJ (2012) Estimates of particulate organic carbon flowing from the pelagic environment to the benthos through sponge assemblages. PLoS ONE 7: e29569.
17. Hill MS (1998) Spongivory on Caribbean reefs releases corals from competition with sponges. Oecologia 117: 143-150.
18. th Int Coral reef Symp 2: 1255-1258.
19. Pawlik JR (2011) The chemical ecology of sponges on Caribbean reefs: natural products shape natural systems. Bioscience 61: 888-898.
20. Pawlik JR, Chanas B, Toonen RJ, Fenical W (1995) Defenses of Caribbean sponges against predatory reef fish. I. chemical deterrency. Mar Ecol Prog Ser 127: 183-194. (Pubitemid 26453120)
21. Becerro MA, Thacker RW, Turon X, Uriz M, Paul VJ (2003) Biogeography of sponge chemical ecology: comparisons of tropical and temperate defenses. Oecologia 135: 91-101. (Pubitemid 36400241)
22. Thoms C, Schupp PJ (2007) Chemical defense strategies in sponges: a review. In: Porifera Research: Biodiversity, Innovation and Sustainability. Custódio MR, Lôbo-Hadju G, Hajdu Muricy G, editors. Série Livros. Museu Nacional, Rio de Janeiro, pp. 627-637.
23. Wulff JL (1997) Parrotfish predation on cryptic sponges of Caribbean coral reefs. Mar Biol 129: 41-52.
24. Wulff JL (2005) Ecological interactions of marine sponges. Can J Zool 84: 146-166.
25. Pawlik JR (1998) Coral reef sponges: Do predatory fishes affect their distribution? Limnol Oceanogr 43: 1396-1399.
26. Rützler K, Macintyre IG (1982) The habitat distribution and community structure of the barrier reef complex at Carrie Bow Cay, Belize. In: The Atlantic Barrier Reef Ecosystem at Carrie Bow Cay, Belize. 1 Structure and Communities. Rützler K, Macintyre IG, editors. Smithsonian Institution Press, Washington, pp. 9-45.
27. Suchanek TH, Carpenter RC, Witman JD, Harvell CD (1984) Sponges as important space competitors in deep Caribbean coral reef communities. In: The ecology of deep and shallow coral reefs. Reaka ML, editor. Symposia Series for Undersea Research, NOAA's Undersea Research Program. U.S. Department of Commerce, pp 55-60.
28. Liddell WD, Avery WE, Ohlhorst SL (1997) Patterns of benthic community structure, 10-250 m, the Bahamas. Proc 8th Int Coral Reef Symp 1: 437-442.
29. Lehnert H, Fischer H (1999) Distribution patterns of sponges and corals down to 107 m off north Jamaica. Mem Queensland Mus 44: 307-316.
30. Lesser MP, Slattery M (2011) Phase Shift to Algal Dominated Communities at Mesophotic Depths Associated With Lionfish (Pterois volitans) Invasion on a Bahamian Coral Reef. Biol Invasions 13: 1855-1868.
31. Slattery M, Lesser MP (2012) Mesophotic Coral Reefs: A Global Model of Community Structure and Function. Ecology of Mesophotic Coral reefs, Proc 12th Int Coral Reef Symp, Cairns, Australia, 9-13 July 2012, 5 pp.
32. Power ME (1992). Top-down and bottom-up forces in food webs: do plants have primacy. Ecology 73: 733-746.
33. Menge BA (1992) Community regulation: under what conditions are bottom-up factors important on rocky shores. Ecol Monogr 73: 755-765.
34. Menge BA (2000) Top-down and bottom-up community regulation in marine rocky intertidal habitats. J Exp Mar Biol Ecol 250: 257-289.
35. Coma R, Ribes M, Gili J-M, Zabala M (2000) Seasonality in coastal benthic ecosystems. Trends Ecol Evol 15: 448-453.
36. Wilkinson CR, Vacelet J (1979) Transplantation of marine sponges to different conditions of light and current. J Exp Mar Biol Ecol 37: 91-104.
37. Alcolado PM (1979) Ecological structure of the sponge fauna in a reef profile of Cuba. In: Biologie des Spongiaires. Levi C, Boury-Esnault N, editors. Colloques Internationaux du C.N.R.S., Paris, France, pp. 297-302.
38. Palumbi SR (1986) How body plan limits acclimation: Responses of a demosponge to wave force. Ecology 67: 208-214.
39. Pawlik JR, Loh T-L, McMurray SE, Finelli CM (2013) Sponge communities on coral reefs are controlled by factors that are top-down, not bottom-up. PLoS ONE 8: e62573.
40. Diamond J (1986) Overview: laboratory experiments, field experiments, and natural experiments. In: Community Ecology. Diamond J, Case TJ, editors. New York: Harper and Row, pp 3 - 22.
41. Lesser MP, Shumway SE, Cucci T, Smith J (1992) Impact of fouling organisms on mussel rope culture: Interspecific competition for food among suspension-feeding invertebrates. J Exp Mar Biol Ecol 165: 91-102. (Pubitemid 23400296)
42. Ducklow HW, Kirchman DL, Quinby HL, Carlson CA, Dam HG (1993) Stocks and dynamics of bacterioplankton carbon during the spring bloom in the eastern North Atlantic Ocean. Deep Sea Res 40: 245-263. (Pubitemid 23400248)
43. Morel A, Ahn YH, Partensky F, Vaulot D, Claustre H (1993) Prochlorococcus and Synechococcus: a comparative study of their optical properties in relation to their size and pigmentation. J Mar Res 51: 617-649. (Pubitemid 24430237)
44. Campbell L, Nolla HA, Vaulot D (1994) The importance of Prochlorococcus to community structure in the central North Pacific Ocean. Limnol Oceanogr 39: 954-960.
45. Parsons TR, Takahashi M, Hargrave B (1984) Biological Oceanographic Processes. 3rd Ed. Pergamon.
46. Hourigan TF, Stanton FG, Motta PJ, Kelley CD, Carlson B (1989) The feeding ecology of three species of Caribbean angelfishes (family Pomacanthidae). Environ Biol Fishes 24:105-116. (Pubitemid 19325767)
47. Partensky F, Hess WR, Vaulot D (1999) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63: 106-127. (Pubitemid 29116088)
48. Ting CS, Rocap G, King J, Chisolm S (2002) Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light harvesting strategies. Trends Microbiol 10: 134-142. (Pubitemid 34178326)
49. Ribes M, Coma R, Atkinson MJ, Kinzie III RA (2003) Particle removal by coral reef communities: picoplankton is a major source of nitrogen. Mar Ecol Prog Ser 257: 13-23. (Pubitemid 37053921)
50. Randall JE, Hartman WD (1968) Sponge-feeding fishes of the West Indies. Mar Biol 1: 216-225.
51. López-Legentil S, Erwin PM, Henkel TP, Loh T-L, Pawlik JR (2010) Phenotypic plasticity in the Caribbean sponge Callyspongia vaginalis (Porifera: Haplosclerida). Scientifica Marina 74: 445-453.
52. Leichter JJ, Shellenbarger G, Genovese SJ, Wing SR (1998) Breaking internal waves on a Florida (USA) coral reef: a plankton pump at work? Mar Ecol Prog Ser 166: 83-97. (Pubitemid 28286437)
53. McMurray SE, Henkel TP, Pawlik JR (2010) Demographics of increasing populations of the giant barrel sponge Xestospongia muta in the Florida Keys. Ecology 91: 560-570.
54. th ed., W.H. Freeman and Co, New York.
55. Leong W, Pawlik JR (2010) Evidence of resource trade-off between growth and chemical defenses among Caribbean coral reef sponges. Mar Ecol Prog Ser 406: 71-78.
56. Miller LP, Gaylord B (2007) Barriers to flow: the effects of experimental cage structures on water velocities in high-energy subtidal and intertidal environments. J Exp Mar Biol Ecol 344: 215-228. (Pubitemid 46453504)
57. Vogel S (1977) Current-induced flow through living sponges in nature. Proc Natl Acad Sci 74: 2069-2071.
58. Leys SP, Yahel G, Reidenbach MA, Tunnicliffe V, Shavit U, et al. (2011) The sponge pump: the role of current induced flow in the design of the sponge body plan. PLoS ONE 6: e27787.
59. Erwin PM, Thacker RW (2007) Incidence and identity of photosynthetic symbionts in Caribbean coral reef sponge assemblages. J Mar Biol Ass UK 87: 1683-1692. (Pubitemid 350211208)
60. Maldonando M, Ribes M, van Duyl FC (2012) Nutrient fluxes through sponges: biology, budgets, and ecological implications. Adv Mar Biol 62: 113-182.
61. Steele MA (1996) Effects of predators on reef fishes: separating cage artifacts from effects of predation. J Exp Mar Biol Ecol 198: 249-267.
62. Connell SD (1997) Exclusion of predatory fish on a coral reef: the anticipation, pre-emption and evaluation of some caging artifacts. J Exp Mar Biol Ecol 213: 181-198.
63. Slattery M, Starmer J, Paul V (2001) Temporal and spatial variation in defensive metabolites of the tropical Pacific soft corals Sinularia maxima and S. polydactyla. Mar Biol 138: 1183-1193. (Pubitemid 32620739)
64. Wulff JL (2005) Trade-offs in resistance to competitors and predators, and their effects on the diversity of tropical marine sponges. J Animal Ecol 74: 313-321.
65. Leichter JJ, Wing SR, Miller SL, Denny MW (1996) Pulsed delivery of subthermocline water to Conch Reef (Florida Keys) by internal tidal bores. Limnol Oceanogr 41: 1490-1501. (Pubitemid 126447244)
66. Leichter JJ, Stewart HL, Miller SJ (2003) Episodic nutrient transport to Florida coral reefs. Limnol Oceanogr 48: 1394-1407. (Pubitemid 36964760)
67. Leichter JJ, Helmuth B, Fischer AM (2006) Variation beneath the surface: quantifying complex thermal environments on coral reefs in the Caribbean, Bahamas and Florida. J Mar Sci 64: 563-588. (Pubitemid 44698215)
68. Mouillot D, Graham NAJ, Villéger S, Mason NWH, Bellwood DR (2013) A functional approach reveals community responses to disturbances. Trends Ecol Evol. 28: 167-168.
69. Cardosa SC, Soares MC, Oxenford HA, Côte IM (2009) Interspecific differences in foraging behavior and functional role of Caribbean parrotfish. Mar Biod Rec 2: e148.
70. Chanas B, Pawlik JR (1995) Defenses of Caribbean sponges against predatory reef fish. II. Spicules, tissue toughness, and nutritional quality. Mar Ecol Prog Ser 127: 195-211. (Pubitemid 26453119)
71. Duffy JE, Paul VJ (1992) Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes. Oecologia 90: 333-339.
72. Gochfeld DJ, Easson CG, Freeman CJ, Thacker RW, Olson JB (2012) Disease and nutrient enrichment as potential stressors on the Caribbean sponge Aplysina cauliformis and its bacterial symbionts. Mar Ecol Prog Ser 456: 101-111.
73. Bell JJ, Davy SK, Jones T, Taylor MW, Webster NS (2013) Could some coral reefs become sponge reefs as our climate changes. Global Change Biol doi: 10.1111/gcb.12212.
74. Colvard NB, Edmunds PJ (2011) Decadal-scale changes in abundance of non-scleractinian invertebrates on a Caribbean coral reef. J Exp Mar Biol Ecol 397: 153-160.
75. Norström AV, Nyström M, Lokrantz J, Folke C (2009) Alternative states on coral reefs: beyond coral-macroalgal phase shifts. Mar Ecol Prog Ser 376: 295-306.
76. Webster NS (2007) Sponge disease: a global threat? Environ Microbiol 9: 1363-1375.
77. Colella MA, Ruzicka RR, Kidney JA, Morrison JM, Brinkhuis VB (2012) Cold-water event of January 2010 results in catastrophic benthic mortality on patch reefs in the Florida Keys. Coral Reefs 31: 621-632.
78. Paddack MJ, Reynolds JD, Aguilar C, Appledoorn RS, Beets J, et al. (2009) Recent region-wide declines in Caribbean reef fish abundance. Current Biol 1: 590-595.
79. Hughes TP, Linares C, Dakos V, van de Leemput IA, van Nes EH (2013) Living dangerously on borrowed time during slow, unrecognized regime shifts. Trends Ecol Evol 28: 149-155.
80. Green SJ, Akins JL, Maljkovic'A, Côte IM (2012) Invasive lionfish drive Atlantic coral reef fish declines. PLoS ONE 7: e32596.
81. LaPointe BE (1997) Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and Southeast Florida. Limnol Oceanogr 42: 1119-1131.
82. Hughes T, Szmant AM, Steneck R, Carpenter R, Miller S (1999) Algal blooms on coral reefs: what are the causes? Limnol Oceanogr 44: 1583-1586.
83. Smith JE, Hunter CL, Smith CM (2010) The effects of top-down versus bottom-up control on benthic coral reef community structure. Oecologia 163: 497-507.
84. Dudgeon SR, Aronson RB, Bruno JF, Precht WF (2010) Phase shifts and stable states on coral reefs. Mar Ecol Prog Ser 413: 201-216.
85. Worm B, Lotze HK, Hillebrand H, Sommer U (2002) Consumer versus resource control of species diversity and ecosystem functioning. Nature 417: 848-851. (Pubitemid 34670330)
86. Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87: 3128-3139. (Pubitemid 44969263)
87. Bruno JF Sweatman H, Precht WF, Selig ER, Schutte VGW (2009) Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology 90: 1478-1484.