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White but not bleached: photophysiological evidence from white Montastraea cavernosa reveals potential overestimation of coral bleaching

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Abstract

Climate change and other types of environmental stress are known to increase corals’ vulnerability to bleaching, a process whereby colonies lose their colour either due to the loss of photosynthetic symbionts or their pigments. Although bleaching leaves the coral skeleton visible under its transparent tissue, not all white coral colonies display this feature. This raises the question as to whether all ‘white’-shaded colonies are indeed bleached. Within this context, Montastraea cavernosa colonies of different colour types (dark brown, light brown, bleached and white) were sampled for photobiological evaluation. Here, we show that, while the conventional spectral reflectance techniques failed to discriminate white from bleached colonies, chlorophyll fluorescence, photosynthetic pigment profile and Symbiodinium density enabled a clear distinction between these shades. Subsequently, video transects from reef monitoring surveys at Todos os Santos Bay (Brazil) revealed that the proportion of bleached and white colonies is similar, thus suggesting that current coral reef surveys may be overestimating the bleaching of M. cavernosa by nearly twofold.

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References

  • Adjeroud M, Michonneau F, Edmunds PJ, Chancerelle Y, Lison de Loma T, Penin L, Thibaut L, Vidal-Dupiol J, Salvat B, Galzin R (2009) Recurrent disturbances, recovery trajectories, and resilience of coral reef assemblages on a South Central Pacific reef. Coral Reefs 28:775–780

    Article  Google Scholar 

  • Alemu IJB, Clement Y (2014) Mass coral bleaching in 2010 in the southern Caribbean. PLoS one 9:e83829

    Article  Google Scholar 

  • Anderson TW (2003) An introduction to multivariate statistical analysis. Wiley, New York

    Google Scholar 

  • Andréfouet S, Berkelmans R, Odriozola L, Done T, Oliver J, Muller-Karger F (2002) Choosing the appropriate spatial resolution for monitoring coral bleaching events using remote sensing. Coral Reefs 21:147–154

    Article  Google Scholar 

  • Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471

    Article  Google Scholar 

  • Borneman E (2003) Coral disease at the flower gardens and stetson banks: a report. Reefkeeping.com

  • Brandt ME (2009) The effect of species and colony size on the bleaching response of reef-building corals in the Florida keys during the 2005 mass bleaching event. Coral Reefs 28:911–924

    Article  Google Scholar 

  • Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138

    Article  Google Scholar 

  • Brown BE, Dunne RP, Warner ME, Ambarsari I, Fitt WK, Gibb SW, Cummings DG (2000) Damage and recovery of photosynthetm II during a manipulative field experiment on solar bleaching in the coral Goniastrea aspera. Mar Ecol Prog Ser 195:117–124

    Article  Google Scholar 

  • Burns JHR, Gregg TM, Takabayashi M (2013) Does coral disease affect Symbiodinium? Investigating the impacts of growth anomaly on symbiont photophysiology. PLoS one 8:e72466

    Article  Google Scholar 

  • Cai W, Borlace S, Lengaigne M, van Rensch P, Collins M, Vecchi G, Timmermann A, Santoso A, McPhaden MJ, Wu L, England MH, Wang G, Guilyardi E, Jin F-F (2014) Increasing frequency of extreme El Niño events due to greenhouse warming. Nat Clim Change 4:111–116

    Article  CAS  Google Scholar 

  • Carleton CB, Done TJ (1995) Quantitative video sampling of coral reef benthos: large-scale application. Coral Reefs 14:35–46

    Article  Google Scholar 

  • Cirano M, Lessa GC (2007) Oceanographic characteristics of Baía de Todos os Santos, Brazil. Rev Bras Geofís 25:363–387

    Article  Google Scholar 

  • Cooper TF, Gilmour JP, Fabricius KE (2009) Bioindicators of changes in water quality on coral reefs: review and recommendations for monitoring programmes. Coral Reefs 28:589–606

    Article  Google Scholar 

  • Costa CF, Sassi R, Amaral FD (2004) Population density and photosynthetic pigment content in symbiotic dinoflagellates in the brazilian scleractinian coral Montastrea cavernosa (Linnaeus, 1767). Braz J Oceanogr 52:93–99

    Google Scholar 

  • Costa CF, Sassi R, Gorlach-Lira K (2013) Diversity and seasonal fluctuations of microsymbionts associated with some scleractinian corals of the Picãozinho reefs of Paraíba State, Brazil. PanAm J Aquat Sci 8:240–252

    Google Scholar 

  • Cruz ICS, Kikuchi RKP, Leão ZMAN (2008) Use of the video transect method for characterizing the Itacolomis reefs, eastern Brazil. Braz J Oceanogr 56:271–280

    Article  Google Scholar 

  • Cruz ICS, Kikuchi RKP, Leão ZMAN (2009) Caracterização dos recifes de corais da área de preservação ambiental da Baía de Todos os Santos para fins de manejo, Bahia, Brasil. Rev Gest Costeira Integr 9:3–23

    Article  Google Scholar 

  • Dalton SJ, Carroll AG (2011) Monitoring coral health to determine coral bleaching response at high latitude eastern Australian reefs: an applied model for a changing climate. Diversity 4:592–610

    Article  Google Scholar 

  • 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. Proc Natl Acad Sci USA 109:17995–17999

    Article  Google Scholar 

  • Done TJ, DeVantier LM, Turak E, Fisk DA, Wakeford M, Van Woesik R (2010) Coral growth on three reegs: development of recovery benchmarks using a space for time approach. Coral Reefs 29:815–833

    Article  Google Scholar 

  • Dove S, Ortiz J, Enriquez S, Fine M, Fisher P, Iglesias-Prieto R, Thornhill D, Hoegh-Guldberg O (2006) Response of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short-term heat stress. Limnol Oceanogr 51:1149–1158

    Article  Google Scholar 

  • Dutra LXC, Kikuchi RKP, Leão ZMAN (2006) Todos os Santos Bay coral reefs, Eastern Brazil, revisited after 40 years. Proceedings of the 10th International Coral Reef Symposium: 1090–1095

  • Ferreira BP, Maida M (2006) Monitoriamento dos recifes de coral do Brasil: Situação atual e perspectivas. Brasilia, Brasil

    Google Scholar 

  • Ferreira BP, Costa MBSF, Coxey MS, Gaspar ALB, Veleda D, Araújo M (2012) The effects of sea surface temperature anomalies on oceanic coral reef systems in the southwestern tropical Atlantic. Coral Reefs 32:441–454

    Article  Google Scholar 

  • Ferreira BP, Costa MBSF, Coxey MS, Gaspar ALB, Veleda D, Araujo M (2013) The effects of sea surface temperature anomalies on oceanic coral reef systems in the southwestern tropical Atlantic. Coral Reefs 32:441–454

    Article  Google Scholar 

  • Fisher L, Banks K, Gilliam D, Dodge RE, Stout D, Vargas-Angel B, Walker BK (2008) Real-time coral stress observations before, during, and after beach nourishment dredging offshore SE Florida. Proceedings of the 11th International Coral Reef Symposium, Ft. Lauderdale, Florida: 34–37

  • Fisher PL, Malme MK, Dove S (2012) The effect of temperature stress on coral–Symbiodinium associations containing distinct symbiont types. Coral Reefs 31:473–485

    Article  Google Scholar 

  • Fitt W, Warner M (1995) Bleaching patterns of four species of Caribbean reef corals. Biol Bull 189:298–307

    Article  Google Scholar 

  • 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  CAS  Google Scholar 

  • Francini-Filho RB, Coni EOC, Meirelles PM, Amado-Filho GM, Thompson FL, Pereira-Filho GH, Bastos AC, Abrantes DP, Ferreira CM, Gibran FZ, Guth AZ, Sumida PYG, Oliveira NL, Kaufman L, Minte-Vera CV, Moura RL (2013) Dynamics of coral reef benthic assemblages of the Abrolhos Bank, eastern Brazil: inferences on natural and anthropogenic drivers. PLoS one 8:e54260

    Article  CAS  Google Scholar 

  • Glynn PW (1984) Widespread coral mortality and the 1982–83 El Niño warming event. Environ Conserv 11:133–146

    Article  Google Scholar 

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

    Google Scholar 

  • Hedley JD, Roelfsema CM, Phinn SR, Mumby PJ (2012) Environmental and sensor limitations in optical remote sensing of coral reefs: implications for monitoring and sensor design. Remote Sensing 4:271–302

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Kabiri K, Pradhan B, Samimi-Namin K, Moradi M (2013) Detecting coral bleaching, using QuickBird multi-temporal data: a feasibility study at Kish Island, the Persian Gulf. Estuar Coast Shelf Sci 117:273–281

    Article  Google Scholar 

  • Kemp DW, Hernandez-Pech X, Iglesias-Prieto R, Fitt WK, Schmidt GW (2014) Community dynamics and physiology of Symbiodinium spp. before, during and after a coral bleaching event. Limnol Oceanogr 59:788–797

    Article  CAS  Google Scholar 

  • Kenkel CD, Aglyamova G, Alamaru A, Bhagooli R, Capper R, Cunning R, deVillers A, Haslun JA, Hedouin L, Keshavmurthy S, Kuehl KA, Mahmoud H, McGinty ES, Montoya-Maya PH, Palmer CV, Pantile R, Sanchez JA, Schils T, Silverstein RN, Squiers LB, Tang PC, Goulet TL, Matz MV (2011) Development of gene expression markers of acute heat-light stress in reef-building corals of the genus Porites. PLoS one 6:e26914

    Article  CAS  Google Scholar 

  • Kenkel CD, Sheridan C, Leal MC, Bhagooli R, Castillo KD, Kurata N, McGinty E, Goulet TL, Matz MV (2014) Diagnostic gene expression biomarkers of coral thermal stress. Mol Ecol Resour 14:667–678

    Article  CAS  Google Scholar 

  • Kikuchi RKP, Leão ZMAN, Oliveira MDM (2010) Conservation status and spatial patterns of AGRRA vitality indices in Southwestern Atlantic reefs. Rev Biol Trop 58:1–31

    Google Scholar 

  • Kramarsky-Winter E, Harel M, Siboni N, Ben Dov E, Brickner I, Loya Y, Kushmaro A (2006) Identification of a protist-coral association and its possible ecological role. Mar Ecol Prog Ser 317:67–73

    Article  Google Scholar 

  • Laborel JL (1970) Madreporaires et hydrocoralliaires recifaux des cotes bresiliennes, Systematique, ecologie, repartition verticale et geographie. Annales de L’Institut oceanographique, Paris, pp 171–229

    Google Scholar 

  • Ladrière O, Penin L, Lierde EV, Vidal-Dupiol J, Kayal M, Roberty S, Poulicek M, Adjeroud M (2013) Natural spatial variability of algal endosymbiont density in the coral Acropora globiceps: a small-scale approach along environmental gradients around Moorea (French Polynesia). J Mar Biol Assoc UK 94:65–74

    Article  Google Scholar 

  • Lang JC, Marks KW, Kramer PA, Kramer PA, Ginsburg RN (2010) AGRRA protocols version 5.4, Miami, FL

  • Leal MC, Jesus B, Ezequiel J, Calado R, Rocha RJM, Cartaxana P, Serôdio J (2014a) Concurrent imaging of chlorophyll fluorescence, chlorophyll a content and green fluorescent proteins-like proteins of symbiotic cnidarians. Mar Ecol. doi:10.1111/maec.12164

    Google Scholar 

  • Leal MC, Ferrier-Pagès C, Calado R, Brandes JA, Frischer ME, Nejstgaard JC (2014b) Trophic ecology of the facultative symbiotic coral Oculina arbuscula. Mar Ecol Prog Ser 504:171–179

    Article  Google Scholar 

  • Leão ZMAN, Kikuchi RKP, Testa V (2003) Corals and coral reefs of Brazil. Lat Am Coral Reefs 13:9–52

    Article  Google Scholar 

  • Leão ZMAN, Kikuchi RKP, Oliveira MDM, Vascocellos V (2010) Status of Eastern Brazilian coral reefs in time of climate changes. PanAm J Aquat Sci 5:224–235

    Google Scholar 

  • Mallela J, Crabbe MJC (2009) Hurricanes and coral bleaching linked to changes in coral recruitment in Tobago. Mar Eviron Res 68:158–162

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Matz MV, Marshall NJ, Vorobyev M (2006) Are corals colorful? Photochem Photobiol 82:345–350

    Article  CAS  Google Scholar 

  • Mendes CR, Cartaxana P, Brotas V (2007) Determination of phytoplankton and microphytobenthos pigments: comparing resolution and sensitivity of a C18 and C8 method. Limnol Oceanogr Methods 5:363–370

    Article  CAS  Google Scholar 

  • Miranda RJ, Cruz ICS, Leão ZMAN (2013) Coral bleaching in the Caramuanas reef (Todos os Santos Bay, Brazil) during the 2010 El Niño event. Lat Am J Aquat Res 41:351–360

    Article  Google Scholar 

  • Mumby PJ, Skirving W, Strong AE, Hardy JT, LeDrew EF, Hochberg EJ, Stumpf RP, David LT (2004) Remote sensing of coral reefs and their physical environment. Mar Pollut Bull 48:219–228

    Article  CAS  Google Scholar 

  • Myers MR, Hardy JT, Mazel CH, Dustan P (1999) Optical spectra and pigmentation of Caribbean reef corals and macroalgae. Coral Reefs 18:179–186

    Article  Google Scholar 

  • Nir O, Gruber DF, Einbinder S, Kark S, Tchernov D (2011) Changes in scleractinian coral Seriatopora hystrix morphology and its endocellular Symbiodinium characteristics along a bathymetric gradient from shallow to mesophotic reef. Coral Reefs 30:1089–1100

    Article  Google Scholar 

  • Page C, Coleman G, Ninio R, Osborne K (2001) Surverys of benthic reef communities using underwater video: long-term monitoring of the Great Barrier Reef. Australia, Townsville, Queensland

    Google Scholar 

  • Philipp E, Fabricius K (2003) Photophysiological stress in scleractinian corals in response to short-term sedimentation. J Exp Mar Biol, Ecol

    Google Scholar 

  • Piniak GA (2007) Effects of two sediment types on the fluorescence yield of two Hawaiian scleractinian corals. Mar Environ Res 64:456–468

    Article  CAS  Google Scholar 

  • Porter JW, Meier OW (1992) Quantification of loss and change in floridian reef coral populations. Integr Comp Biol 32:625–640

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing. In: R Foundation for Statistical Computing (ed). R Foundation for Statistical Computing, Vienna, Austria (http://www.R-project.org)

  • Rocha RJM, Pimentel T, Serôdio J, Rosa R, Calado R (2013a) Comparative performance of light emitting plastma (LEP) and light emitting diode (LED) in ex situ aquaculture of scleractinian corals. Aquaculture 402–403:38–45

    Article  Google Scholar 

  • Rocha RJM, Serôdio J, Leal MC, Cartaxana P, Calado R (2013b) Effect of light intensity on post-fragmentation photobiological performance of the soft coral Sinularia flexibilis. Aquaculture 388–391:24–29

    Article  Google Scholar 

  • Roff G, Kvennefors E, Ulstrup K, Fine M, Hoegh-Guldberg O (2008) Coral disease physiology: the impact of Acroporid white syndrome on Symbiodinium. Coral Reefs 27:373–377

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Rouse J, Haas R, Schell J, Deering D (1973) Monitoring vegetation systems in the Great Plains with ERTS. In: ERTS-1 Symposium, 3rd Greenbelt, MD. NASA, Washington, DC, p 309–317

  • Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62

    Article  CAS  Google Scholar 

  • Scopélitis J, Andrefouet S, Phinn S, Chabanet P, Naim O, Tourrand C, Done T (2009) Changes of coral communities over 35 years: integrating in situ and remote-sensing data on Saint-Leu Reef (la Réunion, Indian Ocean). Estuar Coast Shelf Sci 84:342–352

    Article  Google Scholar 

  • Sheridan C, Kramarsky-Winter E, Sweet M, Kushmaro A, Leal MC (2013) Diseases in coral aquaculture: causes, implications and preventions. Aquaculture 396–399:124–135

    Article  Google Scholar 

  • Siboni N, Rasoulouniriana D, Ben-Dov E, Kramarsky-Winter E, Sivan A, Loya Y, Hoegh-Guldberg O, Kushmaro A (2010) Stramenopile microorganisms associated with the massive coral Favia sp. J Eukaryot Microbiol 57:236–244

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • Suggett DJ, Kikuchi RKP, Oliveira MDM, Spanó S, Carvalho R, Smith DJ (2012) Photobiology of corals from Brazil’s near-shore marginal reefs of Abrolhos. Mar Biol 159:1461–1473

    Article  Google Scholar 

  • Ulstrup K, Hill R, van Oppen M, Larkum A, Ralph P (2008) Seasonal variation in the photo-physiology of homogeneous and heterogeneous Symbiodinium consortia in two scleractinian corals. Mar Ecol Prog Ser 361:139–150

    Article  Google Scholar 

  • Van Veghel MLJ (1993) Multiple species spawning on Curacao reefs. Bull Mar Sci 52:1017–1021

    Google Scholar 

  • Veal CJ, Carmi M, Fine M, Hoegh-Guldberg O (2010) Increasing the accuracy of surface area estimation using single wax dipping of coral fragments. Coral Reefs 29:893–897

    Article  Google Scholar 

  • Venn AA, Wilson MA, Trapido-Rosenthal HG, Keely BJ, Douglas AE (2006) The impact of coral bleaching on the pigment profile of the symbiotic alga, Symbiodinium. Plant Cell Environ 29:2133–2142

    Article  CAS  Google Scholar 

  • Veron JEN (2000) Corals of the World. Australian Institute of Marine Science, Townsville, Qld, Australia

    Google Scholar 

  • Warner M, Fitt W, Schmidt G (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007

    Article  CAS  Google Scholar 

  • Weber M, de Beer D, Lott C, Polerecky L, Kohls K, Abed RMM, Ferdelman TG, Fabricius KE (2012) Mechanisms of damage to corals exposed to sedimentation. Proc Natl Acad Sci 109:E1558–E1567

    Article  CAS  Google Scholar 

  • Wijgerde T, Melis AV, Silva CIF, Leal MC, Vogels L, Mutter C, Osinga R (2014) Red light represses the photophysiology of the scleractinian coral Stylophora pistillata. PLoS one 9:e92781

    Article  Google Scholar 

  • Winters G, Holzman R, Blekhman A, Beer S, Loya Y (2009) Photographic assessment of coral chlorophyll contents: implications for ecophysiological studies and coral monitoring. J Exp Mar Biol Ecol 380:22–35

    Article  Google Scholar 

  • Yamano H (2004) Detection limits of coral reef bleaching by satellite remote sensing: simulation and data analysis. Remote Sens Environ 90:86–103

    Article  Google Scholar 

  • Yamano H (2013) Multispectral applications. In: Goodman JA, Purkis SJ, Phinn SR (eds) Coral reef remote sensing. Springer, Dordrecht, pp 51–78

    Chapter  Google Scholar 

  • Zapata M, Rodríguez F, Garrido JL (2000) Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Mar Ecol Prog Ser 195:29–45

    Article  CAS  Google Scholar 

  • Zar JH (2010) Biostatistical analysis. Prentice Hall, New Jersey

    Google Scholar 

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Acknowledgments

ICSC was supported by a PhD scholarship (Conselho Nacional de Pesquisa, No 556755/2010-3), as well as MCL (SFRH/BD/63783/2009, Fundação para a Ciência e Tecnologia (FCT), QREN-POPH–Type 4.1–Advanced Training, subsidized by the European Social Fund and national funds MCTES). RKPK benefits from CNPq fellowship (PQ 1D), CRM was funded by a postdoc grant from CAPES (Brazil), and RJMR was supported by a postdoc scholarship (BPD/UI88/6077/2014), integrated in the project ‘CENTRO–07–ST24–FEDER–002033: Sustainable Use of Marine Resources–MARES’. This work was supported by European Funds through project SymbioCoRe (FP7–PEOPLE–2011–IRSES, 295191) and COMPETE, and national funds through FCT within project Pest-C/MAR/LA0017/2013. We also thank two anonymous reviewers for their comments to improve the manuscript and to Maria Silva from the University of St. Andrews (UK) for guidance on statistical analysis.

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Correspondence to Igor C. S. Cruz.

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Communicated by L. Mydlarz.

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Cruz, I.C.S., Leal, M.C., Mendes, C.R. et al. White but not bleached: photophysiological evidence from white Montastraea cavernosa reveals potential overestimation of coral bleaching. Mar Biol 162, 889–899 (2015). https://doi.org/10.1007/s00227-015-2633-9

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