Temporal changes in benthic assemblages on Florida Keys reefs 11 years after the 1997/1998 El Niño

Disturbances that result in the mass mortality of reef-building corals are changing the appearance of reefs worldwide. Many reefs are transitioning away from scleractinian-coral- dominated assemblages to benthic communities composed primarily of non-scleractinian taxa. This study evaluated recovery patterns of reef communities in the Florida Keys following the mortality associated with the 1997/1998 El Nino. We examined temporal trends among the 5 most spatially abundant reef taxa and stony coral species from 1999 to 2009 at 3 spatial scales, and applied a Principal Coordinate Analysis (PCoA) to determine whether changes in their cover resulted in a shift in community structure. Trends of decreasing stony coral cover were not identi- fied Keys-wide between 1999 and 2009, but 2 of the 3 habitats examined—shallow and deep for- ereefs—did show a significant decline in cover. Concomitantly, octocoral cover significantly increased Keys-wide and in all 3 habitats. The transition to octocorals was most evident on shallow forereefs, where octocoral cover significantly increased at 9 of 12 reefs and overwhelmingly influ- enced the PCoA. On deep forereefs, octocoral and sponge cover did significantly increase, but did not impart a clearly defined shift in community structure like that observed on shallow forereefs. Community composition at patch reefs was relatively consistent during the study, but the increase in octocoral cover may accelerate further following a cold-water mortality event in 2010. These results demonstrate that octocorals are emerging as the predominant benthic taxa in the Florida Keys. Although the transition to octocorals may have started long ago, their apparent resilience to present-day stressors will likely allow this shift to continue into the foreseeable future.

[1]  D. R. Robertson,et al.  Spread of Diadema Mass Mortality Through the Caribbean , 1984, Science.

[2]  H. Lasker,et al.  Bleaching of reef coelenterates in the San Blas Islands, Panama , 1984, Coral Reefs.

[3]  R. Aronson,et al.  Stasis, biological disturbance, and community structure of a Holocene coral reef , 1997, Paleobiology.

[4]  D. Bellwood,et al.  Confronting the coral reef crisis , 2004, Nature.

[5]  W. Kruczynski,et al.  Water Quality Concerns in the Florida Keys: Sources, Effects, and Solutions , 2001 .

[6]  A. Watkinson,et al.  Measuring coral reef decline through meta-analyses , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[7]  J. Bruno,et al.  Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. , 2009, Ecology.

[8]  A. Grant,et al.  Long-Term Region-Wide Declines in Caribbean Corals , 2003, Science.

[9]  K. Bjorndal,et al.  Global Trajectories of the Long-Term Decline of Coral Reef Ecosystems , 2003, Science.

[10]  C. Rogers,et al.  Management implications of fish trap effectiveness in adjacent coral reef and gorgonian habitats , 1999, Environmental Biology of Fishes.

[11]  R. Aronson,et al.  Conservation, precaution, and Caribbean reefs , 2006, Coral Reefs.

[12]  K. Kim,et al.  Coral bleaching and disease: contributors to 1998 mass mortality in Briareum asbestinum (Octocorallia, Gorgonacea) , 2001, Hydrobiologia.

[13]  M. Callahan,et al.  Catastrophic Loss of Acropora palmata in the Florida Keys : Failure of the ‘ Sorcerer ’ s Apprentice Effect ’ to Aid Recovery Following the 2005 Atlantic Hurricane Season , 2012 .

[14]  R. Aronson,et al.  The 1998 bleaching event and its aftermath on a coral reef in Belize , 2002 .

[15]  D. Kline,et al.  Natural Disease Resistance in Threatened Staghorn Corals , 2008, PloS one.

[16]  J. Bruno,et al.  Rapid phase-shift reversal on a Jamaican coral reef , 2006, Coral Reefs.

[17]  Peter J. Edmunds,et al.  The demographics of a 15-year decline in cover of the caribbean reef coral Montastraea annularis , 2007 .

[18]  Richard T. Barber,et al.  African dust and the demise of Caribbean Coral Reefs , 2000 .

[19]  N. Knowlton,et al.  Taxonomic classification of the reef coral family Mussidae (Cnidaria: Anthozoa: Scleractinia) , 2012 .

[20]  R. Aronson,et al.  White-band disease and the changing face of Caribbean coral reefs , 2001, Hydrobiologia.

[21]  Daniel R. Brumbaugh,et al.  Trophic cascade facilitates coral recruitment in a marine reserve , 2007, Proceedings of the National Academy of Sciences.

[22]  B. Gratwicke,et al.  Fish distribution and ontogenetic habitat preferences in non-estuarine lagoons and adjacent reefs , 2006, Environmental Biology of Fishes.

[23]  L. Kaufman,et al.  Changing Patterns of Microhabitat Utilization by the Threespot Damselfish, Stegastes planifrons, on Caribbean Reefs , 2010, PloS one.

[24]  P. Yoshioka,et al.  A comparison of the survivorship and growth of shallow-water gorgonian species of Puerto Rico , 1991 .

[25]  Junda Lin,et al.  Phase-shift in coral reef communities in the Florida Keys National Marine Sanctuary (FKNMS), USA , 2008 .

[26]  R. Steneck,et al.  Coral Reefs Under Rapid Climate Change and Ocean Acidification , 2007, Science.

[27]  C. Wilkinson.  Status of coral reefs of the world , 2000 .

[28]  Scott C. Burgess,et al.  Disturbance and the Dynamics of Coral Cover on the Great Barrier Reef (1995–2009) , 2011, PloS one.

[29]  Jeff Miller,et al.  Permanent 'phase shifts' or reversible declines in coral cover? Lack of recovery of two coral reefs in St. John, US Virgin Islands , 2006 .

[30]  M. Miller,et al.  Recruitment failure in Florida Keys Acropora palmata, a threatened Caribbean coral , 2008, Coral Reefs.

[31]  S. Delean,et al.  Assessing loss of coral cover on Australia’s Great Barrier Reef over two decades, with implications for longer-term trends , 2011, Coral Reefs.

[32]  J. Bohnsack,et al.  An analysis of the loss of acroporid corals at Looe Key, Florida, USA: 1983–2000 , 2002, Coral Reefs.

[33]  Chuanmin Hu,et al.  Sea Surface Temperature Variability in the Florida Keys and Its Relationship to Coral Cover , 2011 .

[34]  P. Yoshioka,et al.  Octocoral bleaching during unusual thermal stress , 2010, Coral Reefs.

[35]  T. Done.  Phase shifts in coral reef communities and their ecological significance , 1992, Hydrobiologia.

[36]  Carrie V. Kappel,et al.  Are U.S. Coral Reefs on the Slippery Slope to Slime? , 2005, Science.

[37]  R. Carpenter,et al.  Increasing relative abundance of Porites astreoides on Caribbean reefs mediated by an overall decline in coral cover , 2008 .

[38]  J. Connell.  Disturbance and recovery of coral assemblages , 1997, Coral Reefs.

[39]  P. Petraitis,et al.  Detection of alternative stable states in marine communities , 2004 .

[40]  J. Connell,et al.  Mechanisms of Succession in Natural Communities and Their Role in Community Stability and Organization , 1977, The American Naturalist.

[41]  K. Bjorndal,et al.  Historical Overfishing and the Recent Collapse of Coastal Ecosystems , 2001, Science.

[42]  Ouida W. Meier,et al.  Quantification of Loss and Change in Floridian Reef Coral Populations , 1992 .

[43]  A. Agassiz.  Explorations of the Surface Fauna of the Gulf Stream, under the Auspices of the United States Coast Survey: The Tortugas and Florida Reefs , 1885 .

[44]  M. Miller,et al.  Attributing mortality among drivers of population decline in Acropora palmata in the Florida Keys (USA) , 2011, Coral Reefs.

[45]  H. Fox,et al.  Recovery in rubble fields: long-term impacts of blast fishing. , 2003, Marine pollution bulletin.

[46]  M. Greer,et al.  The health and short-term change of two coral patch reefs, Fernandez Bay, San Salvador Island, Bahamas , 1995 .

[47]  R. Aronson,et al.  PHASE SHIFTS, ALTERNATIVE STATES, AND THE UNPRECEDENTED CONVERGENCE OF TWO REEF SYSTEMS , 2004 .

[48]  M. Chiappone,et al.  Density, spatial distribution and size structure of sea urchins in Florida Keys coral reef and hard-bottom habitats , 2002 .

[49]  M. Colella,et al.  Cold-water event of January 2010 results in catastrophic benthic mortality on patch reefs in the Florida Keys , 2012, Coral Reefs.

[50]  T. Goulet,et al.  The genetic identity of dinoflagellate symbionts in Caribbean octocorals , 2004, Coral Reefs.

[51]  P. Picco,et al.  A catastrophic mass‐mortality episode of gorgonians and other organisms in the Ligurian Sea (North‐western Mediterranean), summer 1999 , 2000 .

[52]  Elizabeth R. Selig,et al.  Regional spatio-temporal trends in Caribbean coral reef benthic communities. , 2010 .

[53]  P. Dustan,et al.  Changes in the reef-coral community of Carysfort reef, Key Largo, Florida: 1974 to 1982 , 1987, Coral Reefs.

[54]  T. Hughes.  Catastrophes, Phase Shifts, and Large-Scale Degradation of a Caribbean Coral Reef , 1994, Science.

[55]  I. Macintyre,et al.  Submerged early Holocene barrier reef south-east Florida shelf , 1978, Nature.

[56]  W. Jaap,et al.  Clionid sponge surveys on the Florida Reef Tract suggest land-based nutrient inputs. , 2005, Marine pollution bulletin.

[57]  J. Bruno,et al.  Phase shifts and stable states on coral reefs , 2010 .

[58]  J. Rose,et al.  Preliminary evidence for human fecal contamination in corals of the Florida Keys, USA. , 2002, Marine pollution bulletin.

[59]  Chris P. Tsokos,et al.  Detection of Coral Reef Change by the Florida Keys Coral Reef Monitoring Project , 2001 .

[60]  Cris P Tsokos,et al.  Changes in coral reef communities among the Florida Keys, 1996–2003 , 2008, Coral Reefs.

[61]  Shawn W. Polson,et al.  The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Hugh Sweatman,et al.  Thermal Stress and Coral Cover as Drivers of Coral Disease Outbreaks , 2007, PLoS biology.

[63]  P. Glynn,et al.  Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook , 2008 .

[64]  K. ROTzLER,et al.  Impact of Crustose Clionid Sponges on Caribbean Reef Corals , 2006 .

[65]  J. Mcmanus,et al.  Coral-algal phase shifts on coral reefs: Ecological and environmental aspects [review article] , 2004 .

[66]  B. Stobart,et al.  Coral recovery at Aldabra Atoll, Seychelles: five years after the 1998 bleaching event , 2005, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[67]  W. Fitt,et al.  Catastrophic mortality on inshore coral reefs of the Florida Keys due to severe low‐temperature stress , 2011 .

[68]  E. Shinn,et al.  Distribution of the Reef-Building Community in Florida and the Bahamas: ABSTRACT , 1964 .

[69]  James W. Porter,et al.  Patterns of spread of coral disease in the Florida Keys , 2001, Hydrobiologia.

[70]  A. Szmant.  Nutrient enrichment on coral reefs: Is it a major cause of coral reef decline? , 2002 .

[71]  F. Muller‐Karger,et al.  Severe 2010 Cold-Water Event Caused Unprecedented Mortality to Corals of the Florida Reef Tract and Reversed Previous Survivorship Patterns , 2011, PloS one.

[72]  B. Lapointe,et al.  Effects of stormwater nutrient discharges on eutrophication processes in nearshore waters of the Florida keys , 1996 .

[73]  Loren McClenachan.  Documenting Loss of Large Trophy Fish from the Florida Keys with Historical Photographs , 2009, Conservation biology : the journal of the Society for Conservation Biology.

[74]  S. Ellner,et al.  The rising tide of ocean diseases: unsolved problems and research priorities , 2004 .

[75]  D. Lirman,et al.  Is proximity to land-based sources of coral stressors an appropriate measure of risk to coral reefs? An example from the Florida Reef Tract. , 2007, Marine pollution bulletin.

[76]  Ray Berkelmans,et al.  Doom and Boom on a Resilient Reef: Climate Change, Algal Overgrowth and Coral Recovery , 2009, PloS one.

[77]  P. Sammarco,et al.  Effects of soft corals on scleractinian coral recruitment. II: Allelopathy, spat survivorship and reef community structure , 2001 .

[78]  P. Mumby,et al.  Global disparity in the resilience of coral reefs. , 2012, Trends in ecology & evolution.

[79]  N. Dulvy,et al.  Flattening of Caribbean coral reefs: region-wide declines in architectural complexity , 2009, Proceedings of the Royal Society B: Biological Sciences.

[80]  E. Shinn.  Geologic history of Grecian Rocks, Key Largo Coral Reef Marine Sanctuary. , 1980 .

[81]  V. Tunnicliffe,et al.  Hurricane Allen's Impact on Jamaican Coral Reefs. , 1981, Science.

[82]  P. Kramer,et al.  Species composition, habitat, and water quality influence coral bleaching in southern Florida. , 2010 .

[83]  R. Cowen,et al.  Grazing pressure of herbivorous coral reef fishes on low coral-cover reefs , 2006, Coral Reefs.

[84]  M. Miller,et al.  Coral recruitment and juvenile mortality as structuring factors for reef benthic communities in Biscayne National Park, USA , 2000, Coral Reefs.

[85]  J. Pawlik,et al.  Demographics of increasing populations of the giant barrel sponge Xestospongia muta in the Florida Keys. , 2010, Ecology.

[86]  R. Grosberg,et al.  Climate Change, Human Impacts, and the Resilience of Coral Reefs , 2003, Science.

[87]  D. Bellwood,et al.  No-take areas, herbivory and coral reef resilience. , 2007, Trends in ecology & evolution.

[88]  C. Folke,et al.  Alternative states on coral reefs: beyond coral–macroalgal phase shifts , 2009 .

[89]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[90]  J. Burkholder,et al.  Emerging marine diseases--climate links and anthropogenic factors. , 1999, Science.

[91]  G. De’ath,et al.  The 27–year decline of coral cover on the Great Barrier Reef and its causes , 2012, Proceedings of the National Academy of Sciences.

[92]  W. Precht,et al.  Ecological Shifts along the Florida Reef Tract: The Past as a Key to the Future , 2007 .

[93]  Steven L. Miller,et al.  � 2003, by the American Society of Limnology and Oceanography, Inc. Episodic nutrient transport to Florida coral reefs , 2022 .

[94]  Cover of Sponges and Other Sessile Organisms in Rocky and Coral Reef Habitats of Santa Marta , Colombian Caribbean Sea , 1997 .

[95]  R. Carpenter,et al.  Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[96]  J. Pawlik,et al.  Redwood of the reef: growth and age of the giant barrel sponge Xestospongia muta in the Florida Keys , 2008 .

[97]  J. Pawlik.  The Chemical Ecology of Sponges on Caribbean Reefs: Natural Products Shape Natural Systems , 2011 .

[98]  P. Sammarco,et al.  Effects of soft corals on scleractinian coral recruitment. I:Directional allelopathy and inhibition of settlement , 1995 .

[99]  T. Hughes,et al.  RECRUITMENT FAILURE, LIFE HISTORIES, AND LONG‐TERM DECLINE OF CARIBBEAN CORALS , 2000 .