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The Red Sea: Environmental Gradients Shape a Natural Laboratory in a Nascent Ocean

  • Michael L. BerumenEmail author
  • Christian R. Voolstra
  • Daniele Daffonchio
  • Susana Agusti
  • Manuel Aranda
  • Xabier Irigoien
  • Burton H. Jones
  • Xosé Anxelu G. Morán
  • Carlos M. Duarte
Chapter
Part of the Coral Reefs of the World book series (CORW, volume 11)

Abstract

This chapter introduces the environmental gradients that characterize the broader Red Sea habitat. The Red Sea is formed by an actively spreading rift and notably has only one natural connection to the Indian Ocean – a narrow, shallow opening known as the Strait of Bab al Mandab. The resultant isolation undoubtedly plays a key role in shaping the environmental gradients, species endemism, and distinct evolutionary trajectory observed within the Red Sea. While this young ocean is known to be among the saltiest and warmest seas on Earth, there are important spatial and temporal gradients that likely influence the biological communities residing in its waters.

Keywords

Red Sea Physical environment Ecosystems Environmental gradients Coral reefs Brine pools Seagrass meadows Biogeography 

References

  1. Acker J, Leptoukh G, Shen S, Zhu T, Kempler S (2008) Remotely-sensed chlorophyll a observations of the northern Red Sea indicate seasonal variability and influence of coastal reefs. J Mar Syst 69:191–204CrossRefGoogle Scholar
  2. Al-Aidaroos AM, Karati KK, El-Sherbiny MM, Devassy RP, Kürten B (2017) Latitudinal environmental gradients and diel variability influence abundance and community structure of Chaetognatha in Red Sea coral reefs. Syst Biodivers 15:35–48Google Scholar
  3. Almahasheer H, Aljowair A, Duarte CM, Irigoien X (2016a) Decadal stability of Red Sea mangroves. Estuar Coast Shelf Sci 169:164–172CrossRefGoogle Scholar
  4. Almahasheer H, Duarte CM, Irigoien X (2016b) Nutrient limitation in Central Red Sea mangroves. Front Mar Sci 3:271CrossRefGoogle Scholar
  5. Almazroui M, Nazrul Islam M, Athar H, Jones PD, Rahman MA (2012) Recent climate change in the Arabian Peninsula: annual rainfall and temperature analysis of Saudi Arabia for 1978–2009. Int J Climatol 32:953–966CrossRefGoogle Scholar
  6. Anisimov A, Tao W, Stenchikov G, Kalenderski S, Jish Prakash P, Yang ZL, Shi M (2017) Quantifying local-scale dust emission from the Arabian Red Sea coastal plain. Atmos Chem Phys 17:993–1015Google Scholar
  7. Anton A, Hendriks IE, Marbà N, Krause-Jensen D, Garcias-Bonet N, Duarte CM (2018) Iron deficiency in seagrasses and macroalgae in the Red Sea is unrelated to latitude and physiological performance. Front Mar Sci 5:74Google Scholar
  8. Antonius A (1988) Distribution and dynamics of coral diseases in the Eastern Red Sea. Proceedings of the 6th International Coral Reef Symposium 2:293–298Google Scholar
  9. Aranda M, Li Y, Liew YJ, Baumgarten S, Simakov O, Wilson MC, 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 6:39734Google Scholar
  10. Backer H, Schoell M (1972) New deeps with brines and metalliferous sediments in the Red Sea. Nat Phys Sci 240:153–158CrossRefGoogle Scholar
  11. Bang C, Dagan T, Deines P, Dubilier N, Duschl WJ, Fraune S, Hentschel U, Hirt H, Hulter N, Lachnit T, Picazo D, Pita L, Pogoreutz C, Radecker N, Saad MM, Schmitz RA, Schulenburg H, Voolstra CR, Weiland-Brauer N, Ziegler M, Bosch TCG (2018) Metaorganisms in extreme environments: do microbes play a role in organismal adaptation? Zoology 127:1–19Google Scholar
  12. Banks JR, Brindley HE, Stenchikov G, Schepanski K (2017) Satellite retrievals of dust aerosol over the Red Sea and the Persian Gulf (2005–2015). Atmos Chem Phys 17:3987–4003CrossRefGoogle Scholar
  13. Batang ZB, Papathanassiou E, Al-Suwailem A, Smith C, Salomidi M, Petihakis G, Alikunhi NM, Smith L, Mallon F, Yapici T, Fayad N (2012) First discovery of a cold seep on the continental margin of the Central Red Sea. J Mar Syst 94:247–253Google Scholar
  14. Beal LM, Ffield A, Gordon AL (2000) Spreading of Red Sea overflow waters in the Indian Ocean. J Geophys Res Oceans 105:8549–8564Google Scholar
  15. Berumen ML, Braun CD, Cochran JEM, Skomal GB, Thorrold SR (2014) Movement patterns of juvenile whale sharks tagged at an aggregation site in the Red Sea. PLoS One 9:e103536CrossRefGoogle Scholar
  16. Borin S, Brusetti L, Mapelli F, D’Auria G, Brusa T, Marzorati M, Rizzi A, Yakimov M, Marty D, De Lange GJ, Van der Wielen P, Bolhuis H, McGenity TJ, Polymenakou PN, Malinverno E, Giuliano L, Corselli C, Daffonchio D (2009) Sulfur cycling and methanogenesis primarily drive microbial colonization of the highly sulfidic Urania deep hypersaline basin. Proc Natl Acad Sci U S A 106:9151–9156Google Scholar
  17. Bougouffa S, Yang JK, Lee OO, Wang Y, Batang Z, Al-Suwailem A, Qian PY (2013) Distinctive microbial community structure in highly stratified deep-sea brine water columns. Appl Environ Microbiol 79:3425–3437Google Scholar
  18. Bower AS, Farrar JT (2015) Air–Sea interaction and horizontal circulation in the Red Sea. In: Rasul NMA, Stewart ICF (eds) The Red Sea: the formation, morphology, oceanography and environment of a young ocean basin. Springer, Berlin/Heidelberg, pp 329–342Google Scholar
  19. Cantin NE, Cohen AL, Karnauskas KB, Tarrant AM, McCorkle DC (2010) Ocean warming slows coral growth in the central Red Sea. Science 329:322–325Google Scholar
  20. Chaidez V, Dreano D, Agusti S, Duarte CM, Hoteit I (2017) Decadal trends in Red Sea maximum surface temperature. Sci Rep 7:8144CrossRefGoogle Scholar
  21. Churchill JH, Bower AS, McCorkle DC, Abualnaja Y (2014) The transport of nutrient-rich Indian Ocean water through the Red Sea and into coastal reef systems. J Mar Res 72:165–181CrossRefGoogle Scholar
  22. Clifford M, Horton C, Schmitz J, Kantha LH (1997) An oceanographic nowcast/forecast system for the Red Sea. J Geophys Res Oceans 102:25101–25122CrossRefGoogle Scholar
  23. Daffonchio D, Borin S, Brusa T, Brusetti L, van der Wielen PW, Bolhuis H, Yakimov MM, D’Auria G, Giuliano L, Marty D, Tamburini C, McGenity TJ, Hallsworth JE, Sass AM, Timmis KN, Tselepides A, de Lange GJ, Hubner A, Thomson J, Varnavas SP, Gasparoni F, Gerber HW, Malinverno E, Corselli C, Garcin J, McKew B, Golyshin PN, Lampadariou N, Polymenakou P, Calore D, Cenedese S, Zanon F, Hoog S, Party BS (2006) Stratified prokaryote network in the oxic-anoxic transition of a deep-sea halocline. Nature 440:203–207Google Scholar
  24. Devassy RP, El-Sherbiny MM, Al-Sofyani AM, Al-Aidaroos AM (2017) Spatial variation in the phytoplankton standing stock and diversity in relation to the prevailing environmental conditions along the Saudi Arabian coast of the northern Red Sea. Mar Biodivers 47:995–1008CrossRefGoogle Scholar
  25. DiBattista JD, Berumen ML, Gaither MR, Rocha LA, Eble JA, Choat JH, Craig MT, Skillings DJ, Bowen BW, McClain C (2013) After continents divide: comparative phylogeography of reef fishes from the Red Sea and Indian Ocean. J Biogeogr 40:1170–1181Google Scholar
  26. DiBattista JD, Choat JH, Gaither MR, Hobbs J-PA, Lozano‐Cortés DF, Myers RF, Paulay G, Rocha LA, Toonen RJ, Westneat MW, Berumen ML (2015a) On the origin of endemic species in the Red Sea. J Biogeogr 43:13–30Google Scholar
  27. DiBattista JD, Roberts MB, Bouwmeester J, Bowen BW, Coker DJ, Lozano-Cortés DF, Choat JH, Gaither MR, Hobbs J-PA, Khalil MT, Kochzius M, Myers RF, Paulay G, Robitzch VSN, Saenz-Agudelo P, Salas E, Sinclair-Taylor TH, Toonen RJ, Westneat MW, Williams ST, Berumen ML (2015b) A review of contemporary patterns of endemism for shallow water reef fauna in the Red Sea. J Biogeogr 43:423–439Google Scholar
  28. Froukh T, Kochzius M (2008) Species boundaries and evolutionary lineages in the blue green damselfishes Chromis viridis and Chromis atripectoralis (Pomacentridae). J Fish Biol 72:451–457Google Scholar
  29. Furby KA, Bouwmeester J, Berumen ML (2013) Susceptibility of central Red Sea corals during a major bleaching event. Coral Reefs 32:505–513Google Scholar
  30. Garcia-Castellanos D, Villaseñor A (2011) Messinian salinity crisis regulated by competing tectonics and erosion at the Gibraltar arc. Nature 480:359–363CrossRefGoogle Scholar
  31. Giles EC, Saenz-Agudelo P, Hussey NE, Ravasi T, Berumen ML (2015) Exploring seascape genetics and kinship in the reef sponge Stylissa carteri in the Red Sea. Ecol Evol 5:2487–2502Google Scholar
  32. Golani D, Bogorodsky SV (2010) The fishes of the Red Sea – reappraisal and updated checklist. Zootaxa 2463:1-135Google Scholar
  33. Grotzinger SW, Karan R, Strillinger E, Bader S, Frank A, Al Rowaihi IS, Akal A, Wackerow W, Archer JA, Rueping M, Weuster-Botz D, Groll M, Eppinger J, Arold ST (2018) Identification and experimental characterization of an extremophilic brine pool alcohol dehydrogenase from single amplified genomes. ACS Chem Biol 13:161–170Google Scholar
  34. Hickey SM, Phinn SR, Callow NJ, Van Niel KP, Hansen JE, Duarte CM (2017) Is climate change shifting the poleward limit of mangroves? Estuar Coasts 40:1215–1226Google Scholar
  35. Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs J-PA, Hoey AS, Hoogenboom M, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83Google Scholar
  36. 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 U S A 113:4416–4421Google Scholar
  37. Jin D, Kite-Powell H, Hoagland P, Solow A (2012) A bioeconomic analysis of traditional fisheries in the Red Sea. Mar Resour Econ 27:137–148CrossRefGoogle Scholar
  38. Jish Prakash P, Stenchikov G, Kalenderski S, Osipov S, Bangalath H (2015) The impact of dust storms on the Arabian Peninsula and the Red Sea. Atmos Chem Phys 15:199–222CrossRefGoogle Scholar
  39. Jish Prakash P, Stenchikov G, Tao W, Yapici T, Warsama B, Engelbrecht JP (2016) Arabian Red Sea coastal soils as potential mineral dust sources. Atmos Chem Phys 16:11991–12004Google Scholar
  40. Khalil MT, Bouwmeester J, Berumen ML (2017) Spatial variation in coral reef fish and benthic communities in the central Saudi Arabian Red Sea. PeerJ 5:e3410CrossRefGoogle Scholar
  41. Kheireddine M, Ouhssain M, Claustre H, Uitz J, Gentili B, Jones BH (2017) Assessing pigment-based phytoplankton community distributions in the Red Sea. Front Mar Sci 4:132Google Scholar
  42. Kürten B, Khomayis HS, Devassy R, Audritz S, Sommer U, Struck U, El‐Sherbiny MM, Al‐Aidaroos AM (2014) Ecohydrographic constraints on biodiversity and distribution of phytoplankton and zooplankton in coral reefs of the Red Sea, Saudi Arabia. Mar Ecol 36:1195–1214Google Scholar
  43. Kürten B, Al-Aidaroos AM, Kürten S, El-Sherbiny MM, Devassy RP, Struck U, Zarokanellos N, Jones BH, Hansen T, Bruss G, Sommer U (2016) Carbon and nitrogen stable isotope ratios of pelagic zooplankton elucidate ecohydrographic features in the oligotrophic Red Sea. Prog Oceanogr 140:69–90Google Scholar
  44. Li W, El-Askary H, ManiKandan K, Qurban M, Garay M, Kalashnikova O (2017) Synergistic use of remote sensing and modeling to assess an anomalously high chlorophyll-a event during summer 2015 in the South Central Red Sea. Remote Sens 9:778Google Scholar
  45. Malcolm HA, Jordan A, Smith SDA (2010) Biogeographical and cross-shelf patterns of reef fish assemblages in a transition zone. Mar Biodivers 40:181–193CrossRefGoogle Scholar
  46. 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 U S A 110:3229–3236Google Scholar
  47. Mervis J (2009) The big gamble in the Saudi Desert. Science 326:354–357CrossRefGoogle Scholar
  48. Monroe A, Ziegler M, Roik A, Röthig T, Hardestine R, Emms M, Jensen R, Voolstra CR, Berumen ML (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:e0195814Google Scholar
  49. Nanninga GB, Saenz-Agudelo P, Manica A, Berumen ML (2014) Environmental gradients predict the genetic population structure of a coral reef fish in the Red Sea. Mol Ecol 23:591–602CrossRefGoogle Scholar
  50. Ngugi DK, Stingl U (2012) Combined analyses of the ITS loci and the corresponding 16S rRNA genes reveal high micro- and macrodiversity of SAR11 populations in the Red Sea. PLoS One 7:e50274CrossRefGoogle Scholar
  51. Ngugi DK, Antunes A, Brune A, Stingl U (2012) Biogeography of pelagic bacterioplankton across an antagonistic temperature-salinity gradient in the Red Sea. Mol Ecol 21:388–405CrossRefGoogle Scholar
  52. Ngugi D, Blom J, Alam I, Rashid M, Ba-Alawi W, Zhang G, Hikmawan T, Guan Y, Antunes A, Siam R, El Dorry H, Bajic V, Stingl U (2015) Comparative genomics reveals adaptations of a halotolerant thaumarchaeon in the interfaces of brine pools in the Red Sea. ISME J 9:396–411Google Scholar
  53. Osipov S, Stenchikov G (2018) Simulating the regional impact of dust on the Middle East climate and the Red Sea. J Geophys Res Oceans 123:1032–1047CrossRefGoogle Scholar
  54. 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:e474–e484Google Scholar
  55. Patzert WC (1974) Wind-induced reversal in Red Sea circulation. Deep-Sea Res 21:109–121Google Scholar
  56. Pautot G, Guennoc P, Coutelle A, Lyberis N (1984) Discovery of a large brine deep in the northern Red Sea. Nature 310:133–136CrossRefGoogle Scholar
  57. Pearman JK, Kurten S, Sarma YV, Jones BH, Carvalho S (2016) Biodiversity patterns of plankton assemblages at the extremes of the Red Sea. FEMS Microbiol Ecol 92Google Scholar
  58. Pearman JK, Ellis J, Irigoien X, Sarma YVB, Jones BH, Carvalho S (2017) Microbial planktonic communities in the Red Sea: high levels of spatial and temporal variability shaped by nutrient availability and turbulence. Sci Rep 7:6611Google Scholar
  59. Post AF, Dedej Z, Gottlieb R, Li H, Thomas DN, El-Absawi M, El-Naggar A, El-Gharabawi M, Sommer U (2002) Spatial and temporal distribution of Trichodesmium spp. in the stratified Gulf of Aqaba, Red Sea. Mar Ecol Prog Ser 239:241–250Google Scholar
  60. Price ARG, Crossland CJ, Dawson Shepherd AR, McDowall RJ, Medley PAH, Stafford Smith MG, Ormond RFG, Wrathall TJ (1988) Aspects of seagrass ecology along the eastern coast of the Red Sea. Bot Mar 31:83Google Scholar
  61. Priest MA, DiBattista JD, McIlwain JL, Taylor BM, Hussey NE, Berumen ML (2016) A bridge too far: dispersal barriers and cryptic speciation in an Arabian Peninsula grouper (Cephalopholis hemistiktos). J Biogeogr 43:820–832Google Scholar
  62. Qurban MA, Wafar M, Jyothibabu R, Manikandan KP (2017) Patterns of primary production in the Red Sea. J Mar Syst 169:87–98CrossRefGoogle Scholar
  63. Racault M-F, Raitsos DE, Berumen ML, Brewin RJW, Platt T, Sathyendranath S, Hoteit I (2015) Phytoplankton phenology indices in coral reef ecosystems: application to ocean-color observations in the Red Sea. Remote Sens Environ 160:222–234Google Scholar
  64. Raitsos DE, Hoteit I, Prihartato PK, Chronis T, Triantafyllou G, Abualnaja Y (2011) Abrupt warming of the Red Sea. Geophys Res Lett 38:L14601Google Scholar
  65. Raitsos DE, Pradhan Y, Brewin RJW, Stenchikov G, Hoteit I (2013) Remote sensing the phytoplankton seasonal succession of the Red Sea. PLoS One 8:e64909Google Scholar
  66. Raitsos DE, Brewin RJW, Zhan P, Dreano D, Pradhan Y, Nanninga GB, Hoteit I (2017) Sensing coral reef connectivity pathways from space. Sci Rep 7:9338Google Scholar
  67. Riegl BM, Bruckner AW, Rowlands GP, Purkis SJ, Renaud P (2012) Red Sea coral reef trajectories over 2 decades suggest increasing community homogenization and decline in coral size. PLoS One 7:e38396CrossRefGoogle Scholar
  68. Roberts CM, Alexander RDS, Rupert FGO (1992) Large-scale variation in assemblage structure of Red Sea butterflyfishes and angelfishes. J Biogeogr 19:239–250CrossRefGoogle Scholar
  69. Roberts MB, Jones GP, McCormick MI, Munday PL, Neale S, Thorrold S, Robitzch VSN, Berumen ML (2016) Homogeneity of coral reef communities across 8 degrees of latitude in the Saudi Arabian Red Sea. Mar Pollut Bull 105:558–565Google Scholar
  70. Robitzch V, Banguera-Hinestroza E, Sawall Y, Al-Sofyani A, Voolstra CR (2015) Absence of genetic differentiation in the coral along environmental gradients of the Saudi Arabian Red Sea. Front Mar Sci 2:5Google Scholar
  71. Robitzch VS, Lozano-Cortes D, Kandler NM, Salas E, Berumen ML (2016) Productivity and sea surface temperature are correlated with the pelagic larval duration of damselfishes in the Red Sea. Mar Pollut Bull 105:566–574CrossRefGoogle Scholar
  72. 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 3:2802Google Scholar
  73. Roik A, Roethig T, Ziegler M, Voolstra CR (2015a) Coral bleaching event in the Central Red Sea. In Mideast Coral Reef Society Newsletter, vol 3, p 3Google Scholar
  74. Roik A, Röthig T, Roder C, Müller PJ, Voolstra CR (2015b) Captive rearing of the deep-sea coral Eguchipsammia fistula from the Red Sea demonstrates remarkable physiological plasticity. PeerJ 3:e734CrossRefGoogle Scholar
  75. 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:e0163939Google Scholar
  76. 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 7:44714CrossRefGoogle Scholar
  77. Saenz-Agudelo P, DiBattista JD, Piatek MJ, Gaither MR, Harrison HB, Nanninga GB, Berumen ML (2015) Seascape genetics along environmental gradients in the Arabian Peninsula: insights from ddRAD sequencing of anemonefishes. Mol Ecol 24:6241–6255Google Scholar
  78. 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:e103179CrossRefGoogle Scholar
  79. 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 5:8940Google Scholar
  80. Schardt C (2016) Hydrothermal fluid migration and brine pool formation in the Red Sea: the Atlantis II deep. Mineral Deposita 51:89–111CrossRefGoogle Scholar
  81. Searle RC, Ross DA (2007) A geophysical study of the Red Sea axial trough between 20.5° and 22°N. Geophys J R Astron Soc 43:555–572Google Scholar
  82. Sheppard CRC, Sheppard ALS (1991) Corals and coral communities of Arabia. Fauna Saudi Arabia 12:3–170Google Scholar
  83. Shibl AA, Haroon MF, Ngugi DK, Thompson LR, Stingl U (2016) Distribution of Prochlorococcus ecotypes in the Red Sea Basin based on analyses of rpoC1 sequences. Front Mar Sci 3:104Google Scholar
  84. Silva L, Calleja ML, Huete-Stauffer TM, Ivetic S, Ansari MI, Viegas M, Morán XAG (2019) Low abundances but high growth rates of coastal heterotrophic bacteria in the Red Sea. Front Microbiol 9:3244Google Scholar
  85. Sofianos SS, Johns WE (2002) An Oceanic General Circulation Model (OGCM) investigation of the Red Sea circulation, 1. Exchange between the Red Sea and the Indian Ocean. J Geophys Res Oceans 107(C11):3196Google Scholar
  86. Sofianos SS, Johns WE (2003) An Oceanic General Circulation Model (OGCM) investigation of the Red Sea circulation: 2. Three-dimensional circulation in the Red Sea. J Geophys Res Oceans 108:3066Google Scholar
  87. Sofianos SS, Johns WE (2007) Observations of the summer Red Sea circulation. J Geophys Res Oceans 112:C06025Google Scholar
  88. Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M, Halpern BS, Jorge MA, Lombana A, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57:573–583Google Scholar
  89. Swift SA, Bower AS, Schmitt RW (2012) Vertical, horizontal, and temporal changes in temperature in the Atlantis II and Discovery hot brine pools, Red Sea. Deep-Sea Res I Oceanogr Res Pap 64:118–128Google Scholar
  90. Thompson LR, Williams GJ, Haroon MF, Shibl A, Larsen P, Shorenstein J, Knight R, Stingl U (2016) Metagenomic covariation along densely sampled environmental gradients in the Red Sea. ISME J 11:138Google Scholar
  91. Tragou E, Garrett C, Outerbridge R, Gilman C (1999) The heat and freshwater budgets of the Red Sea. J Phys Oceanogr 29:2504–2522CrossRefGoogle Scholar
  92. Vestheim H, Kaartvedt S (2016) A deep sea community at the Kebrit brine pool in the Red Sea. Mar Biodivers 46:59–65CrossRefGoogle Scholar
  93. 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 7:17583Google Scholar
  94. Wafar M, Ashraf M, Manikandan KP, Qurban MA, Kattan Y (2016a) Propagation of Gulf of Aden Intermediate Water (GAIW) in the Red Sea during autumn and its importance to biological production. J Mar Syst 154:243–251CrossRefGoogle Scholar
  95. Wafar M, Qurban MA, Ashraf M, Manikandan KP, Flandez AV, Balala AC (2016b) Patterns of distribution of inorganic nutrients in Red Sea and their implications to primary production. J Mar Syst 156:86–98Google Scholar
  96. Wilson SN (2017) Assessment of genetic connectivity between Sudan and Saudi Arabia for commercially important fish species. MSc thesis. King Abdullah University of Science and Technology, Saudi ArabiaGoogle Scholar
  97. Xu W, Ruch J, Jónsson S (2015) Birth of two volcanic islands in the southern Red Sea. Nat Commun 6:7104CrossRefGoogle Scholar
  98. Yao FC, Hoteit I, Pratt LJ, Bower AS, Zhai P, Kohl A, Gopalakrishnan G (2014) Seasonal overturning circulation in the Red Sea: 1. Model validation and summer circulation. J Geophys Res Oceans 119:2238–2262Google Scholar
  99. 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 7:6442Google Scholar
  100. Zarokanellos ND, Papadopoulos VP, Sofianos SS, Jones BH (2017a) Physical and biological characteristics of the winter-summer transition in the Central Red Sea. J Geophys Res Oceans 122:6355–6370CrossRefGoogle Scholar
  101. Zarokanellos ND, Kürten B, Churchill JH, Roder C, Voolstra CR, Abualnaja Y, Jones BH (2017b) Physical mechanisms routing nutrients in the Central Red Sea. J Geophys Res Oceans 122:9032–9046Google Scholar
  102. Zhai P, Bower A (2013) The response of the Red Sea to a strong wind jet near the Tokar Gap in summer. J Geophys Res Oceans 118:421–434CrossRefGoogle Scholar
  103. Zhai P, Pratt LJ, Bower A (2015) On the crossover of boundary currents in an idealized model of the Red Sea. J Phys Oceanogr 45:1410–1425CrossRefGoogle Scholar
  104. Zhan P, Subramanian AC, Yao F, Hoteit I (2014) Eddies in the Red Sea: a statistical and dynamical study. J Geophys Res Oceans 119:3909–3925CrossRefGoogle Scholar
  105. Ziegler M, Arif C, Burt JA, Dobretsov S, Roder C, LaJeunesse TC, Voolstra CR (2017) Biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the Arabian Peninsula. J Biogeogr 44:674–686Google Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Michael L. Berumen
    • 1
    Email author
  • Christian R. Voolstra
    • 1
  • Daniele Daffonchio
    • 1
  • Susana Agusti
    • 1
  • Manuel Aranda
    • 1
  • Xabier Irigoien
    • 2
  • Burton H. Jones
    • 1
  • Xosé Anxelu G. Morán
    • 1
  • Carlos M. Duarte
    • 1
  1. 1.Red Sea Research Center, Division of Biological and Environmental Science and EngineeringKing Abdullah University of Science and TechnologyThuwalSaudi Arabia
  2. 2.AZTIPasaiaSpain

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