Abstract
Hard coral (Scleractinia and Milleporina) cover data were examined from 37 sites surveyed annually from 1996 to 2003 in the Florida reef tract, USA. Analyses of species numbers and total cover showed that site-to-site differences were generally very much greater than differences among times within sites. There were no significant differences among different geographical areas within the reef tract (Upper, Middle and Lower Keys). Large-scale changes documented included a reduction in species numbers and total cover on both deep and shallow offshore reefs between 1997 and 1999 followed by no recovery in cover, and only scant evidence of any recovery in species numbers by 2003. These changes coincided with bleaching events in 1997 and 1998, and the passage of Hurricane Georges through the Lower Keys in 1998. The lack of recovery among offshore reefs suggests that they were no longer resilient. Multivariate analyses revealed that some sites showed relatively little temporal variation in community composition, essentially random in direction, while others showed relatively large year-on-year changes. There was little evidence of any major region-wide changes affecting assemblage composition, or of any events that had impacted all of the sampling sites in any single year. Instead, different sites exhibited differing patterns of temporal variation, with certain sites displaying greater variation than others. Changes in community composition at some sites are interpreted in the light of knowledge of events at those sites and the relative sensitivities of species to various stressors, such as changes in cover of Acropora palmata and Millepora complanata at Sand Key following the bleaching events and hurricane in 1998, and declines in Montastraea annularis at Smith Shoal following a harmful algal bloom in 2002. For most sites, however, it is impossible to determine the causes of observed variation.
References
Agassiz A (1882) Explorations of the surface fauna of the Gulf Stream under the auspices of the United States Coast Survey II. The Tortugas and Florida Reefs. Mem Am Acad Arts Sci Centennial 2:107–134
Agassiz L (1852) Annual report of the Superintendent of the Coast Survey, showing the progress of that work during the year ending November, 1851. Robert Armstrong, Washington. pp 107–134
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Angeles ME, Gonzalez JE, Erickson DJ, Hernandez JL (2007) Predictions of future climate change in the Caribbean region using global general circulation models. Int J Climatol 27:555–569
Aronson RB, Precht WF (2001) White-band disease and the changing face of Caribbean coral reefs. Hydrobiologia 460:25–38
Bohnsack JA (1979) Photographic quantitative sampling of hard bottom benthic communities. Bull Mar Sci 29:242–252
Brown BE, Clarke KR, Warwick RM (2002) Serial patterns of biodiversity change in corals across shallow reef flats in Ko Phuket, Thailand, due to the effects of local (sedimentation) and regional (climatic) perturbations. Mar Biol 141:21–29
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 Programme (CRAMP) in Hawai’i. Pac Sci 58:145–158
Bruno JF, Petes LE, Harvell CD, Hettinger A (2003) Nutrient enrichment can increase the severity of coral diseases. Ecol Lett 6:1056–1061
Bythell JC, Hillis-Starr ZM, Rogers C (2000) Local variability but landscape stability in coral reef communities following repeated hurricane impacts. Mar Ecol Prog Ser 204:93–100
Carlton JH, Done TJ (1995) Long-term monitoring of coral reef benthos: large-scale application. Coral Reefs 14:35–46
Clarke KR (1993) Non-parametric multivariate analyses of change in community structure. Aust J Ecol 18:117–143
Clarke KR, Gorley RN (2006) PRIMER v6: User manual/Tutorial. PRIMER-E Ltd, Plymouth
Clarke KR, Green RH (1988) Statistical design and analysis for a ‘biological effects’ study. Mar Ecol Prog Ser 46:213–226
Clarke KR, Somerfield PJ, Chapman MG (2006) On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray-Curtis coefficient for denuded assemblages. J Exp Mar Biol Ecol 330:55–80
Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E Ltd, Plymouth
Clarke KR, Warwick RM, Brown BE (1993) An index showing breakdown of seriation, related to disturbance, in a coral-reef assemblage. Mar Ecol Prog Ser 102:153–160
Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310
Connell JH (1997) Disturbance and recovery of coral assemblages. Coral Reefs 16:101–113
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 67:461–488
Côté IM, Gill JA, Gardner TA, Watkinson AR (2005) Measuring coral reef decline through meta-analyses. Philos Trans R Soc Lond B 360:385–395
Cuet P, Naim O (1992) Analysis of a blatant reef flat degradation in La Réunion Island ľEtang-Salé fringing reef. Proc 7th Int Coral Reef Symp 1:313–322
Curtis ASG (1968) Quantitative photography. In: Engle C (ed) Photography for the scientist. Academic Press, London, pp 438–512
Davis GE (1982) A century of natural change in coral distribution at the Dry Tortugas: a comparison of reef maps from 1881–1976. Bull Mar Sci 32:608–623
Edmunds PJ (2002) Long-term dynamics of coral reefs in St John, US Virgin Islands. Coral Reefs 21:357–367
Edmunds PJ (2007) Evidence for a decadal-scale decline in the growth rates of juvenile scleractinian corals. Mar Ecol Prog Ser 341:1–13
Register Federal (2006) Endangered and threatened species: final listing determinations for elkhorn coral and staghorn coral. Federal Register 71:26852–26872
Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960
Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2005) Hurricanes and Caribbean coral reefs: impacts, recovery patterns, and role in long-term decline. Ecology 86:174–184
Gibson PJ, Boyer JN, Smith NP (2008) Nutrient mass flux between Florida Bay and the Florida Keys National Marine Sanctuary. Estuaries and coasts 31:21–32
Goreau TJ, Hayes RM (1994) Coral bleaching and ocean “Hot spots”. Ambio 23:176–180
Hallock P, Schlager W (1986) Nutrient excess and the demise of coral reefs and carbonate platforms. Palios 1:389–398
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866
Hu C, Hackett K, Callahan MK, Andréfouët S, Wheaton JW, Porter JW, Muller-Karger FE (2003) The 2002 ocean color anomaly in the Florida Bight: a cause of local coral reef decline. Geophys Res Lett 30:1151–1154
Hughes TP, Connell JH (1999) Multiple stressors on coral reefs: a long-term perspective. Limnol Oceanogr 44:932–940
Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933
Jaap WC (1979) Observation on zooxanthellae expulsion at Middle Sambo Reef, Florida Keys. Bull Mar Sci 29:414–422
Jaap WC (2000) Coral reef restoration. Ecol Eng 15:345–364
Jaap WC, Halas JC, Muller RG (1988) Community dynamics of stony corals (Milleporina and Scleractinia) at Key Largo National Marine Sanctuary, Florida during 1981–1986. Proc 6th Int Coral Reef Symp 2:237–243
Jaap WC, Hallock P (1990) Coral reefs. In: Myers RL, Ewell JJ (eds) Ecosystems of Florida. University of Central Florida Press, Orlando, pp 574–616
Jaap WC, McField MD (2001) Video sampling for monitoring coral reef benthos. Bull Biol Soc Wash 10:269–273
Jokiel PL, Brown EK, Friedlander A, Rodgers SK, Smith WR (2004) Hawai’i Coral Reef Assessment and Monitoring Program: spatial patterns and temporal dynamics in reef coral communities. Pac Sci 58:159–174
Kramer PA (2003) Synthesis of coral reef health indicators for the Western Atlantic: Results of the AGRRA program (1997–2003) In: Lang JC (ed) Status of coral reefs in the western Atlantic: Results of initial surveys, Atlantic and Gulf Rapid Reef Assessment (AGRRA) Program. Atoll Res Bull 496:1–58
Kruskal JB (1964) Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29:1–27
Lapointe BE, Barile PJ, Matzie WR (2004) Anthropogenic nutrient enrichment of seagrass and coral reef communities in the Lower Florida Keys: discrimination of local versus regional nitrogen sources. J Exp Mar Biol Ecol 308:23–58
Lesser MP, Bythell JC, Gates RD, Johnstone RW, Hoegh-Guldberg O (2007) Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data. J Exp Mar Biol Ecol 346:36–44
Lidz BH, Reich CD, Peterson RL, Shinn EA (2006) New maps, new information: coral reefs of the Florida Keys. J Coast Res 22:260–282
Lirman D, Fong P (1997) Patterns of damage to the branching coral Acropora palmata following Hurricane Andrew: damage and survivorship of hurricane-generated asexual recruits. J Coast Res 13:67–72
Lirman D, Fong P (2007) Is proximity to land-based sources of coral stressors an appropriate measure of risk to coral reefs? An example from the Florida Reef Tract. Mar Pollut Bull 54:779–791
Mayer AG (1914) The effect of temperature upon tropical marine animals. Pap Tortugas Lab Carnegie Inst Wash 6:1–24
McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297
Miller SL, Swanson DW, Chiappone M (2002) Multiple spatial scale assessment of coral reef and hard-bottom community structure in the Florida Keys National Marine Sanctuary. Proc 9th Int Coral Reef Symp 1:69–74
Murdoch TJT, Aronson RB (1999) Scale-dependent spatial variability of coral assemblages along the Florida Reef Tract. Coral Reefs 18:341–351
Ninio R, Meekan M, Done T, Sweatman H (2000) Temporal patterns in coral assemblages of the Great Barrier reef from local to large spatial scales. Mar Ecol Prog Ser 194:65–74
Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner GK, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig MF, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686
Overton WS, White D, Stevens DL Jr (1990) Design report for EMAP environmental monitoring and assessment program. US EPA report 600/3-91/053, Corvallis
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 301:955–957
Pandolfi JM, Jackson JBC, Baron N, Bradbury RH, Guzman HM, Hughes TP, Kappel CV, Micheli F, Ogden JC, Possingham HP, Sala E (2005) Are U.S. coral reefs on the slippery slope to slime? Science 307:1725–1726
Patterson KL, Porter JW, Ritchie KE, Polson SW, Mueller E, Peters EC, Santavy DL, Smiths GW (2002) The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata. Proc Natl Acad Sci USA 99:8725–8730
Porter JW, Meier OW (1992) Quantification of loss and change in Floridian reef coral populations. Am Zool 32:625–640
Porter JW, Lewis SK, Porter K (1999) The effect of multiple stressors on the Florida Keys coral reef ecosystem: a landscape hypothesis and a physiological test. Limnol Oceanogr 44:941–949
Porter JW, Dustan P, Jaap WC, Patterson KL, Kosmynin V, Meier OW, Patterson ME, Parsons M (2001) Patterns of spread of coral disease in the Florida Keys. Hydrobiologia 460:1–24
Porter JW, Kosmynin V, Patterson KL, Porter KG, Jaap WC, Wheaton JL, Hackett K, Lybolt M, Tsokos CP, Yanev G, Marcinek DM, Dotten J, Eaken D, Patterson M, Meier OW, Brill M, Dustan P (2002) Detection of coral reef change by the Florida Keys coral reef monitoring project. In: Porter JW, Porter KG (eds) The Everglades, Florida Bay, and coral reefs of the Florida Keys: an ecosystem sourcebook. CRC Press, Boca Raton, Florida, pp 749–769
Precht WF, Robbart ML, Aronson RB (2004) The potential listing of Acropora species under the US Endangered Species Act. Mar Pollut Bull 49:534–536
Reaser JK, Pomerance R, Thomas PO (2000) Coral bleaching and global climate change: scientific findings and policy recommendations. Conserv Biol 14:1500–1511
Roberts HH, Rouse LJ Jr, Walker ND, Hudson H (1982) Cold water stress in Florida Bay and northern Bahamas: a product of winter frontal passages. J Sediment Petrol 52:145–155
Sanders TJ, Rekab K, HC S, Swart PK, Healy GF, Dodge RE, Kramer P, Hudson JH, Halley RB, Robblee MB (1996) The stable oxygen and carbon isotope record from a coral growing in Florida Bay: a 160 year record of climatic and anthopogenic influence. Palaeogeog Palaeoclimatol Palaeoecol 123:219–237
Smith SV, Kimmer WJ, Lewis E, Brock R, Walsh TW (1981) Kaneohe Bay sewage diversion in perspective on ecosystem response to nutrient perturbation. Pac Sci 35:279–395
Solecki WD, Long J, Harwell CC, Myers V, Zubrow E, Ankerson T, Deren C, Feanny C, Hamann R, Hornung L, Murphy C, Snyder G (1999) Human–environment interactions in South Florida’s Everglades region: Systems of ecological degradation and restoration. Urban Ecosystems 3:305–343
Springer VG, McErlean A (1962) A study of the behavior of some tagged south Florida coral reef fishes. Am Midl Nat 67:386–397
Stark WA II, Davis WP (1966) Night habits of fishes of Alligator Reef, Florida. Ichthyologica 38:313–356
Suman DO (1997) The Florida Keys National Marine Sanctuary: a case study of an innovative federal-state partnership in marine resource management. Coast Manage 25:293–324
Szmant AM (2002) Nutrient enrichment on coral reefs: is it a major cause of coral reef decline? Estuaries 25:743–766
Tomascik T, Sander F (1985) Effects of eutrophication on reef-building corals: I. Growth-rate of the reef-building coral Montastrea annularis. Mar Biol 87:143–155
Tuya F, Haroun RJ, Boyra A, Sanchez-Jerez P (2005) Sea urchin Diadema antillarum: different functions in the structure and dynamics of reefs on both sides of the Atlantic. Mar Ecol Prog Ser 302:307–310
UNESCO (1998) CARICOMP – Caribbean coral reef, seagrass and mangrove sites. Coastal region and small island papers 3. UNESCO, Paris
Vaughan TW (1915) The geologic significance of the growth rate of the Floridian and Bahaman shoal-water corals. J Wash Acad Sci 5:591–600
Warwick RM, Clarke KR, Suharsono (1990) A statistical analysis of coral community responses to the 1982–83 El Niño in the Thousand Islands, Indonesia. Coral Reefs 8:171–179
Wilkinson C (ed) (2004) Status of coral reefs of the world. Australian Institute of Marine Science, Townsville
Acknowledgements
Funding to support this work was provided from State of Florida general revenue funds, US Environmental Protection Agency grant X-97468002-0, and National Oceanic and Atmospheric Administration grant NA160P2554. We thank all who worked to collect, compile and analyse these data, especially C. Beaver, D. Johnson, and S. Wade of the Florida Fish and Wildlife Research Institute, and Florida Keys National Marine Sanctuary personnel for station installation and logistic support. The US Environmental Protection Agency provided time on the survey vessel Peter Anderson. We thank T. Done, S. Gittings, R. Muller, and C. Rogers for sampling strategy advice. PJS and KRC acknowledge support for methods development from UK Defra, project No. ME3109.
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Somerfield, P.J., Jaap, W.C., Clarke, K.R. et al. Changes in coral reef communities among the Florida Keys, 1996–2003. Coral Reefs 27, 951–965 (2008). https://doi.org/10.1007/s00338-008-0390-7
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DOI: https://doi.org/10.1007/s00338-008-0390-7