Application of the coral health chart to determine bleaching status of Acropora downingi in a subtropical coral reef

Abstract

The ‘Coral Health Chart’ has become a popular tool for monitoring coral bleaching worldwide. The scleractinian coral Acropora downingi (Wallace 1999) is highly vulnerable to temperature anomalies in the Persian Gulf. Our study tested the reliability of Coral Health Chart scores for the assessment of bleaching-related changes in the mitotic index (MI) and density of zooxanthellae cells in A. downingi in Qeshm Island, the Persian Gulf. The results revealed that, at least under severe conditions, it can be used as an effective proxy for detecting changes in the density of normal, transparent, or degraded zooxanthellae and MI. However, its ability to discern changes in pigment concentration and total zooxanthellae density should be viewed with some caution in the Gulf region, probably because the high levels of environmental variability in this region result in inherent variations in the characteristics of zooxanthellae among “healthy” looking corals.

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References

  1. Arar EJ (1997) In vitro determination of chlorophylls a, b, c1, +c2 and pheopigments in marine and freshwater algae by visible spectrophotometry. US Environmental Protection Agency, Washington DC

    Google Scholar 

  2. Baker AC (1999) Symbiosis ecology of reef-building corals. Ph.D. Thesis, University of Miami, 122 p

    Google Scholar 

  3. Bhagooli R, Hidaka M (2004) Release of zooxanthellae with intact photosynthetic activity by the coral Galaxea fascicularis in response to high temperature stress. Mar Biol 145:329–337

    Article  Google Scholar 

  4. Bolouki M, Savari A, Nabavi MB, Rounagh MT, Daneshmand A (2013) Comparison of symbiotic algae densities in coral comparison of symbiotic algae densities in coral. J Oceanogr 4:45–51

    Google Scholar 

  5. Brown BE (1992) Comparative measurements of mitotic index in zooxanthellae from a symbiotic cnidarian subject to temperature increase. J Exp Mar Biol Ecol 158(2): 179–188

    Article  Google Scholar 

  6. Brown BE, Dunne RP, Goodson MS, Douglas AE (2000) Marine ecology: bleaching patterns in reef corals. Nature 404:142–143

    Article  Google Scholar 

  7. Chow MH, Tsang RHL, Lam EKY, Ang P (2016) Quantifying the degree of coral bleaching using digital photographic technique. J Exp Mar Biol Ecol 479:60–68

    Article  Google Scholar 

  8. Cohen J (1988) Statistical power analysis for the behavioral sciences (2nd ed). Routledge, New York, 400 p

    Google Scholar 

  9. Cruz ICS, Leal MC, Mendes CR, Kikuchi RKP, Rosa R, Soares AMVM, Serôdio J, Calado R, Rocha RJM (2015) White but not bleached: photophysiological evidence from white Montastraea cavernosa reveals potential overestimation of coral bleaching. Mar Biol 162:889–899

    Article  Google Scholar 

  10. De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27–year decline of coral cover on the Great Barrier Reef and its causes. P Natl Acad Sci USA 109:17995–17999

    Article  Google Scholar 

  11. Dimond J, Carrington E (2008) Symbiosis regulation in a facultatively symbiotic temperate coral: zooxanthellae division and expulsion. Coral Reefs 27:601–604

    Article  Google Scholar 

  12. Dunn SR, Bythell JC, Le Tissier MDA, Burnett WJ, Thomason JC (2002) Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the symbiotic sea anemone Aiptasia sp. J Exp Mar Biol Ecol 272:29–53

    Article  Google Scholar 

  13. Fadlallah YH, Allen KW, Estudillo RA (1995) Mortality of shallow reef corals in the western Arabian Gulf following aerial exposure in winter. Coral Reefs 14(2): 99–107

    Article  Google Scholar 

  14. Fagoonee I, Wilson HB, Hassell MP, Turner JR (1999) The dynamics of zooxanthellae populations: a long-term study in the field. Science 283:843–845

    Article  Google Scholar 

  15. Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L (1993) Population control in symbiotic corals. Bioscience 43:606–611

    Article  Google Scholar 

  16. Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685

    Article  Google Scholar 

  17. Fujise L, Yamashita H, Suzuki G, Koike K (2013) Expulsion of zooxanthellae (Symbiodinium) from several species of scleractinian corals: comparison under non-stress conditions and thermal stress conditions. Galaxea JCRS 15:29–36

    Article  Google Scholar 

  18. Fujise L, Yamashita H, Suzuki G, Sasaki K, Liao LM, Koike K (2014) Moderate thermal stress causes active and immediate expulsion of photosynthetically damaged zooxanthellae (Symbiodinium) from Corals. PLoS One 9:e114321. doi:10.1371/journal.pone.0114321

    Article  Google Scholar 

  19. Glynn PW (1990) Coral mortality and disturbances to coral reefs in the tropical eastern Pacific. In: Glynn PW (ed) Global ecological consequences of the 1982–83 El Niño-Southern Oscillation. Elsevier, Amsterdam, pp 55–126

    Google Scholar 

  20. Goreau TJ, Hayes RL (1994) Coral bleaching and ocean hot spots. Ambio 23:176–180

    Google Scholar 

  21. Hill J, Wilkinson C (2004) Methods for ecological monitoring of coral reefs: a resource for managers. Australian Institute of Marine Science (AIMS), Townsville, 117 p

    Google Scholar 

  22. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshwater Res 50:839–866

    Article  Google Scholar 

  23. 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

    Article  Google Scholar 

  24. Jeong HJ, Lee SY, Kang NS, Yoo YD, Lim AS, Lee MJ, LaJeunesse TC (2014) Genetics and morphology characterize the dinoflagellate Symbiodinium voratum, (Dinophyceae) as the sole representative of Symbiodinium clade E. J Eukaryot Microbiol 61(1): 75–94

    Article  Google Scholar 

  25. Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:1219–1230

    Article  Google Scholar 

  26. Kavousi J, Tavakoli-Kolour P, Mohammadizadeh M, Bahrami A, Barkhordari A (2014) Mass coral bleaching in the northern Persian Gulf, 2012. Sci Mar 78(3): 397–404

    Article  Google Scholar 

  27. Kuroki T, van Woesik RV (1999) Changes in zooxanthellae characteristics in the coral Stylophora pistillata during the 1998 bleaching event. Galaxea JCRS 1999:97–101

    Article  Google Scholar 

  28. Ladrière O, Penin L, Van Lierde E, Vidal-Dupiol J, Kayal M, Roberty S, Poulicek M, Adjeroud M (2014) Natural spatial variability of algal endosymbiont density in the coral Acropora globiceps: a small-scale approach along environmental gradients around Moorea (French Polynesia). Mar Biol Assoc UK 94:65–74

    Article  Google Scholar 

  29. LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura, DO, Hoegh-Guldberg O, Fitt WK (2010) Longstanding environmental conditions, geographic isolation and host–symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeogr 37(5): 785–800

    Article  Google Scholar 

  30. Lesser MP, Farrell JH (2004) Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23:367–377

    Article  Google Scholar 

  31. Marsh JA (1970) Primary productivity of reef-building calcareous red algae. Ecology 51:255–263

    Article  Google Scholar 

  32. Marshall NJ, Kleine DA, Dean AJ (2012) CoralWatch: education, monitoring, and sustainability through citizen science. Front Ecol Environ 10:332–334

    Article  Google Scholar 

  33. Mise T, Hidaka M (2003) Degradation of zooxanthellae in the coral Acropora nasuta during bleaching. Galaxea JCRS 5:33–39

    Article  Google Scholar 

  34. Montano S, Seveso D, Galli P, Obura DO (2010) Assessing coral bleaching and recovery with a color reference card in Watamu Marine Park, Kenya. Hydrobiologia 655:99–108

    Article  Google Scholar 

  35. Muller-Parker G (1987) Seasonal variation in light-shade adaptation of natural populations of the symbiotic sea anemone Aiptasia pulchella (Carlgren, 1943) in Hawaii. J Exp Mar Biol Ecol 112:165–183

    Article  Google Scholar 

  36. Mumby PJ, Skirving W, Strongb AE, Hardyc JT, LeDrewd EF, Hochberge EJ, Stumpff RP, David LT (2004) Remote sensing of coral reefs and their physical environment. Mar Pollut Bull 48:219–228

    Article  Google Scholar 

  37. Muscatine L, Falkowski PG, Dubinsky Z, Cook PA, McCloskey LR (1989) The effect of external nutrient resources on the population dynamics of zooxanthellae in a reef coral. P Roy Soc Lond B Bio 236:311–324

    Article  Google Scholar 

  38. Parkinson JE, Yang S, Kawamura I, Byron G, Todd PA, Reimer JD (2016) A citizen science approach to monitoring bleaching in the zoantharian Palythoa tuberculosa. PeerJ 4:e1815. doi:10.7717/peerj.1815

    Article  Google Scholar 

  39. Pochon X, Montoya-Burgos JI, Stadelmann B, Pawlowski J (2006) Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol Phylogenet Evol 38:20–30

    Article  Google Scholar 

  40. Putnam HM, Edmunds PJ (2011) The physiological response of reef corals to diel fluctuations in seawater temperature. J Exp Mar Biol Ecol 396:216–223

    Article  Google Scholar 

  41. Reimer AA (1971) Observations on the relationships between several species of tropical zoanthids (Zoanthidea, coelenterata) and their Zooxanthellae. J Exp Mar Biol Ecol 7:207–214

    Article  Google Scholar 

  42. Riegl BM, Purkis SJ (2012) Coral reefs of the gulf: adaptation to climatic extremes in the world’s hottest sea. Springer, New York, 379 p

    Google Scholar 

  43. Rudolph P, Peters J, Lorenz D, Schmidt D, Parwaresch R (1998) Correlation between mitotic and Ki-67 labeling indices in paraffin-embedded carcinoma specimens. Hum Pathol 29(11): 1216–1222

    Article  Google Scholar 

  44. Shenkar N, Fine M, Kramarsky-Winter E, Loya Y (2006) Population dynamics of zooxanthellae during a bacterial bleaching event. Coral Reefs 25:223–227

    Article  Google Scholar 

  45. Sheppard C, Price A, Roberts C (1992) Marine ecology of the Arabian region: patterns and processes in extreme tropical environments. Academic Press, London, 359 p

    Google Scholar 

  46. Siebeck UE, Marshall NJ, Klüter A, Hoegh-Guldberg O (2006) Monitoring coral bleaching using a color reference card. Coral Reefs 25:453–460

    Article  Google Scholar 

  47. Stimson J, Kinzie RA (1991) The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen-enrichment and control conditions. J Exp Mar Biol Ecol 153(1): 63–74

    Article  Google Scholar 

  48. Strychar KB, Coates M, Sammarco PW, Piva TJ (2004) Bleaching as a pathogenic response in scleractinian corals, evidenced by high concentrations of apoptotic and necrotic zooxanthellae J Exp Mar Biol Ecol 304:99–121

  49. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  Google Scholar 

  50. Titlyanov EA, Titlyanova TV, Leletkin VA, Tsukahara J, van Woesik R, Yamazato K (1996) Degradation of zooxanthellae and regulation of their density in hermatypic corals. Mar Ecol-Prog Ser 139:167–178

    Article  Google Scholar 

  51. Wake B (2016) Snapshot: snow white coral. Nat Clim Chang 6:439–439

    Article  Google Scholar 

  52. Wilkerson FP, Muller G, Muscatine PL (1983) Temporal patterns of cell division in natural populations of endosymbiotic algae. Limnol Oceanogr 28:1009–1014

    Article  Google Scholar 

  53. Wilkerson, FP, Kobayashi D, Muscatine L (1988) Mitotic index and size of symbiotic algae in Caribbean reef corals. Coral Reefs 7(1): 29–36

    Article  Google Scholar 

  54. Williams E, Bunkley-Williams L (1990) The world-wide coral reef bleaching cycle and related sources of coral mortality. Atoll Res Bull 335:1–71

    Article  Google Scholar 

  55. Zar JH (1998) Biostatistical analysis. Prentice Hall, New Jersey, 929 p

    Google Scholar 

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Correspondence to Mohammad Reza Shokri.

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Oladi, M., Shokri, M.R. & Rajabi-Maham, H. Application of the coral health chart to determine bleaching status of Acropora downingi in a subtropical coral reef. Ocean Sci. J. 52, 267–275 (2017). https://doi.org/10.1007/s12601-017-0025-4

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Key words

  • Symbiodinium
  • bleaching
  • zooxanthellae density
  • mitotic index
  • chlorophyll content