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2019 | OriginalPaper | Chapter

3. Ecophysiology of Reef-Building Corals in the Red Sea

Authors : Maren Ziegler, Anna Roik, Till Röthig, Christian Wild, Nils Rädecker, Jessica Bouwmeester, Christian R. Voolstra

Published in: Coral Reefs of the Red Sea

Publisher: Springer International Publishing

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Abstract

The Red Sea is one of the warmest and most saline seas on the planet. Yet, scleractinian corals have managed to flourish under these distinct conditions supporting one of the largest networks of coral reef ecosystems worldwide. Here, we summarize current knowledge on the ecophysiology of reef-building corals gained from 60 years of research in the Red Sea starting from insights in the 1960s to the most recent studies of the past few years. We provide a brief overview over seasonal dynamics and environmental gradients in the Red Sea that are used to study ecophysiological processes of corals under changing environmental and extreme conditions (i.e., temperature, salinity, nutrient, and light availability). We then focus on how this environmental variability shapes the central processes of coral physiology in the Red Sea covering the topics of photosynthesis, calcification, nutrient cycling, and reproduction. We continue by reporting the first physiological measurements of Red Sea deep-sea corals. Last, we discuss how, through the integration of traditional methods with recent developments in the omics field and model systems, we are now beginning to understand the complexity of processes that contribute to the ecological success of corals under these variable conditions. This synthesis may serve as a basis for future studies that aim to contribute to a better understanding of the impacts of environmental change on coral reefs in the Red Sea and the rest of the world.

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Al-Horani FA, Al-Moghrabi SM, de Beer D (2003) Microsensor study of photosynthesis and calcification in the scleractinian coral, Galaxea fascicularis: active internal carbon cycle. J Exp Mar Biol Ecol 288:1–15CrossRef

Allemand D, Tambutté É, Zoccola D, Tambutté S (2011) Coral calcification, cells to reefs. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht, pp 119–150CrossRef

Al-Lihaibi SS, Al-Sofyani AA, Niaz GR (1998) Chemical composition of corals in Saudi Red Sea Coast. Oceanol Acta 21:495–501CrossRef

Alongi DM, Trott LA, Møhl M (2011) Strong tidal currents and labile organic matter stimulate benthic decomposition and carbonate fluxes on the southern Great Barrier Reef shelf. Cont Shelf Res 31:1384–1395CrossRef

Al-Sofyani A (1994) Variation in Evels and location of lipids in corals tissue of the ROPME Sea area. JKAU Mar Sci 5:121–131CrossRef

Aranda M, Li Y, Liew YJ, Baumgarten S, Simakov O, Wilson M, Piel J, Ashoor H, Bougouffa S, Bajic VB, Ryu T, Ravasi T, Bayer T, Micklem G, Kim H, Bhak J, LaJeunesse TC, Voolstra CR (2016) Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Sci Rep 6:39734CrossRef

Auld JR, Agrawal AA, Relyea RA (2010) Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc R Soc Lond B Biol Sci 277:503–511CrossRef

Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, Wallace CC, Willis BL (1986) Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef. Mar Biol 90:379–394CrossRef

Badran MI (2001) Dissolved oxygen, chlorophyll a and nutrients: seasonal cycles in waters of the Gulf of Aquaba, Red Sea. Aquat Ecosyst Health Manage 4:139–150CrossRef

Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Evol Syst 40:551–571CrossRef

Bang C, Dagan T, Deines P, Dubilier N, Duschl WJ, Fraune S, Hentschel U, Hirt H, Hülter N, Lachnit T, Picazo D, Pita L, Pogoreutz C, Rädecker N, Saad MM, Schmitz RA, Schulenburg H, Voolstra CR, Weiland-Bräuer N, Ziegler M, Bosch TCG (2018) Metaorganisms in extreme environments: do microbes play a role in organismal adaptation? Zoology 127:1–19CrossRef

Basaham AS, Al-Sofyani AA (2007) Observations based on the variation in alkaline earth elements’ (Ca, Mg, Ba and Sr) distribution in the Porites Skeleton of the central west coast of Saudi Arabia. JKAU Mar Sci 18:213–223CrossRef

Bastidas C, Cróquer A, Zubillaga AL, Ramos R, Kortnik V, Weinberger C, Márquez LM (2005) Coral mass- and split-spawning at a coastal and an offshore Venezuelan reefs, southern Caribbean. Hydrobiologia 541:101–106CrossRef

Baumgarten S, Simakov O, Esherick LY, Liew YJ, Lehnert EM, Michell CT, Li Y, Hambleton EA, Guse A, Oates ME, Gough J, Weis VM, Aranda M, Pringle JR, Voolstra CR (2015) The genome of Aiptasia, a sea anemone model for coral symbiosis. Proc Natl Acad Sci 112:11893–11898CrossRef

Bellworthy J, Fine M (2017) Beyond peak summer temperatures, branching corals in the Gulf of Aqaba are resilient to thermal stress but sensitive to high light. Coral Reefs 36(4):1071–1082CrossRef

Bernstein WN, Hughen KA, Langdon C, McCorkle DC, Lentz SJ (2016) Environmental controls on daytime net community calcification on a Red Sea reef flat. Coral Reefs 35:697–711CrossRef

Bhattacharya D, Agrawal S, Aranda M, Baumgarten S, Belcaid M, Drake J, Erwin D, Foret S, Gates RD, Gruber DF, Hanna B, Lesser MP, Levy O, Liew YJ, MacManes M, Mass T, Medina M, Mehr S, Meyer E, Price DC, Putnam HM, Qiu H, Shinzato C, Shoguchi E, Stokes AJ, Tambutte S, Tchernov D, Voolstra CR, Wagner N, Walker CW, Weber APM, Weiss V, Zelzion E, Zoccola D, Falkowski PG (2016) Comparative genomics explains the evolutionary success of reef-forming corals. eLife 5:e13288CrossRef

Bongiorni L, Shafir S, Angel D, Rinkevich B (2003) Survival, growth and gonad development of two hermatypic corals subjected to in situ fish-farm nutrient enrichment. Mar Ecol Prog Ser 253:137–144CrossRef

Bouwmeester J, Berumen ML (2015) High reproductive synchrony of Acropora (Anthozoa: Scleractinia) in the Gulf of Aqaba, Red Sea. F1000Research 4:2

Bouwmeester J, Berumen ML, Baird AH (2011a) Daytime broadcast spawning of Pocillopora verrucosa on coral reefs of the Central Red Sea. Galaxea J Coral Reef Stud 13:23–24CrossRef

Bouwmeester J, Khalil MT, De La Torre P, Berumen ML (2011b) Synchronous spawning of Acropora in the Red Sea. Coral Reefs 30:1011–1011CrossRef

Bouwmeester J, Baird AH, Chen CJ, Guest JR, Vicentuan KC, Voolstra CR, Berumen ML (2015) Multi-species spawning synchrony within scleractinian coral assemblages in the Red Sea. Coral Reefs 34:65–77. erratum 34:79–79CrossRef

Bouwmeester J, Gatins R, Giles EC, Sinclair-Taylor TH, Berumen ML (2016) Spawning of coral reef invertebrates and a second spawning season for scleractinian corals in the central Red Sea. Invertebr Biol 135:273–284CrossRef

Brüwer JD, Voolstra CR (2018) First insight into the viral community of the cnidarian model metaorganism Aiptasia using RNA-Seq data. PeerJ 6:e4449CrossRef

Burriesci MS, Raab TK, Pringle JR (2012) Evidence that glucose is the major transferred metabolite in dinoflagellate – cnidarian symbiosis. J Exp Biol 215:3467–3477CrossRef

Cantin NE, Cohen AL, Karnauskas KB, Tarrant AM, McCorkle DC (2010) Ocean warming slows coral growth in the central Red Sea. Science 329:322–325CrossRef

Cardini U, Bednarz VN, Naumann MS, van Hoytema N, Rix L, Foster RA, Al-Rshaidat MMD, Wild C (2015) Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions. Proc R Soc Lond Ser B Biol Sci 282:20152257CrossRef

Cardini U, Bednarz VN, van Hoytema N, Rovere A, Naumann MS, Al-Rshaidat MMD, Wild C (2016) Budget of primary production and dinitrogen fixation in a highly seasonal Red Sea Coral Reef. Ecosystems 19(5):771–785

Cook CB, Davy SK (2001) Are free amino acids responsible for the ‘host factor’ effects on symbiotic zooxanthellae in extracts of host tissue? Hydrobiologia 461:71–78CrossRef

Carricart-Ganivet JP (2004) Sea surface temperature and the growth of the West Atlantic reef-building coral Montastraea annularis. J Exp Mar Biol Ecol 302:249–260CrossRef

Clausen CD, Roth AA (1975) Effect of temperature and temperature adaptation on calcification rate in the hermatypic coral Pocillopora damicornis. Mar Biol 33:93–100CrossRef

Comeau S, Edmunds PJ, Spindel NB, Carpenter RC (2013) The responses of eight coral reef calcifiers to increasing partial pressure of CO₂ do not exhibit a tipping point. Limnol Oceanogr 58:388–398CrossRef

Comeau S, Carpenter RC, Edmunds PJ (2014a) Effects of irradiance on the response of the coral Acropora pulchra and the calcifying alga Hydrolithon reinboldii to temperature elevation and ocean acidification. J Exp Mar Biol Ecol 453:28–35CrossRef

Comeau S, Carpenter RC, Nojiri Y, Putnam HM, Sakai K, Edmunds PJ (2014b) Pacific-wide contrast highlights resistance of reef calcifiers to ocean acidification. Proc R Soc Lond B Biol Sci 281:20141339CrossRef

Cook CB, Davy SK (2001) Are free amino acids responsible for the ‘host factor’ effects on symbiotic zooxanthellae in extracts of host tissue? Hydrobiologia 461:71–78CrossRef

Couce E, Ridgwell A, Hendy EJ (2012) Environmental controls on the global distribution of shallow-water coral reefs. J Biogeogr 39:1508–1523CrossRef

Crossland CJ (1984) Seasonal variations in the rates of calcification and productivity in the coral Acropora formosa on a high-latitude reef. Mar Ecol Prog Ser 15:135–140CrossRef

D’Angelo C, Wiedenmann J (2014) Impacts of nutrient enrichment on coral reefs: new perspectives and implications for coastal management and reef survival. Curr Opin Environ Sustain 7:82–93CrossRef

Daniels C, Baumgarten S, Yum LK, Michell CT, Bayer T, Arif C, Roder C, Weil E, Voolstra CR (2015) Metatranscriptome analysis of the reef-building coral Orbicella faveolata indicates holobiont response to coral disease. Front Mar Sci 2:62CrossRef

Davies AJ, Wisshak M, Orr JC, Murray Roberts J (2008) Predicting suitable habitat for the cold-water coral Lophelia pertusa (Scleractinia). Deep-Sea Res I Oceanogr Res Pap 55:1048–1062CrossRef

DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81CrossRef

Dubinsky Z, Jokiel PL (1994) Ratio of energy and nutrient fluxes regulates symbiosis between zooxanthellae and corals. Pac Sci 48:313–324

Dubinsky Z, Stambler N (2009) Photoacclimation processes in phytoplankton: mechanisms, consequences, and applications. Aquat Microb Ecol 56:163–176CrossRef

Dubinsky Z, Stambler N, Ben-Zion M, McCloskey LR, Muscatine L, Falkowski PG (1990) The effect of external nutrient resources on the optical properties and photosynthetic efficiency of Stylophora pistillata. Proc R Soc Lond Ser B Biol Sci 239:231–246CrossRef

Edwards AJ (1987) Climate and oceanography. In: Edwards AJ, Head SM (eds) Red Sea. Pergamon Press & International Union for Conservation of Nature and Natural Resources, Oxford, pp 45–69CrossRef

Enriquez S, Mendez ER, Iglesias-Prieto R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Oceanogr 50:1025–1032CrossRef

Eyal-Shaham L, Eyal G, Tamir R, Loya Y (2016) Reproduction, abundance and survivorship of two Alveopora spp. in the mesophotic reefs of Eilat, Red Sea. Sci Rep 6:20964CrossRef

Fadlallah Y (1985) Reproduction in the coral Pocillopora verrucosa on the reefs adjacent to the industrial city of Yanbu (Red Sea, Saudi Arabia). Proceedings of the Fifth International Coral Reef Congress, Tahiti, pp 313–318

Fadlallah YH, Lindo RT (1988) Contrasting cycles of reproduction in Stylophora pistillata from the Red Sea and the Arabian Gulf, with emphasis on temperature. 6th International Coral Reef Symposium, Australia, pp 225–230

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

Falkowski PG, Dubinsky Z (1981) Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eilat. Nature 289:172–174CrossRef

Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and the bioenergetics of a symbiotic coral. Bioscience 34:705–709CrossRef

Falkowski PG, Jokiel PL, Kinzie RA (1990) Irradiance and corals. In: Dubinsky Z (ed) Ecosystems of the world. Coral Reefs. Elsevier, Amsterdam, pp 89–108

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

Ferrier-Pagès C, Gattuso JP, Dallot S, Jaubert J (2000) Effect of nutrient enrichment on growth and photosynthesis of the zooxanthellate coral Stylophora pistillata. Coral Reefs 19:103–113CrossRef

Fine M, Gildor H, Genin A, (2013) A coral reef refuge in the Red Sea. Global Change Biology 19 (12):3640–3647

Foster T, Short JA, Falter JL, Ross C, McCulloch MT (2014) Reduced calcification in Western Australian corals during anomalously high summer water temperatures. J Exp Mar Biol Ecol 461:133–143CrossRef

Freiwald A, Fosså JH, Grehan A, Koslow T, Roberts JM (2004) Cold-water coral reefs. UNEP-WCMC, Cambridge, p 84

Freudenthal HD (1962) Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a Zooxanthella: taxonomy, life cycle, and morphology. J Protozool 9:45–52CrossRef

Furby KA, Bouwmeester J, Berumen ML (2013) Susceptibility of Central Red Sea corals during a major bleaching event. Coral Reefs 32:505–513CrossRef

Gates RD, Hoegh-Guldberg O, McFall-Ngai MJ, Bil KY, Muscatine L (1995) Free amino acids exhibit anthozoan “host factor” activity: they induce the release of photosynthate from symbiotic dinoflagellates in vitro. Proc Natl Acad Sci 92:7430–7434CrossRef

Gattuso J-P, Allemand D, Frankignoulle M (1999) Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. Am Zool 39:160–183CrossRef

Gegner HM, Ziegler M, Rädecker N, Buitrago-López C, Aranda M, Voolstra CR (2017) High salinity conveys thermotolerance in the coral model Aiptasia. Biol Open 6:1943–1948CrossRef

Gilmour JP, Smith LD, Heyward AJ, Baird AH, Pratchett MS (2013) Recovery of an isolated coral reef system following severe disturbance. Science 340:69–71CrossRef

Gilmour JP, Underwood JN, Howells EJ, Gates E, Heyward AJ (2016) Biannual spawning and temporal reproductive isolation in Acropora corals. PLoS One 11:e0150916CrossRef

Gladstone W (1996) Unique annual aggregation of longnose parrotfish (Hipposcarus harid) at Farasan Island (Saudi Arabia, Red Sea). Copeia 1996:483–485

Glynn PW, Riegl B, Purkis S, Kerr JM, Smith TB (2015) Coral reef recovery in the Galápagos Islands: the northernmost islands (Darwin and Wenman). Coral Reefs 34:421–436CrossRef

Goreau TF, Goreau NI (1959) The physiology of skeleton formation in corals. II. Calcium deposition by hermatypic corals under various conditions in the reef. Biol Bull 117:239–250CrossRef

Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189CrossRef

Grover R, Maguer JF, Reynaud-Vaganay S, Ferrier-Pages C (2002) Uptake of ammonium by the scleractinian coral Stylophora pistillata: effect of feeding, light, and ammonium concentrations. Limnol Oceanogr 47:782–790CrossRef

Grover R, Maguer J-F, Allemand D, Ferrier-Pages C (2003) Nitrate uptake in the scleractinian coral Stylophora pistillata. Limnol Oceanogr 48:2266–2274CrossRef

Guest JR, Baird AH, Goh BPL, Chou LM (2012) Sexual systems in scleractinian corals: an unusual pattern in the reef-building species Diploastrea heliopora. Coral Reefs 31:705–713CrossRef

Haas AF, Wild C (2010) Composition analysis of organic matter released by cosmopolitan coral reef-associated green algae. Aquat Biol 10:131–138CrossRef

Hanafy MH, Aamer MA, Habib M, Rouphael AB, Baird AH (2010) Synchronous reproduction of corals in the Red Sea. Coral Reefs 29:119–124CrossRef

Hanna RG, Muir GL (1990) Red Sea corals as biomonitors of trace metal pollution. Environ Monit Assess 14:211–222CrossRef

Hansen T (1964) Arabia Felix. The Danish expedition of 1761–1767. Collins, London

Harland AD, Navarro JC, Spencer Davies P, Fixter LM (1993) Lipids of some Caribbean and Red Sea corals: total lipid, wax esters, triglycerides and fatty acids. Mar Biol 117:113–117CrossRef

Harrison P, Wallace C (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Ecosystems of the world. Elsevier, Amsterdam, pp 133–207

Hatcher BG (1990) Coral reef primary productivity: a hierarchy of pattern and process. Trends Ecol Evol 5:149–155CrossRef

Head SM (1987) Introduction. In: Edwards AJ, Head SM (eds) Red Sea. Pergamon Press & International Union for Conservation of Nature and Natural Resources, Oxford, pp 1–21

Hibino K, van Woesik R (2000) Spatial differences and seasonal changes of net carbonate accumulation on some coral reefs of the Ryukyu Islands, Japan. J Exp Mar Biol Ecol 252:1–14CrossRef

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

Hoegh-Guldberg O, McCloskey LR, Muscatine L (1987) Expulsion of zooxanthellae by symbiotic cnidarians from the Red Sea. Coral Reefs 5:201–204CrossRef

Hooper LV, Littman DR, Macpherson AJ (2012) Interactions between the microbiota and the immune system. Science 336:1268–1273CrossRef

Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17CrossRef

Hoytema N, Bednarz VN, Cardini U, Naumann MS, Al-Horani FA, Wild C (2016) The influence of seasonality on benthic primary production in a Red Sea coral reef. Mar Biol 163:1–14CrossRef

Hume BCC, Voolstra CR, Arif C, D’Angelo C, Burt JA, Eyal G, Loya Y, Wiedenmann J (2016) Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proc Natl Acad Sci 113:4416–4421CrossRef

Iglesias-Prieto R, Beltran VH, LaJeunesse TC, Reyes-Bonilla H, Thome PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc R Soc Lond Ser B Biol Sci 271:1757–1763CrossRef

Johannes RE, Coles SL, Kuenzel NT (1970) The role of zooplankton in the nutrition of some scleractinian corals. Limnol Oceanogr 15:579–586CrossRef

Kahng SE, Hochberg EJ, Apprill A, Wagner D, Luck DG, Perez D, Bidigare RR (2012) Efficient light harvesting in deep-water zooxanthellate corals. Mar Ecol Prog Ser 455:65–77CrossRef

Kahng SE, Copus JM, Wagner D (2014) Recent advances in the ecology of mesophotic coral ecosystems (MCEs). Curr Opin Environ Sustain 7:72–81CrossRef

Kaniewska P, Magnusson SH, Anthony KRN, Reef R, Kühl M, Hoegh-Guldberg O (2011) Importance of macro-versus microstructure in modulating light levels inside coral colonies. J Phycol 47:846–860CrossRef

Kaniewska P, Alon S, Karako-Lampert S, Hoegh-Guldberg O, Levy O (2015) Signaling cascades and the importance of moonlight in coral broadcast mass spawning. eLife 4:e09991CrossRef

Keeling RF, Körtzinger A, Gruber N (2010) Ocean deoxygenation in a warming world. Annu Rev Mar Sci 2:199–229CrossRef

Keith SA, Maynard JA, Edwards AJ, Guest JR, Bauman AG, van Hooidonk R, Heron SF, Berumen ML, Bouwmeester J, Piromvaragorn S, Rahbek C, Baird AH (2016) Coral mass spawning predicted by rapid seasonal rise in ocean temperature. Proc R Soc Lond Ser B Biol Sci 283(1830):20160011CrossRef

Kleypas JA, McManus JW, Menez LAB (1999) Environmental limits to coral reef development: where do we draw the line? Am Zool 39:146–159CrossRef

Kleypas JA, Danabasoglu G, Lough JM (2008) Potential role of the ocean thermostat in determining regional differences in coral reef bleaching events. Geophys Res Lett 35:L03613CrossRef

Kopp C, Domart-Coulon I, Escrig S, Humbel BM, Hignette M, Meibom A (2015) Subcellular investigation of photosynthesis-driven carbon assimilation in the symbiotic reef coral Pocillopora damicornis. MBio 6:e02299–e02214CrossRef

Kotb MMA (2001) Growth rates of three reef-building coral species in the Northern Red Sea, Egypt. Egypt J Aquat Biol Fish 5:165–185CrossRef

Kramarsky-Winter E, Loya Y (1998) Reproductive strategies of two fungiid corals from the northern Red Sea: environmental constraints? Mar Ecol Prog Ser 174:175–182CrossRef

Krueger T, Horwitz N, Bodin J, Giovani M-E, Escrig S, Meibom A, Fine M (2017) Common reef-building coral in the northern Red Sea resistant to elevated temperature and acidification. R Soc Open Sci 4(5):170038CrossRef

Kuffner IB, Hickey TD, Morrison JM (2013) Calcification rates of the massive coral Siderastrea siderea and crustose coralline algae along the Florida keys (USA) outer-reef tract. Coral Reefs 32:987–997CrossRef

Kürten B, Al-Aidaroos AM, Struck U, Khomayis HS, Gharbawi WY, Sommer U (2014) Influence of environmental gradients on C and N stable isotope ratios in coral reef biota of the Red Sea, Saudi Arabia. J Sea Res 85:379–394CrossRef

LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570–2580. https://doi.org/10.1016/j.cub.2018.07.008 CrossRef

Lampert-Karako S, Stambler N, Katcoff DJ, Achituv Y, Dubinsky Z, Simon-Blecher N (2008) Effects of depth and eutrophication on the zooxanthella clades of Stylophora pistillata from the Gulf of Eilat (Red Sea). Aquat Conserv Mar Freshwat Ecosyst 18:1039–1045CrossRef

Lin S, Cheng S, Song B, Zhong X, Lin X, Li W, Li L, Zhang Y, Zhang H, Ji Z, Cai M, Zhuang Y, Shi X, Lin L, Wang L, Wang Z, Liu X, Yu S, Zeng P, Hao H, Zou Q, Chen C, Li Y, Wang Y, Xu C, Meng S, Xu X, Wang J, Yang H, Campbell DA, Sturm NR, Dagenais-Bellefeuille S, Morse D (2015) The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science 350:691–694CrossRef

Lough JM, Barnes DJ (2000) Environmental controls on growth of the massive coral Porites. J Exp Mar Biol Ecol 245:225–243CrossRef

Loya Y, Kramarsky-Winter E (2003) In situ eutrophication caused by fish farms in the northern Gulf of Eilat (Aqaba) is beneficial for its coral reefs: a critique. Mar Ecol Prog Ser 261:299–303CrossRef

Loya Y, Lubinevsky H, Rosenfeld M, Kramarsky-Winter E (2004) Nutrient enrichment caused by in situ fish farms at Eilat, Red Sea is detrimental to coral reproduction. Mar Pollut Bull 49:344–353CrossRef

Loya Y, Rosenfeld M, Kramarsky-Winter E (2005) Nutrient enrichment and coral reproduction: empty vessels make the most sound (response to a critique by B. Rinkevich). Mar Pollut Bull 50:114–118CrossRef

Macdonald AH, Sampayo E, Ridgway T, Schleyer M (2008) Latitudinal symbiont zonation in Stylophora pistillata from Southeast Africa. Mar Biol 154:209–217CrossRef

Marenzeller EV (1907) Expedition SM Schiff “Pola” in das Rote Meer, nördliche und südliche Hälfte 1895

Markell DA, Trench RK (1993) Macromolecules exuded by symbiotic dinoflagellates in culture: amino acids and sugar composition. J Phycol 29:64–68CrossRef

Marshall AT, Clode P (2004) Calcification rate and the effect of temperature in a zooxanthellate and an azooxanthellate scleractinian reef coral. Coral Reefs 23:218–224

Mass T, Einbinder S, Brokovich E, Shashar N, Vago R, Erez J, Dubinsky Z (2007) Photoacclimation of Stylophora pistillata to light extremes: metabolism and calcification. Mar Ecol Prog Ser 334:93–102CrossRef

van der Merwe R, Röthig T, Voolstra CR, Ochsenkühn MA, Lattemann S, Amy GL (2014) High salinity tolerance of the Red Sea coral Fungia granulosa under desalination concentrate discharge conditions: an in situ photophysiology experiment. Front Mar Sci 1:58

McCloskey LR, Muscatine L (1984) Production and respiration in the Red Sea coral Stylophora pistillata as a function of depth. Proc R Soc Lond Ser B Biol Sci 222:215–230CrossRef

McCulloch M, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Chang 2:623–627CrossRef

McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci 110:3229–3236CrossRef

Mohamed T, Kotb M, Ghobashy A, Deek M (2007) Reproduction and growth rate of two scleractinian coral species in the northern Red Sea, Egypt. Egypt J Aquat Res 33:70–86

Monroe A, Ziegler M, Roik A, Röthig T, Hardestine R, Emms M, Jensen T, Voolstra CR, Berumen M (2018) In situ observations of coral bleaching in the central Saudi Arabian Red Sea during the 2015/2016 global coral bleaching event. PLoS One 13(4):e0195814CrossRef

Moran NA, Yun Y (2015) Experimental replacement of an obligate insect symbiont. Proc Natl Acad Sci 112:2093–2096CrossRef

Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky Z (ed) Ecosystems of the world. Coral reefs. Elsevier, Amsterdam, pp 75–87

Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460CrossRef

Naumann MS, Richter C, Mott C, El-Zibdah M, Manasrah R, Wild C (2012) Budget of coral-derived organic carbon in a fringing coral reef of the Gulf of Aqaba, Red Sea. J Mar Syst 105-108:20–29CrossRef

Naumann MS, Orejas C, Ferrier-Pagès C (2014) Species-specific physiological response by the cold-water corals Lophelia pertusa and Madrepora oculata to variations within their natural temperature range. Deep-Sea Res II Top Stud Oceanogr 99:36–41CrossRef

Neave MJ, Michell CT, Apprill A, Voolstra CR (2014) Whole-genome sequences of three symbiotic Endozoicomonas strains. Genome Announc 2:e00802–e00814CrossRef

Neave MJ, Michell CT, Apprill A, Voolstra CR (2017) Endozoicomonas genomes reveal functional adaptation and plasticity in bacterial strains symbiotically associated with diverse marine hosts. Sci Rep 7:40579CrossRef

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 30:1089–1100CrossRef

Nir O, Gruber DF, Shemesh E, Glasser E, Tchernov D (2014) Seasonal Mesophotic coral bleaching of Stylophora pistillata in the northern Red Sea. PLoS One 9:e84968CrossRef

Ochsenkühn MA, Röthig T, D’Angelo C, Wiedenmann J, Voolstra CR (2017) The role of floridoside in osmoadaptation of coral-associated algal endosymbionts to high-salinity conditions. Sci Adv 3:e1602047CrossRef

Oren OH (1962) The Israel South Red Sea expedition. Nature 194:1134–1137CrossRef

Osman EO, Smith DJ, Ziegler M, Kürten B, Conrad C, El-Haddad KM, Voolstra CR, Suggett DJ (2018) Thermal refugia against coral bleaching throughout the northern Red Sea. Glob Chang Biol 24:1354–1013CrossRef

Pernice M, Meibom A, Van Den Heuvel A, Kopp C, Domart-Coulon I, Hoegh-Guldberg O, Dove S (2012) A single-cell view of ammonium assimilation in coral-dinoflagellate symbiosis. ISME J 6:1314–1324CrossRef

Pogoreutz C, Rädecker N, Cárdenas A, Gärdes A, Voolstra CR, Wild C (2017) Sugar enrichment provides evidence for a role of nitrogen fixation in coral bleaching. Glob Chang Biol 23:3838–3848CrossRef

Pogoreutz C, Rädecker N, Cárdenas A, Gärdes A, Wild C, Voolstra CR (2018) Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome. Ecol Evol 8:2240–2252

Pörtner HO (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol A Mol Integr Physiol 132:739–761CrossRef

Pörtner H-O (2010) Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213:881–893CrossRef

Price ARG, Jobbins G, Shepherd ARD, Ormond RFG (1998) An integrated environmental assessment of the Red Sea coast of Saudi Arabia. Environ Conserv 25:65–76CrossRef

Qurban MA, Krishnakumar PK, Joydas TV, Manikandan KP, Ashraf TTM, Quadri SI, Wafar M, Qasem A, Cairns SD (2014) In-situ observation of deep water corals in the northern Red Sea waters of Saudi Arabia. Deep-Sea Res I Oceanogr Res Pap 89:35–43CrossRef

Rädecker N, Pogoreutz C, Voolstra CR, Wiedenmann J, Wild C (2015) Nitrogen cycling in corals: the key to understanding holobiont functioning? Trends Microbiol 23:490–497CrossRef

Raitsos DE, Hoteit I, Prihartato PK, Chronis T, Triantafyllou G, Abualnaja Y (2011) Abrupt warming of the Red Sea. Geophys Res Lett 38:L14601CrossRef

Raitsos DE, Pradhan Y, Brewin RJ, Stenchikov G, Hoteit I (2013) Remote sensing the phytoplankton seasonal succession of the Red Sea. PLoS One 8:e64909CrossRef

Reaka-Kudla ML (1997) Global biodiversity of coral reefs: a comparison with rainforests. In: Reaka-Kudla ML, Wilson DE (eds) Biodiversity II: understanding and protecting our biological resources. Joseph Henry Press, Washington, DC, pp 83–108

Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E (2006) The coral probiotic hypothesis. Environ Microbiol 8:2068–2073CrossRef

Rinkevich B (2005) Nutrient enrichment and coral reproduction: between truth and repose (a critique of Loya et al.). Mar Pollut Bull 50:111–113. author reply 114–118CrossRef

Rinkevich B, Loya Y (1979) The reproduction of the Red Sea coral Stylophora pistillata. II. Synchronization in breeding and seasonality of planulae shedding. Mar Ecol Prog Ser 1:145–152CrossRef

Rinkevich B, Angel D, Shafir S, Bongiorni L (2003) ‘Fair is foul and foul is fair’: response to a critique. Mar Ecol Prog Ser 261:305–309

Roberts CM, McClean CJ, Veron JE, Hawkins JP, Allen GR, McAllister DE, Mittermeier CG, Schueler FW, Spalding M, Wells F, Vynne C, Werner TB (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295:1280–1284CrossRef

Roberts JM, Wheeler AJ, Freiwald A (2006) Reefs of the deep: the biology and geology of cold-water coral ecosystems. Science 312:543–547CrossRef

Robitzch V, Banguera-Hinestroza E, Sawall Y, Al-Sofyani A, Voolstra CR (2015) Absence of genetic differentiation in the coral Pocillopora verrucosa along environmental gradients of the Saudi Arabian Red Sea. Front Mar Sci 2:5CrossRef

Roder C, Berumen ML, Bouwmeester J, Papathanassiou E, Al-Suwailem A, Voolstra CR (2013) First biological measurements of deep-sea corals from the Red Sea. Sci Rep 3:2802CrossRef

Roder C, Bayer T, Aranda M, Kruse M, Voolstra CR (2015) Microbiome structure of the fungid coral Ctenactis echinata aligns with environmental differences. Mol Ecol 24:3501–3511CrossRef

Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10CrossRef

Roik A, Roder C, Röthig T, Voolstra CR (2015a) Spatial and seasonal reef calcification in corals and calcareous crusts in the Central Red Sea. Coral Reefs 35(2):1–13

Roik A, Röthig T, Ziegler M, Voolstra CR (2015b) Coral bleaching event in the central Red Sea. Mideast Coral Reef Soc Newsl 3:3

Roik A, Röthig T, Roder C, Müller PJ, Voolstra CR (2015c) Captive rearing of the deep-sea coral Eguchipsammia fistula from the Red Sea demonstrates remarkable physiological plasticity. PeerJ 3:e734

Roik A, Röthig T, Roder C, Ziegler M, Kremb SG, Voolstra CR (2016) Year-long monitoring of physico-chemical and biological variables provide a comparative baseline of coral reef functioning in the Central Red Sea. PLoS One 11:e0163939CrossRef

Roik A, Röthig T, Pogoreutz C, Saderne V, Voolstra CR (2018) Coral reef carbonate budgets and ecological drivers in the central Red Sea – a naturally high temperature and high total alkalinity environment. Biogeosciences 15:6277–6296CrossRef

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 5:355–362CrossRef

Ross CL, Falter JL, Schoepf V, McCulloch MT (2015) Perennial growth of hermatypic corals at Rottnest Island, Western Australia (32°S). PeerJ 3:e781CrossRef

Röthig T, Costa RM, Simona F, Baumgarten S, Torres AF, Radhakrishnan A, Aranda M, Voolstra CR (2016) Distinct bacterial communities associated with the coral model Aiptasia in aposymbiotic and symbiotic states with Symbiodinium. Front Mar Sci 3:234CrossRef

Röthig T, Ochsenkühn MA, Roik A, van der Merwe R, Voolstra CR (2016b) Long-term salinity tolerance is accompanied by major restructuring of the coral bacterial microbiome. Mol Ecol 25(6):1308–1323CrossRef

Röthig T, Yum LK, Kremb SG, Roik A, Voolstra CR (2017) Microbial community composition of deep-sea corals from the Red Sea provides insight into functional adaption to a unique environment. Sci Rep 7:44714CrossRef

Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral algal symbiosis. Proc Natl Acad Sci 92:2850–2853CrossRef

Sampayo EM, Franceschinis L, Hoegh-Guldberg O, Dove S (2007) Niche partitioning of closely related symbiotic dinoflagellates. Mol Ecol 16:3721–3733CrossRef

Sawall Y, Al-Sofyani A (2015) Biology of Red Sea corals: metabolism, reproduction, acclimatization, and adaptation. In: Rasul MAN, Stewart CFI (eds) The Red Sea: the formation, morphology, oceanography and environment of a young ocean basin. Springer, Berlin, Heidelberg, pp 487–509

Sawall Y, Al-Sofyani A, Banguera-Hinestroza E, Voolstra CR (2014) Spatio-temporal analyses of Symbiodinium physiology of the coral Pocillopora verrucosa along large-scale nutrient and temperature gradients in the Red Sea. PLoS One 9:e103179CrossRef

Sawall Y, Al-Sofyani A, Hohn S, Banguera-Hinestroza E, Voolstra CR, Wahl M (2015) Extensive phenotypic plasticity of a Red Sea coral over a strong latitudinal temperature gradient suggests limited acclimatization potential to warming. Sci Rep 5:8940CrossRef

Schlichter D, Fricke HW, Weber W (1986) Light harvesting by wavelength transformation in a symbiotic coral of the Red Sea twilight zone. Mar Biol 91:403–407CrossRef

Schneider K, Erez J (2006) The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol Oceanogr 51:1284–1293CrossRef

Schoepf V, Grottoli AG, Warner ME, Cai W-J, Melman TF, Hoadley KD, Pettay DT, Hu X, Li Q, Xu H, Wang Y, Matsui Y, Baumann JH (2013) Coral energy reserves and calcification in a high-CO₂ world at two temperatures. PLoS One 8:e75049CrossRef

Sheppard C, Price A, Roberts C (1992) Marine ecology of the Arabian region. Academic, London

Shlesinger Y, Loya Y (1985) Coral community reproductive patterns: red sea versus the Great Barrier Reef. Science 228:1333–1335CrossRef

Shlesinger Y, Goulet T, Loya Y (1998) Reproductive patterns of scleractinian corals in the northern Red Sea. Mar Biol 132:691–701CrossRef

Silverman J, Lazar B, Erez J (2007a) Community metabolism of a coral reef exposed to naturally varying dissolved inorganic nutrient loads. Biogeochemistry 84:67–82CrossRef

Silverman J, Lazar B, Erez J (2007b) Effect of aragonite saturation, temperature, and nutrients on the community calcification rate of a coral reef. J Geophys Res 112:C05004

Sorek M, Díaz-Almeyda EM, Medina M, Levy O (2014) Circadian clocks in symbiotic corals: the duet between Symbiodinium algae and their coral host. Mar Genomics 14:47–57CrossRef

Stambler N, Levy O, Vaki L (2008) Photosynthesis and respiration of hermatypic zooxanthellate Red Sea corals from 5-75-m depth. Isr J Plant Sci 56:45–53CrossRef

Steiner Z, Erez J, Shemesh A, Yam R, Katz A, Lazar B (2014) Basin-scale estimates of pelagic and coral reef calcification in the Red Sea and Western Indian Ocean. Proc Natl Acad Sci 111:16303–16308CrossRef

Sweeney AM, Boch CA, Johnsen S, Morse DE (2011) Twilight spectral dynamics and the coral reef invertebrate spawning response. J Exp Biol 214:770–777CrossRef

Tambutté S, Holcomb M, Ferrier-Pagès C, Reynaud S, Tambutté É, Zoccola D, Allemand D (2011) Coral biomineralization: from the gene to the environment. J Exp Mar Biol Ecol 408:58–78CrossRef

Thiel H (1987) Benthos of the deep Red Sea. In: Edwards AJ, Head SM (eds) Red Sea. Pergamon Press & International Union for Conservation of Nature and Natural Resources, Oxford, pp 112–127CrossRef

Todd PA (2008) Morphological plasticity in scleractinian corals. Biol Rev 83:315–337CrossRef

Tolosa I, Treignier C, Grover R, Ferrier-Pagès C (2011) Impact of feeding and short-term temperature stress on the content and isotopic signature of fatty acids, sterols, and alcohols in the scleractinian coral Turbinaria reniformis. Coral Reefs 30:763–774CrossRef

Tremaroli V, Backhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489:242–249CrossRef

van der Land J (ed) (2008) UNESCO-IOC Register of Marine Organisms (URMO). Available online at http://www.marinespecies.org/urmo

Van Woesik R, Lacharmoise F, Köksal S (2006) Annual cycles of solar insolation predict spawning times of Caribbean corals. Ecol Lett 9:390–398CrossRef

Villanueva RD, Yap HT, Montano MNE (2008) Timing of planulation by pocilloporid corals in the northwestern Philippines. Mar Ecol Prog Ser 370:111–119CrossRef

Voolstra CR (2013) A journey into the wild of the cnidarian model system Aiptasia and its symbionts. Mol Ecol 22:4366–4368CrossRef

Voolstra CR, Miller DJ, Ragan MA, Hoffmann A, Hoegh-Guldberg O, Bourne D, Ball E, Ying H, Foret S, Takahashi S, Weynberg KD, van Oppen MJ, Morrow K, Chan CX, Rosic N, Leggat W, Sprungala S, Imelfort M, Tyson GW, Kassahn K, Lundgren P, Beeden R, Ravasi T, Berumen M, Abel E, Fyffe T (2015) The ReFuGe 2020 consortium–using ‘omics’ approaches to explore the adaptability and resilience of coral holobionts to environmental change. Front Mar Sci 2:68

Voolstra CR, Li Y, Liew YJ, Baumgarten S, Zoccola D, Flot J-F, Tambutté S, Allemand D, Aranda M (2017) Comparative analysis of the genomes of Stylophora pistillata and Acropora digitifera provides evidence for extensive differences between species of corals. Sci Rep 7:17583CrossRef

Walker DI, Ormond RFG (1982) Coral death from sewage and phosphate pollution at Aqaba, Red Sea. Mar Pollut Bull 13:21–25CrossRef

Wangpraseurt D, Larkum AW, Ralph PJ, Kühl M (2012) Light gradients and optical microniches in coral tissues. Front Microbiol 3:316CrossRef

Weis VM (2008) Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066CrossRef

Weis VM, Davy SK, Hoegh-Guldberg O, Rodriguez-Lanetty M, Pringle JR (2008) Cell biology in model systems as the key to understanding corals. Trends Ecol Evol 23:369–376CrossRef

Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYM, Jorgensen BB (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70CrossRef

Wild C, Niggl W, Naumann M, Haas A (2010) Organic matter release by Red Sea coral reef organisms—potential effects on microbial activity and in situ O₂ availability. Mar Ecol Prog Ser 411:61–71CrossRef

Willis BL, Babcock RC, Harrison PL, Oliver JK, Wallace CC (1985) Patterns in the mass spawning of corals on the Great Barrier Reef from 1981 to 1984, 5th International Coral Reef Symposium, pp 343–348

Yum LK, Baumgarten S, Röthig T, Roder C, Roik A, Michell C, Voolstra CR (2017) Transcriptomes and expression profiling of deep-sea corals from the Red Sea provide insight into the biology of azooxanthellate corals. Sci Rep 7:6442CrossRef

Zakai D, Dubinsky Z, Avishai A, Caaras T, Chadwick NE (2006) Lunar periodicity of planula release in the reef-building coral Stylophora pistillata. Mar Ecol Prog Ser 311:93–102CrossRef

Ziegler M, Roder CM, Büchel C, Voolstra CR (2014) Limits to physiological plasticity of the coral Pocillopora verrucosa from the Central Red Sea. Coral Reefs 33:1115–1129CrossRef

Ziegler M, Roder C, Büchel C, Voolstra CR (2015a) Niche acclimatization in Red Sea corals is dependent on flexibility of host-symbiont association. Mar Ecol Prog Ser 533:149–161CrossRef

Ziegler M, Roder CM, Büchel C, Voolstra CR (2015b) Mesophotic coral depth acclimatization is a function of host-specific symbiont physiology. Front Mar Sci 2:4CrossRef

Ziegler M, Roik A, Porter A, Zubier K, Mudarris MS, Ormond R, Voolstra CR (2016) Coral microbial community dynamics in response to anthropogenic impacts near a major city in the Central Red Sea. Mar Pollut Bull 105:629–640CrossRef

Ziegler M, Arif C, Burt J, Dobretsov SV, Roder C, LaJeunesse TC, Voolstra CR (2017a) Biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the Arabian Peninsula. J Biogeogr 44:674–686CrossRef

Ziegler M, Seneca FO, Yum LK, Palumbi SR, Voolstra CR (2017b) Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat Commun 8:14213

Title: Ecophysiology of Reef-Building Corals in the Red Sea
Authors: Maren Ziegler
Anna Roik
Till Röthig
Christian Wild
Nils Rädecker
Jessica Bouwmeester
Christian R. Voolstra
Publisher: Springer International Publishing
Book: Coral Reefs of the Red Sea
Print ISBN: 978-3-030-05800-5

Electronic ISBN: 978-3-030-05802-9

Copyright Year: 2019
DOI: https://doi.org/10.1007/978-3-030-05802-9_3