Coral Reefs

, Volume 36, Issue 3, pp 861–872 | Cite as

Localised hydrodynamics influence vulnerability of coral communities to environmental disturbances

  • George Shedrawi
  • James L. Falter
  • Kim J. Friedman
  • Ryan J. Lowe
  • Morgan S. Pratchett
  • Christopher J. Simpson
  • Conrad W. Speed
  • Shaun K. Wilson
  • Zhenlin Zhang


The movement of water can have a significant influence on the vulnerability of hermatypic corals to environmental disturbances such as cyclone damage, heat stress and anoxia. Here, we explore the relationship between small reef-scale water circulation patterns and measured differences in the abundance, composition and vulnerability of coral assemblages over decades. Changes in coral cover and community structure within Bill’s Bay (Ningaloo Reef, Western Australia) over a 22-yr period, during which multiple disturbance events (including mass bleaching, anoxia, and tropical cyclones) have impacted the area, were compared with spatial variation in water residence times (WRT). We found that reef sites associated with longer water residence times (WRT >15 h) experienced higher rates of coral mortality during acute environmental disturbances compared to reef sites with shorter WRT. Shifts in coral community composition from acroporid to faviid-dominated assemblages were also more prominent at sites with long WRT compared to reef sites with shorter WRT, although shifts in community composition were also observed at sites close to shore. Interestingly, these same long-WRT sites also tended to have the fastest recovery rates so that coral cover was returned to original levels of approximately 20% over two decades. This study provides empirical evidence that spatial patterns in water circulation and flushing can influence the resilience of coral communities, thus identifying areas sensitive to emerging threats associated with global climate change.


Climate change Coral-reef dynamics Disturbance Recovery Hydrodynamics Marine protected area 



The authors would like to thank the Department of Parks and Wildlife Exmouth regional office for their support of research and monitoring within the World Heritage Ningaloo Marine Park. Comments from the editor and two anonymous reviewers and Dr. Rebecca Fisher greatly improved the manuscript.

Supplementary material

338_2017_1576_MOESM1_ESM.eps (11 kb)
Supplementary material 1 (EPS 11 kb)
338_2017_1576_MOESM2_ESM.docx (53 kb)
Supplementary material 2 (DOCX 54 kb)


  1. Akaike H (1973) Maximum likelihood identification of Gaussian autoregressive moving average models. Biometrika 60:255–265CrossRefGoogle Scholar
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  3. Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253PubMedCrossRefGoogle Scholar
  4. Armstrong S (2007) Ningaloo Marine Park Drupella long-term monitoring program: results of the 2006 survey. Data report NIN/NMP-2007/03 Marine Science Program, Department of Environment and Conservation, Perth, Western Australia (unpublished report)Google Scholar
  5. Baird A, Marshall PA (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar Ecol Prog Ser 237:133–141CrossRefGoogle Scholar
  6. Baird ME, Atkinson MJ (1997) Measurement and prediction of mass transfer to experimental coral reef communities. Limnol Oceanogr 42:1685–1693CrossRefGoogle Scholar
  7. Bak RP (1978) Lethal and sublethal effects of dredging on reef corals. Mar Pollut Bull 9:14–16CrossRefGoogle Scholar
  8. Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471CrossRefGoogle Scholar
  9. Berkelmans R (2009) Bleaching and mortality thresholds: how much is too much? In: van Oppen MJH, Lough JM (eds) Coral bleaching: patterns, processes, causes and consequences. Springer, Berlin, pp 103–119CrossRefGoogle Scholar
  10. Berkelmans R, De’ath G, Kininmonth S, Skirving WJ (2004) A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions. Coral Reefs 23:74–83CrossRefGoogle Scholar
  11. Berumen ML, Pratchett MS (2006) Recovery without resilience: persistent disturbance and long-term shifts in the structure of fish and coral communities at Tiahura Reef, Moorea. Coral Reefs 25:647–653CrossRefGoogle Scholar
  12. Brown E, Cox E, Jokiel P, Rodgers K, Smith W, Tissot B, Coles SL, Hultquist J (2004) Development of benthic sampling methods for the Coral Reef Assessment and Monitoring Program (CRAMP) in Hawai’i. Pacific Science 58:145–158CrossRefGoogle Scholar
  13. Burnham KP, Anderson DR (2001) Kullback-Leibler information as a basis for strong inference in ecological studies. Wildl Res 28:111–119CrossRefGoogle Scholar
  14. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, NetherlandsGoogle Scholar
  15. Burrows MT, Schoeman DS, Richardson AJ, Molinos JG, Hoffmann A, Buckley LB, Moore PJ, Brown CJ, Bruno JF, Duarte CM, Halpern BS, Hoegh-Guldberg O, Kappel CV, Kiessling W, O’Connor MI, Pandolfi JM, Parmesan C, Sydeman WJ, Ferrier S, Williams KJ, Poloczanska ES (2014) Geographical limits to species-range shifts are suggested by climate velocity. Nature 507:492–495PubMedCrossRefGoogle Scholar
  16. Burt J, Bartholomew A, Usseglio P (2008) Recovery of corals a decade after a bleaching event in Dubai, United Arab Emirates. Mar Biol 154:27–36CrossRefGoogle Scholar
  17. Cacciapaglia C, van Woesik R (2015) Reef-coral refugia in a rapidly changing ocean. Glob Chang Biol 21:2272–2282PubMedCrossRefGoogle Scholar
  18. Clarke KR, Gorley RN (2006) PRIMER v6 user manual and program. Primer-E Ltd, Plymouth, UKGoogle Scholar
  19. Coker DJ, Wilson SK, Pratchett MS (2013) Importance of live coral habitat for reef fishes. Rev Fish Biol Fish 24:89–126CrossRefGoogle Scholar
  20. Cole AJ, Pratchett MS, Jones GP (2008) Diversity and functional importance of coral-feeding fishes on tropical coral reefs. Fish Fish 9:286–307CrossRefGoogle Scholar
  21. Connell JH, Hughes TP, Wallace CC (1997) A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecol Monogr 67:461–488CrossRefGoogle Scholar
  22. Davison AC, Hinkley DV (1997) Bootstrap methods and their application. Cambridge University Press, CambridgeGoogle Scholar
  23. De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci U S A 109:17995–17999PubMedPubMedCentralCrossRefGoogle Scholar
  24. Dayton PK (1971) Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol Monogr 41:351–389CrossRefGoogle Scholar
  25. Dennison WC, Barnes DJ (1988) Effect of water motion on coral photosynthesis and calcification. J Exp Mar Bio Ecol 115:67–77CrossRefGoogle Scholar
  26. Depczynski M, Gilmour JP, Ridgway T, Barnes H, Heyward AJ, Holmes TH, Moore JAY, Radford BT, Thomson DP, Tinkler P, Wilson SK (2013) Bleaching, coral mortality and subsequent survivorship on a west Australian fringing reef. Coral Reefs 32:233–238CrossRefGoogle Scholar
  27. Enquist BJ, Enquist CA (2011) Long-term change within a neotropical forest: assessing differential functional and floristic responses to disturbance and drought. Glob Chang Biol 17:1408–1424CrossRefGoogle Scholar
  28. Erftemeijer PLA, Riegl B, Hoeksema BW, Todd PA (2012) Environmental impacts of dredging and other sediment disturbances on corals: a review. Mar Pollut Bull 64:1737–1765PubMedCrossRefGoogle Scholar
  29. Fabricius KE, Mieog JC, Colin PL, Idip D, van Oppen MJH (2004) Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol Ecol 13:2445–2458PubMedCrossRefGoogle Scholar
  30. Facon M, Pinault M, Obura D, Pioch S, Pothin K, Bigot L, Garnier R, Quod J-P (2016) A comparative study of the accuracy and effectiveness of line and point intercept transect methods for coral reef monitoring in the southwestern Indian Ocean islands. Ecol Indic 60:1045–1055CrossRefGoogle Scholar
  31. Falter JL, Atkinson MJ, Merrifield MA (2004) Mass-transfer limitation of nutrient uptake by a wave-dominated reef flat community. Limnol Oceanogr 49:1820–1831CrossRefGoogle Scholar
  32. Falter JL, Lowe RJ, Zhang Z, McCulloch M (2013) Physical and biological controls on the carbonate chemistry of coral reef waters: effects of metabolism, wave forcing, sea level, and geomorphology. PLoS One 8:e53303PubMedPubMedCentralCrossRefGoogle Scholar
  33. Falter JL, Zhang Z, Lowe RJ, McGregor F, Keesing J, McCulloch MT (2014) Assessing the drivers of spatial variation in thermal forcing across a nearshore reef system and implications for coral bleaching. Limnol Oceanogr 59:1241–1255CrossRefGoogle Scholar
  34. Fan T-Y, Dai C-F (1999) Reproductive plasticity in the reef coral Echinopora lamellosa. Mar Ecol Prog Ser 190:297–301CrossRefGoogle Scholar
  35. Game ET, McDonald-Madden E, Puotinen ML, Possingham HP (2008) Should we protect the strong or the weak? Risk, resilience, and the selection of marine protected areas. Conserv Biol 22:1619–1629PubMedCrossRefGoogle Scholar
  36. Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960PubMedCrossRefGoogle Scholar
  37. Gove JM, Williams GJ, McManus MA, Heron SF, Sandin SA, Vetter OJ, Foley DG (2013) Quantifying climatological ranges and anomalies for Pacific coral reef ecosystems. PLoS One 8:e61974PubMedPubMedCentralCrossRefGoogle Scholar
  38. Graham EM, Baird AH, Connolly SR (2008) Survival dynamics of scleractinian coral larvae and implications for dispersal. Coral Reefs 27:529–539CrossRefGoogle Scholar
  39. Graham NAJ, Nash KL, Kool JT (2011) Coral reef recovery dynamics in a changing world. Coral Reefs 30:283–294CrossRefGoogle Scholar
  40. Graham NAJ, Jennings S, MacNeil MA, Mouillot D, Wilson SK (2015) Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518:94–97PubMedCrossRefGoogle Scholar
  41. Halford AR, Perret J (2009) Patterns of recovery in catastrophically disturbed reef fish assemblages. Mar Ecol Prog Ser 383:261–272CrossRefGoogle Scholar
  42. Hare JA, Morrison WE, Nelson MW, Stachura MM, Teeters EJ, Griffis RB, Alexander MA, Scott JD, Alade L, Bell RJ, Chute AS, Curti KL, Curtis TH, Kircheis D, Kocik JF, Lucey SM, McCandless CT, Milke LM, Richardson DE, Robillard E, Walsh HJ, McManus MC, Marancik KE, Griswold CA (2016) A vulnerability assessment of fish and invertebrates to climate change on the northeast U.S. continental shelf. PLoS One 11:e0146756PubMedPubMedCentralCrossRefGoogle Scholar
  43. Hinrichs S, Patten NL, Feng M, Strickland D, Waite AM (2013) Which environmental factors predict seasonal variation in the coral health of Acropora digitifera and Acropora spicifera at Ningaloo Reef? PLoS One 8:e60830PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866CrossRefGoogle Scholar
  45. Holling CS (1973) Resilience and stability of ecological systems. Annu Rev Ecol Syst 4:1–23CrossRefGoogle Scholar
  46. Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551PubMedCrossRefGoogle Scholar
  47. Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263CrossRefGoogle Scholar
  48. Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365PubMedCrossRefGoogle Scholar
  49. Hurvich CM, Tsai C-L (1993) A corrected Akaike information criterion for vector autoregressive model selection. J Time Ser Anal 14:271–279CrossRefGoogle Scholar
  50. Jokiel PL (1978) Effects of water motion on reef corals. J Exp Mar Bio Ecol 35:87–97CrossRefGoogle Scholar
  51. Kaiser MJ, Clarke KR, Hinz H, Austen MCV, Somerfield PJ, Karakassis I (2006) Global analysis of response and recovery of benthic biota to fishing. Mar Ecol Prog Ser 311:1–14CrossRefGoogle Scholar
  52. Karlson RH, Hurd LE (1993) Disturbance, coral reef communities, and changing ecological paradigms. Coral Reefs 12:117–125CrossRefGoogle Scholar
  53. Legendre P, Fortin M-J (1989) Spatial pattern and ecological analysis. Vegetatio 80:107–138CrossRefGoogle Scholar
  54. Lenihan HS, Holbrook SJ, Schmitt RJ, Brooks AJ (2011) Influence of corallivory, competition, and habitat structure on coral community shifts. Ecology 92:1959–1971PubMedCrossRefGoogle Scholar
  55. Lenihan HS, Adjeroud M, Kotchen MJ, Hench JL, Nakamura T (2008) Reef structure regulates small-scale spatial variation in coral bleaching. Mar Ecol Prog Ser 370:127–141CrossRefGoogle Scholar
  56. Lenihan HS, Hench JL, Holbrook SJ, Schmitt RJ, Potoski M (2015) Hydrodynamics influence coral performance through simultaneous direct and indirect effects. Ecology 96:1540–1549CrossRefGoogle Scholar
  57. Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192CrossRefGoogle Scholar
  58. Lesser MP, Weis VM, Patterson MR, Jokiel PL (1994) Effects of morphology and water motion on carbon delivery and productivity in the reef coral, Pocillopora damicornis (Linnaeus): diffusion barriers, inorganic carbon limitation, and biochemical plasticity. J Exp Mar Bio Ecol 178:153–179CrossRefGoogle Scholar
  59. Leujak W, Ormond RFG (2007) Comparative accuracy and efficiency of six coral community survey methods. J Exp Mar Bio Ecol 351:168–187CrossRefGoogle Scholar
  60. Liu G, Strong AE, Skirving W, Arzayus LF (2006) Overview of NOAA coral reef watch program’s near-real time satellite global coral bleaching monitoring activities. In: Proceeding of the 10th international coral reef symposium, vol 1. pp 1783–1793Google Scholar
  61. Lowe RJ, Falter JL (2015) Oceanic forcing of coral reefs. Annu Rev Mar Sci 7:43–66CrossRefGoogle Scholar
  62. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131CrossRefGoogle Scholar
  63. Madin JSC (2006) Ecological consequences of major hydrodynamic disturbances on coral reefs. Nature 444:477–480PubMedCrossRefGoogle Scholar
  64. McClanahan T, Polunin N, Done T (2002) Ecological states and the resilience of coral reefs. Conservation Ecology 6:18CrossRefGoogle Scholar
  65. McClanahan TR, Baird AH, Marshall PA, Toscano MA (2004) Comparing bleaching and mortality responses of hard corals between southern Kenya and the Great Barrier Reef, Australia. Mar Pollut Bull 48:327–335PubMedCrossRefGoogle Scholar
  66. Moore JAY, Bellchambers LM, Depczynski M, Evans RD, Evans SN, Field SN, Friedman K, Gilmour JP, Holmes TH, Middlebrook R, Radford B, Ridgway T, Shedrawi G, Taylor H, Thomson DP, Wilson SK (2012) Unprecedented mass bleaching and loss of coral across 12° of latitude in Western Australia in 2010–11. PLoS One 7:e51807PubMedPubMedCentralCrossRefGoogle Scholar
  67. Mosquera I, Cote IM, Jennings S, Reynolds JD (2000) Conservation benefits of marine reserves for fish populations. Animal Conservation 3:321–332CrossRefGoogle Scholar
  68. Muir PR, Wallace CC, Done T, Aguirre JD (2015) Limited scope for latitudinal extension of reef corals. Science 348:1135–1138PubMedCrossRefGoogle Scholar
  69. Mumby PJ, Chisholm JRM, Edwards AJ, Andrefouet S, Jaubert J (2001) Cloudy weather may have saved Society Island reef corals during the 1998 ENSO event. Mar Ecol Prog Ser 222:209–216CrossRefGoogle Scholar
  70. Nakamura T, Van Woesik R (2001) Water-flow rates and passive diffusion partially explain differential survival of corals during the 1998 bleaching event. Mar Ecol Prog Ser 212:301–304CrossRefGoogle Scholar
  71. Nakamura T, Yamasaki H (2005) Requirement of water-flow for sustainable growth of pocilloporid corals during high temperature periods. Mar Pollut Bull 50:1115–1120PubMedCrossRefGoogle Scholar
  72. Nakamura T, Van Woesik R, Yamasaki H (2005) Photoinhibition of photosynthesis is reduced by water flow in the reef-building coral Acropora digitifera. Mar Ecol Prog Ser 301:109–118CrossRefGoogle Scholar
  73. Nyström M, Graham NAJ, Lokrantz J, Norström AV (2008) Capturing the cornerstones of coral reef resilience: linking theory to practice. Coral Reefs 27:795–809CrossRefGoogle Scholar
  74. Oliver TA, Palumbi SR (2011) Many corals host thermally resistant symbionts in high-temperature habitat. Coral Reefs 30:241–250CrossRefGoogle Scholar
  75. Onton K, Page C, Wilson S, Neale S, Armstrong S (2011) Distribution and drivers of coral disease at Ningaloo reef, Indian Ocean. Mar Ecol Prog Ser 433:75–84CrossRefGoogle Scholar
  76. Osborne K, Dolman AM, Burgess SC, Johns KA (2011) Disturbance and the dynamics of coral cover on the Great Barrier Reef (1995–2009). PLoS One 6:e17516PubMedPubMedCentralCrossRefGoogle Scholar
  77. Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJH, Paredes G, Warner RR, Jackson JBC (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–958PubMedCrossRefGoogle Scholar
  78. Patterson MR, Sebens KP (1989) Forced convection modulates gas exchange in cnidarians. Proc Natl Acad Sci U S A 86:8833–8836PubMedPubMedCentralCrossRefGoogle Scholar
  79. Patterson MR, Sebens KP, Olson RR (1991) In situ measurements of flow effects on primary production and dark respiration in reef corals. Limnol Oceanogr 36:936–948CrossRefGoogle Scholar
  80. Pickett ST, White PS (1985) The ecology of natural disturbance and patch dynamics. Academic Press, Cambridge, MAGoogle Scholar
  81. Pinheiro J, Bates D (2000) Extending the basic linear mixed-effects model. In: Splettstoesser J (ed) Mixed-effects models in S and S-PLUS. Springer, New York, pp 201–270CrossRefGoogle Scholar
  82. Pisapia C, Pratchett MS (2014) Spatial variation in background mortality among dominant coral taxa on Australia’s Great Barrier Reef. PLoS One 9:e100969PubMedPubMedCentralCrossRefGoogle Scholar
  83. Pratchett MS, Trapon M, Berumen ML, Chong-Seng K (2011) Recent disturbances augment community shifts in coral assemblages in Moorea, French Polynesia. Coral Reefs 30:183–193CrossRefGoogle Scholar
  84. Pratchett MS, Munday P, Wilson SK, Graham NA, Cinner JE, Bellwood DR, Jones GP, Polunin NV, McClanahan TR (2008) Effects of climate-induced coral bleaching on coral-reef fishes. Oceanogr Mar Biol Annu Rev 46:251–296Google Scholar
  85. Price JF, Morzel J, Niiler PP (2008) Warming of SST in the cool wake of a moving hurricane. J Geophys Res Oceans 113:C07010CrossRefGoogle Scholar
  86. R Core Development Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  87. Richmond RH (1997) Reproduction and recruitment in corals: critical links in the persistence of reefs. In: Birkeland C (ed) Life and death of coral reefs. Chapman & Hall, New York, pp 175–197CrossRefGoogle Scholar
  88. Richmond RH, Hunter CL (1990) Reproduction and recruitment of corals: comparisons among the Caribbean, the tropical Pacific, and the Red Sea. Mar Ecol Prog Ser 60:185–203CrossRefGoogle Scholar
  89. Roberts CM, McClean CJ, Veron JEN, 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 295:1280–1284PubMedCrossRefGoogle Scholar
  90. Schutter M, Crocker J, Paijmans A, Janse M, Osinga R, Verreth AJ, Wijffels RH (2010) The effect of different flow regimes on the growth and metabolic rates of the scleractinian coral Galaxea fascicularis. Coral Reefs 29:737–748CrossRefGoogle Scholar
  91. Sebens KP (1997) Adaptive responses to water flow: morphology, energetics, and distribution of reef corals. Proc 8th Int Coral Reef Symp 2:1053–1058Google Scholar
  92. Sebens KP, Helmuth B, Carrington E, Agius B (2003) Effects of water flow on growth and energetics of the scleractinian coral Agaricia tenuifolia in Belize. Coral Reefs 22:35–47Google Scholar
  93. Shashar N, Kinane S, Jokiel PL, Patterson MR (1996) Hydromechanical boundary layers over a coral reef. J Exp Mar Bio Ecol 199:17–28CrossRefGoogle Scholar
  94. Simpson CJ, Cary JL, Masini RJ (1993) Destruction of corals and other reef animals by coral spawn slicks on Ningaloo Reef, Western Australia. Coral Reefs 12:185–191CrossRefGoogle Scholar
  95. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. WH Freeman, LondonGoogle Scholar
  96. Sousa WP (1984) The role of disturbance in natural communities. Annu Rev Ecol Syst 15:353–391CrossRefGoogle Scholar
  97. Speed CW, Babcock RC, Bancroft KP, Beckley LE, Bellchambers LM, Depczynski M, Field SN, Friedman KJ, Gilmour JP, Hobbs J-PA, Kobryn HT, Moore JAY, Nutt CD, Shedrawi G, Thomson DP, Wilson SK (2013) Dynamic stability of coral reefs on the west Australian coast. PLoS One 8:e69863PubMedPubMedCentralCrossRefGoogle Scholar
  98. Taebi S, Lowe RJ, Pattiaratchi CB, Ivey GN, Symonds G (2012) A numerical study of the dynamics of the wave-driven circulation within a fringing reef system. Ocean Dyn 62:585–602CrossRefGoogle Scholar
  99. Taebi S, Lowe RJ, Pattiaratchi CB, Ivey GN, Symonds G, Brinkman R (2011) Nearshore circulation in a tropical fringing reef system. J Geophys Res Oceans 116:C02016CrossRefGoogle Scholar
  100. Thomas FIM, Atkinson MJ (1997) Ammonium uptake by coral reefs: effects of water velocity and surface roughness on mass transfer. Limnol Oceanogr 42:81–88CrossRefGoogle Scholar
  101. Toohey BD, Kendrick GA (2007) Survival of juvenile Ecklonia radiata sporophytes after canopy loss. J Exp Mar Bio Ecol 349:170–182CrossRefGoogle Scholar
  102. Toohey BD, Kendrick GA, Harvey ES (2007) Disturbance and reef topography maintain high local diversity in Ecklonia radiata kelp forests. Oikos 116:1618–1630CrossRefGoogle Scholar
  103. Turner SJ (1994) Spatial variability in the abundance of the corallivorous gastropod Drupella cornus. Coral Reefs 13:41–48CrossRefGoogle Scholar
  104. Van Schoubroeck P, Long S (2007) Disturbance history of coral reef communities in Bill’s Bay, Ningaloo Marine Park, 1989–2007. Marine Science Program, Department of Environment and Conservation, Perth, AustraliaGoogle Scholar
  105. Venti A, Kadko D, Andersson AJ, Langdon C, Bates NR (2012) A multi-tracer model approach to estimate reef water residence times. Limnol Oceanogr Methods 10:1078–1095CrossRefGoogle Scholar
  106. Wakeford M, Done TJ, Johnson CR (2007) Decadal trends in a coral community and evidence of changed disturbance regime. Coral Reefs 27:1–13CrossRefGoogle Scholar
  107. Wall M, Schmidt GM, Janjang P, Khokiattiwong S, Richter C (2012) Differential impact of monsoon and large amplitude internal waves on coral reef development in the Andaman Sea. PLoS One 7:e50207PubMedPubMedCentralCrossRefGoogle Scholar
  108. West JM, Salm RV (2003) Resistance and resilience to coral bleaching: implications for coral reef conservation and management. Conserv Biol 17:956–967CrossRefGoogle Scholar
  109. White PS, Pickett ST (1985) Natural disturbance and patch dynamics: an introduction. In: Pickett STA, White PS (eds) The ecology of natural disturbance and patch dynamics. Academic Press, Cambridge, MAGoogle Scholar
  110. Willis BL, Oliver JK (1990) Direct tracking of coral larvae: implications for dispersal studies of planktonic larvae in topographically complex environments. Ophelia 32:145–162CrossRefGoogle Scholar
  111. Wilson SK, Depczynski M, Fisher R, Holmes TH, O’Leary RA, Tinkler P (2010) Habitat associations of juvenile fish at Ningaloo Reef, Western Australia: the importance of coral and algae. PLoS One 5:e15185PubMedPubMedCentralCrossRefGoogle Scholar
  112. Zhang Z, Falter J, Lowe R, Ivey G (2012) The combined influence of hydrodynamic forcing and calcification on the spatial distribution of alkalinity in a coral reef system. J Geophys Res Oceans 117:C04034Google Scholar
  113. Zhang Z, Falter J, Lowe R, Ivey G, McCulloch M (2013) Atmospheric forcing intensifies the effects of regional ocean warming on reef-scale temperature anomalies during a coral bleaching event. J Geophys Res Oceans 118:4600–4616CrossRefGoogle Scholar
  114. Zhu B, Wang G, Huang B, Tseng CK (2004) Effects of temperature, hypoxia, ammonia and nitrate on the bleaching among three coral species. Chin Sci Bull 49:1923–1928CrossRefGoogle Scholar
  115. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, DordrechtGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • George Shedrawi
    • 1
  • James L. Falter
    • 2
    • 3
    • 4
  • Kim J. Friedman
    • 1
    • 2
  • Ryan J. Lowe
    • 2
    • 3
    • 4
  • Morgan S. Pratchett
    • 5
  • Christopher J. Simpson
    • 1
  • Conrad W. Speed
    • 1
    • 2
  • Shaun K. Wilson
    • 1
    • 2
  • Zhenlin Zhang
    • 2
    • 3
    • 4
  1. 1.Department of Parks and Wildlife, Science and Conservation DivisionMarine Science ProgramKensingtonAustralia
  2. 2.The UWA Oceans InstituteCrawleyAustralia
  3. 3.School of Earth and EnvironmentUniversity of Western AustraliaPerthAustralia
  4. 4.ARC Centre of Excellence for Coral Reef StudiesUniversity of Western AustraliaPerthAustralia
  5. 5.ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia

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