Abstract
Coral mechanisms of resilience and resistance to stressors such as increasing sea surface temperature and ocean acidification must first be understood in order to facilitate the survival of coral reefs as we know them. One such mechanism is production of the protective surface mucopolysaccharide layer (SML). In this study, we investigated changes in the thickness of the SML in response to increasing temperature and acidification for the three Caribbean scleractinian coral species of the genus Diploria, which have been shown to exhibit differential resilience to disease and bleaching. Among the three species, Diploria strigosa is known to have a higher susceptibility to disease, Diploria labyrinthiformis is known to bleach more quickly, and Diploria clivosa is relatively unstudied. When temperature was increased from 25 to 31 °C over a 1- or 6-week period, the overall thickness of the SML decreased from 33 to 55 % for all three species. Average SML thickness at 25 °C for all three species ranged from 106 to 156 μm, while average thickness at 31 °C ranged from 64 to 86 μm. SML thickness was significantly different among species at 25 °C, but not at 31 °C. D. labyrinthiformis demonstrated lower fragment mortality due to thermal stress when compared to the other Diploria species. Acidification from pH 8.2 to 7.7 over 5 weeks had no effect on SML thickness for any species. The observed decrease in SML thickness in response to increased temperature might be attributed to a decrease in the production of mucus or an increase in the viscosity of the SML. These findings may help to explain the increased prevalence of coral disease during the warmer months, since increased temperature compromises an important aspect of coral innate immunity, as well as differences in disease and bleaching susceptibilities between Diploria species.
References
Barshis DJ, Ladner JT, Oliver TA, Seneca FO, Traylor-Knowles N, Palumbi SR (2013) Genomic basis for coral resilience to climate change. Proc Natl Acad Sci USA 110:1387–1392
Bourne D (2005) Microbiological assessment of a disease outbreak on corals from Magnetic Island (Great Barrier Reef, Australia). Coral Reefs 24:304–312
Brown BE, Bythell JC (2005) Perspectives on mucus secretion in reef corals. Mar Ecol Prog Ser 296:291–309
Brown B, Downs C, Dunne R, Gibb S (2002) Exploring the basis of thermotolerance in the reef coral Goniastrea aspera. Mar Ecol Prog Ser 242:119–129
Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD, Sweatman H, Melendy AM (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biology 5:1220–1227
Bythell JC, Wild C (2011) Biology and ecology of coral mucus release. J Exp Mar Biol Ecol 408:88–93
Calnan JM, Smith TB, Nemeth RS, Kadison E, Blondeau J (2008) Coral disease prevalence and host susceptibility on mid-depth and deep reefs in the United States Virgin Islands. Rev Biol Trop 56:223–234
Cook CB, Logan A, Ward J, Luckhurst B, Berg CJ (1990) Elevated temperatures and bleaching on a high-latitude coral reef: The 1988 Bermuda event. Coral Reefs 9:45–49
Doney S, Fabry V, Feely R, Kleypas J (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192
Edmunds PJ (1991) Extent and effect of black band disease on a Caribbean reef. Coral Reefs 10:161–165
Fine M, Tchernov D (2007) Scleractinian coral species survive and recover from decalcification. Science 315:1811
Fournie JW, Vivian DN, Yee SH, Courtney LA, Barron MG (2012) Comparative sensitivity of six scleractinian corals to temperature and solar radiation. Dis Aquat Org 99:85–93
Goulet T, Coffroth M (2004) The genetic identity of dinoflagellate symbionts in Caribbean octocorals. Coral Reefs 23:465–472
Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189
Guppy R, Bythell JC (2006) Environmental effects on bacterial diversity in the surface mucus layer of the reef coral Montastraea faveolata. Mar Ecol Prog Ser 328:133–142
Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742
Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642
Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933
Jatkar A, Brown B, Bythell J, Guppy R, Morris N, Pearson J (2010a) Measuring mucus thickness in reef corals using a technique devised for vertebrate applications. Mar Biol 157:261–267
Jatkar AA, Brown BE, Bythell JC, Guppy R, Morris NJ, Pearson JP (2010b) Coral mucus: the properties of its constituent mucins. Biomacromolecules 11:883–888
Jones R, Johnson R, Noyes T, Parsons R (2012) Spatial and temporal patterns of coral black band disease in relation to a major sewage outfall. Mar Ecol Prog Ser 462:79
Jordan N, Newton J, Pearson J, Allen A (1998) A novel method for the visualization of the in situ mucus layer in rat and man. Clin Sci 95:97–106
Kaczmarsky LT, Draud M, Williams EH (2005) Is there a relationship between proximity to sewage effluent and the prevalence of coral disease? Caribb J Sci 41:124–137
Kellogg C (2004) Tropical Archaea: diversity associated with the surface microlayer of corals. Mar Ecol Prog Ser 273:81–88
Kvennefors ECE, Sampayo E, Kerr C, Vieira G, Roff G, Barnes AC (2012) Regulation of bacterial communities through antimicrobial activity by the coral holobiont. Microb Ecol 63:605–618
Leclercq N, Gattuso J, Jaubert J (2000) CO2 partial pressure controls the calcification rate of a coral community. Global Change Biol 6:329–334
Lieleg O, Ribbeck K (2011) Biological hydrogels as selective diffusion barriers. Trends Cell Biol 21:543–551
Littman RA, Willis BL, Pfeffer C, Bourne DG (2009) Diversities of coral-associated bacteria differ with location, but not species, for three Acroporid corals on the Great Barrier Reef. FEMS Microbiol Ecol 68:152–163
McCormick D, Horton L, Mee A (1990) Mucin depletion in inflammatory bowel-disease. J Clin Pathol 43:143–146
Meikle P, Richards G, Yellowlees D (1988) Structural investigations on the mucus from 6 species of coral. Mar Biol 99:187–193
Meron D, Atias E, Kruh LI, Elifantz H, Minz D, Fine M, Banin E (2011) The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J 5:51–60
Miller J, Waara R, Muller E, Rogers C (2006) Coral bleaching and disease combine to cause extensive mortality on reefs in US Virgin Islands. Coral Reefs 25:418-418
Muller EM, Rogers CS, Spitzack AS, van Woesik R (2008) Bleaching increases likelihood of disease on Acropora palmata (Lamarck) in Hawksnest Bay, St John, US Virgin Islands. Coral Reefs 27:191–195
Mydlarz LD, Couch CS, Weil E, Smith G, Harvell CD (2009) Immune defenses of healthy, bleached and diseased Montastraea faveolata during a natural bleaching event. Dis Aquat Org 87:67–78
Nakajima R, Yoshida T, Azman B, Zaleha K, Othman B, Toda T (2009) In situ release of coral mucus by Acropora and its influence on the heterotrophic bacteria. Aquat Ecol 43:815–823
Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422
Petersson J, Schreiber O, Hansson GC, Gendler SJ, Velcich A, Lundberg JO, Roos S, Holm L, Phillipson M (2011) Importance and regulation of the colonic mucus barrier in a mouse model of colitis. Am J Physiol Gastroin Liver Physiol 300:G327–G333
Piggot AM, Fouke BW, Sivaguru M, Sanford RA, Gaskins HR (2009) Change in zooxanthellae and mucocyte tissue density as an adaptive response to environmental stress by the coral, Montastraea annularis. Mar Biol 156:2379–2389
Pullan R, Thomas G, Rhodes M, Newcombe R, Williams G, Allen A, Rhodes J (1994) Thickness of adherent mucus gel on colonic mucosa in humans and its relevance to colitis. Gut 35:353–359
Renegar DA, Riegl BM (2005) Effect of nutrient enrichment and elevated CO2 partial pressure on growth rate of Atlantic scleractinian coral Acropora cervicornis. Mar Ecol Prog Ser 293:69–76
Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E (2006) The coral probiotic hypothesis. Environ Microbiol 8:2068–2073
Ritchie K (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14
Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10
Rosenberg E, Ben-Haim Y (2002) Microbial diseases of corals and global warming. Environ Microbiol 4:318–326
Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362
Rosenberg E, Loya Y (eds) (2004) Coral health and disease. Springer
Rützler K, Santavy DL (1983) The black band disease of Atlantic reef corals. Mar Ecol 4:301–319
Schade C, Flemstrong G, Holm L (1994) Hydrogen-ion concentration in the mucus layer on top of acid-stimulated and acid-inhibited rat gastric-mucosa. Gastroenterology 107:180–188
Sekar R, Kaczmarsky LT, Richardson LL (2008) Microbial community composition of black band disease on the coral host Siderastrea siderea from three regions of the wider Caribbean. Mar Ecol Prog Ser 362:85–98
Sharp KH, Ritchie KB (2012) Multi-partner interactions in corals in the face of climate change. Biol Bull 223:66–77
Shnit-Orland M, Kushmaro A (2009) Coral mucus-associated bacteria: a possible first line of defense coral mucus-associated bacteria. FEMS Microbiol Ecol 67:371–380
Sutherland KP, Porter JW, Torres C (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Mar Ecol Prog Ser 266:273–302
Sweet MJ, Croquer A, Bythell JC (2011) Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30:39–52
Tremblay P, Weinbauer MG, Rottier C, Guerardel Y, Nozais C, Ferrier-Pages C (2011) Mucus composition and bacterial communities associated with the tissue and skeleton of three scleractinian corals maintained under culture conditions. J Mar Biol Assoc U K 91:649–657
Vega Thurber RV, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F, Dinsdale E, Kelly L, Rohwer F (2009) Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11:2148–2163
Villamizar E, Camisotti H, Rodriguez B, Perez J, Romero M (2008) Impacts of the 2005 Caribbean bleaching event at Archipielago de Los Roques National Park. Venezuela. Rev Biol Trop Suppl 1:255–270
Wild C, Woyt H, Huettel M (2005) Influence of coral mucus on nutrient fluxes in carbonate sands. Mar Ecol Prog Ser 287:87–98
Wild C, Huettel M, Klueter A, Kremb S, Rasheed M, Jorgensen B (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70
Wooldridge SA (2009) A new conceptual model for the enhanced release of mucus in symbiotic reef corals during ‘bleaching’ conditions. Mar Ecol Prog Ser 396:145–152
Acknowledgments
We thank Lauri MacLaughlin for assistance with coral collections. Coral were collected under permit # FKNMS-2009-045-A3. This work was supported by the College of Arts and Sciences, Florida International University. Z.P. was supported by the MBRS-RISE Program, Florida International University. This is contribution #269 from the Tropical Biology Program of Florida International University.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Biology Editor Dr. Anastazia Banaszak
Rights and permissions
About this article
Cite this article
Pratte, Z.A., Richardson, L.L. Impacts of temperature increase and acidification on thickness of the surface mucopolysaccharide layer of the Caribbean coral Diploria spp.. Coral Reefs 33, 487–496 (2014). https://doi.org/10.1007/s00338-013-1115-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-013-1115-0