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Trade-offs in disease and bleaching susceptibility among two color morphs of the Hawaiian reef coral, Montipora capitata

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Abstract

Two threats impacting coral reefs are bleaching and disease, and differential susceptibility to both exists among and within coral taxa. Bleaching resistance is commonly linked to the clade of endosymbiotic Symbiodinium, but may come at a cost to other biological traits. Montipora capitata is an Indo-Pacific reef-building coral with two color morphs, red and orange, which harbor different clades of Symbiodinium. We explored whether these color morphs displayed differences in bleaching/disease susceptibility and other biological traits (growth rate, reproductive output, and lipid content). We found a trade-off between disease and bleaching susceptibility. The orange morph had significantly higher disease prevalence, whereas the red morph had significantly higher bleaching prevalence. Thermal stress experiments found that bleaching and loss of photochemical efficiency occurred significantly faster in the red morph, but at normal temperatures, the red morph had a significantly higher growth rate. Higher abundance of the red morph in the field suggests that disease resistance is a more successful strategy in the absence of thermal stress events. The orange morph may better tolerate increases in sea temperatures, but may not persist due to decreased growth rate and increased disease susceptibility. Trade-offs in response to stressors highlight the need to consider local and global threats to coral reefs.

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References

  • Abrego D, Ulstrup K, Willis B, van Oppen M (2008) Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc R Soc B 275:2273–2282

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aeby GS, Bourne DG, Wilson B, Work TM (2011a) Coral Diversity and the Severity of Disease Outbreaks: A Cross-Regional Comparison of Acropora White Syndrome in a Species-Rich Region (American Samoa) with a Species-Poor Region (Northwestern Hawaiian Islands). J Mar Biol 2011:490198

    Article  Google Scholar 

  • Aeby GS, Callahan SM, Cox EF, Runyon CM, Smith A, Stanton F, Ushijima B, Work TM (2016) Emerging coral diseases in Kaneohe Bay, Oahu, Hawaii (USA): two major disease outbreaks of acute Montipora white syndrome. Dis Aquat Organ 119:189–198

    Article  PubMed  Google Scholar 

  • Aeby GS, Ross M, Williams GJ, Lewis TD, Work TM (2010) Disease dynamics of Montipora white syndrome within Kaneohe Bay, Oahu, Hawaii: distribution, seasonality, virulence, and transmissibility. Dis Aquat Organ 91:1–8

    Article  PubMed  CAS  Google Scholar 

  • Aeby GS, Williams GJ, Franklin EC, Kenyon J, Cox EF, Coles S, Work TM (2011b) Patterns of coral disease across the Hawaiian Archipelago: relating disease to environment. PLoS one 6:e20370

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ansley M (2015) Characterizing innate immunity in the Hawaiian coral, Montipora capitata. M.Sc. Thesis, University of Mississippi

  • Bahr K, Jokiel P, Rodgers K (2015a) The 2014 coral bleaching and freshwater flood events in Kāne‘ohe Bay, Hawai‘i. PeerJ 3:e1136

    Article  PubMed  PubMed Central  Google Scholar 

  • Bahr K, Jokiel P, Toonen R (2015b) The unnatural history of Kaneohe Bay: coral reef resilience in the face of centuries of anthropogenic impacts. PeerJ 3:e950

    Article  PubMed  PubMed Central  Google Scholar 

  • Baird AH, Bhagooli R, Ralph PJ, Takahashi S (2009) Coral bleaching: the role of the host. Trends Ecol Evol 24:16–20

    Article  PubMed  Google Scholar 

  • Bay L, Doyle J, Logan M, Berkelmans R (2016) Recovery from bleaching is mediated by threshold densities of background thermo-tolerant symbiont types in a reef-building coral. R Soc Open Sci 3:160322

    Article  PubMed  PubMed Central  Google Scholar 

  • Bellantuono AJ, Hoegh-guldberg O, Rodriguez-Lanetty M (2012) Resistance to thermal stress in corals without changes in symbiont composition. Proc R Soc B 279:1100–1107

    Article  PubMed  CAS  Google Scholar 

  • Berkelmans R, van Oppen M (2006) The role of zooxanthellae in the thermal tolerance of corals: a “nugget of hope” for coral reefs in an era of climate change. Proc R Soc B 273:2305–2312

    Article  PubMed  PubMed Central  Google Scholar 

  • Beurmann S, Ushijima B, Videau P, Svoboda CM, Smith AM, Rivers OS, Aeby GS, Callahan SM (2017) Pseudoalteromonas piratica strain OCN003 is a coral pathogen that causes a switch from chronic to acute Montipora white syndrome in Montipora capitata. PLoS ONE 12:1–20

    Article  CAS  Google Scholar 

  • Bourne DG, Morrow KM, Webster NS (2016) Insights into the Coral Microbiome: Underpinning the Health and Resilience of Reef Ecosystems. Annu Rev Microbiol 70:317–340

    Article  PubMed  CAS  Google Scholar 

  • Bruno JF, Petes LE, Harvell CD, Hettinger A (2003) Nutrient enrichment can increase the severity of coral diseases. Ecol Lett 6:1056–1061

    Article  Google Scholar 

  • Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD, Sweatman H, Melendy AM (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol 5:1220–1227

    Article  CAS  Google Scholar 

  • Cantin N, van Oppen M, Willis B, Mieog J, Negri A (2009) Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28:405–414

    Article  Google Scholar 

  • Chen C, Lam K, Nakano Y, Tsai W (2003) A stable association of the stress-tolerant zooxanthellae, Symbiodinium clade D, with the low-temperature-tolerant coral, Oulastrea crispata (Scleractinia: Faviidae) in Subtropical Non-Reefal Coral Communities. Zool Stud 42:540–550

    Google Scholar 

  • Chen C, Yang Y, Wei N, Tsai W, Fang L (2005) Symbiont diversity in scleractinian corals from tropical reefs and subtropical non-reef communities in Taiwan. Coral Reefs 24:11–22

    Article  CAS  Google Scholar 

  • Correa AMS, Brandt ME, Smith TB, Thornhill D, Baker A (2009) Symbiodinium associations with diseased and healthy scleractinian corals. Coral Reefs 28:437–448

    Article  Google Scholar 

  • Cox E (1986) The effects of a selective corallivore on growth rates and competition for space between two species of Hawaiian corals. J Exp Mar Bio Ecol 101:161–174

    Article  Google Scholar 

  • Cox E (2007) Continuation of sexual reproduction in Montipora capitata following bleaching. Coral Reefs 26:721–724

    Article  Google Scholar 

  • Cox E, Ribes M, Kinzie R (2006) Temporal and spatial scaling of planktonic responses to nutrient inputs into a subtropical embayment. Mar Ecol Prog Ser 324:19–35

    Article  CAS  Google Scholar 

  • Cróquer A, Weil E (2009) Spatial variability in distribution and prevalence of Caribbean scleractinian coral and octocoral diseases. II. Genera-level analysis. Dis Aquat Organ 83:209–222

    Article  PubMed  Google Scholar 

  • Cunning R, Baker A (2012) Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3:259–262

    Article  Google Scholar 

  • Cunning R, Ritson-Williams R, Gates R (2016) Patterns of bleaching and recovery of Montipora capitata in Kaneohe Bay, Hawaii, USA. Mar Ecol Prog Ser 551:131–139

    Article  CAS  Google Scholar 

  • Darling E, Alvarez-Filip L, Oliver T, McClanahan T, Côté I (2012) Evaluating life-history strategies of reef corals from species traits. Ecol Lett 15:1378–1386

    Article  PubMed  Google Scholar 

  • Darling E, McClanahan T, Côté I (2013) Life histories predict coral community disassembly under multiple stressors. Glob Chang Biol 19:1930–1940

    Article  PubMed  Google Scholar 

  • Dove G, Hoegh-guldberg O (2006) The cell physiology of coral bleaching. In: Phinney J (ed) Coral reefs and climate change: science and management. American Geophysical Union, Washington, DC, pp 55–71

    Chapter  Google Scholar 

  • Fitt WK, Gates RD, Hoegh-Guldberg O, Bythell JC, Jatkar A, Grottoli AG, Gomez M, Fisher P, Lajuenesse TC, Pantos O, Iglesias-Prieto R, Franklin DJ, Rodrigues LJ, Torregiani JM, van Woesik R, Lesser MP (2009) Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: the host does matter in determining the tolerance of corals to bleaching. J Exp Mar Biol Ecol 373:102–110

    Article  Google Scholar 

  • Friedlander A, Aeby G, Brown E, Clark A, Coles S, Dollar S, Hunter C, Jokiel P, Smith J, Walsh B, Williams I, Wiltse W (2005) The state of coral reef ecosystems of the main Hawaiian Islands. ecosystems of the United States and Pacific freely associated state. National Oceanic and Atmospheric Administration, Silver Spring, MD, pp 222–269

  • Gates R (1990) Seawater temperature and sublethal coral bleaching in Jamaica. Coral Reefs 8:193–197

    Article  Google Scholar 

  • Gleason D (1993) Differential effects of ultraviolet radiation on green and brown morphs of the Caribbean coral Porites astreoides. Limnol Oceanogr 38:1452–1463

    Article  Google Scholar 

  • Glynn P, Mate J, Baker A, Calderon M (2001) Coral bleaching and mortality in Panama and Ecuador during the 1997-1998 El Nino-Southern Oscillation event: spatial/temporal patterns and comparisons with the 1982–1983 event. Bull Mar Sci 69:79–109

    Google Scholar 

  • Gochfeld D, Ansley M, Ankisetty S, Aeby G (2014) Antibacterial chemical resistance to disease in the Hawaiian coral Montipora capitata. In: Proceedings of the 14th Annual Oxford International Conference on the Science of Botanicals. Planta Medica 80:CL31

  • Grime J, Pierce S (2012) The evolutionary strategies that shape ecosystems. Wiley-Blackwell, Oxford

    Book  Google Scholar 

  • Grottoli A, Rodrigues L, Juarez C (2004) Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar Biol 145:621–631

    Article  CAS  Google Scholar 

  • Hagedorn M, Carter V, Lager C, Camperio Ciani J, Dygert A, Schleiger R, Henley E (2016) Potential bleaching effects on coral reproduction. Reprod Fertil Dev 28:1061–1071

    Article  CAS  Google Scholar 

  • Harvell D, Jordán-Dahlgren E, Merkel S, Rosenberg E, Raymundo L, Smith G, Weil E, Willis B (2007) Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20:172–195

    Article  Google Scholar 

  • Higuchi T, Agostini S, Estela B, Yoshinaga K, Suzuki T, Nakano Y, Fujimura H, Suzuki Y (2013) Bacterial enhancement of bleaching and physiological impacts on the coral Montipora digitata. J Exp Mar Bio Ecol 440:54–60

    Article  Google Scholar 

  • Hughes T, Baird A, Bellwood D, Card M, Connolly S, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson J, Kleypas J, Lough J, Marshall P, Nystrom M, Palumbi J, Pandolfi J, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  PubMed  CAS  Google Scholar 

  • Jokiel P (1987) Ecology, biogeography and evolution of corals in Hawaii. Trends Ecol Evol 2:179–182

    Article  PubMed  CAS  Google Scholar 

  • Jokiel P (2004) Temperature stress and coral bleaching. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin, pp 401–425

    Chapter  Google Scholar 

  • Jokiel P, Brown E (2004) Global warming, regional trends and inshore environmental conditions influence coral bleaching in Hawaii. Glob Chang Biol 10:1627–1641

    Article  Google Scholar 

  • Jones R, Kildea T, Hoegh-Guldberg O (1999) PAM chlorophyll fluorometry: a new in situ technique for stress assessment in scleractinian corals, used to examine the effects of cyanide from cyanide fishing. Mar Pollut Bull 38:864–874

    Article  CAS  Google Scholar 

  • Kolinski S, Cox E (2003) An update on modes and timing of gamete and planula release in Hawaiian Scleractinian corals with implications for conservation and management. Pacific Sci 57:17–27

    Article  Google Scholar 

  • LaJeunesse T, Thornhill D, Cox E, Stanton F, Fitt W, Schmidt G (2004) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23:596–603

    Google Scholar 

  • Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192

    Article  Google Scholar 

  • Little A, van Oppen M, Willis B (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494

    Article  PubMed  CAS  Google Scholar 

  • Littman R, Willis B, Bourne D (2009) Bacterial communities of juvenile corals infected with different Symbiodinium (dinoflagellate) clades. Mar Ecol Prog Ser 389:45–59

    Article  Google Scholar 

  • Marshall P, Baird A (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral reefs 19:155–163

    Article  Google Scholar 

  • Mieog J, Olsen J, Berkelmans R, Bleuler-Martinez S, Willis B, van Oppen M (2009) The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS one 4:e6364

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Miller J, Muller E, Rogers C, Waara R, Atkinson A, Whelan KRT, Patterson M, Witcher B (2009) Coral disease following massive bleaching in 2005 causes 60% decline in coral cover on reefs in the US Virgin Islands. Coral Reefs 28:925–937

    Article  Google Scholar 

  • Muller E, Rogers C, Spitzack A, Van Woesik R (2008) Bleaching increases likelihood of disease on Acropora palmata (Lamarck) in Hawksnest Bay, St John, US Virgin Islands. Coral Reefs 27:191–195

    Article  Google Scholar 

  • Muller EM, van Woesik R (2014) Genetic susceptibility, colony size, and water temperature drive white-pox disease on the coral Acropora palmata. PLoS one 9:e110759

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Padilla-Gamino J, Pochon X, Bird C, Concepcion G, Gates R (2012) From parent to gamete: vertical transmission of Symbiodinium (Dinophyceae) ITS2 sequence assemblages in the reef building coral Montipora capitata. PLoS one 7:e38440

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Palmer CV, Bythell JC, Willis BL (2010) Levels of immunity parameters underpin bleaching and disease susceptibility of reef corals. FASEB J 24:1935–1946

    Article  PubMed  CAS  Google Scholar 

  • Rinkevich B (1996) Do reproduction and regeneration in damaged corals compete for energy allocation? Mar Ecol Prog Ser 143:297–302

    Article  Google Scholar 

  • Rouzé H, Lecellier G, Saulnier D, Berteaux-Lecellier V (2016) Symbiodinium clades A and D differentially predispose Acropora cytherea to disease and Vibrio spp. colonization. Ecol Evol 6:560–572

    Article  PubMed  PubMed Central  Google Scholar 

  • Rowan R (2004) Coral bleaching: thermal adaptation in reef coral symbionts. Nature 430:742

    Article  PubMed  CAS  Google Scholar 

  • Rowan R, Powers D (1991a) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar Ecol Prog Ser 71:65–73

    Article  CAS  Google Scholar 

  • Rowan R, Powers D (1991b) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251:1348–1351

    Article  PubMed  CAS  Google Scholar 

  • Salih A, Larkum A, Cox G, Kühl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408:850–853

    Article  PubMed  CAS  Google Scholar 

  • Santos SR, Taylor DJ, Kinzie RA III, Hidaka M, Sakai K, Coffroth MA (2002) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S) rDNA sequences. Mol Phylogenet Evol 23:97–111

    Article  PubMed  CAS  Google Scholar 

  • Sheridan C, Grosjean P, Leblud J, Palmer C, Kushmaro A, Eeckhaut I (2014) Sedimentation rapidly induces an immune response and depletes energy stores in a hard coral. Coral Reefs 33:1067–1076

    Article  Google Scholar 

  • Shore-Maggio A, Runyon C, Ushijima B, Aeby G, Callahan S (2015) Differences in bacterial community structure in two color morphs of the Hawaiian reef coral, Montipora capitata. Appl Environ Microbiol 81:7312–7318

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stat M, Morris E, Gates R (2008) Functional diversity in coral-dinoflagellate symbiosis. Proc Natl Acad Sci USA 105:9256–9261

    Article  PubMed  PubMed Central  Google Scholar 

  • Stearns S (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268

    Article  Google Scholar 

  • Stimson J (1987) Location, quantity, and rate of change in quantity of lipids in tissue of Hawaiian hermatypic corals. Bull Mar Sci 41:889–904

    Google Scholar 

  • Stimson J (1997) The annual cycle of density of zooxanthellae in the tissues of field and laboratory-held Pocillopora damicornis (Linnaeus). J Exp Mar Bio Ecol 214:35–48

    Article  Google Scholar 

  • Sutherland KP, Porter JW, Torres C (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Mar Ecol Prog Ser 266:273–302

    Article  Google Scholar 

  • Tarrant A, Atkinson M, Atkinson S (2004) Effects of steroidal estrogens on coral growth and reproduction. Mar Ecol Prog Ser 269:121–129

    Article  CAS  Google Scholar 

  • Toller W, Rowan R, Knowlton N (2001) Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biol Bull 201:360–373

    Article  PubMed  CAS  Google Scholar 

  • Ulstrup K, Berkelmans R, Ralph P, van Oppen M (2006) Variation in bleaching sensitivity of two coral species across a latitudinal gradient on the Great Barrier Reef: the role of zooxanthellae. Mar Ecol Prog Ser 314:135–148

    Article  Google Scholar 

  • Ushijima B, Smith A, Aeby GS, Callahan SM (2012) Vibrio owensii Induces the tissue loss disease Montipora white syndrome in the Hawaiian Reef Coral Montipora capitata. PLoS ONE 7:e46717

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ushijima B, Videau P, Burger AH, Shore-Maggio A, Runyon CM, Sudek M, Aeby GS, Callahan SM (2014) Vibrio coralliilyticus strain OCN008 is an etiological agent of acute Montipora white syndrome. Appl Environ Microbiol 80:2102–2109

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vargas-Ángel B (2009) Coral health and disease assessment in the US Pacific remote island areas. Bull Mar Sci 84:211–227

    Google Scholar 

  • Vega Thurber R, Burkepile D, Fuchs C, Shantz A, Mcminds R, Zaneveld J (2014) Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Glob Chang Biol 20:544–554

    Article  PubMed  Google Scholar 

  • Vollmer S, Kline D (2008) Natural disease resistance in threatened staghorn corals. PLoS ONE 3:e3718

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Work T, Russell R, Aeby G (2012) Tissue loss (white syndrome) in the coral Montipora capitata is a dynamic disease with multiple host responses and potential causes. Proc R Soc B 279:4334–4341

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This project was supported by NSF Grant OCE-0961814. We would like to thank Dr. Fenny Cox for her advice with reproductive, growth rate, and thermal tolerance experiments. We would like to thank Christina Runyon, Helena Eitel, and a host of other volunteers for assistance with field surveys, reproduction experiments, and growth rate experiments. The authors declare no conflicts of interest.

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Correspondence to Amanda Shore-Maggio.

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Shore-Maggio, A., Callahan, S.M. & Aeby, G.S. Trade-offs in disease and bleaching susceptibility among two color morphs of the Hawaiian reef coral, Montipora capitata. Coral Reefs 37, 507–517 (2018). https://doi.org/10.1007/s00338-018-1675-0

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