Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-10T10:54:37.014Z Has data issue: false hasContentIssue false
  • English
  • Français

Species variability in the response to elevated temperature of select corals in north-western Philippines

Published online by Cambridge University Press:  25 March 2019

Jeric P. Da-Anoy Open the ORCID record for Jeric P. Da-Anoy [Opens in a new window] ,
Patrick C. Cabaitan  and
Cecilia Conaco
Jeric P. Da-Anoy
Affiliation:
Marine Science Institute, College of Science, University of the Philippines, Diliman, Quezon City, 1101, Philippines
Patrick C. Cabaitan
Affiliation:
Marine Science Institute, College of Science, University of the Philippines, Diliman, Quezon City, 1101, Philippines
Cecilia Conaco*
Affiliation:
Marine Science Institute, College of Science, University of the Philippines, Diliman, Quezon City, 1101, Philippines
*
Author for correspondence: Cecilia Conaco, E-mail: cconaco@msi.upd.edu.ph
Get access Rights & Permissions [Opens in a new window]

Abstract

Thermal stress events threaten coral populations by disrupting symbiosis between the coral animal and microalgal symbionts in its tissues. These symbionts are key players in the response of the coral holobiont to elevated temperature. However, little is known about the microalgal symbiont type in select corals in the north-western Philippines and how they contribute to the differential responses of coral species. Based on sequencing of major ITS2 bands from DGGE, the dominant algal symbiont in Acropora digitifera, A. millepora, A. tenuis and Favites colemani was identified to be closely related to ITS2 type C3u, Montipora digitata contained ITS2 type C15, and Seriatopora caliendrum hosted ITS2 types similar to C3-Gulf and D1. Thin branching corals, such as A. tenuis and S. caliendrum, exhibited the greatest reduction in photochemical efficiency (Fv/Fm) and symbiont density at elevated temperature, followed by M. digitata and A. millepora, to a lesser extent. A. digitifera and F. colemani were least affected by the temperature treatment. Reduction in Fv/Fm and symbiont density was more apparent in A. tenuis and A. millepora than in M. digitata and F. colemani, although these species all host ITS2 type C3u symbionts. These results suggest that the impact of elevated temperature is influenced by factors apart from symbiont type. This highlights the importance of further studies on the diversity of corals and their microalgal symbionts in the region to gain insights into their potential resilience to recurring thermal stress events.

Keywords

Coral bleachingITS2photochemical efficiency
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 6 , September 2019 , pp. 1273 - 1279
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Baird, AH and Marshall, PA (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Marine Ecology Progress Series 237, 133–141.Google Scholar
Baird, AH, Bhagooli, R, Ralph, PJ and Takahashi, S (2009) Coral bleaching: the role of the host. Trends in Ecology and Evolution 24, 16–20.Google Scholar
Barshis, DJ, Ladner, JT, Oliver, TA, Seneca, FO, Traylor-Knowles, N and Palumbi, SR (2013) Genomic basis for coral resilience to climate change. Proceedings of the National Academy of Sciences USA 110, 1387–1392.Google Scholar
Bay, RA and Palumbi, SR (2015) Rapid acclimation ability mediated by transcriptome changes in reef-building corals. Genome Biology and Evolution 7, 1602–1612.Google Scholar
Bellantuono, AJ, Hoegh-Guldberg, O and Rodriguez-Lanetty, M (2011) Resistance to thermal stress in corals without changes in symbiont composition. Proceedings of the Royal Society B: Biological Sciences 279, 1100–1107.Google Scholar
Brown, B, Dunne, R, Goodson, M and Douglas, A (2002) Experience shapes the susceptibility of a reef coral to bleaching. Coral Reefs 21, 119–126.Google Scholar
Carpenter, KE, Abrar, M, Aeby, G, Aronson, RB, Banks, S, Bruckner, A, Chiriboga, A, Cortés, J, Delbeek, JC, Devantier, L, Edgar, GJ, Edwards, AJ, Fenner, D, Guzmán, HM, Hoeksema, BW, Hodgson, G, Johan, O, Licuanan, WY, Livingstone, SR, Lovell, ER, Moore, JA, Obura, DO, Ochavillo, D, Polidoro, BA, Precht, WF, Quibilan, MC, Reboton, C, Richards, ZT, Rogers, AD, Sanciangco, J, Sheppard, A, Sheppard, C, Smith, J, Stuart, S, Turak, E, Veron, JE, Wallace, C, Weil, E and Wood, E (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321, 560.Google Scholar
Coles, SL and Brown, BE (2003) Coral bleaching – capacity for acclimatization and adaptation. Advances in Marine Biology 46, 183–223.Google Scholar
DeSalvo, MK, Sunagawa, S, Fisher, PL, Voolstra, CR, Iglesias-Prieto, R and Medina, M (2010) Coral host transcriptomic states are correlated with Symbiodinium genotypes. Molecular Ecology 19, 1174–1186.Google Scholar
Dimond, JL, Holzman, BJ and Bingham, BL (2012) Thicker host tissues moderate light stress in a cnidarian endosymbiont. Journal of Experimental Biology 215, 2247–2254.Google Scholar
Dornelas, M, Madin, JS, Baird, AH and Connolly, SR (2017) Allometric growth in reef-building corals. Proceedings of The Royal Society B, Biological Sciences 284, 1851. https://doi.org/10.1098/rspb.2017.0053.Google Scholar
Dove, SG, Lovell, C, Fine, M, Deckenback, J, Hoegh-Guldberg, O, Iglesias-Prieto, R and Anthony, KRN (2008) Host pigments: potential facilitators of photosynthesis in coral symbioses. Plant, Cell & Environment 31, 1523–1533.Google Scholar
Edgar, RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113.Google Scholar
Enríquez, S, Méndez, ER and Prieto, RI (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnology and Oceanography 50, 1025–1032.Google Scholar
Fisher, PL, Malme, MK and Dove, S (2012) The effect of temperature stress on coral–Symbiodinium associations containing distinct symbiont types. Coral Reefs 31, 473–485.Google Scholar
Franklin, EC, Stat, M, Pochon, X, Putnam, HM and Gates, RD (2011) Geosymbio: a hybrid, cloud-based web application of global geospatial bioinformatics and ecoinformatics for Symbiodinium–host symbioses. Molecular Ecology Resources 12, 369–373.Google Scholar
Gajigan, AP and Conaco, C (2017) A microRNA regulates the response of corals to thermal stress. Molecular Ecology 26, 3472–3483.Google Scholar
Hoegh-Guldberg, O, Poloczanska, ES, Skirving, W and Dove, S (2017) Coral reef ecosystems under climate change and ocean acidification. Frontiers in Marine Science 4, 158.Google Scholar
Hoogenboom, MO, Frank, GE, Chase, TJ, Jurriaans, S, Álvarez-Noriega, M, Peterson, K, Critchell, K, Berry, KLE, Nicolet, KJ, Ramsby, B and Paley, AS (2017) Environmental drivers of variation in bleaching severity of Acropora species during an extreme thermal anomaly. Frontiers in Marine Science 4, 376.Google Scholar
Hou, J, Xu, T, Su, D, Wu, Y, Cheng, L, Wang, J, Zhou, Z and Wang, Y (2018) RNA-Seq reveals extensive transcriptional response to heat stress in the stony coral Galaxea fascicularis. Frontiers in Genetics 9, 37.Google Scholar
Howells, EJ, Berkelmans, R, van Oppen, MJH, Willis, BL and Bay, LK (2013) Historical thermal regimes define limits to coral acclimatization. Ecology 94, 1078–1088.Google Scholar
Hughes, TP, Kerry, JT, Álvarez-Noriega, M, Álvarez-Romero, JG, Anderson, KD, Baird, AH, Babcock, RC, Beger, M, Bellwood, DR, Berkelmans, R, Bridge, TC, Butler, IR, Byrne, M, Cantin, NE, Comeau, S, Connolly, SR, Cumming, GC, Dalton, SJ, Diaz-Pulido, G, Eakin, CM, Figueira, WF, Gilmour, JP, Harrison, HB, Heron, SF, Hoey, AS, Hobbs, JPA, Hoogenboom, MO, Kennedy, EV, Kuo, CY, Lough, JM, Lowe, RJ, Liu, G, McCulloch, MT, Malcolm, HA, McWilliam, MJ, Pandolfi, JM, Pears, RJ, Pratchett, MS, Schoepf, S, Simpson, T, Skirving, WJ, Sommer, B, Torda, G, Wachenfeld, DR, Willis, BL and Wilson, SK (2017) Global warming and recurrent mass bleaching of corals. Nature 543, 373.Google Scholar
Hume, BC, D'Angelo, C, Smith, EG, Stevens, JR, Burt, J and Wiedenmann, J (2015) Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world's hottest sea, the Persian/Arabian Gulf. Scientific Reports 5, 8562.Google Scholar
Jokiel, PL (2004) Temperature stress and coral bleaching. In Rosenberg E and Loya Y (eds), Coral Health and Disease. Berlin: Springer, pp. 401–425.Google Scholar
Keshavmurthy, S, Meng, PJ, Wang, JK, Kuo, CY and Yang, SY (2014) Can resistant coral–Symbiodinium associations enable coral communities to survive climate change? A study of a site exposed to long-term hot water input. PeerJ 2, e327.Google Scholar
Knowlton, N, Brainard, RE, Fisher, R, Moews, M, Plaisance, L and Caley, MJ (2010) Coral reef biodiversity. In McIntyre AD (ed.), Life in the World's Oceans. Oxford: Wiley-Blackwell, pp. 65–78.Google Scholar
Krueger, T, Hawkins, TD, Becker, S, Pontasch, S, Dove, S, Hoegh-Guldberg, O, Leggat, W, Fisher, PL, and Davy, SK (2015) Differential coral bleaching – contrasting the activity and response of enzymatic antioxidants in symbiotic partners under thermal stress. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 190, 15–25.Google Scholar
Kuguru, B, Winters, G, Beer, S, Santos, SR and Chadwick, NE (2007) Adaptation strategies of the corallimorpharian Rhodactis rhodostoma to irradiance and temperature. Marine Biology 151, 1287–1298.Google Scholar
LaJeunesse, T (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Marine Biology 141, 387–400.Google Scholar
LaJeunesse, TC and Trench, RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biological Bulletin 199, 126–134.Google Scholar
LaJeunesse, TC, Pettay, DT, Sampayo, EM, Phongsuwan, N, Brown, B, Obura, DO, Hoegh-Guldberg, O and Fitt, WK (2010) Long-standing environmental conditions, geographic isolation and host–symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. Journal of Biogeography 37, 785–800.Google Scholar
LeGresley, M and McDermott, G (2010) Counting chamber methods for quantitative phytoplankton analysis – haemocytometer, Palmer-Maloney cell and Sedgewick-Rafter cell. In Karlson, B, Cusack, C and Bresnan, E (eds), Microscopic and Molecular Methods for Quantitative Phytoplankton Analysis. Paris: UNESCO, pp. 25–30.Google Scholar
Lesser, MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16, 187–192.Google Scholar
Lesser, MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annual Review of Physiology 68, 253–278.Google Scholar
Li, S, Yu, KF and Shi, Q (2008) Experimental study of stony coral response to the high temperature in Luhuitou of Hainan Island. Tropical Geography 28, 534–539.Google Scholar
Loya, Y, Sakai, K, Yamazato, K, Nakano, Y, Sambali, H and van Woesik, R (2001) Coral bleaching: the winners and the losers. Ecology Letters 28, 534–539.Google Scholar
Marshall, PA and Baird, AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19, 155–163.Google Scholar
McPhaden, MJ, Zebiak, SE and Glantz, MH (2006) ENSO as an integrating concept in Earth science. Science 314, 1740.Google Scholar
Meyer, E, Aglyamova, GV and Matz, MV (2011) Profiling gene expression responses of coral larvae (Acropora millepora) to elevated temperature and settlement inducers using a novel RNA-Seq procedure. Molecular Ecology 20, 3599–3616.Google Scholar
Middlebrook, R, Hoegh-Guldberg, O and Leggat, W (2008) The effect of thermal history on the susceptibility of reef-building corals to thermal stress. Journal of Experimental Biology 211, 1050–1056.Google Scholar
Muscatine, L and Porter, JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience 27, 454–460.Google Scholar
Oakley, CA, Durand, E, Wilkinson, SP, Peng, L, Weis, VM, Grossman, AR and Davy, SK (2017) Thermal shock induces host proteostasis disruption and endoplasmic reticulum stress in the model symbiotic Cnidarian Aiptasia. Journal of Proteome Research 16, 2121–2134.Google Scholar
Parkinson, JE, Banaszak, AT, Altman, NS, LaJeunesse, TC and Baums, IB (2015) Intraspecific diversity among partners drives functional variation in coral symbioses. Scientific Reports 5, 15667.Google Scholar
Peñaflor, EL, Skirving, WJ, Strong, AE, Heron, SF and David, LT (2009) Sea-surface temperature and thermal stress in the Coral Triangle over the past two decades. Coral Reefs 28, 841.Google Scholar
Putnam, HM, Edmunds, PJ and Fan, T-Y (2010) Effect of a fluctuating thermal regime on adult and larval reef corals. Invertebrate Biology 129, 199–209.Google Scholar
Ralph, PJ, Hill, R, Doblin, MA and Davy, SK (2015) Theory and application of pulse amplitude modulated chlorophyll fluorometry in coral health assessment. In Woodley, CM, Downs, CA, Bruckner, AW, Porter, JW and Galloway, SB (eds) Diseases of Coral. Hoboken, NJ: John Wiley & Sons, pp. 506–523.Google Scholar
Richier, S, Furla, P, Plantivaux, A, Merle, PL and Allemand, D (2005) Symbiosis-induced adaptation to oxidative stress. Journal of Experimental Biology 208, 277–285.Google Scholar
Rodriguez-Lanetty, M, Harii, S and Hoegh-Guldberg, O (2009) Early molecular responses of coral larvae to hyperthermal stress. Molecular Ecology 18, 5101–5114.Google Scholar
Rohwer, F, Seguritan, V, Azam, F and Knowlton, N (2002) Diversity and distribution of coral-associated bacteria. Marine Ecology Progress Series 243, 1–10.Google Scholar
Rowan, R (2004) Coral bleaching: thermal adaptation in reef coral symbionts. Nature 430, 742.Google Scholar
Salih, A, Larkum, A, Cox, G, Kühl, M and Hoegh-Guldberg, O (2000) Fluorescent pigments in corals are photoprotective. Nature 408, 850.Google Scholar
Sampayo, EM, Dove, S and Lajeunesse, TC (2009) Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Molecular Ecology 18, 500–519.Google Scholar
Silverstein, RN, Cunning, R and Baker, AC (2015) Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Global Change Biology 21, 236–249.Google Scholar
Stat, M and Gates, RD (2011) Clade D Symbiodinium in scleractinian corals: a “nugget” of hope, a selfish opportunist, an ominous sign, or all of the above? Journal of Marine Biology 730715, 9.Google Scholar
Talavera, G, Castresana, J, Kjer, K, Page, R and Sullivan, J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564–577.Google Scholar
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Traylor-Knowles, N, Rose, NH, Sheets, EA and Palumbi, SR (2017) Early transcriptional responses during heat stress in the coral Acropora hyacinthus. Biological Bulletin 232, 91–100.Google Scholar
Truett, GE, Heeger, P, Mynatt, RL, Truett, AA, Walker, JA and Warman, ML (2000) Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotechniques 29, 52, 54.Google Scholar
Veal, CJ, Carmi, M, Fine, M and Hoegh-Guldberg, O (2010) Increasing the accuracy of surface area estimation using single wax dipping of coral fragments. Coral Reefs 29, 893–897.Google Scholar
Yakovleva, I, Bhagooli, R, Takemura, A and Hidaka, M (2004) Differential susceptibility to oxidative stress of two scleractinian corals: antioxidant functioning of mycosporine-glycine. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 139, 721–730.Google Scholar
Yamashita, H, Suzuki, G, Kai, S, Hayashibara, T and Koike, K (2014) Establishment of coral-algal symbiosis requires attraction and selection. PLoS ONE 9, e97003.Google Scholar
Yap, HT, Espita, DML, Montaño, MNE, Benjamin, C and Gomez, ED (2014) Biochemical comparison of bleaching and non-bleaching Montipora digitata (Order Scleractinia) in the Philippines. Philippine Science Letters 7, 293–299.Google Scholar
Yu, K (2012) Coral reefs in the South China Sea: their response to and records on past environmental changes. Science China Earth Sciences 55, 1217–1229.Google Scholar
Zar, JH (1984) Biostatistical Analysis. London: Prentice Hall.Google Scholar