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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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
Alemu IJB, Clement Y (2014) Mass coral bleaching in 2010 in the southern Caribbean. PLoS one 9:e83829
Anderson TW (2003) An introduction to multivariate statistical analysis. Wiley, New York
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
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
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
Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138
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
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
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
Carleton CB, Done TJ (1995) Quantitative video sampling of coral reef benthos: large-scale application. Coral Reefs 14:35–46
Cirano M, Lessa GC (2007) Oceanographic characteristics of Baía de Todos os Santos, Brazil. Rev Bras Geofís 25:363–387
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
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
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
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
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
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
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
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
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
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
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
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
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
Fitt W, Warner M (1995) Bleaching patterns of four species of Caribbean reef corals. Biol Bull 189:298–307
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
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
Glynn PW (1984) Widespread coral mortality and the 1982–83 El Niño warming event. Environ Conserv 11:133–146
Goreau TJ, Hayes RL (1994) Coral bleaching and ocean “hot spots”. Ambio 23:176–180
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
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866
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
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
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
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
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
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
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
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
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
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
Leão ZMAN, Kikuchi RKP, Testa V (2003) Corals and coral reefs of Brazil. Lat Am Coral Reefs 13:9–52
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
Mallela J, Crabbe MJC (2009) Hurricanes and coral bleaching linked to changes in coral recruitment in Tobago. Mar Eviron Res 68:158–162
Marshall NJ, Kleine DA, Dean AJ (2012) CoralWatch: education, monitoring, and sustainability through citizen science. Front Ecol Environ 10:332–334
Matz MV, Marshall NJ, Vorobyev M (2006) Are corals colorful? Photochem Photobiol 82:345–350
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
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
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
Myers MR, Hardy JT, Mazel CH, Dustan P (1999) Optical spectra and pigmentation of Caribbean reef corals and macroalgae. Coral Reefs 18:179–186
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
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
Philipp E, Fabricius K (2003) Photophysiological stress in scleractinian corals in response to short-term sedimentation. J Exp Mar Biol, Ecol
Piniak GA (2007) Effects of two sediment types on the fluorescence yield of two Hawaiian scleractinian corals. Mar Environ Res 64:456–468
Porter JW, Meier OW (1992) Quantification of loss and change in floridian reef coral populations. Integr Comp Biol 32:625–640
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
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
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
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
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
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
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
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
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
Siebeck UE, Marshall NJ, Kluter A, Hoegh-Guldberg O (2006) Monitoring coral bleaching using a colour reference card. Coral Reefs 25:453–460
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
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
Van Veghel MLJ (1993) Multiple species spawning on Curacao reefs. Bull Mar Sci 52:1017–1021
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
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
Veron JEN (2000) Corals of the World. Australian Institute of Marine Science, Townsville, Qld, Australia
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
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
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
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
Yamano H (2004) Detection limits of coral reef bleaching by satellite remote sensing: simulation and data analysis. Remote Sens Environ 90:86–103
Yamano H (2013) Multispectral applications. In: Goodman JA, Purkis SJ, Phinn SR (eds) Coral reef remote sensing. Springer, Dordrecht, pp 51–78
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
Zar JH (2010) Biostatistical analysis. Prentice Hall, New Jersey
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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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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DOI: https://doi.org/10.1007/s00227-015-2633-9