, Volume 818, Issue 1, pp 193–209 | Cite as

The hidden dynamics of low coral cover communities

  • Peter J. Edmunds
Primary Research Paper


The coral reef crisis has resulted in many reefs stabilizing in a low coral cover state, and this condition is exemplified by the fringing reefs of St. John, US Virgin Islands, where coral cover has remained low for decades. To evaluate the demographic features maintaining this condition, a decade of coral abundance was examined in three domains: recruits, small colonies (≤ 40-mm diameter), and cover. While cover was stable from 2007 to 2016, other aspects of coral community structure changed in taxonomically unique ways differing among domains. Most changes occurred gradually, although the warm year of 2010 was associated with perturbations in growth, mortality, and density that differed among domains and taxa, and summed to a weak signal distinguishing communities before and after ~ 2011/2012. As a result, coral community structure was taxonomically shuffled within each domain, while low cover was maintained. These low coral cover communities may be characterized by functional redundancy among taxa and a weakening of interactions among them that traditionally have supported emergent properties like community calcification. With persistent failure of recruitment to augment coral cover, some corals may already occur at such low abundances that they cannot perform the ecological services with which they were once associated.


Scleractinia Caribbean St. John Recruitment Dynamics Demography 



This work was funded by the US National Science Foundation (DEB 03-43570, 08-41441, and 13-50146), and was completed under research permits issued by the Virgin Islands National Park (most recently VIIS-2016-SCI-0031). I am indebted to my graduate students who have made decades of fieldwork possible in St. John, the staff at VIERS who have made me welcome at the field site, and S. Prosterman and V. Powell for on-site logistical support. This is contribution number 278 of the CSUN marine biology program.

Supplementary material

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Supplementary material 1 (DOCX 803 kb)


  1. Alvarez-Filip, L., J. P. Carricart-Ganivet, G. Horta-Puga & R. Iglesias-Prieto, 2013. Shifts in coral-assemblage composition do not ensure persistence of reef functionality. Scientific Reports 3: 3486.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Angert, A. L., T. E. Huxman, P. Chesson & D. L. Venable, 2009. Functional tradeoffs determine species coexistence via the storage effect. Proceedings of the National Academy of Sciences 106: 11641–11645.CrossRefGoogle Scholar
  3. Arnold, S. N. & R. S. Steneck, 2011. Settling into an increasingly hostile world: the rapidly closing “recruitment window” for corals. PLoS One 6: e28681.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Arnold, S. N., R. S. Steneck & P. J. Mumby, 2010. Running the gauntlet: inhibitory effects of algal turfs on the processes of coral recruitment. Marine Ecology Progress Series 414: 91–105.CrossRefGoogle Scholar
  5. Aronson, R. B. & W. F. Precht, 2001. White-band disease and the changing face of Caribbean coral reefs. Hydrobiologia 460: 25–38.CrossRefGoogle Scholar
  6. Aronson, R. B., W. F. Precht, I. G. Macintyre & T. J. Murdoch, 2000. Ecosystems: coral bleach-out in Belize. Nature 405: 36.PubMedCrossRefGoogle Scholar
  7. Babcock, R. C., 1991. Comparative demography of three species of scleractinian corals using age-and size-dependent classifications. Ecological Monographs 61: 225–244.CrossRefGoogle Scholar
  8. Babcock, R. C., A. H. Baird, S. Piromvaragorn, D. P. Thomson & B. L. Willis, 2003. Identification of scleractinian coral recruits from Indo-Pacific reefs. Zoological Studies 42: 211–226.Google Scholar
  9. Baird, A. H., A. Salih & A. Jones, 2006. Fluorescence census techniques for the early detection of coral recruits. Coral Reefs 25: 73–76.CrossRefGoogle Scholar
  10. Barberán, A., E. O. Casamayor & N. Fierer, 2014. The microbial contribution to macroecology. Frontiers in Microbiology. Scholar
  11. Beets, J. P., L. Lewand & E. S. Zullo, 1986. Marine community descriptions and maps of bays within the Virgin Islands National Park/Biosphere Reserve. US Department of the Interior, National Park Service.Google Scholar
  12. Bell, J. J., S. K. Davy, T. Jones, M. W. Taylor & N. S. Webster, 2013. Could some coral reefs become sponge reefs as our climate changes? Global Change Biology 19: 2613–2624.PubMedCrossRefGoogle Scholar
  13. Black, K. P., P. J. Moran & L. S. Hammond, 1991. Numerical models show coral reefs can be self-seeding. Marine Ecology Progress Series 74: 1–11.CrossRefGoogle Scholar
  14. Box, S. J. & P. J. Mumby, 2007. Effect of macroalgal competition on growth and survival of juvenile Caribbean corals. Marine Ecology Progress Series 342: 139–149.CrossRefGoogle Scholar
  15. Bramanti, L. & P. J. Edmunds, 2016. Density-associated recruitment mediates coral population dynamics on a coral reef. Coral reefs 35: 543–553.CrossRefGoogle Scholar
  16. Bruno, J. F., 2013. Coral reefs: building a better crystal ball. Current Biology 23: R473–R475.PubMedCrossRefGoogle Scholar
  17. Bruno, J. F. & E. R. Selig, 2007. Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS One 2: e711.PubMedPubMedCentralCrossRefGoogle Scholar
  18. Burman, S. G., R. B. Aronson & R. van Woesik, 2012. Biotic homogenization of coral assemblages along the Florida reef tract. Marine Ecology Progress Series 467: 89–96.CrossRefGoogle Scholar
  19. Caley, M. J., M. H. Carr, M. A. Hixon, T. P. Hughes, G. P. Jones & B. A. Menge, 1996. Recruitment and the local dynamics of open marine populations. Annual Review of Ecology and Systematics 27: 477–500.CrossRefGoogle Scholar
  20. Carlon, D. B. & R. R. Olson, 1993. Larval dispersal distance as an explanation for adult spatial pattern in two Caribbean reef corals. Journal of Experimental Marine Biology and Ecology 173: 247–263.CrossRefGoogle Scholar
  21. Carpenter, K. E., M. Abrar, G. Aeby, R. B. Aronson, S. Banks, A. Bruckner, A. Chiriboga, J. Cortés, J. C. Delbeek, L. DeVantier & G. J. Edgar, 2008. One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321: 560–563.PubMedCrossRefGoogle Scholar
  22. Chadwick, N.E. & K.M. Morrow, 2011. Competition among sessile organisms on coral reefs. In Coral Reefs: an ecosystem in transition: 347–371.Google Scholar
  23. Chiappone, M. & K. M. Sullivan, 1996. Distribution, abundance and species composition of juvenile scleractinian corals in the Florida reef tract. Bulletin of Marine Science 58: 555–569.Google Scholar
  24. Clark, D. A. & D. B. Clark, 1999. Assessing the growth of tropical rain forest trees: issues for forest modeling and management. Ecological Applications 9: 981–997.CrossRefGoogle Scholar
  25. Comeau, S., P. J. Edmunds, N. B. Spindel & R. C. Carpenter, 2014. Fast coral reef calcifiers are more sensitive to ocean acidification in short-term laboratory incubations. Limnology and Oceanography 59: 1081–1091.CrossRefGoogle Scholar
  26. Connell, J. H., 1978. Diversity in tropical rain forests and coral reefs. Science 199: 1302–1310.PubMedCrossRefGoogle Scholar
  27. Cunning, R., R.D. Gates, & P.J. Edmunds, 2017. Using high-throughput sequencing of ITS2 to describe Symbiodinium metacommunities in St. John, US Virgin Islands. PeerJ: e2925v1.Google Scholar
  28. Darling, E. S., L. Alvarez-Filip, T. A. Oliver, T. R. McClanahan & I. M. Côté, 2012. Evaluating life-history strategies of reef corals from species traits. Ecology Letters 15: 378–1386.CrossRefGoogle Scholar
  29. Dayton, P. K., M. J. Tegner, P. B. Edward & K. L. Riser, 1998. Sliding baselines, ghosts, and reduced expectations in kelp forest communities. Ecological Applications 8: 309–322.CrossRefGoogle Scholar
  30. De Bakker, D. M., E. H. Meesters, R. P. M. Bak, G. Nieuwland & F. C. van Duyl, 2016. Long-term shifts in coral communities on shallow to deep reef slopes of Curaçao and Bonaire: are there any winners? Frontiers in Marine Science 3: 247.CrossRefGoogle Scholar
  31. De Bakker, D. M., F. C. van Duyl, R. P. M. Bak, M. M. Nugues, G. Nieuwland & E. H. Meesters, 2017. 40 years of benthic community change on the Caribbean reefs of Curaçao and Bonaire: the rise of slimy cyanobacterial mats. Coral Reefs 36: 355–367.CrossRefGoogle Scholar
  32. De’ath, G., K. E. Fabricius, H. Sweatman & M. Puotinen, 2012. The 27–year decline of coral cover on the Great Barrier Reef and its causes. Proceedings of the National Academy of Sciences 109: 17995–17999.CrossRefGoogle Scholar
  33. Dirzo, R., H. S. Young, M. Galetti, G. Ceballos, N. J. Isaac & B. Collen, 2014. Defaunation in the Anthropocene. Science 345: 401–406.PubMedCrossRefGoogle Scholar
  34. Doropoulos, C., S. Ward, G. Roff, M. González-Rivero & P. J. Mumby, 2015. Linking demographic processes of juvenile corals to benthic recovery trajectories in two common reef habitats. PLoS One 10: e0128535.PubMedPubMedCentralCrossRefGoogle Scholar
  35. Doropoulos, C., G. Roff, Y. Bozec, M. Zupan, J. Werminghausen & P. J. Mumby, 2016a. Characterizing the ecological trade-offs throughout the early ontogeny of coral recruitment. Ecological Monographs 86: 20–44.Google Scholar
  36. Doropoulos, C., G. Roff, M. S. Visser & P. J. Mumby, 2016b. Sensitivity of coral recruitment to subtle shifts in early community succession. Ecology 98: 304–314.CrossRefGoogle Scholar
  37. Edmunds, P. J., 2000. Patterns in the distribution of juvenile corals and coral reef community structure in St. John, US Virgin Islands. Marine Ecology Progress Series 202: 113–124.CrossRefGoogle Scholar
  38. Edmunds, P. J., 2013. Decadal-scale changes in the community structure of coral reefs of St. John, US Virgin Islands. Marine Ecology Progress Series 489: 107–123.CrossRefGoogle Scholar
  39. Edmunds, P. J., 2017. Intraspecific variation in growth rate is a poor predictor of fitness for reef corals. Ecology 98: 2191–2200.PubMedCrossRefGoogle Scholar
  40. Edmunds, P. J. & R. Elahi, 2007. The demographics of a 15-year decline in cover of the Caribbean reef coral Montastraea annularis. Ecological Monographs 77: 3–18.CrossRefGoogle Scholar
  41. Edmunds, P. J. & S. Gray, 2014. The effects of storms, heavy rain, and sedimentation on the shallow coral reefs of St. John. US Virgin Islands. Hydrobiologia 734: 143–158.CrossRefGoogle Scholar
  42. Edmunds, P. J. & H. R. Lasker, 2016. Cryptic regime shift in benthic community structure on shallow reefs in St. John, US Virgin Islands. Marine Ecology Progress Series 559: 1–12.CrossRefGoogle Scholar
  43. Edmunds, P. J., D. A. Roberts & R. Singer, 1990. Reefs of the northeastern Caribbean I. Scleractinian populations. Bulletin of Marine Science 46: 780–789.Google Scholar
  44. Fadlallah, Y. H., 1983. Sexual reproduction, development and larval biology in scleractinian corals. Coral reefs 2: 129–150.CrossRefGoogle Scholar
  45. Gardner, T. A., I. M. Côté, J. A. Gill, A. Grant & A. R. Watkinson, 2003. Long-term region-wide declines in Caribbean corals. Science 301: 958–960.PubMedCrossRefGoogle Scholar
  46. Gilmour, J. P., L. D. Smith, A. J. Heyward, A. H. Baird & M. S. Pratchett, 2013. Recovery of an isolated coral reef system following severe disturbance. Science 340: 69–71.PubMedCrossRefGoogle Scholar
  47. Glynn, P. W., B. Riegl, S. Purkis, J. M. Kerr & T. B. Smith, 2015. Coral reef recovery in the Galápagos Islands: the northernmost islands (Darwin and Wenman). Coral Reefs 34: 421–436.CrossRefGoogle Scholar
  48. Goreau, T. F., 1959. The ecology of Jamaican coral reefs I. Species composition and zonation. Ecology 40: 67–90.Google Scholar
  49. Goreau, T. F., N. J. Goreau & C. M. Yonge, 1971. Reef Corals: autotrophs or Heterotrophs? Biological Bulletin 141: 247–260.CrossRefGoogle Scholar
  50. Goreau, N. I., T. J. Goreau & R. L. Hayes, 1981. Settling, survivorship and spatial aggregation in planulae and juveniles of the coral Porites porites (Pallas). Bull Mar Sci 31: 424–435.Google Scholar
  51. Graham, N. A., J. E. Cinner, A. V. Norström & M. Nyström, 2014. Coral reefs as novel ecosystems: embracing new futures. Current Opinion in Environmental Sustainability 7: 9–14.CrossRefGoogle Scholar
  52. Graham, N. A., S. Jennings, M. A. MacNeil, D. Mouillot & S. K. Wilson, 2015. Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518: 94–97.PubMedCrossRefGoogle Scholar
  53. Gross, K. & P. J. Edmunds, 2015. Stability of Caribbean coral communities quantified by long-term monitoring and autoregression models. Ecology 96: 1812–1822.PubMedCrossRefGoogle Scholar
  54. Grottoli, A. G., D. Tchernov & G. Winters, 2017. Physiological and Biogeochemical Responses of Super-Corals to Thermal Stress from the Northern Gulf of Aqaba Red Sea. Frontiers in Marine Science 4: 215.CrossRefGoogle Scholar
  55. Hellmann, J. J., J. E. Byers, B. G. Bierwagen & J. S. Dukes, 2008. Five potential consequences of climate change for invasive species. Conservation Biology 22: 534–543.PubMedCrossRefGoogle Scholar
  56. Hobbs, R. J., S. Arico, J. Aronson, J. S. Baron, P. Bridgewater, V. A. Cramer, P. R. Epstein, J. J. Ewel, C. A. Klink, A. E. Lugo & D. Norton, 2006. Novel ecosystems: theoretical and management aspects of the new ecological world order. Global Ecology and Biogeography 15: 1–7.CrossRefGoogle Scholar
  57. Holstein, D. M., C. B. Paris & P. J. Mumby, 2014. Consistency and inconsistency in multispecies population network dynamics of coral reef ecosystems. Marine Ecology Progress Series 499: 1–18.CrossRefGoogle Scholar
  58. Hull, P. M., S. A. F. Darroch & D. H. Erwin, 2015. Rarity in mass extinctions and the future of ecosystems. Nature 528: 345–351.PubMedCrossRefGoogle Scholar
  59. Hughes, T. P., 1984. Population dynamics based on individual size rather than age: a general model with a reef coral example. The American Naturalist 123: 778–795.CrossRefGoogle Scholar
  60. Hughes, T. P., 1996. Demographic approaches to community dynamics: a coral reef example. Ecology 77: 2256–2260.CrossRefGoogle Scholar
  61. Hughes, T. P. & J. E. Tanner, 2000. Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81: 2250–2263.CrossRefGoogle Scholar
  62. Hughes, T. P. N. A., J. B. Graham, P. J. Mumby Jackson & R. S. Steneck, 2010. Rising to the challenge of sustaining coral reef resilience. Trends Ecology Evolution 25: 633–642.PubMedCrossRefGoogle Scholar
  63. Huston, M. A., 1985. Patterns of species diversity on coral reefs. Annual Review of Ecology and Systematics 16: 149–177.CrossRefGoogle Scholar
  64. Jackson, J. B. C., 1977. Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies. The American Naturalist 111: 743–767.CrossRefGoogle Scholar
  65. Jackson, J. B., 1997. Reefs Since Columbus. Coral reefs 16: S23–S32.CrossRefGoogle Scholar
  66. Jackson, J. B. C., M. K. Donovan, K. L. Cramer & V. V. Lam, 2014. Status and trends of Caribbean coral reefs. Global Coral Reef Monitoring Network, IUCN.Google Scholar
  67. Johnson, K. G., 1992. Population dynamics of a free-living coral: recruitment, growth and survivorship of Manicina areolata (Linnaeus) on the Caribbean coast of Panama. Journal of Experimental Marine Biology and Ecology 164: 171–191.CrossRefGoogle Scholar
  68. Jones, C. G., J. H. Lawton & M. Shachak, 1994. Organisms as ecosystem engineers. Oikos 69: 373–386.CrossRefGoogle Scholar
  69. Kumpf, H. E. & H. A. Randall, 1961. Charting the marine environments of St. John, US Virgin Islands. Bulletin of Marine Science 11: 543–551.Google Scholar
  70. LaJeunesse, T., 2002. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Marine Biology 141: 387–400.CrossRefGoogle Scholar
  71. Lang, J., 1973. Coral reef project—papers in memory of Dr. Thomas F. Goreau. 11. Interspecific aggression by scleractinian corals. 2. Why the race is not only to the swift. Bulletin of Marine Science 23: 260–279.Google Scholar
  72. Lawton, J.H. & V.K. Brown, 1993. Redundancy in ecosystems. In Schultze, E.D. & H.A Mooney (eds), Biodiversity and ecosystem function. Springer-Verlag, Berlin: 255–270Google Scholar
  73. Lenz, E. A., L. Bramanti, H. R. Lasker & P. J. Edmunds, 2015. Long-term variation of octocoral populations in St. John. US Virgin Islands. Coral Reefs 34: 1099–1109.CrossRefGoogle Scholar
  74. Lesser, M.P., 2011. Coral bleaching: causes and mechanisms. In. Dubinsky, Z. & N. Stambler (eds), Coral Reefs: an Ecosystem in Transition. Springer, Dordrecht: 405–419.Google Scholar
  75. Levitan, D. R., P. J. Edmunds & K. E. Levitan, 2014. What makes a species common? No evidence of density-dependent recruitment or mortality of the sea urchin Diadema antillarum after the 1983–1984 mass mortality. Oecologia 175: 117–128.PubMedCrossRefGoogle Scholar
  76. Loya, Y., 1976. Recolonization of Red Sea corals affected by natural catastrophes and man-made perturbations. Ecology 57: 278–289.CrossRefGoogle Scholar
  77. Loya, Y., K. Sakai, K. Yamazato, Y. Nakano, H. Sambali & R. van Woesik, 2001. Coral bleaching: the winners and the losers. Ecology Letters 4: 122–131.CrossRefGoogle Scholar
  78. Meesters, E. H., M. Hilterman, E. Kardinaal, M. Keetman, M. De Vries & R. P. M. Bak, 2001. Colony size-frequency distributions of scleractinian coral populations: spatial and interspecific variation. Marine Ecology Progress Series 209: 43–54.CrossRefGoogle Scholar
  79. Miller, J., R. Waara, E. Muller & C. Rogers, 2006. Coral bleaching and disease combine to cause extensive mortality on reefs in US Virgin Islands. Coral Reefs 25: 418–418.CrossRefGoogle Scholar
  80. Miller, J., E. Muller, C. Rogers, R. Waara, A. Atkinson, K. R. T. Whelan, M. Patterson & B. Witcher, 2009. Coral disease following massive bleaching in 2005 causes 60% decline in coral cover on reefs in the US Virgin Islands. Coral Reefs 28: 925.CrossRefGoogle Scholar
  81. Miller, M., D. E. Williams, B. E. Huntington, G. A. Piniak & M. J. Vermeij, 2016. Decadal comparison of a diminishing coral community: a study using demographics to advance inferences of community status. PeerJ 4: e1643.PubMedPubMedCentralCrossRefGoogle Scholar
  82. Mundy, C. N., 2000. An appraisal of methods used in coral recruitment studies. Coral Reefs 19: 124–131.CrossRefGoogle Scholar
  83. Osborne, K., A. A. Thompson, A. J. Cheal, M. J. Emslie, K. A. Johns, M. J. Jonker, M. Logan, I. R. Miller & H. Sweatman, 2017. Delayed coral recovery in a warming ocean. Global Change Biology 23: 3869–3881.PubMedCrossRefGoogle Scholar
  84. Paine, R. T., 1974. Intertidal community structure. Oecologia 15: 93–120.PubMedCrossRefGoogle Scholar
  85. Paine, R. T., 1984. Ecological determinism in the competition for space: the Robert H MacArthur Award Lecture. Ecology 65: 1339–1348.CrossRefGoogle Scholar
  86. Parmesan, C., 2006. Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution and Systematics 37: 637–669.CrossRefGoogle Scholar
  87. Parmesan, C. & G. Yohe, 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37.PubMedCrossRefGoogle Scholar
  88. Perry, C. T., G. N. Murphy, P. S. Kentch, S. G. Smithers, E. N. Edinger, R. S. Steneck & P. J. Mumby, 2013. Caribbean-wide decline in carbonate production threatens coral reef growth. Nature Communications 4: 1402.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Petersen, D., M. Laterveer & H. Schuhmacher, 2005. Spatial and temporal variation in larval settlement of reef building corals in mariculture. Aquaculture 249: 317–327.CrossRefGoogle Scholar
  90. Piniak, G. A., N. D. Fogarty, C. M. Addison & W. J. Kenworthy, 2005. Fluorescence census techniques for coral recruits. Coral Reefs 24: 496–500.CrossRefGoogle Scholar
  91. Porter, J. W., 1972. Patterns of species diversity in Caribbean reef corals. Ecology 53: 745–748.CrossRefGoogle Scholar
  92. Porter, J. W., 1974. Community structure of coral reefs on opposite sides of the Isthmus of Panama. Science 186: 543–545.CrossRefGoogle Scholar
  93. Porter, J. W., 1976. Autotrophy, heterotrophy, and resource partitioning in Caribbean reef-building corals. The American Naturalist 110: 731–742.CrossRefGoogle Scholar
  94. Raimondi, P. T. & A. N. Morse, 2000. The consequences of complex larval behavior in a coral. Ecology 81: 3193–3211.CrossRefGoogle Scholar
  95. Randall, J. E., 1963. An analysis of the fish populations of artificial and natural reefs in the Virgin Islands. Caribbean Journal of Science 3: 31–47.Google Scholar
  96. Rankin, D.W., 2002. Geology of St. John, US Virgin Islands (No. 1631). US Geological Survey.Google Scholar
  97. Reaka-Kudla, M. L., D. E. Wilson & E. O. Wilson, 1997. Biodiversity II: understanding and protecting our biological resources. Journal of Insect Conservation 1: 247–250.CrossRefGoogle Scholar
  98. Riegl, B. & S. Purkis, 2015. Coral population dynamics across consecutive mass mortality events. Global Change Biology 21: 3995–4005.PubMedCrossRefGoogle Scholar
  99. Roff, G. & P. J. Mumby, 2012. Global disparity in the resilience of coral reefs. TREE 27: 404–413.PubMedGoogle Scholar
  100. Sears, L. W. & P. Chesson, 2007. New methods for quantifying the spatial storage effect: an illustration with desert annuals. Ecology 88: 2240–2247.PubMedCrossRefGoogle Scholar
  101. Smith, F. G. W., 1971. Atlantic reef corals. University of Miami Press, Coral Gables.Google Scholar
  102. Smith, T. B., M. E. Brandt, J. M. Calnan, R. S. Nemeth, J. Blondeau, E. Kadison, M. Taylor & P. Rothenberger, 2013. Convergent mortality responses of Caribbean coral species to seawater warming. Ecosphere 4: 1–40.CrossRefGoogle Scholar
  103. Smith, J. E., R. Brainard, A. Carter, S. Grillo, C. Edwards, J. Harris, L. Lewis, D. Obura, F. Rohwer, E. Sala, P. S. Vroom & S. Sandin, 2016. Re-evaluating the health of coral reef communities: baselines and evidence for human impacts across the central Pacific. Proceedings of the Royal Society B 283: 20151985.PubMedPubMedCentralCrossRefGoogle Scholar
  104. Soong, K., 1993. Colony size as a species character in massive reef corals. Coral Reefs 12: 77–83.CrossRefGoogle Scholar
  105. St Gelais, A. T., A. Chaves-Fonnegra, A. S. Brownlee, V. N. Kosmynin, A. L. Moulding & D. S. Gilliam, 2016. Fecundity and sexual maturity of the coral Siderastrea siderea at high latitude along the Florida Reef Tract, USA. Invertebrate Biology 135: 46–57.CrossRefGoogle Scholar
  106. Stella, J. S., M. S. Pratchett, P. A. Hutchings & G. P. Jones, 2011. Coral-associated invertebrates: diversity, ecological importance and vulnerability to disturbance. Oceanography and Marine Biology: An Annual Review 49: 43–104.Google Scholar
  107. Szmant, A. M., 1986. Reproductive ecology of Caribbean reef corals. Coral Reefs 5: 43–53.CrossRefGoogle Scholar
  108. Sutherland, J. P., 1974. Multiple stable points in natural communities. The American Naturalist 108: 859–873.CrossRefGoogle Scholar
  109. Tsounis, G., P. J. Edmunds, L. Bramanti, B. Gambrel & H. R. Lasker, 2018. Variability of size structure and species composition in Caribbean octocoral communities under contrasting environmental conditions. Marine Biology 165: 29–42.CrossRefGoogle Scholar
  110. Hooidonk, R., J. A. Maynard, D. Manzello & S. Planes, 2014. Opposite latitudinal gradients in projected ocean acidification and bleaching impacts on coral reefs. Global Change Biology 20: 103–112.PubMedCrossRefGoogle Scholar
  111. van Oppen, M. J., J. K. Oliver, H. M. Putnam & R. D. Gates, 2015. Building coral reef resilience through assisted evolution. Proceedings of the National Academy of Sciences 112: 2307–2313.CrossRefGoogle Scholar
  112. Vermeij, M. J. A., 2005. Substrate composition and adult distribution determine recruitment patterns in a Caribbean brooding coral. Marine Ecology Progress Series 295: 123–133.CrossRefGoogle Scholar
  113. Vermeij, M. J. A., 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.CrossRefGoogle Scholar
  114. Vermeij, M. J. & S. A. Sandin, 2008. Density-dependent settlement and mortality structure the earliest life phases of a coral population. Ecology 89: 1994–2004.PubMedCrossRefGoogle Scholar
  115. Vermeij, M. J., J. Bakker, N. V. D. Hal & R. P. M. Bak, 2011. Juvenile coral abundance has decreased by more than 50% in only three decades on a small Caribbean island. Diversity 3: 296–307.CrossRefGoogle Scholar
  116. Veron, J.E.N. & M. Stafford-Smith, 2000. Corals of the world, Vol 1–3. Australian Institute of Marine Science.Google Scholar
  117. Violle, C., W. Thuiller, N. Mouquet, F. Munoz, N. J. B. Kraft, M. W. Cadotte, S. W. Livingstone & D. Mouillot, 2017. Functional rarity: the ecology of outliers. TREE 32: 356–367.PubMedPubMedCentralGoogle Scholar
  118. Walther, G. R., E. Post, P. Convey, A. Menzel, C. Parmesan, T. J. Beebee, J. M. Fromentin, O. Hoegh-Guldberg & F. Bairlein, 2002. Ecological responses to recent climate change. Nature 416: 389–395.PubMedCrossRefGoogle Scholar
  119. Walther, G. R., S. Berger & M. T. Sykes, 2005. An ecological ‘footprint’of climate change. Proceedings of the Royal Society of London B: Biological Sciences 272: 1427–1432.CrossRefGoogle Scholar
  120. Warner, R. R. & P. L. Chesson, 1985. Coexistence mediated by recruitment fluctuations: a field guide to the storage effect. The American Naturalist 125: 769–787.CrossRefGoogle Scholar
  121. Weil, E., & C.S. Rogers, 2011. Coral reef diseases in the Atlantic-Caribbean. In. Dubinsky, Z. & N. Stambler (eds), Coral Reefs: an ecosystem in transition. Springer, Dordrecht: 465–491.Google Scholar
  122. Weil, E., C. S. Rogers & A. Croquer, 2017. Octocoral diseases in a changing ocean. In Rossi, S., L. Bramanti, A. Gori & C. Orejas (eds.), Marine Animal Forests. Springer International Publishing, Switzerland: 1109–1163.CrossRefGoogle Scholar
  123. Werner, E. E. & J. F. Gilliam, 1984. The ontogenetic niche and species interactions in size-structured populations. Annual Review of Ecology and Systematics 15: 393–425.CrossRefGoogle Scholar
  124. Weijerman, M., C. Birkeland, G. A. Piniak, M. W. Miller, C. M. Eakin, P. McElhany, M. J. Dunlap, M. Patterson & R. E. Brainard, 2014. Endangered Species Act listing: three case studies of data deficiencies and consequences of ESA ‘threatened’ listing on research output. Current Opinion in Environmental Sustainability 7: 15–21.CrossRefGoogle Scholar
  125. Whelan, K. R. T., J. Miller, O. Sanchez & M. Patterson, 2007. Impact of the 2005 coral bleaching event on Porites porites and Colpophyllia natans at Tektite Reef, US Virgin Islands. Coral Reefs 26: 689–693.CrossRefGoogle Scholar
  126. Woodley, J. D., E. A. Chornesky, P. A. Clifford, J. B. C. Jackson, L. S. Kaufman, N. Knowlton, J. C. Lang, M. P. Pearson, J. W. Porter, M. C. Rooney, K. W. Rylaarsdam, V. J. Tunnicliffe, C. M. Wahle, J. L. Wulff, A. S. G. Curtis, M. D. Dallmeyer, B. P. Jupp, M. A. R. Koehl, J. Neigel & E. M. Sides, 1981. Hurricane Allen’s impact on Jamaican coral reefs. Science 214: 749–755.PubMedCrossRefGoogle Scholar
  127. Wright, J. P. & C. G. Jones, 2006. The concept of organisms as ecosystem engineers ten years on: progress, limitations, and challenges. BioScience 56: 203–209.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiologyCalifornia State UniversityNorthridgeUSA

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