Sponge biomass and bioerosion rates increase under ocean warming and acidification

Global Change Biology

Volumn 19, Issue 12, 2013, Pages 3581-3591

  Fang, James K H ^a   Mello Athayde, Matheus A ^a   Schönberg, Christine H L ^b   Kline, David I ^a   Hoegh Guldberg, Ove ^a   Dove, Sophie ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Acidification; Bioerosion; Carbon dioxide; Climate change; Coral reefs; Sponges; Temperature

Indexed keywords

ACIDIFICATION; BIOEROSION; BIOMASS; CARBON DIOXIDE; CARBON EMISSION; CARBONATE; CLIMATE CHANGE; CORAL REEF; EROSION RATE; GLOBAL CHANGE; SPONGE;

ANTHOZOA; CLIONA ORIENTALIS; DINOPHYCEAE; SYMBIODINIUM;

CARBON DIOXIDE; SEA WATER;

ACIDIFICATION; ANIMAL; ARTICLE; BIOEROSION; BIOMASS; CHEMISTRY; CLIMATE CHANGE; CORAL REEF; DINOFLAGELLATE; PH; PHYSIOLOGY; POPULATION DYNAMICS; SEA; SPONGE (PORIFERA); SPONGES; TEMPERATURE;

ACIDIFICATION; BIOEROSION; CARBON DIOXIDE; CLIMATE CHANGE; CORAL REEFS; SPONGES; TEMPERATURE;

ANIMALS; BIOMASS; CLIMATE CHANGE; CORAL REEFS; DINOFLAGELLIDA; HYDROGEN-ION CONCENTRATION; OCEANS AND SEAS; POPULATION DYNAMICS; PORIFERA; SEAWATER;

EID: 84887442076     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/gcb.12334     Document Type: Article

References (70)

1. Acker KL, Risk MJ (1985) Substrate destruction and sediment production by the boring sponge Cliona caribbaea on Grand Cayman Island. Journal of Sedimentary Petrology, 55, 705-711.
2. Barthel D (1986) On the ecophysiology of the sponge Halichondria panicea in Kiel Bight. I. Substrate specificity, growth and reproduction. Marine Ecology Progress Series, 32, 291-298.
3. Barthel D (1988) On the ecophysiology of the sponge Halichondria panicea in Kiel Bight. II. Biomass, production, energy budget and integration in environmental processes. Marine Ecology Progress Series, 43, 87-93.
4. 2 growth from economic activity, carbon intensity, and efficiency of natural sinks. Proceedings of the National Academy of Sciences USA, 104, 18866-18870.
5. Clark KB, Jensen KR (1982) Effects of temperature on carbon fixation and carbon budget partitioning in the zooxanthellal symbiosis of Aiptasia pallida (Verrill). Journal of Experimental Marine Biology and Ecology, 64, 215-230.
6. Coles SL, Jokiel PL (1977) Effects of temperature on photosynthesis and respiration in hermatypic corals. Marine Biology, 43, 209-216.
7. Conover WJ, Iman RL (1981) Rank transformations as a bridge between parametric and nonparametric statistics. The American Statistician, 35, 124-129.
8. Cooper TF, De'ath G, Fabricius KE, Lough JM (2008) Declining coral calcification in massive Porites in two nearshore regions of the northern Great Barrier Reef. Global Change Biology, 14, 529-538.
9. Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecology Letters, 11, 1304-1315.
10. Crawley A, Kline DI, Dunn S, Anthony K, Dove S (2010) The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Global Change Biology, 16, 851-863.
11. Darling ES, Côté IM (2008) Quantifying the evidence for ecological synergies. Ecology Letters, 11, 1278-1286.
12. De'ath G, Lough JM, Fabricius KE (2009) Declining coral calcification on the Great Barrier Reef. Science, 323, 116-119.
13. Diaz-Pulido G, Anthony KRN, Kline DI, Dove S, Hoegh-Guldberg O (2012) Interactions between ocean acidification and warming on the mortality and dissolution of coralline algae. Journal of Phycology, 48, 32-39.
14. 2 analysis: a method for the certification of total alkalinity. Marine Chemistry, 80, 185-197.
15. Dove S, Ortiz JC, Enríquez S et al. (2006) Response of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short-term heat stress. Limnology and Oceanography, 51, 1149-1158.
16. Duchassaing de Fonbressin P, Michelotti G (1864) Natuurkundige Verhandelingen van de Hollandsche Maatschappij der Wetenschappen te Haarlem: Spongiaires de la Mer Caraïbe. Les Héritiers Loosjes, Haarlem.
17. Duckworth AR, Peterson BJ (2013) Effects of seawater temperature and pH on the boring rates of the sponge Cliona celata in scallop shells. Marine Biology, 160, 27-35.
18. 2 on the calcification and survival of coral recruits. Proceedings of the Royal Society B Biological Sciences, 279, 2951-2958.
19. Fang JKH, Schönberg CHL, Kline DI, Hoegh-Guldberg O, Dove S (2013) Methods to quantify components of the excavating sponge Cliona orientalis Thiele, 1900. Marine Ecology, 34, 193-206.
20. 2 world. Oceanography, 22, 36-47.
21. Fütterer DK (1974) Significance of the boring sponge Cliona for the origin of fine grained material of carbonate sediments. Journal of Sedimentary Petrology, 44, 79-84.
22. 2 and saturation state variability in a coral reef ecosystem. Global Biogeochemical Cycles, 26, GB3012.
23. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in leached corals. Nature, 440, 1186-1189.
24. Harvey BP, Gwynn-Jones D, Moore PJ (2013) Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecology and Evolution, 3, 1016-1030.
25. Hill MS (1996) Symbiotic zooxanthellae enhance boring and growth rates of the trophic sponge Anthosigmella varians forma varians. Marine Biology, 125, 649-654.
26. Hill M, Hill A (2012) The magnesium inhibition and arrested phagosome hypotheses: new perspectives on the evolution and ecology of Symbiodinium symbioses. Biological Reviews, 87, 804-821.
27. Hill M, Wilcox T (1998) Unusual mode of symbiont repopulation after bleaching in Anthosigmella varians: acquisition of different zooxanthellae strains. Symbiosis, 25, 279-289.
28. Hoegh-Guldberg O, Mumby PJ, Hooten AJ et al. (2007) Coral reefs under rapid climate change and ocean acidification. Science, 318, 1737-1742.
29. IPCC (2007) Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge.
30. 2 enrichment experiment on Heron Island (GBR). Scientific Reports, 2, e413.
31. Kohler KE, Gill SM (2006) Coral Point Count with Excel extensions (CPCe): a visual basic program for the determination of coral and substrate coverage using random point count methodology. Computer and Geosciences, 32, 1259-1269.
32. Lazar B, Loya Y (1991) Bioerosion of coral reefs - A chemical approach. Limnology and Oceanography, 36, 377-383.
33. Le Campion-Alsumard T, Golubic S, Hutchings P (1995) Microbial endoliths in skeletons of live and dead corals: Porites lobata (Moorea, French Polynesia). Marine Ecology Progress Series, 117, 149-157.
34. Lough J (2009) Temperature. In: Marine Climate Change Impacts and Adaptation Report Card for Australia 2009 (eds Poloczanska ES, Hobday AJ, Richardson AJ), Publication 05/09, ISBN 978-1-921609-03-9. pp. 1-14. NCCARF, Australia.
35. MacGeachy JK (1977) Factors controlling sponge boring in Barbados reef corals. In: Proceedings of the 3rd International Coral Reef Symposium (ed. Taylor DL), pp. 477-483. Rosenstiel School of Marine and Atmospheric Science, The University of Miami, Miami.
36. 2 world. Proceedings of the National Academy of Sciences USA, 105, 10450-10455.
37. Massaro AJ, Weisz JB, Hill MS, Webster NS (2012) Behavioral and morphological changes caused by thermal stress in the Great Barrier reef sponge Rhopaloeides odorabile. Journal of Experimental Marine Biology and Ecology, 416, 55-60.
38. Meehl GA, Stocker TF, Collins WD et al. (2007) Global climate projections. In: Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL), pp. 747-845. Cambridge University Press, Cambridge and New York.
39. Moberg F, Folke C (1999) Ecological goods and services of coral reef ecosystems. Ecological Economics, 29, 215-233.
40. Nava H, Carballo JL (2008) Chemical and mechanical bioerosion of boring sponges from Mexican Pacific coral reefs. Journal of Experimental Marine Biology and Ecology, 211, 2827-2831.
41. Parsons TR, Maita Y, Lalli CM (1984) A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, Oxford, New York, Sydney.
42. Putnam HM, Edmunds PJ (2011) The physiological responses of reef corals to diel fluctuations in seawater temperature. Journal of Experimental Marine Biology and Ecology, 396, 216-223.
43. Raven J, Caldeira K, Elderfield H et al. (2005) Ocean Acidification Due to Increasing Carbon Dioxide. Policy Document 12/05, The Royal Society, London.
44. Reyes-Nivia C, Diaz-Pulido G, Kline DI, Hoegh-Guldberg O, Dove S (2013) Ocean acidification and warming scenarios increase microbioerosion of coral skeletons. Global Change Biology, 19, 1919-1929.
45. Ridley SO, Dendy A (1886) Preliminary report on the Monaxonida collected by HMS 'Challenger'. Annals and Magazine of Natural History, 18, 325-351.
46. Riisgård 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. Marine Ecology Progress Series, 96, 177-188.
47. Robbins LL, Hansen ME, Kleypas JA, Meylan SC (2010) CO2calc-A User-friendly Seawater Carbon Calculator for Windows, Max OS X, and iOS (iPhone). US Geological Survey Open-File Report 2010-1280, pp. 17.
48. Rogelj J, Meinshausen M, Knutti R (2012) Global warming under old and new scenarios using IPCC climate sensitivity range estimates. Nature Climate Change, 2, 248-253.
49. Rosell D (1993) Effects of reproduction in Cliona viridis (Hadromerida) on zooxanthellae. Scientia Marina, 57, 405-413.
50. Rützler K (1975) The role of burrowing sponges in bioerosion. Oecologia, 19, 203-216.
51. Rützler K (2002) Impact of crustose clionid sponges on Caribbean reef corals. Acta Geologica Hispanica, 37, 61-72.
52. Sampayo EM (2007) Diversity and Ecology of Symbiodinium in Pocilloporid Corals. Unpublished PhD Thesis, The University of Queensland, Brisbane.
53. Schönberg CHL (2000) Bioeroding sponges common to the central Australian Great Barrier Reef: descriptions of three new species, two new records, and additions to two previously described species. Senckenbergiana Maritima, 30, 161-221.
54. Schönberg CHL (2002) Sponges of the 'Cliona viridis complex' - a key for species identification. In: Proceedings of the 9th International Coral Reef Symposium (eds Moosa MK, Soemodihardjo S, Soegiarto A, Romimohtarto K, Nontji A, Soekarno, Suharsono ), pp. 295-300. International Society for Reef Studies, Indonesian Ministry of Environment and Indonesian Institute of Sciences, Bali.
55. Schönberg CHL (2006) Growth and erosion of the zooxanthellate Australian bioeroding sponge Cliona orientalis are enhanced in light. In: Proceedings of 10th International Coral Reef Symposium (eds Suzuki Y, Nakamori T, Hidaka M, Kayanne H, Casareto BE, Nadaoka K, Yamano H, Tsuchiya M), pp. 168-174. Japanese Coral Reef Society and International Society for Reef Studies, Okinawa.
56. Schönberg CHL (2008) A history of sponge erosion: from past myths and hypothesis to recent approaches. In: Current Developments in Bioerosion (eds Wisshak M, Tapanila L), pp. 165-202. Springer-Verlag, Berlin Heidelberg.
57. Schönberg CHL, Ortiz J-C (2009) Is sponge bioerosion increasing?. In: Proceedings of 11th International Coral Reef Symposium (eds Riegl BM, Dodge RE), pp. 520-523. International Society for Reef Studies, Fort Lauderdale.
58. Schönberg CHL, Wilkinson CR (2001) Induced colonization of corals by a clionid bioeroding sponge. Coral Reefs, 20, 69-76.
59. Schmidt O (1862) Die Spongien des adriatischen Meeres. Wilhelm Engelmann, Leipzig.
60. Thiele J (1900) Kieselschwämme von Ternate I. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft, 25, 19-80, pls 2-3.
61. 2 on dissolution of coral carbonates by microbial euendoliths. Global Biogeochemical Cycles, 23, GB3008.
62. Tribollet A, Golubic S (2011) Reef bioerosion: agents and processes. In: Coral Reefs: An Ecosystem in Transition (eds Dubinsky Z, Stambler N), pp. 435-449. Springer, Heidelberg.
63. Van Soest RWM, Boury-Esnault N, Hooper JNA et al. (2013) World Porifera database. Available at: http://www.marinespecies.org/porifera (accessed 28 March 2013).
64. Verde EA, McCloskey LR (2001) A comparative analysis of the photobiology of zooxanthellae and zoochlorellae symbiotic with the temperate clonal anemone Anthopleura elegantissima (Brandt). Marine Biology, 138, 477-489.
65. Vicente VP (1990) Response of sponges with autotrophic endosymbionts during the coral-bleaching episode in Puerto Rico. Coral Reefs, 8, 199-202.
66. Weisz JB, Massaro AJ, Ramsby BD, Hill MS (2010) Zooxanthellar symbionts shape host sponge trophic status through translocation of carbon. The Biological Bulletin, 219, 189-197.
67. Wernberg T, Smale DA, Thomsen MS (2012) A decade of climate change experiments on marine organisms: procedures, patterns and problems. Global Change Biology, 18, 1491-1498.
68. Wisshak M, Schönberg CHL, Form A, Freiwald A (2012) Ocean acidification accelerates reef bioerosion. PLoS ONE, 7, e45124.
69. Zar JH (1999) Biostatistical Analysis, 4th edn, Prentice-Hall, Upper Saddle River.
70. Zundelevich A, Lazar B, Ilan M (2007) Chemical versus mechanical bioerosion of coral reefs by boring sponges - lessons from Pione cf. vastifica. Journal of Experimental Biology, 210, 91-96.