Skip to main content

Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs

Coral Reefs volume 29, pages 309–327 (2010)Cite this article

Abstract

Coral reefs in shallow-water environments (<30 m) are in decline due to local and global anthropogenic stresses. This has led to renewed interest in the ‘deep reef refugia’ hypothesis (DRRH), which stipulates that deep reef areas (1) are protected or dampened from disturbances that affect shallow reef areas and (2) can provide a viable reproductive source for shallow reef areas following disturbance. Using the Caribbean as an example, the assumptions of this hypothesis were explored by reviewing the literature for scleractinian corals—the reef framework builders on tropical reefs. Although there is evidence to support that deep reefs (>30 m) can escape the direct effects of storm-induced waves and thermal bleaching events, deep reefs are certainly not immune to disturbance. Additionally, the potential of deep reefs to provide propagules for shallow reef areas seems limited to ‘depth-generalist’ coral species, which constitute only ~25% of the total coral biodiversity. Larval connectivity between shallow and deep populations of these species may be further limited due to specific life history traits (e.g., brooding reproductive strategy and vertical symbiont acquisition mode). This review exposes how little is known about deep reefs and coral reproduction over depth. Hence, a series of urgent research priorities are proposed to determine the extent to which deep reefs may act as a refuge in the face of global reef decline.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

References

  • Alamaru A, Loya Y, Brokovich E, Yam R, Shemesh A (2009) Carbon and nitrogen utilization in two species of Red Sea corals along a depth gradient: Insights from stable isotope analysis of total organic material and lipids. Geochim Cosmochim Acta 73:5333–5342

    CAS  Article  Google Scholar 

  • Albins MA, Hixon MA (2008) Invasive Indo-Pacific lionfish Pterois volitans reduce recruitment of Atlantic coral-reef fishes. Mar Ecol Prog Ser 367:233–238

    Article  Google Scholar 

  • Armstrong RA (2007) Deep zooxanthellate coral reefs of the Puerto Rico: US Virgin Islands insular platform. Coral Reefs 26:945

    Article  Google Scholar 

  • Armstrong RA, Singh H, Torres J, Nemeth RS, Can A, Roman C, Eustice R, Riggs L, Garcia-Moliner G (2006) Characterizing the deep insular shelf coral reef habitat of the Hind Bank Marine Conservation District (US Virgin Islands) using the Seabed autonomous underwater vehicle. Cont Shelf Res 26:194–205

    Article  Google Scholar 

  • Aronson RB, Precht WF (2001) White-band disease and the changing face of Caribbean coral reefs. Hydrobiologia 460:25–38

    Article  Google Scholar 

  • Aronson RB, Sebens KP, Ebersole JP (1994) Hurricane Hugo’s impact on Salt River submarine canyon, St. Croix, US Virgin Islands. In: Ginsburg RN (ed) Proceedings of the colloquium on global aspects of coral reefs: Health, hazards and history. Rosenstiel School of Marine and Atmospheric Science, Miami, pp 189–195

    Google Scholar 

  • Ayre DJ, Hughes TP (2000) Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia. Evolution 54:1590–1605

    CAS  PubMed  Google Scholar 

  • Baird AH, Babcock RC, Mundy CP (2003) Habitat selection by larvae influences the depth distribution of six common coral species. Mar Ecol Prog Ser 252:289–293

    Article  Google Scholar 

  • Bak RPM (1977) Coral reefs and their zonation in Netherlands Antilles. Studies in Geology 4:3–16

    Google Scholar 

  • Bak RPM, Luckhurst BE (1980) Constancy and change in coral reef habitats along depth gradients at Curaçao. Oecologia 47:145–155

    Article  Google Scholar 

  • Bak RPM, Engel MS (1979) Distribution, abundance and survival of juvenile hermatypic corals (Scleractinia) and the importance of life history strategies in the parent coral community. Mar Biol 54:341–352

    Article  Google Scholar 

  • Bak RPM, Nieuwland G (1995) Long-term change in coral communities along depth gradients over leeward reefs in the Netherlands Antilles. Bull Mar Sci 56:609–619

    Google Scholar 

  • Bak RPM, Nieuwland G, Meesters EH (2005) Coral reef crisis in deep and shallow reefs: 30 years of constancy and change in reefs of Curaçao and Bonaire. Coral Reefs 24:475–479

    Article  Google Scholar 

  • Bak RPM, Nieuwland G, Meesters EH (2009) Coral growth rates revisited after 31 years : what is causing lower extension rates in Acropora palmata? Bull Mar Sci 84:287–294

    Google Scholar 

  • Baker AC, Rowan R, Knowlton N (1997) Symbiosis ecology of two Caribbean acroporid corals. Proc 8th Int Coral Reef Symp 2:1295–1300

    CAS  Google Scholar 

  • Banner AH (1961) Submarine effects of the typhoon. Atoll Res Bull 75:75–78

    Google Scholar 

  • Baums IB, Miller MW, Hellberg ME (2005) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390

    CAS  PubMed  Article  Google Scholar 

  • Baums IB (2008) A restoration genetics guide for coral reef conservation. Mol Ecol 17:2796–2811

    PubMed  Article  Google Scholar 

  • Birkeland C (ed) (1997) Life and death of coral reefs. Chapman, New York, pp 140–147

    Google Scholar 

  • Brakel WH (1979) Small-scale spatial variation in light available to coral reef benthos: quantum irradiance measurements from a Jamaican reef. Bull Mar Sci 29:406–413

    Google Scholar 

  • Brokovich E, Ayalon I, Einbinder S, Segev N, Shaked Y, Genin A, Kark S, Kiflawi M (2010) Grazing pressure on coral reefs decreases across a wide depth gradient in the Gulf of Aqaba, Red Sea. Mar Ecol Prog Ser (in press)

  • Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:129–138

    Article  Google Scholar 

  • Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS One 8:e711

    Article  Google Scholar 

  • Bunkley-Williams LC, Morelock J, Williams EH (1991) Lingering effects of the 1987 mass bleaching of Puerto Rican coral reefs in mid to late 1988. J Aquat Anim Health 3:242–247

    Article  Google Scholar 

  • Calnan JM, Smith TB, Nemeth RS, Kadison E, Blondeau J (2008) Coral disease prevalence and host susceptibility on mid-depth and deep reefs in the United States Virgin Islands. Rev Biol Trop 56:223–234

    Google Scholar 

  • Coffroth MA, Santos SR, Goulet TL (2001) Early ontogenic expression of specificity in a cnidarian-algal symbiosis. Mar Ecol Prog Ser 222:85–96

    Article  Google Scholar 

  • Coles SL, Eldredge LG (2002) Non-indigenous species introductions on coral reefs: A need for information. Pac Sci 56:191–209

    Article  Google Scholar 

  • Coles SL, Brown BE (2003) Coral bleaching—capacity for acclimitization and adaptation. Adv Mar Biol 46:183–223

    CAS  PubMed  Article  Google Scholar 

  • Colgan MW (1987) Coral reef recovery on Guam (Micronesia) after catastrophic predation by Acanthaster planci. Ecology 68:1592–1605

    Article  Google Scholar 

  • Cooper TF, De’ath G, Fabricius KE, Lough JM (2008) Declining coral calcification in massive Porites in two nearshore regions of the northern Great Barrier Reef. Global Change Biol 14:529–538

    Article  Google Scholar 

  • Connell JH (1997) Disturbance and recovery of coral assemblages. Coral Reefs 16(Suppl):S101–S113

    Article  Google Scholar 

  • Culter JK, Ritchie KB, Earle SA, Guggenheim DE, Halley RB, Ciembronowicz KT, Hine AC, Jarrett BD, Locker SD, Jaap WC (2006) Pulley reef: a deep photosynthetic coral reef on the West Florida Shelf, USA. Coral Reefs 25:228

    Article  Google Scholar 

  • De’ath G, Lough JM, Fabricius KE (2009) Declining coral calcification on the Great Barrier Reef. Science 323:116–119

    PubMed  Article  CAS  Google Scholar 

  • DeVantier LM, Deacon G (1990) Distribution of Acanthaster planci at Lord Howe Island, the southern-most Indo-Pacific reef. Coral Reefs 9:145–148

    Article  Google Scholar 

  • Dollar SJ (1982) Wave stress and coral community structure in Hawaii. Coral Reefs 1:71–81

    Article  Google Scholar 

  • Feingold J (2001) Responses of three coral communities to the 1997–98 El Niño-Southern Oscillation: Galapagos Islands, Ecuador. Bull Mar Sci 69:61–77

    Google Scholar 

  • Fenner D, Banks K (2004) Orange cup coral Tubastrea coccinea invades Florida and the flower Garden Banks, Northwestern Gulf of Mexico. Coral Reefs 23:505–507

    Google Scholar 

  • Fisk D, Done T (1985) Taxonomic and bathymetric patterns of bleaching in corals, Myrmidon Reef (Queensland). Proc 5th Int Coral Reef Symp 6:149–154

  • Frade PR, Jongh de F, Vermeulen F, van Bleijswijk J, Bak RPM (2008) Variation in symbiont distribution between closely related coral species over large depth ranges. Mol Ecol 17:691–703

    CAS  PubMed  Google Scholar 

  • Fricke HW, Schuhmacher H (1983) The depth limits of Red Sea stony corals: An ecophysiological problem (a deep diving survey by submersible). Mar Ecol 4:163–194

    Article  Google Scholar 

  • Fricke H, Meischner D (1985) Depth limits of Bermudan scleractinian corals: a submersible survey. Mar Biol 88:175–187

    Article  Google Scholar 

  • García-Sais JR, Appeldoorn R, Battista T, Bauer L, Bruckner A, Caldow C, Carrubba L, Corredor J, Diaz E, Lilyestrom C, García-Moliner G, Hernández-Delgado E, Menza C, Morell J, Pait A, Sabater J, Weil E, Williams E, Williams S (2008) The state of coral reef ecosystems of the Commonwealth of Puerto Rico. In: Waddell J, Clarke A (eds) The state of coral reef ecosystems of the United States and Pacific Freely Associated States: 2008 NOAA Technical Memorandum NOS NCCOS 78. NOAA/NCCOS Center for Coastal Monitoring and Assessment’s Biogeography Team, Silver Spring, MD, pp 75–116

    Google Scholar 

  • Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960

    CAS  PubMed  Article  Google Scholar 

  • Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Global Change Biol 2:495–509

    Article  Google Scholar 

  • Glynn PW, Almodovar LR, Gonzalez JG (1964) Effects of hurricane Edith on marine life in La Parguera, Puerto Rico. Caribb J Sci 4:335–345

    Google Scholar 

  • Glynn PW, Mate JL, Baker AC, Calderon MO (2001) Coral bleaching and mortality in Panama and Ecuador during the 1997–1998 El Niño–Southern Oscillation even. Spatial/temporal patterns and comparison with the 1982–1983 event. Bull Mar Sci 69:79–109

    Google Scholar 

  • Goldberg WM (1973) The ecology of the coral octocoral communities off the southeast Florida coast: geomorphology, species composition and zonation. Bull Mar Sci 23:465–488

    Google Scholar 

  • Gómez-Cabrera MC, Ortiz J, Loh W, Ward S, Hoegh-Guldberg O (2007) Acquisition of symbiotic dinoflagellates (Symbiodinium) by juveniles of the coral Acropora longicyathus. Coral Reefs 27:219–226

    Article  Google Scholar 

  • Goreau TF, Goreau NI (1973) The ecology of Jamaican coral reefs. II. Geomorphology, zonation, and sedimentary phases. Bull Mar Sci 23:399–464

    Google Scholar 

  • Goreau TF, Wells JW (1967) The shallow-water Scleractinia of Jamaica: revised list of species and their vertical distribution ranges. Bull Mar Sci 17:442–453

    Google Scholar 

  • Green SJ, Cote IM (2009) Record densities of Indo-Pacific lionfish on Bahamian coral reefs. Coral Reefs 28:107

    Article  Google Scholar 

  • Grigg RW (2006) Depth limit for reef building corals in the Au’au Channel. S.E. Hawaii. Coral Reefs 25:77–84

    Article  Google Scholar 

  • Grigg RW, Epp D (1989) Critical depth for the survival of coral islands: effects on the Hawaiian archipelago. Science 243:638–641

    PubMed  Article  CAS  Google Scholar 

  • Grigg RW, Maragos JE (1974) Recolonization of hermatypic corals on submerged lava flows in Hawaii. Ecology 55:387–395

    Article  Google Scholar 

  • Halfar J, Godinez-Orta L, Riegl B, Valdez-Holguin JE, Borges JM (2005) Living on the edge: high-latitude Porites carbonate production under temperate eutrophic conditions. Coral Reefs 24:582–592

    Article  Google Scholar 

  • Hallock P, Schlager W (1986) Nutrient excess and the demise of coral reefs and carbonate platforms. Palaios 1:389–398

    Article  Google Scholar 

  • Harmelin-Vivien ML, Laboute P (1986) Catastrophic impact of hurricanes on atoll outer reef slopes in the Tuamotu (French Polynesia). Coral Reefs 5:55–62

    Article  Google Scholar 

  • Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstien PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus ADME, Overstreet RM, Porter JW, Smith GW, Vasta GR (1999) Emerging marine diseases - Climate links and anthropogenic factors. Science 285:1505–1510

    CAS  PubMed  Article  Google Scholar 

  • Hay ME, Colburn T, Downing D (1983) Spatial and temporal patterns in herbivory on a Caribbean fringing reef: the effects on plant distribution. Oecologia 58:299–308

    Article  Google Scholar 

  • Hickerson EL, Schmahl GP, Robbart M, Precht WF, Caldow C (2008) State of coral reef ecosystems of the Flower Garden Banks, Stetson Bank, and Other Banks in the Northwestern Gulf of Mexico. In: Waddell JE, Clarke AM (eds), The state of coral reef ecosystems of the United States and Pacific Freely Associated States: 2008. NOAA Technical Memorandum NOS NCCOS 73. NOAA/NCCOS Center for Coastal Monitoring and Assessment’s Biogeography Team. Silver Spring, MD

  • Highsmith R, Riggs A, D’Antonio C (1980) Survival of hurricane-generated coral fragments and a disturbance model of reef calcification/growth rates. Oecologia 46:322–329

    Google Scholar 

  • Hinderstein LM, Marr JCA, Martinez FA, Dowgiallo MJ, Puglise KA, Zawada D, Pyle R (2010) Introduction to mesophotic coral ecosystems: Characterization, ecology, and management. Coral Reefs (this issue)

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

    Article  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    CAS  PubMed  Article  Google Scholar 

  • Hoegh-Guldberg O, Hughes L, McIntyre S, Lindenmayer DB, Parmesan C, Possingham HP, Thomas CD (2008) Assisted colonization and rapid climate change. Science 321:345–346

    CAS  PubMed  Article  Google Scholar 

  • Hubbard DK (1989) The shelf-edge reefs of Davis and Cane Bays, northwestern St. Croix, U.S.V.I. In: Hubbard DK (ed) Terrestrial and marine geology of St. Croix, US Virgin Islands. West Indies Lab. Special Publ No 8, pp 167–179

  • Hubbard DK (1992) Hurricane-induced sediment transport in open-shelf tropical systems–an example from St Croix, United States Virgin Islands. J Sediment Petrol 62:946–960

    Google Scholar 

  • Hubbard JAEB, Pocock YP (1972) Sediment rejection by recent scleractinian corals: a key to paleo-environmental reconstruction. Geol Rundsch 61:598–626

    Article  Google Scholar 

  • Hughes TP, Jackson JBC (1985) Population dynamics and life histories of foliaceous corals. Ecol Monogr 55:141–166

    Article  Google Scholar 

  • Hughes TP, Connell JH (1999) Multiple stressors on coral reefs: A long-term perspective. Limnol Oceanogr 44:932–940

    Google Scholar 

  • Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263

    Article  Google Scholar 

  • Hughes TP, Rodrigues RJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj L, Pratchett MS, Steneck R, Willis B (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365

    CAS  PubMed  Article  Google Scholar 

  • Humann P, DeLoach N (2002) Reef coral identification, Florida Caribbean Bahamas including marine plants. New World, Jacksonville, FL

    Google Scholar 

  • Hunte W, Wittenberg M (1992) Effects of eutrophication and sedimentation on juvenile corals. I. Abundance, mortality and community structure. Mar Biol 114:625–631

    Article  Google Scholar 

  • Huston MA (1985) Patterns of species diversity on coral reefs. Annu Rev Ecol Syst 16:149–177

    Article  Google Scholar 

  • Iglesias-Prieto R, Trench RK (1997) Photoadaptation, photoacclimation and niche diversification in invertebrate-dinoflagellate symbioses. Proc 8th Int Coral Reef Symp 2:1319–1324

    Google Scholar 

  • 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 271:1757–1763

    CAS  Article  Google Scholar 

  • CC IP (2007) Climate Change 2007: The physical science basis. Miller Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, NY

    Google Scholar 

  • Jackson JBC, Kirby MX, Berher WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandsson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638

    CAS  PubMed  Article  Google Scholar 

  • Jarrett BD, Hine AC, Halley RB, Naar DF, Locker SD, Neumann AC, Twichell D, Hu C, Donahue BT, Jaap WC, Palandro D, Ciembronowicz K (2005) Strange bedfellows-a deep-water hermatypic coral reef superimposed on a drowned barrier island: Southern Pulley Ridge, SW Florida platform margin. Mar Geol 214:295–307

    Article  Google Scholar 

  • Jokiel PL, Coles SL (1977) Effects of temperature on the mortality and growth of Hawaiian reef corals. Mar Biol 43:201–208

    Article  Google Scholar 

  • Kahng SE, Kelley CD (2007) Vertical zonation of megabenthic taxa on a deep photosynthetic reef (50–140 m) in the Au’au Channel, Hawaii. Coral Reefs 26:679–687

    Article  Google Scholar 

  • Kahng SE, Garcia R, Spalding HL, Brokovich E, Wagner D, Weil E, Hinderstein L, Toonen RJ (2010) Community ecology of mesophotic coral reef ecosystems. Coral Reefs (this issue)

  • Kjerfve B, Magill KE, Porter JW, Woodley JD (1986) Hindcasting of hurricane characteristics and observed storm damage on a fringing reef, Jamaica, West Indies. J Mar Res 44:119–148

    Article  Google Scholar 

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

    Google Scholar 

  • Kobluk DR, Lysenko MA (1992) Storm features on a southern Caribbean fringing coral reef. Palaios 7:213–221

    Article  Google Scholar 

  • Kobluk DR, Lysenko MA (1994) “Ring” bleaching in southern Caribbean Agaricia agaricites during a rapid water cooling. Bull Mar Sci 54:142–150

    Google Scholar 

  • Kühlmann D (1983) Composition and ecology of deep-water coral associations. Helgol Mar Res 36:183–204

    Google Scholar 

  • Lang JC, Wicklund RI, Dill RF (1988) Depth- and habitat related bleaching of zooxanthellate reef organisms near Lee Stocking Island, Exuma Cays, Bahamas. Proc 6th Int Coral Reef Symp 3:269–274

  • Lapointe BE (1997) Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and southeast Florida. Limnol Oceanogr 42:1119–1131

    CAS  Article  Google Scholar 

  • Lapointe BE, Barile PJ, Littler MM, Littler DS, Bedford BJ, Gasque C (2005) Macroalgal blooms on southeast Florida coral reefs: I. Nutrient stoichiometry of the invasive green alga Codium isthmocladum in the wider Caribbean indicates nutrient enrichment. Harmful Algae 4:1092–1105

    CAS  Article  Google Scholar 

  • Leichter JJ, Genovese SJ (2006) Intermittent upwelling and subsidized growth of the scleractinian coral Madracis mirabilis on the deep fore-reef slope of Discovery Bay, Jamaica. Mar Ecol Prog Ser 316:95–103

    Article  Google Scholar 

  • Leichter JJ, Wing SR, Miller SL, Denny MW (1996) Pulsed delivery of subthermocline water to Conch Reef (Florida Keys) by internal tidal bores. Limnol Oceanogr 41:1490–1501

    CAS  Article  Google Scholar 

  • Lesser MP, Slattery M, Leichter JJ (2009a) Ecology of mesophotic coral reefs. J Exp Mar Biol Ecol 375:1–8

    Article  Google Scholar 

  • Lesser MP, Slattery M, Stat M, Ojimi M, Gates RD, Grottoli (2009b) Photoacclimatization by the coral Montastraea cavernosa in the Mesophotic Zone: Light, food, and genetics. Ecology (in press)

  • Lessios HA (1988) Mass mortality of Diadema antillarum in the Caribbean: what have we learned? Annu Rev Ecol Syst 19:371–393

    Google Scholar 

  • Liddell WD, Ohlhorst SL (1988) Hard substrata community patterns, 1–120 m, north Jamaica. Palaios 3:413–423

    Article  Google Scholar 

  • Liddell WD, Avery WE (2000) Temporal change in hard substrate communities 10–250 m, the Bahamas. Proc 10th Int Coral Reef Symp 1:437–442

    Google Scholar 

  • Liddell WD, Avery WE, Ohlhorst SL (1997) Patterns of benthic community structure, 10–250 m, the Bahamas. Proc 8th Int Coral Reef Symp 1:437–442

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

    CAS  PubMed  Article  Google Scholar 

  • Littler MM, Littler DS, Hanisak MD (1991) Deepwater rhodolith distribution, productivity, and growth history at sites of formation and subsequent degradation. J Exp Mar Biol Ecol 150:163–182

    Article  Google Scholar 

  • Macintyre IG, Rützler K, Norris JN, Smith KP, Cairns SD, Bucher KE, Steneck RS (1991) An early Holocene reef on the western Atlantic: submersible investigations off the west coast of Barbados. W.I. Coral Reefs 10:167–174

    Article  Google Scholar 

  • Maragos JE, Jokiel PL (1986) Reef corals of Johnston Atoll: one of the world’s most isolated reefs. Coral Reefs 4:141–150

    Article  Google Scholar 

  • 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 334:93–102

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

  • Menza C, Kendall M, Rogers C, Miller J (2007) A deep reef in deep trouble. Cont Shelf Res 27:2224–2230

    Article  Google Scholar 

  • Menza C, Kendall M, Hile S (2008) The deeper we go the less we know. Rev Biol Trop 56:11–24

    Google Scholar 

  • Merks RMH, Hoekstra AG, Kaandorp JA, Sloot PMA (2004) Polyp oriented modelling of coral growth. J Theor Biol 228:559–576

    PubMed  Article  Google Scholar 

  • Morrison D (1988) Comparing fish and urchin grazing in shallow and deeper coral reef algal communities. Ecology 69:1367–1382

    Article  Google Scholar 

  • Mundy CN, Babcock RC (1998) Role of light intensity and spectral quality in coral settlement: Implications for depth-dependent settlement? J Exp Mar Biol Ecol 223:235–255

    Article  Google Scholar 

  • Mundy CN, Babcock RC (2000) Are vertical distribution patterns of scleractinian corals maintained by pre-or post-settlement processes? A case study of three contrasting species. Mar Ecol Prog Ser 198:109–119

    Article  Google Scholar 

  • Nagelkerken I (2006) Relationship between antrhropogenic impacts and bleaching-associated tissue mortality of corals in Curacao (Netherlands Antilles). Rev Biol Trop 54(Suppl. 3):31–43

    Google Scholar 

  • Pandolfi JM (2002) Coral community dynamics at multiple scales. Coral Reefs 21:13–23

    Google Scholar 

  • Phillips NW, Gettleson DA, Spring KD (1990) Benthic biological studies of the southwest Florida shelf. Am Zool 30:65–75

    Google Scholar 

  • Polunin NVC, Roberts CM (1993) Greater biomass and value of target coral-reef fishes in two small Caribbean marine reserves. Mar Ecol Prog Ser 100:167–176

    Article  Google Scholar 

  • Pomar L (2001) Types of carbonate platforms: a genetic approach. Basin Res 3:313–334

    Article  Google Scholar 

  • Porter JW (1973) Ecology and composition of deep reef communities off the Tongue of the Ocean, Bahama Island. Discovery 9:3–12

    Google Scholar 

  • Proni JR, Huang H, Dammann WP (1994) Initial dilution of Southeast Florida ocean outfalls. J Hydr Eng 120:1409–1425

    Article  Google Scholar 

  • Rahmstorf S, Cazenave A, Church JA, Hansen JE, Keeling RF, Parker DE, Somerville RCJ (2007) Recent climate observations compared to projections. Science 316:709

    CAS  PubMed  Article  Google Scholar 

  • Reed JK (1985) Deepest distribution of Atlantic hermatypic corals discovered in the Bahamas. Proc 5th Int Coral Reef Symp 6:249–254

  • Rezak R, Gittings SR, Bright TJ (1990) Biotic assemblages and ecological controls on reefs and banks of the northwest Gulf of Mexico. Am Zool 30:23–35

    Google Scholar 

  • Ridgway T, Hoegh-Guldberg O (2002) Reef recovery in disturbed coral reef ecosystems. Proc 9th Int Coral Reef Symp 2:1117–1121

    Google Scholar 

  • Riegl B, Piller WE (2003) Possible refugia for reefs in time of environmental stress. Int J Earth Sci 92:520–531

    Article  Google Scholar 

  • Rivero-Calle S, Armstrong RA, Soto-Santiago FJ (2009) Biological and physical characteristics of a mesophotic coral reef: Black Jack reef, Vieques, Puerto Rico. Proc 11th Int Coral Reef Symp (in press)

  • Robbart ML, Aronson RB, Duncan L, Zimmer B (2009) Post-hurricane assessment of sensitive habitats of the Flower Garden Banks Vicinity. U.S. Department of the Interior, Minerals Management Service, Gulf of Mexico OCS Region, New Orleans, Louisiana. OCS Study MMS

  • Rodriguez-Lanetty M, Krupp D, Weis VM (2004) Distinct ITS types of Symbiodinium in clade C correlate to cnidarian/dinoflagellate specificity during symbiosis onset. Mar Ecol Prog Ser 275:97–102

    CAS  Article  Google Scholar 

  • Rogers CS, Suchanek TH, Pecora FA (1982) Effects of Hurricanes David and Frederic (1979) on shallow Acropora palmata reef communities: St. Croix, US Virgin Islands. Bull Mar Sci 32:532–548

    Google Scholar 

  • Rogers CS, Gilnack MG, Fitz HC III (1983) Monitoring of coral reefs with linear transects: a study of storm damage. J Exp Mar Biol Ecol 66:285–300

    Article  Google Scholar 

  • Rowan R (1998) Diversity and ecology of zooxanthallae on coral reefs. J Phycol 34:407–417

    Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Saunders MA, Lea AS (2008) Large contribution of sea surface warming to recent increase in Atlantic hurricane activity. Nature 451:557–560

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Selig, ER, Harvell CD, Bruno JF, Willis BL, Page CA, Casey KS, Sweatman H (2006) Analyzing the relationship between ocean temperature anomalies and coral disease outbreaks at broad spatial scales. In: Phinney J, Hoegh-Guldberg O, Kleypas J, Skirving W, Strong A (eds) Coral reefs and climate change: science and management. AGU Coastal and Estuarine Series, vol 61

  • Sheppard C (1981) The reef and soft-substrate coral fauna of Chagos, Indian Ocean. J Nat Hist 15:607–621

    Article  Google Scholar 

  • Sheppard CRC (1982) Coral populations on reef slopes and their major controls. Mar Ecol Prog Ser 7:83–115

    Article  Google Scholar 

  • Smith TB, Nemeth RS, Blondeau J, Calnan JM, Kadison E, Herzlieb S (2008) Assessing coral reef health across onshore to offshore stress gradients in the US Virgin Islands. Mar Pollut Bull 56:1983–1991

    CAS  PubMed  Article  Google Scholar 

  • Smith T, Blondeau J, Nemeth R, Pittman S, Calnan J, Kadison E, Gass J (2010) Benthic structure and cryptic mortality in a Caribbean mesophotic coral reef bank system, the Hind Bank Marine Conservation District, U.S. Virgin Islands. Coral Reefs (this issue)

  • Stafford-Smith MG, Ormond RFG (1992) Sediment rejection mechanisms of 42 species of Australian scleractinian corals. Aust J Mar Freshw Res 43:683–705

    Article  Google Scholar 

  • Stallings CD (2009) Fishery-independent data reveal negative effect of human population density on Caribbean predatory fish communities. PLoS ONE 4:e5333

    PubMed  Article  CAS  Google Scholar 

  • Stoddart DR (1962) Catastrophic effects on the British Honduras reefs and cays. Nature 196:512–515

    Article  Google Scholar 

  • Titlyanov EA (1987) Structure and morphological differences of colonies of reef-building branched corals from habitats with different light conditions. Mar Biol (Vladivostok) 1:32–36

    Google Scholar 

  • Toller WW, Rowan R, Knowlton N (2001) Zooxanthellae of the Montastraea annularis species complex: patterns of distribution of four taxa of Symbiodinium across different reefs and across depths. Biol Bull 201:348–359

    CAS  PubMed  Article  Google Scholar 

  • Toller W, Lundvall S, Hoetjes P (2008) Some observations made from ROV on mid-depth habitats and reef fish communities of Saba Bank, Netherlands Antilles. Saba Conservation Foundation

  • Tomasik T, van Woesik R, Mah A (1996) Rapid coral colonization of a recent lava flow following a volcanic eruption, Banda Islands, Indonesia. Coral Reefs 15:169–175

    Google Scholar 

  • Trnka M, Moulding AL (2006) Scientific review, compilation, and assessment of coral spawning time in the Atlantic/Caribbean. http://www.nova.edu/ncri/research/a21.html

  • Turner SJ (1994) Spatial variability in the abundance of the corallivorous gastropod Drupella cornus. Coral Reefs 13:41–48

    Article  Google Scholar 

  • Underwood JN, Smith LD, van Oppen MJH, Gilmour JP (2007) Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching. Mol Ecol 16:771–784

    CAS  PubMed  Article  Google Scholar 

  • Van den Hoek C, Breeman AM, Bak RPM, van Buurt G (1978) The distribution of algae, corals, and gorgonians in relation to depth, light attenuation, water movement, and grazing pressure in the fringing coral reef of Curaçao, Netherlands Antilles. Aquat Bot 5:1–46

    Article  Google Scholar 

  • Van der Land J (1977) The Saba Bank – A large atoll in the northeastern Caribbean. FAO Fisheries Report No 200, pp 469-481

  • Venn AA, Weber FK, Loram JE, Jones RJ (2009) Deep zooxanthellate corals at the high latitude Bermuda Seamount. Coral Reefs 28:135

    Article  Google Scholar 

  • Vermeij GJ (1986) Survival during biotic crises: the properties and evolutionary significance of refuges. In: Elliott DK (ed) Dynamics of extinction. Wiley, New York, pp 231–246

    Google Scholar 

  • Vermeij MJA (2005) A novel growth strategy allows Tubastrea coccinea to escape small-scale adverse conditions and start over again. Coral Reefs 24:442

    Article  Google Scholar 

  • Vermeij MJA (2006) Early life-history dynamics of Caribbean coral species on artificial substratum: the importance of competition, growth and variation in life-history strategy. Coral Reefs 25:59–71

    Article  Google Scholar 

  • Vermeij MJA, Bak RPM (2002) How are coral populations structured by light? Marine light regimes and the distribution of Madracis. Mar Ecol Prog Ser 233:105–116

    Article  Google Scholar 

  • Vermeij MJA, Bak RPM (2003) Species-specific population structure of closely related coral morphospecies along a depth gradient (5–60 m) over a Caribbean reef slope. Bull Mar Sci 73:725–744

    Google Scholar 

  • Vize PD (2006) Deepwater broadcast spawning by Montastraea cavernosa, Montastraea franksi, and Diploria strigosa at the Flower Garden Banks, Gulf of Mexico. Coral Reefs 25:169–171

    Article  Google Scholar 

  • Warner ME, LaJeunesse TC, Robison JD, Thur RM (2006) The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: potential implications for coral bleaching. Limnol Oceanogr 51:1887–1897

    Article  Google Scholar 

  • Webster PJ, Holland GJ, Curry JA, Chang H-R (2005) Changes in tropical cyclone number, duration, and intensity in a warming environment. Science 309:1844–1846

    CAS  PubMed  Article  Google Scholar 

  • West JM, Salm RV (2003) Resistance and resilience to coral bleaching: implications for coral reef conservation and management. Conserv Biol 17:956–967

    Article  Google Scholar 

  • Weil E (2004) Coral reef diseases in the wider Caribbean: status and prognosis. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, New York, pp 35–68

    Google Scholar 

  • Weis VM, Reynolds WS, deBoer MD, Krupp DA (2001) Host-symbiont specificity during onset of symbiosis between the dinoflagellates Symbiodinium spp. and planula larvae of the scleractinian coral Fungia scutaria. Coral Reefs 20:301–308

    Article  Google Scholar 

  • Whitfield PE, Hare JA, David AW, Harter SL, Munoz RC, Addison CM (2007) Abundance estimates of the Indo-Pacific lionfish Pterois volitans/miles complex in the Western North Atlantic. Biol Invasions 9:53–64

    Article  Google Scholar 

  • Wilkinson CR (2004) Status of coral reefs of the world 2004. Australian Institute of Marine Science, Townsville

    Google Scholar 

  • Wilkinson C, Souter D (2008) The status of Caribbean coral reefs after bleaching and hurricanes in 2005. Coral Reef Monitoring Network, Townsville

    Google Scholar 

  • Willis BL, van Oppen MJH, Miller DJ, Vollmer SV, Ayre DJ (2006) The role of hybridization in the evolution of reef corals. Annu Rev Ecol Evol Syst 37:489–517

    Article  Google Scholar 

  • Woodley JD, Chornesky EA, Clifford PA, Jackson JBC, Kaufman LA, Knowlton N, Land JC, Pearson MP, Porter JW, Rooney KW, Tunnicliffe VJ, Wahle CM, Wulff JL, Curtis ASG, Dallmeyer MD, Jupp BP, Koehl MAR, Niegel J, Sides EM (1981) Hurricane Allen’s impact on Jamaican coral reefs. Science 214:749–754

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Mark Vermeij, Tyler Smith, Thomas Bridge, Kyra Hay, Cynthia Riginos, Petra Visser, and five anonymous reviewers for valuable comments that significantly improved the manuscript. The authors of this study were supported by the Coral Reef Targeted Research Project (www.gefcoral.org) and the Australian Research Council Centre of Excellence in Coral Reef Studies. This is a contribution from the Coral Reef Ecosystems Laboratory at The University of Queensland (www.coralreefecosystems.org).

Author information

Author notes

  1. T. Ridgway

    Present address: Climate Change Group, Great Barrier Reef Marine park Authority, Townsville, QLD, 4810, Australia

  2. E. M. Sampayo

    Present address: Department of Biology, Pennsylvania State University, University Park, PA, 16802, USA

Authors and Affiliations

  1. Centre for Marine Studies, and ARC Centre of Excellence for Coral Reef Studies, The University of Queensland, St Lucia, QLD, 4072, Australia

    P. Bongaerts, T. Ridgway, E. M. Sampayo & O. Hoegh-Guldberg

  2. CARMABI Research Institute, Piscaderabaai z/n, PO Box 2090, Willemstad, Curaçao

    P. Bongaerts

Authors
  1. P. Bongaerts
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Ridgway
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. M. Sampayo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. O. Hoegh-Guldberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. Bongaerts.

Additional information

Communicated by Guest Editor Dr. John Marr

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bongaerts, P., Ridgway, T., Sampayo, E.M. et al. Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs. Coral Reefs 29, 309–327 (2010). https://doi.org/10.1007/s00338-009-0581-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-009-0581-x

Keywords

  • Deep coral reef
  • Refugia
  • Mesophotic
  • Global climate change
  • Disturbance