Coral Reefs

, Volume 36, Issue 3, pp 749–761 | Cite as

Dissepiments, density bands and signatures of thermal stress in Porites skeletons

  • Thomas M. DeCarloEmail author
  • Anne L. Cohen


The skeletons of many reef-building corals are accreted with rhythmic structural patterns that serve as valuable sclerochronometers. Annual high- and low-density band couplets, visible in X-radiographs or computed tomography scans, are used to construct age models for paleoclimate reconstructions and to track variability in coral growth over time. In some corals, discrete, anomalously high-density bands, called “stress bands,” preserve information about coral bleaching. However, the mechanisms underlying the formation of coral skeletal density banding remain unclear. Dissepiments—thin, horizontal sheets of calcium carbonate accreted by the coral to support the living polyp—play a key role in the upward growth of the colony. Here, we first conducted a vital staining experiment to test whether dissepiments were accreted with lunar periodicity in Porites coral skeleton, as previously hypothesized. Over 6, 15, and 21 months, dissepiments consistently formed in a 1:1 ratio to the number of full moons elapsed over each study period. We measured dissepiment spacing to reconstruct multiple years of monthly skeletal extension rates in two Porites colonies from Palmyra Atoll and in another from Palau that bleached in 1998 under anomalously high sea temperatures. Spacing between successive dissepiments exhibited strong seasonality in corals containing annual density bands, with narrow (wide) spacing associated with high (low) density, respectively. A high-density “stress band” accreted during the 1998 bleaching event was associated with anomalously low dissepiment spacing and missed dissepiments, implying that thermal stress disrupts skeletal extension. Further, uranium/calcium ratios increased within stress bands, indicating a reduction in the carbonate ion concentration of the coral’s calcifying fluid under stress. Our study verifies the lunar periodicity of dissepiments, provides a mechanistic basis for the formation of annual density bands in Porites, and reveals the underlying cause of high-density stress bands.


Coral Calcification Density banding Sclerochronology Stress bands Bleaching 



We thank Yimnang Golbuu (Palau International Coral Reef Center) for assistance with permits and hosting us at PICRC, Hannah Barkley, G.P. Lohmann, Chip Young, and Kathryn Pietro for help with fieldwork, Burnham Petrographics for mounting and polishing sections, and Horst Marschall for assistance with microscope analyses. We thank two anonymous reviewers for their helpful comments. This work was supported by NSF Grants OCE 1220529 and OCE 1605365 awarded to A.L. Cohen, a WHOI Ocean Ventures Fund award to T.M. DeCarlo, a WHOI Coastal Ocean Institute award to T.M. DeCarlo, and an NSF Graduate Research Fellowship to T.M. DeCarlo.

Supplementary material

338_2017_1566_MOESM1_ESM.pdf (19.1 mb)
Supplementary material 1 (PDF 19545 kb)


  1. Abe N (1937) Postlarval development of the coral Fungia actiniformis var. palawensis Doderlein. Palao Tropical Biological Station Studies 1:73–93Google Scholar
  2. Barkley HC, Cohen AL (2016) Skeletal records of community-level bleaching in Porites corals from Palau. Coral Reefs 35:1407–1417CrossRefGoogle Scholar
  3. Barkley HC, Cohen AL, Golbuu Y, Starczak VR, DeCarlo TM, Shamberger KE (2015) Changes in coral reef communities across a natural gradient in seawater pH. Sci Adv 1:e1500328CrossRefPubMedPubMedCentralGoogle Scholar
  4. Barnes DJ (1970) Coral skeletons: an explanation of their growth and structure. Science 170:1305–1308CrossRefPubMedGoogle Scholar
  5. Barnes DJ, Lough JM (1989) The nature of skeletal density banding in scleractinian corals: fine banding and seasonal patterns. J Exp Mar Bio Ecol 126:119–134CrossRefGoogle Scholar
  6. Barnes DJ, Lough JM (1992) Systematic variations in the depth of skeleton occupied by coral tissue in massive colonies of Porites from the Great Barrier Reef. J Exp Mar Bio Ecol 159:113–128CrossRefGoogle Scholar
  7. Barnes DJ, Lough JM (1993) On the nature and causes of density banding in massive coral skeletons. J Exp Mar Bio Ecol 167:91–108CrossRefGoogle Scholar
  8. Bruno J, Siddon C, Witman J, Colin P, Toscano M (2001) El Niño-related coral bleaching in Palau, western Caroline Islands. Coral Reefs 20:127–136CrossRefGoogle Scholar
  9. Buddemeier RW (1974) Environmental controls over annual and lunar monthly cycles in hermatypic coral calcification. Proc 2nd Int Coral Reef Symp 2:259–267Google Scholar
  10. Buddemeier RW, Kinzie RA (1975) The chronometric reliability of contemporary corals. In: Rosenberg G, Runcorn S (eds) Growth rhythms and the history of the earth’s rotation. Wiley, London, pp 135–147Google Scholar
  11. Buddemeier RW, Maragos JE, Knutson DW (1974) Radiographic studies of reef coral exoskeletons: rates and patterns of coral growth. J Exp Mar Bio Ecol 14:179–199CrossRefGoogle Scholar
  12. Cai W-J, Ma Y, Hopkinson BM, Grottoli AG, Warner ME, Ding Q, Hu X, Yuan X, Schoepf V, Xu H, Han C, Melman T, Hoadley KD, Pettay DT, Matsui Y, Baumann JH, Levas S, Ying Y, Wang Y (2016) Microelectrode characterization of coral daytime interior pH and carbonate chemistry. Nat Commun 7:11144CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cantin NE, Lough JM (2014) Surviving coral bleaching events: Porites growth anomalies on the Great Barrier Reef. PLoS One 9:e88720CrossRefPubMedPubMedCentralGoogle Scholar
  14. Cantin NE, Cohen AL, Karnauskas KB, Tarrant AM, McCorkle DC (2010) Ocean warming slows coral growth in the central Red Sea. Science 329:322–325CrossRefPubMedGoogle Scholar
  15. Carilli JE, Norris RD, Black B, Walsh SM, McField M (2009a) Century-scale records of coral growth rates indicate that local stressors reduce coral thermal tolerance threshold. Glob Chang Biol 16:1247–1257CrossRefGoogle Scholar
  16. Carilli JE, Norris RD, Black BA, Walsh SM, McField M (2009b) Local stressors reduce coral resilience to bleaching. PLoS One 4:e6324CrossRefPubMedPubMedCentralGoogle Scholar
  17. Castillo KD, Ries JB, Weiss JM, Lima FP (2012) Decline of forereef corals in response to recent warming linked to history of thermal exposure. Nat Clim Chang 2:756–760CrossRefGoogle Scholar
  18. Cobb KM, Charles CD, Cheng H, Edwards RL (2003) El Niño/Southern oscillation and tropical Pacific climate during the last millennium. Nature 424:271–276CrossRefPubMedGoogle Scholar
  19. Cohen AL, McConnaughey TA (2003) Geochemical perspectives on coral mineralization. Reviews in Mineralogy and Geochemistry 54:151–187CrossRefGoogle Scholar
  20. Cohen AL, Holcomb M (2009) Why corals care about ocean acidification: uncovering the mechanism. Oceanography 22:118–127CrossRefGoogle Scholar
  21. Cohen AL, Layne GD, Hart SR, Lobel PS (2001) Kinetic control of skeletal Sr/Ca in a symbiotic coral: implications for the paleotemperature proxy. Paleoceanography 16:20–26CrossRefGoogle Scholar
  22. Cohen AL, Owens KE, Layne GD, Shimizu N (2002) The effect of algal symbionts on the accuracy of Sr/Ca paleotemperatures from coral. Science 296:331–333CrossRefPubMedGoogle Scholar
  23. DeCarlo TM, Cohen AL (2016) coralCT: software tool to analyze computed tomography (CT) scans of coral skeletal cores for calcification and bioerosion rates. Zenodo. doi: 10.5281/zenodo.57855 Google Scholar
  24. DeCarlo TM, Gaetani GA, Holcomb M, Cohen AL (2015a) Experimental determination of factors controlling U/Ca of aragonite precipitated from seawater: implications for interpreting coral skeleton. Geochim Cosmochim Acta 162:151–165CrossRefGoogle Scholar
  25. DeCarlo TM, Gaetani GA, Cohen AL, Foster GL, Alpert AE, Stewert J (2016) Coral Sr–U thermometry. Paleoceanography 31:626–638CrossRefGoogle Scholar
  26. DeCarlo TM, Cohen AL, Barkley HC, Cobban Q, Young C, Shamberger KE, Brainard RE, Golbuu Y (2015b) Coral macrobioerosion is accelerated by ocean acidification and nutrients. Geology 43:7–10CrossRefGoogle Scholar
  27. Dodge RE, Vaisnys JR (1975) Hermatypic coral growth banding as environmental recorder. Nature 258:706–708CrossRefGoogle Scholar
  28. Dodge RE, Szmant AM, Garcia R, Swart PK, Forester A, Leder JJ (1993) Skeletal structural basis of density banding in the reef coral Montastrea annularis. In: Proc 7th Int Coral Reef Symp 1: 186–195Google Scholar
  29. Gladfelter EG (1983) Skeletal development in Acropora cervicornis: II. Diel patterns of calcium carbonate accretion. Coral Reefs 2:91–100CrossRefGoogle Scholar
  30. Gorbunov MY, Falkowski PG (2002) Photoreceptors in the cnidarian hosts allow symbiotic corals to sense blue moonlight. Limnol Oceanogr 47:309–315CrossRefGoogle Scholar
  31. Goreau TF, Goreau NI (1959) The physiology of skeleton formation in corals. II. Calcium deposition by hermatypic corals under various conditions in the reef. Biol Bull 117:239–250CrossRefGoogle Scholar
  32. Harrison PL, Babcock RC, Bull GD, Oliver JK, Wallace CC, Willis BL (1984) Mass spawning in tropical reef corals. Science 223:1186–1189CrossRefPubMedGoogle Scholar
  33. Helmle K, Dodge R (2011) Sclerochronology. In: Hopley D (ed) Encyclopedia of modern coral reefs. Springer, Netherlands, pp 958–966CrossRefGoogle Scholar
  34. Highsmith RC (1979) Coral growth rates and environmental control of density banding. J Exp Mar Bio Ecol 37:105–125CrossRefGoogle Scholar
  35. 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 318:1737–1742CrossRefPubMedGoogle Scholar
  36. Holcomb M, Cohen AL, McCorkle DC (2013) An evaluation of staining techniques for marking daily growth in scleractinian corals. J Exp Mar Bio Ecol 440:126–131CrossRefGoogle Scholar
  37. Hudson JH (1981a) Response of Montastrea annularis to environmental change in the Florida Keys. Proc 4th Int Coral Reef Symp 2: 233–240Google Scholar
  38. Hudson JH (1981b) Growth rates in Montastrea annularis: a record of environmental change in Key Largo Coral Reef Marine Sanctuary, Florida. Bull Mar Sci 31:444–459Google Scholar
  39. Hudson JH, Shinn EA, Halley RB, Lidz B (1976) Sclerochronology: a tool for interpreting past environments. Geology 4:361–364CrossRefGoogle Scholar
  40. Jokiel PL, Ito RY, Liu PM (1985) Night irradiance and synchronization of lunar release of planula larvae in the reef coral Pocillopora damicornis. Mar Biol 88:167–174CrossRefGoogle Scholar
  41. Kaniewska P, Alon S, Karako-Lampert S, Hoegh-Guldberg O, Levy O (2015) Signaling cascades and the importance of moonlight in coral broadcast mass spawning. eLife 4:e09991CrossRefPubMedPubMedCentralGoogle Scholar
  42. Knutson DW, Buddemeier RW, Smith SV (1972) Coral chronometers: seasonal growth bands in reef corals. Science 177:270–272CrossRefPubMedGoogle Scholar
  43. Lough JM, Barnes DJ (1990) Intra-annual timing of density band formation of Porites coral from the central Great Barrier Reef. J Exp Mar Bio Ecol 135:35–57CrossRefGoogle Scholar
  44. Lough JM, Barnes DJ (1992) Comparisons of skeletal density variations in Porites from the central Great Barrier Reef. J Exp Mar Bio Ecol 155:1–25CrossRefGoogle Scholar
  45. Mallela J, Hetzinger S, Halfar J (2015) Thermal stress markers in Colpophyllia natans provide an archive of site-specific bleaching events. Coral Reefs 35:181–186CrossRefGoogle Scholar
  46. Mendes JM, Woodley JD (2002) Effect of the 1995–1996 bleaching event on polyp tissue depth, growth, reproduction and skeletal band formation in Montastraea annularis. Mar Ecol Prog Ser 235:93–102CrossRefGoogle Scholar
  47. Reynolds RW, Rayner NA, Smith TM, Stokes DC, Wang W (2002) An improved in situ and satellite SST analysis for climate. J Clim 15:1609–1625CrossRefGoogle Scholar
  48. Rotmann S, Thomas S (2012) Coral tissue thickness as a bio-indicator of mine-related turbidity stress on coral reefs at Lihir Island, Papua New Guinea. Oceanography 25:52–63CrossRefGoogle Scholar
  49. Saenger C, Cohen AL, Oppo DW, Halley RB, Carilli JE (2009) Surface-temperature trends and variability in the low-latitude North Atlantic since 1552. Nat Geosci 2:492–495CrossRefGoogle Scholar
  50. Schoepf V, McCulloch MT, Warner ME, Levas SJ, Matsui Y, Aschaffenburg MD, Grottoli AG (2014) Short-term coral bleaching is not recorded by skeletal boron isotopes. PLoS One 9:e112011CrossRefPubMedPubMedCentralGoogle Scholar
  51. Shamberger KE, Cohen AL, Golbuu Y, McCorkle DC, Lentz SJ, Barkley HC (2014) Diverse coral communities in naturally acidified waters of a Western Pacific reef. Geophys Res Lett 41:499–504CrossRefGoogle Scholar
  52. Shirai K, Sowa K, Watanabe T, Sano Y, Nakamura T, Clode P (2012) Visualization of sub-daily skeletal growth patterns in massive Porites corals grown in Sr-enriched seawater. J Struct Biol 180:47–56CrossRefPubMedGoogle Scholar
  53. Smith SV, Buddemeier RW, Redalje RC, Houck JE (1979) Strontium-calcium thermometry in coral skeletons. Science 204:404–407CrossRefPubMedGoogle Scholar
  54. Smithers SG, Woodroffe CD (2001) Coral microatolls and 20th century sea level in the eastern Indian Ocean. Earth Planet Sci Lett 191:173–184CrossRefGoogle Scholar
  55. Soong K, Chen C, Chang J-C (1999) A very large poritid colony at Green Island, Taiwan. Coral Reefs 18:42CrossRefGoogle Scholar
  56. Sorauf J (1970) Microstructure and formation of dissepiments in the skeleton of the recent Scleractinia (hexacorals). Biomineralization 2:1–22Google Scholar
  57. Suzuki A, Gagnon MK, Fabricius K, Isdale PJ, Yukino I, Kawahata H (2003) Skeletal isotope microprofiles of growth perturbations in Porites corals during the 1997–1998 mass bleaching event. Coral Reefs 22:357–369CrossRefGoogle Scholar
  58. Swart PK, Hubbard JAEB (1982) Uranium in scleractinian coral skeletons. Coral Reefs 1:13–19CrossRefGoogle Scholar
  59. Sweeney AM, Boch CA, Johnsen S, Morse DE (2011) Twilight spectral dynamics and the coral reef invertebrate spawning response. J Exp Biol 214:770–777CrossRefPubMedGoogle Scholar
  60. Taylor RB, Barnes DJ, Lough JM (1993) Simple models of density band formation in massive corals. J Exp Mar Bio Ecol 167:109–125CrossRefGoogle Scholar
  61. Thompson WG, Spiegelman MW, Goldstein SL, Speed RC (2003) An open-system model for U-series age determinations of fossil corals. Earth Planet Sci Lett 210:365–381CrossRefGoogle Scholar
  62. van Woesik R, van Woesik K, van Woesik L, van Woesik S (2013) Effects of ocean acidification on the dissolution rates of reef-coral skeletons. PeerJ 1:e208CrossRefPubMedPubMedCentralGoogle Scholar
  63. Venn A, Tambutté E, Holcomb M, Allemand D, Tambutté S (2011) Live tissue imaging shows reef corals elevate pH under their calcifying tissue relative to seawater. PLoS One 6:e20013CrossRefPubMedPubMedCentralGoogle Scholar
  64. Veron JEN (1986) Corals of Australia and the Indo-Pacific. Angus & Robertson, Sydney, AustraliaGoogle Scholar
  65. Weber JN, Woodhead PMJ (1972) Temperature dependence of oxygen-18 concentration in reef coral carbonates. J Geophys Res 77:463–473CrossRefGoogle Scholar
  66. Wells JW (1963) Coral growth and geochronometry. Nature 197:948–950CrossRefGoogle Scholar
  67. Winter A, Sammarco PW (2010) Lunar banding in the scleractinian coral Montastraea faveolata: fine-scale structure and influence of temperature. J Geophys Res 115:G04007Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Massachusetts Institute of Technology/Woods Hole Oceanographic Institution Joint Program in Oceanography and Applied Ocean Science and EngineeringWoods HoleUSA
  2. 2.Woods Hole Oceanographic InstitutionWoods HoleUSA
  3. 3.School of Earth and EnvironmentThe University of Western AustraliaCrawleyAustralia

Personalised recommendations