Advertisement

Marine Biology

, 166:108 | Cite as

Nitrogen enrichment, altered stoichiometry, and coral reef decline at Looe Key, Florida Keys, USA: a 3-decade study

  • Brian E. LapointeEmail author
  • Rachel A. Brewton
  • Laura W. Herren
  • James W. Porter
  • Chuanmin Hu
Highlight Article

Abstract

Increased loadings of nitrogen (N) from fertilizers, top soil, sewage, and atmospheric deposition are important drivers of eutrophication in coastal waters globally. Monitoring seawater and macroalgae can reveal long-term changes in N and phosphorus (P) availability and N:P stoichiometry that are critical to understanding the global crisis of coral reef decline. Analysis of a unique 3-decade data set for Looe Key reef, located offshore the lower Florida Keys, showed increased dissolved inorganic nitrogen (DIN), chlorophyll a, DIN:soluble reactive phosphorus (SRP) ratios, as well as higher tissue C:P and N:P ratios in macroalgae during the early 1990s. These data, combined with remote sensing and nutrient monitoring between the Everglades and Looe Key, indicated that the significant DIN enrichment between 1991 and 1995 at Looe Key coincided with increased Everglades runoff, which drains agricultural and urban areas extending north to Orlando, Florida. This resulted in increased P limitation of reef primary producers that can cause metabolic stress in stony corals. Outbreaks of stony coral disease, bleaching, and mortality between 1995 and 2000 followed DIN enrichment, algal blooms, and increased DIN:SRP ratios, suggesting that eutrophication interacted with other factors causing coral reef decline at Looe Key. Although water temperatures at Looe Key exceeded the 30.5 °C bleaching threshold repeatedly over the 3-decade study, the three mass bleaching events occurred only when DIN:SRP ratios increased following heavy rainfall and increased Everglades runoff. These results suggest that Everglades discharges, in conjunction with local nutrient sources, contributed to DIN enrichment, eutrophication, and increased N:P ratios at Looe Key, exacerbating P limitation, coral stress and decline. Improved management of water quality at the local and regional levels could moderate N inputs and maintain more balanced N:P stoichiometry, thereby reducing the risk of coral bleaching, disease, and mortality under the current level of temperature stress.

Notes

Acknowledgements

This research was inspired by early discussions with John Ryther, Peter Glynn, Charlie Yentsch, and Phil Dustan. Dr. Larry Brand provided assistance with chlorophyll a analysis and Carl Zimmerman provided nutrient analytical support. Many staff, volunteers, and colleagues assisted with logistics and field monitoring efforts in the Keys over the long-term study, including Roger Bewig, Julie Bishop, Richard and Barbara Brown, Mark and Diane Littler, Mark Clark, Bill Matzie, David Tomasko, Peter Barile, Maggie Vogelsang, John November, Diana Bolton, Carl Hampp, Marie Tarnowski, and Tanju Mishara. Strike Zone Charters and the Looe Key Reef Resort Dive Shop provided boat support for many sampling events. The authors are grateful to Alex Tewfik, Elizabeth Babcock, Ed Proffitt, and several anonymous reviewers for their constructive comments. The authors also wish to thank the U.S. Geological Survey, NASA, and NOAA for providing satellite data and imagery. This is contribution #2210 from Florida Atlantic University, Harbor Branch Oceanographic Institute.

Funding

Financial support for this research was provided by the National Oceanic and Atmospheric Administration (NOAA, National Marine Sanctuaries Program), Monroe County, Herbert W. Hoover Foundation, John D. and Catherine T. MacArthur Foundation, United States Environmental Protection Agency (US EPA), National Aeronautics and Space Administration (NASA) ROSES (contract #NNX10AB69G), the “Save Our Seas” Specialty License Plate funds granted through the Harbor Branch Oceanographic Institute Foundation, and the Coastal Ocean Association of Science and Technology (COAST).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights statement

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Agassiz L (1852) Florida reefs and coast. In: Annual report to the superintendent of the coast survey for 1851, pp 107–134Google Scholar
  2. Anderson J, United States Department of Commerce, National Oceanic and Atmospheric Administration, National Ocean Service, Office of National Marine Sanctuaries, Florida Keys National Marine Sanctuary (2011) Continuous bottom temperature measurements in strategic areas of the Florida Reef Tract at Looe Buoy, 1988–2004 (NODC Accession 0002616). Version 1.1. National Oceanographic Data Center. https://data.nodc.noaa.gov/cgi-bin/iso?id=gov.noaa.nodc:0014271. Accessed 13 July 2017
  3. Anthony K, Maynard JA, Diaz-Pulido G, Mumby PJ, Marshall PA, Cao L, Hoegh-Guldberg O (2011) Ocean acidification and warming will lower coral reef resilience. Glob Change Biol 17(5):1798–1808.  https://doi.org/10.1111/j.1365-2486.2010.02364.x CrossRefGoogle Scholar
  4. Aspila KI, Agemian H, Chau AS (1976) A semi-automated method for the determination of inorganic, organic and total phosphate in sediments. Analyst 101(1200):187–197.  https://doi.org/10.1039/AN9760100187 CrossRefPubMedGoogle Scholar
  5. Atkinson MJ (1987) Rates of phosphate uptake by coral reef flat communities. Limnol Oceanogr 32(2):426–435.  https://doi.org/10.4319/lo.1987.32.2.0426 CrossRefGoogle Scholar
  6. Atkinson MJ, Smith SV (1983) C:N:P ratios of benthic marine plants. Limnol Oceanogr 28(3):568–574.  https://doi.org/10.4319/lo.1983.28.3.0568 CrossRefGoogle Scholar
  7. 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(4):435–471.  https://doi.org/10.1016/j.ecss.2008.09.003 CrossRefGoogle Scholar
  8. Banner AH (1974) Kaneohe Bay, Hawaii; Urban pollution and a coral reefs ecosystem. In: Proceedings of the second international coral reef symposium, pp 685–702Google Scholar
  9. Barnes BB, Hu C, Holekamp KL, Blonski S, Spiering BA, Palandro D, Lapointe B (2014) Use of Landsat data to track historical water quality changes in Florida Keys marine environments. Remote Sens Environ 140:485–496.  https://doi.org/10.1016/j.rse.2013.09.020 CrossRefGoogle Scholar
  10. Barnes BB, Garcia R, Hu C, Lee Z (2018) Multi-band spectral matching inversion algorithm to derive water column properties in optically shallow waters: an optimization of parameterization. Remote Sens Environ 204:424–438.  https://doi.org/10.1016/j.rse.2017.10.013 CrossRefGoogle Scholar
  11. Bell PR (1992) Eutrophication and coral reefs—some examples in the Great Barrier Reef Lagoon. Water Res 26(5):553–568.  https://doi.org/10.1016/0043-1354(92)90228-V CrossRefGoogle Scholar
  12. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429(6994):827–833.  https://doi.org/10.1016/0043-1354(92)90228-V CrossRefPubMedPubMedCentralGoogle Scholar
  13. Birkeland C (1977) The importance of rate of biomass accumulation in early succession stages of benthic communities to the survival of coral recruits. In: Proceedings of the third international coral reef symposium, pp 16–21Google Scholar
  14. Birkeland C (1997) Life and death of coral reefs. Springer Science and Business Media, New YorkCrossRefGoogle Scholar
  15. Birkeland C (2004) Ratcheting down the coral reefs. Bioscience 54(11):1021–1027.  https://doi.org/10.1641/0006-3568(2004)054%5b1021:RDTCR%5d2.0.CO;2 CrossRefGoogle Scholar
  16. Bohnsack JA, Harper DE, McClellan DB, Sutherland DL, White MW (1987) Resource survey of fishes within Looe Key National Marine Sanctuary. NOAA Tech Memo. NOS MEMD 5:1–108Google Scholar
  17. Boyer JN, Jones RD (2002) A view from the bridge: External and internal forces affecting the ambient water quality of the Florida Keys National Marine Sanctuary. In: Porter JW, Porter KG (eds) The Everglades, Florida Bay, and Coral Reefs of the Florida Keys. CRC Press, Boca Raton, pp 609–628Google Scholar
  18. Boyer JN, Fourqurean JW, Jones RJ (1999) Seasonal and long-term trends in the water quality of Florida Bay. Estuaries 22(2):417–430CrossRefGoogle Scholar
  19. Boyer JN, Kelble CR, Ortner PB, Rudnick DT (2009) Phytoplankton bloom status: chlorophyll a biomass as an indicator of water quality condition in the southern estuaries of Florida, USA. Ecol Indic 9(6):S56–S67CrossRefGoogle Scholar
  20. Brand LE (2002) The transport of terrestrial nutrients to South Florida coastal waters. In: Porter JW, Porter KG (eds) The Everglades, Florida Bay, and Coral Reefs of the Florida Keys. CRC Press, Boca Raton, pp 353–406Google Scholar
  21. Briceno HO, Boyer JN (2018) 2017 Annual Report of the Water Quality Monitoring Project for the Water Quality Protection Program of the Florida Keys National Marine Sanctuary. Technical Report of the Southeast Environmental Research Center, Florida International UniversityGoogle Scholar
  22. Brodie J, De’ath G, Devlin M, Furnas M, Wright M (2007) Spatial and temporal patterns of near-surface chlorophyll a in the Great Barrier Reef lagoon. Mar Freshw Res 58(4):342–353.  https://doi.org/10.1071/MF06236 CrossRefGoogle Scholar
  23. Bruno JF, Petes LE, Drew Harvell C, Hettinger A (2003) Nutrient enrichment can increase the severity of coral diseases. Ecol Lett 6(12):1056–1061.  https://doi.org/10.1046/j.1461-0248.2003.00544.x CrossRefGoogle Scholar
  24. Brzezinski MA (1985) The Si:C:N ratio of marine diatoms: interspecific variability and the effect of some environmental variables. J Phycol 21(3):347–357.  https://doi.org/10.1111/j.0022-3646.1985.00347.x CrossRefGoogle Scholar
  25. Burdette MK, United States Department of Commerce, National Oceanic and Atmospheric Administration, National Weather Service, National Data Buoy Center (2010) Temperature and salinity data from the SEAKEYS project in the Florida Keys from 1991-05-15 to 1995-11-15 (NODC Accession 9600071). Version 1.1. National Oceanographic Data Center. https://data.nodc.noaa.gov/cgi-bin/iso?id=gov.noaa.nodc:9600071. Accessed 13 July 2017
  26. Burkholder JM, Tomasko DA, Touchette BW (2007) Seagrasses and eutrophication. J Exp Mar Biol Ecol 350:46–72.  https://doi.org/10.1016/j.jembe.2007.06.024 CrossRefGoogle Scholar
  27. Burnison BK (1980) Modified dimethyl sulfoxide (DMSO) extraction for chlorophyll analysis of phytoplankton. Can J Fish Aquat Sci 37(4):729–733.  https://doi.org/10.1139/f80-095 CrossRefGoogle Scholar
  28. Butler MJ, Dolan TW (2017) Potential impacts of Everglades Restoration on lobster and hard bottom communities in the Florida Keys, FL (USA). Estuar Coast 40(6):1523–1539.  https://doi.org/10.1007/s1223 CrossRefGoogle Scholar
  29. Butler MJ, Hunt JH, Herrnkind WF, Childress MJ, Bertelsen R, Sharp W, Matthews T, Field JM, Marshall HG (1995) Cascading disturbances in Florida Bay, USA: cyanobacteria blooms, sponge mortality, and implications for juvenile spiny lobsters Panulirus argus. Mar Ecol Prog Ser 129:119–125CrossRefGoogle Scholar
  30. Cane MA (1983) Oceanographic events during El Niño. Science 222(4629):1189–1195CrossRefGoogle Scholar
  31. Caperon J, Harvey WA, Steinhilper FA (1976) Particulate organic carbon, nitrogen, and chlorophyll as measures of phytoplankton and detritus standing crops in Kaneohe Bay, Oahu, Hawaiian Islands. Pac Sci 30(4):317–327Google Scholar
  32. Caputo M (1996) 29 April) Bay remedy could be backfiring, freshwater flows may be causing red tide. Key West Citizen, Key WestGoogle Scholar
  33. Causey B (2008) The history of massive coral bleaching and other perturbations in the Florida Keys. In: Wilkinson CR, Souter DN (eds) Status of Caribbean coral reefs after bleaching and hurricanes in 2005, vol 148. Global Coral Reef Monitoring Network, and Reef and Rainforest Research Centre, Townsville, pp 61–72Google Scholar
  34. Conley DJ, Paerl HW, Howarth RW, Boesch DF, Seitzinger SP, Havens KE, Lancelot C, Likens GE (2009) Controlling eutrophication: nitrogen and phosphorus. Science 323:1014–1015.  https://doi.org/10.1126/science.1167755 CrossRefGoogle Scholar
  35. Continental Shelf Associates (1991) Water Quality Protection Program for the Florida Keys National Marine Sanctuary, Phase I Report to the United States Environmental Protection AgencyGoogle Scholar
  36. Cook CB, Mueller EM, Ferrier MD, Annis E (2002) The influence of nearshore waters on corals of the Florida Reef Tract. In: Porter JW, Porter KG (eds) The Everglades, Florida Bay, and Coral Reefs of the Florida Keys. CRC Press, Boca Raton, pp 771–788Google Scholar
  37. Coral Reef Ecosystems Research and Protection (1992) Joint Hearing before the Subcommittee on Environment, of the Committee on Science, Space, and Technology, and the Subcommittee on Oceanography, Great Lakes, and the Outer Continental Shelf of the Committee on merchant Marine and Fisheries, U.S. House of Representatives. 102nd Congress (Testimony of Jim Porter)Google Scholar
  38. Crossland CJ, Hatcher BG, Atkinson MJ, Smith SV (1984) Dissolved nutrients of a high-latitude coral reef, Houtman Abrolhos Islands, Western Australia. Mar Ecol Prog Ser 14(2):159–163CrossRefGoogle Scholar
  39. Cunning R, Baker AC (2013) Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat Clim Change 3:259–262.  https://doi.org/10.1038/nclimate1711 CrossRefGoogle Scholar
  40. D’Angelo C, Wiedenmann J (2014) Impacts of nutrient enrichment on coral reefs: new perspectives and implications for coastal management and reef survival. Curr Opin Environ Sustain 7:82–93.  https://doi.org/10.1016/j.cosust.2013.11.029 CrossRefGoogle Scholar
  41. D’Elia CF, Webb KL (1977) The dissolved nitrogen flux of reef corals. In: Proceedings of the third international coral reef symposium, pp 325–331Google Scholar
  42. D’Elia CF, Webb KL, Porter JW (1981) Nitrate-rich groundwater inputs to Discovery Bay, Jamaica: a significant source of N to local coral reefs? Bull Mar Sci 31(4):903–910Google Scholar
  43. D’Elia CF, Buddemeier RW, Smith SV (1991) A workshop on coral bleaching, coral reef ecosystems and global change: report of proceedings. Maryland Seagrant, University of Maryland, College ParkGoogle Scholar
  44. D’Elia CF, Connor EE, Kaumeyer NL, Keefe CW, Wood KV, Zimmerman CF (1997) Nutrient analytical services: standard operating procedures. Technical Report Series No. 158-97. Chesapeake Biological Laboratory, SolomonsGoogle Scholar
  45. Darwin C (1842) The structure and distribution of coral reefs. Smith, Elder, and Company, LondonGoogle Scholar
  46. De’ath G, Fabricius K (2010) Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef. Ecol Appl 20(3):840–850.  https://doi.org/10.1890/08-2023.1 CrossRefPubMedGoogle Scholar
  47. 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 109(44):17995–17999.  https://doi.org/10.1073/pnas.1208909109 CrossRefPubMedGoogle Scholar
  48. DeMaria K (1996) Changes in the Florida Keys Marine Ecosystem based upon interviews with experienced residents. The Nature Conservancy and Center for Marine Conservation, Key WestGoogle Scholar
  49. Devlin MJ, Brodie J (2005) Terrestrial discharge into the Great Barrier Reef Lagoon: nutrient behavior in coastal waters. Mar Pollut Bull 51(1–4):9–22.  https://doi.org/10.1016/j.marpolbul.2004.10.037 CrossRefPubMedGoogle Scholar
  50. Downing JA, McClain M, Twilley R, Melack JM, Elser J, Rabalais NN, Lewis WM, Turner RE, Corredor J, Soto D, Yanez-Arancibia A (1999) The impact of accelerating land-use change on the N-cycle of tropical aquatic ecosystems: current conditions and projected changes. Biogeochemistry 46(1–3):109–148.  https://doi.org/10.1023/A:100615621 CrossRefGoogle Scholar
  51. Drog M (2017) C-111 Spreader Canal Western Project. USACE, JacksonvilleGoogle Scholar
  52. Duarte C (1990) Seagrass nutrient content. Mar Ecol Prog Ser 61:201–207CrossRefGoogle Scholar
  53. Dubinsky ZVY, Stambler N (1996) Marine pollution and coral reefs. Glob Change Biol 2(6):511–526.  https://doi.org/10.1111/j.1365-2486.1996.tb00064.x CrossRefGoogle Scholar
  54. Duprey NN, Yasuhara M, Baker DM (2016) Reefs of tomorrow: eutrophication reduces coral biodiversity in an urbanized seascape. Glob Change Biol 22(11):3550–3565.  https://doi.org/10.1111/gcb.13432 CrossRefGoogle Scholar
  55. Dustan P (1977) Vitality of reef coral populations off Key Largo, Florida: recruitment and mortality. Environ Geol 2(1):51–58.  https://doi.org/10.1007/bf02430665 CrossRefGoogle Scholar
  56. Dustan P, Halas JC (1987) Changes in the reef-coral community of Carysfort Reef, Key Largo, Florida: 1974 to 1982. Coral Reefs 6(2):91–106.  https://doi.org/10.1007/bf00301378 CrossRefGoogle Scholar
  57. Eakin CM, Liu G, Gomez AM, De La Cour JL, Heron SF, Skirving WJ, Geiger EF, Tirak KV, Strong AE (2016) Global coral bleaching 2014–2017: status and an appeal for observations. Reef Encounter 31(1):20–26Google Scholar
  58. Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50(2):125–146.  https://doi.org/10.1016/j.marpolbul.2004.11.028 CrossRefPubMedGoogle Scholar
  59. Fabricius KE, Logan M, Weeks SJ, Lewis SE, Brodie J (2016) Changes in water clarity in response to river discharges on the Great Barrier Reef continental shelf: 2002–2013. Estuar Coast Shelf Sci 173:A1–A15.  https://doi.org/10.1016/j.ecss.2016.03.001 CrossRefGoogle Scholar
  60. Fagoonee I, Wilson HB, Hassell MP, Turner JR (1999) The dynamics of zooxanthellae populations: a long-term study in the field. Science 283(5403):843–845.  https://doi.org/10.1126/science.283.5403.843 CrossRefPubMedGoogle Scholar
  61. Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L (1993) Population control in symbiotic corals. Bioscience 43(9):606–611.  https://doi.org/10.2307/1312147 CrossRefGoogle Scholar
  62. Furnas MJ, Mitchell AW, Skuza M (1995) Nitrogen and phosphorus budgets for the central Great Barrier Reef Shelf. A report to the Great Barrier Reef Marine Park Authority, TownsvilleGoogle Scholar
  63. Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301(5635):958–960.  https://doi.org/10.1126/science.1086050 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Ginsburg RN (1994) Proceedings of the colloquium on global aspects of coral reefs: health, hazards, and history, 1993. University of Miami, MiamiGoogle Scholar
  65. Ginsburg RN, Shinn EA (1993) Preferential distribution of reefs in the Florida Reef Tract: the past is the key to the present. H21–H26. In: Proceedings of the colloquium on global aspects of coral reefs: health, hazards, and history, 1993. University of Miami, MiamiGoogle Scholar
  66. Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Glob Change Biol 2(6):495–509.  https://doi.org/10.1111/j.1365-2486.1996.tb00063.x CrossRefGoogle Scholar
  67. Going with the flow? (2002) The Economist. https://www.economist.com/node/1465617. Accessed 20 July 2018
  68. Goreau TF (1964) Mass expulsion of zooxanthellae from Jamaican reef communities after Hurricane Flora. Science 145(3630):383–386.  https://doi.org/10.1126/science.145.3630.383 CrossRefPubMedGoogle Scholar
  69. Goreau TJ, Hayes RL (1994) Coral bleaching and ocean “hot spots”. Ambio-J Hum Environ Res Manag 23(3):176–180Google Scholar
  70. Guiry MD, Guiry GM (2013) AlgaeBase. World-Wide Electronic Publication, National University of Ireland, Galway. http://www.algaebase.org. Accessed 30 Nov 2018
  71. Hall MO, Furman BT, Merello M, Durako MJ (2016) Recurrence of Thalassia testudinum seagrass die-off in Florida Bay, USA: initial observations. Mar Ecol Prog Ser 560:243–249CrossRefGoogle Scholar
  72. Hallock P, Schlager W (1986) Nutrient excess and the demise of coral reefs and carbonate platforms. Palaios 1:389–398.  https://doi.org/10.2307/3514476 CrossRefGoogle Scholar
  73. Harrell FE (2019) Hmisc: Harrell Miscellaneous (R package version 4.2-0)Google Scholar
  74. Harrison WG, Platt T, Lewis MR (1987) f-Ratio and its relationship to ambient nitrate concentration in coastal waters. J Plankton Res 9(1):235–248.  https://doi.org/10.1093/plankt/9.1.235 CrossRefGoogle Scholar
  75. Hatcher BG, Larkum AWD (1983) An experimental analysis of factors controlling the standing crop of the epilithic algal community on a coral reef. J Exp Mar Biol Ecol 69(1):61–84.  https://doi.org/10.1016/0022-0981(83)90172-7 CrossRefGoogle Scholar
  76. Heaton TH (1986) Isotopic studies of nitrogen pollution in the hydrosphere and atmosphere: a review. Chem Geol 59:87–102.  https://doi.org/10.1016/0009-2541(86)90046-x CrossRefGoogle Scholar
  77. Hebbali A (2018) olsrr: tools for building OLS regression models (R package version 0.5.2)Google Scholar
  78. Heil CA, Revilla M, Glibert PM, Murasko S (2007) Nutrient quality drives differential phytoplankton community composition on the southwest Florida shelf. Limnol Oceanogr 52(3):1067–1078.  https://doi.org/10.4319/lo.2007.52.3.1067 CrossRefGoogle Scholar
  79. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N (2007) Coral reefs under rapid climate change and ocean acidification. Science 318(5857):1737–1742.  https://doi.org/10.1126/science.1152509 CrossRefPubMedGoogle Scholar
  80. Howarth R, Paerl HW (2008) Coastal marine eutrophication: control of both nitrogen and phosphorus is necessary. PNAS 105(49):E103.  https://doi.org/10.1073/pnas.0807266106 CrossRefPubMedGoogle Scholar
  81. Hu C, The South West Florida Dark Water Observation Group et al (2002) Satellite images track “black water” event off Florida coast. EOS AGU Trans 83(26):281–285.  https://doi.org/10.1029/2002EO000199 CrossRefGoogle Scholar
  82. Hu C, Hackett KE, Callahan MK, Andréfouët S, Wheaton JL, 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(3):1151.  https://doi.org/10.1029/2002gl016479 CrossRefGoogle Scholar
  83. Hu C, Muller-Karger FE, Vargo GA, Neely MB, Johns E (2004) Linkages between coastal runoff and the Florida Keys ecosystem: a study of a dark plume event. Geophys Res Lett 31(15):L15307.  https://doi.org/10.1029/2004gl020382 CrossRefGoogle Scholar
  84. Hubbard DK (1996) Reefs as dynamic systems. In: Birkeland C (ed) The life and death of coral reefs. Chapman and Hall, New York, pp 43–67Google Scholar
  85. Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265(5178):1547–1551.  https://doi.org/10.1016/0006-3207(95)93800-r CrossRefPubMedPubMedCentralGoogle Scholar
  86. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JB, Kleypas J, Lough JM (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301(5635):929–933.  https://doi.org/10.1126/science.1085046 CrossRefPubMedGoogle Scholar
  87. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC (2017) Global warming and recurrent mass bleaching of corals. Nature 543(7645):373.  https://doi.org/10.1038/nature21707 CrossRefPubMedGoogle Scholar
  88. Jaap WC (1988) The 1987 zooxanthellae expulsion event at Florida reefs. Mass bleaching of coral reefs: a research strategy. National Undersea Research Program Report 88:24–29Google Scholar
  89. Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293(5530):629–637.  https://doi.org/10.1126/science.1059199 CrossRefPubMedGoogle Scholar
  90. Joyner JL, Sutherland KP, Kemp D, Berry B, Griffin A, Porter J, Amador MH, Noren HK, Lipp EK (2015) Systematic analysis of white pox disease in Acropora palmata of the Florida Keys and role of Serratia marcescens. Appl Environ Microbiol 81(13):4451–4457.  https://doi.org/10.1128/AEM.00116-15 CrossRefPubMedPubMedCentralGoogle Scholar
  91. Kassambara A (2018) ggpubr: “ggplot2” based publication ready plots (R package version 3.1.00)Google Scholar
  92. Kendall C, Elliott EM, Wankel SD (2007) Tracing anthropogenic inputs of nitrogen to ecosystems. Stable Isot Ecol Environ Sci 2:375–449.  https://doi.org/10.1002/9780470691854.ch12 CrossRefGoogle Scholar
  93. Kim K, Harvell CD (2004) The rise and fall of a six-year coral-fungal epizootic. Am Nat 164(S5):S52–S63CrossRefGoogle Scholar
  94. Klein CJ III, Orlando SP Jr (1994) A spatial framework for water-quality management in the Florida Keys National Marine Sanctuary. Bull Mar Sci 54(3):1036–1044Google Scholar
  95. Kleypas JA, Feely RA, Fabry VJ, Langdon C, Sabine CL, Robbins LL (2006) Impacts of ocean acidification on coral reefs and other marine calcifiers: a guide for future research. Report of a workshop sponsored by the National Science Foundation, National Oceanic and Atmospheric Administration, and United States Geological Survey, St. PetersburgGoogle Scholar
  96. Klingener N (1995 22 February) Red tide fish kill the worst in years, algae scourge rounds the Keys. Miami Herald, MiamiGoogle Scholar
  97. Kourafalou VH, Kang H (2012) Florida Current meandering and evolution of cyclonic eddies along the Florida Keys Reef Tract: are they interconnected? J Geophys Res 117:C05028.  https://doi.org/10.1029/2011JC007383 CrossRefGoogle Scholar
  98. Kramer BJ, Davis TW, Meyer KA, Rosen BH, Goleski JA, Dick GJ, Oh G, Gobler CJ (2018) Nitrogen limitation, toxin synthesis potential, and toxicity of cyanobacterial populations in Lake Okeechobee and the St. Lucie River Estuary, Florida, during the 2016 state of emergency event. PLoS One 13(5):e0196278.  https://doi.org/10.1371/journal.pone.0196278 CrossRefPubMedPubMedCentralGoogle Scholar
  99. Kruczynski WL, McManus F (2002) Water quality concerns in the Florida Keys: sources, effects, and solutions. In: Porter JW, Porter KG (eds) The Everglades, Florida Bay, and Coral Reefs of the Florida Keys. CRC Press, Boca Raton.  https://doi.org/10.1201/9781420039412-37 Google Scholar
  100. Lapointe BE (1987) Phosphorus-and nitrogen-limited photosynthesis and growth of Gracilaria tikvahiae (Rhodophyceae) in the Florida Keys: an experimental field study. Mar Biol 93(4):561–568.  https://doi.org/10.1007/BF00392794 CrossRefGoogle Scholar
  101. 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.  https://doi.org/10.4319/lo.1997.42.5_part_2.1119 CrossRefGoogle Scholar
  102. Lapointe BE, Clark MW (1992) Nutrient inputs from the watershed and coastal eutrophication in the Florida Keys. Estuar Coasts 15(4):465–476.  https://doi.org/10.2307/1352391 CrossRefGoogle Scholar
  103. Lapointe BE, Matzie WR (1996) Effects of stormwater nutrient discharges on eutrophication processes in nearshore waters of the Florida Keys. Estuaries 19(2):422–435.  https://doi.org/10.2307/1352460 CrossRefGoogle Scholar
  104. Lapointe BE, Smith NP (1987) A preliminary investigation of upwelling as a source of nutrients to Looe Key National Marine Sanctuary. NOAA Technical Memorandum, Washington, DCGoogle Scholar
  105. Lapointe BE, O’Connell JD, Garrett GS (1990) Nutrient couplings between on-site sewage disposal systems, groundwaters, and nearshore surface waters of the Florida Keys. Biogeochemistry 10(3):289–307.  https://doi.org/10.1007/bf00003149 CrossRefGoogle Scholar
  106. Lapointe BE, Littler MM, Littler DS (1992) Nutrient availability to marine macroalgae in siliciclastic versus carbonate-rich coastal waters. Estuaries 15(1):75–82.  https://doi.org/10.2307/1352712 CrossRefGoogle Scholar
  107. Lapointe BE, Littler MM, Littler DS (1993) Modification of benthic community structure by natural eutrophication: the Belize Barrier Reef. In: Proceedings of the seventh international coral reef symposium, pp 323–334Google Scholar
  108. Lapointe BE, Tomasko DA, Matzie WR (1994) Eutrophication and trophic state classification of seagrass communities in the Florida Keys. Bull Mar Sci 54(3):696–717Google Scholar
  109. Lapointe BE, Matzie WR, Barile PJ (2002) Biotic phase-shifts in Florida Bay and fore reef communities of the Florida Keys: linkages with historical freshwater flows and nitrogen loading from Everglades runoff. In: Porter JW, Porter KG (eds) The Everglades, Florida Bay, and Coral Reefs of the Florida Keys. CRC Press, Boca Raton, pp 629–648.  https://doi.org/10.1201/9781420039412-28 Google Scholar
  110. 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(1):23–58.  https://doi.org/10.1016/j.jembe.2004.01.019 CrossRefGoogle Scholar
  111. Lapointe BE, Thacker K, Hanson C, Getten L (2011) Sewage pollution in Negril, Jamaica: effects on nutrition and ecology of coral reef macroalgae. Chin J Oceanol Limnol 29:775–789.  https://doi.org/10.1007/s00343-011-0506-8 CrossRefGoogle Scholar
  112. Lapointe BE, Herren LW, Paule AL (2017) Septic systems contribute to nutrient pollution and harmful algal blooms in the St. Lucie Estuary, Southeast Florida, USA. Harmful Algae 70:1–22CrossRefGoogle Scholar
  113. Laws EA, Redalje DG (1979) Effect of sewage enrichment on the phytoplankton population of a subtropical estuary. Pac Sci 33(2):129–144Google Scholar
  114. Laws EA, Redalje DG (1982) Sewage diversion effects on the water column of a subtropical estuary. Mar Environ Res 6(4):265–279.  https://doi.org/10.1016/0141-1136(82)90041-1 CrossRefGoogle Scholar
  115. Lee TN, Leaman K, Williams E, Berger T, Atkinson L (1995) Florida Current meanders and gyre formation in the southern Straits of Florida. J Geophys Res 100(C5):8607–8620.  https://doi.org/10.1029/94JC02795 CrossRefGoogle Scholar
  116. Leichter JJ, Stewart HL, Miller SL (2003) Episodic nutrient transport to Florida coral reefs. Limnol Oceanogr 48:1394–1407CrossRefGoogle Scholar
  117. Lesser MP, Falcón LI, Rodríguez-Román A, Enríquez S, Hoegh-Guldberg O, Iglesias-Prieto R (2007) Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar Ecol Prog Ser 346:143–152.  https://doi.org/10.3354/meps07008 CrossRefGoogle Scholar
  118. Lessios HA, Robertson DR, Cubit JD (1984) Spread of Diadema mass mortality through the Caribbean. Science 226(4672):335–337CrossRefGoogle Scholar
  119. Levin SA (1992) The problem of pattern and scale in ecology: the Robert H. MacArthur award lecture. Ecology 73(6):1943–1967.  https://doi.org/10.2307/1941447 CrossRefGoogle Scholar
  120. Light SS, Dineen JW (1994) Water control in the Everglades: a historical perspective. Everglades: Ecosyst Restor 5:47–84Google Scholar
  121. Littler DS, Littler MM (2000) Caribbean Reef Plants. Offshore GraphicsGoogle Scholar
  122. Littler MM, Littler DS, Lapointe BE (1986) Baseline studies of herbivory and eutrophication on dominant reef communities of Looe Key National Marine Sanctuary. US Department of Commerce, National Oceanic and Atmospheric Administration, National Ocean Service, Washington, DCGoogle Scholar
  123. Magnuson JJ (1990) Long-term ecological research and the invisible present. Bioscience 40(7):495–501.  https://doi.org/10.2307/1311317 CrossRefGoogle Scholar
  124. Manfrino C, Jacoby CA, Camp E, Frazer TK (2013) A positive trajectory for corals at Little Cayman Island. PLoS One 8(10):e75432.  https://doi.org/10.1371/journal.pone.0075432 CrossRefPubMedPubMedCentralGoogle Scholar
  125. Manzello DP (2015) Rapid recent warming of coral reefs in the Florida Keys. Sci Rep 5:16762.  https://doi.org/10.1038/srep16762 CrossRefPubMedPubMedCentralGoogle Scholar
  126. Manzello DP, Berkelmans R, Hendee JC (2007) Coral bleaching indices and thresholds for the Florida reef tract, Bahamas, and St. Croix, US Virgin Islands. Mar Pollut Bull 54(12):1923–1931.  https://doi.org/10.1016/j.marpolbul.2007.08.009 CrossRefPubMedGoogle Scholar
  127. McCarthy JJ, Taylor WR, Taft JL (1975) The dynamics of nitrogen and phosphorus cycling in the open waters of Chesapeake Bay. In: Church TM (ed) Marine chemistry of the coastal environment. ACS Symposium Series, vol 18. American Chemical Society, Washington, DC, pp. 664–681.  https://doi.org/10.1021/bk-1975-0018.ch040 Google Scholar
  128. McIvor CC, Ley JA, Bjork RD (1994) Changes in freshwater inflow from the Everglades to Florida Bay including effects on biota and biotic processes. In: Davis SM, Ogden JC (eds) Everglades: the ecosystem and its restoration. St. Lucie Press, Delray Beach, pp 117–146Google Scholar
  129. McMurray SE, Henkel TP, Pawlik JR (2010) Demographics of increasing populations of the giant barrel sponge Xestospongia muta in the Florida Keys. Ecology 91(2):560–570.  https://doi.org/10.1890/08-2060.1 CrossRefPubMedGoogle Scholar
  130. McMurray SE, Finelli CM, Pawlik JR (2015) Population dynamics of giant barrel sponges on Florida coral reefs. J Exp Mar Biol Ecol 473:73–80.  https://doi.org/10.1016/j.jembe.2015.08.007 CrossRefGoogle Scholar
  131. Mikelsons K, Wang M (2018) Interactive online maps make satellite ocean data accessible. EOS.  https://doi.org/10.1029/2018EO096563 CrossRefGoogle Scholar
  132. Millennium Ecosystem Assessment (MEA) (2005) Ecosystems and human well-being: wetlands and water synthesis. World Resources Institute, Washington, DCGoogle Scholar
  133. Miller M, Bourque A, Bohnsack J (2002) An analysis of the loss of acroporid corals at Looe Key, Florida, USA: 1983–2000. Coral Reefs 21(2):179–182.  https://doi.org/10.1007/s00338-002-0228-7 CrossRefGoogle Scholar
  134. Montagnes DJ, Berges JA, Harrison PJ, Taylor F (1994) Estimating carbon, nitrogen, protein, and chlorophyll a from volume in marine phytoplankton. Limnol Oceanogr 39(5):1044–1060.  https://doi.org/10.4319/lo.1994.39.5.1044 CrossRefGoogle Scholar
  135. Muehllehner N, Langdon C, Venti A, Kadko D (2016) Dynamics of carbonate chemistry, production, and calcification of the Florida Reef Tract (2009–2010): evidence for seasonal dissolution. Glob Biogeochem Cycles 30(5):661–688.  https://doi.org/10.1002/2015GB005327 CrossRefGoogle Scholar
  136. Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27(7):454–460.  https://doi.org/10.2307/1297526 CrossRefGoogle Scholar
  137. National Oceanic and Atmospheric Administration (NOAA) (1988) Results of a workshop on coral reef research and management in the Florida Keys: a blueprint for action. National Undersea Research ProgramGoogle Scholar
  138. National Research Council (NRC) (2000) Clean coastal waters: understanding and reducing the effects of nutrient pollution. Ocean Studies Board, Water Science and Technology Board. National Academy Press, Washington DC.  https://doi.org/10.17226/9812
  139. National Research Council (NRC) (2002) Florida Bay research programs and their relation to the Comprehensive Everglades Restoration Plan. National Academy Press, Washington DCGoogle Scholar
  140. Nelson NG, Munoz-Carpena R, Phlips EJ (2017) A novel quantile method reveals spatiotemporal shifts in phytoplankton biomass descriptors between bloom and non-bloom conditions in a subtropical estuary. Mar Ecol Prog Ser 567:57–78.  https://doi.org/10.3354/meps12054 CrossRefGoogle Scholar
  141. NOAA (1988) Results of a workshop on coral reef research and management in the Florida Keys: a blueprint for action. Technical Report. National Undersea Research Program, FloridaGoogle Scholar
  142. NOAA (1996) Florida Keys National Marine Sanctuary Final Management Plan/Environmental Impact Statement, vol 1. NOAA, Silver SpringGoogle Scholar
  143. Nugues MM, Smith GW, Hooidonk RJ, Seabra MI, Bak RP (2004) Algal contact as a trigger for coral disease. Ecol Lett 7(10):919–923.  https://doi.org/10.1111/j.1461-0248.2004.00651.x CrossRefGoogle Scholar
  144. O’Neil JM, Capone DG (2008) Nitrogen cycling in coral reef environments. In: Capone DG, Bronk DA, Mulholland MR, Carpenter EJ (eds) Nitrogen in the marine environment, 2nd edn. Academic Press, San Diego, pp 949–989.  https://doi.org/10.1016/b978-0-12-372522-6.00021-9 CrossRefGoogle Scholar
  145. O’Brien JM, Scheibling RE (2018) Turf wars: competition between foundation and turf-forming species on temperate and tropical reefs and its role in regime shifts. Mar Ecol Prog Ser 590:1–17.  https://doi.org/10.3354/meps12530 CrossRefGoogle Scholar
  146. Odum HT, Odum EP (1955) Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll. Ecol Monogr 25(3):291–320CrossRefGoogle Scholar
  147. Ogden JC, Porter JW, Smith NP, Szmant AM, Jaap WD, Forcucci D (1994) A long-term interdisciplinary study of the Florida Keys Seascape. Bull Mar Sci 54:1059–1071Google Scholar
  148. Ogle D (2019) FSA: simple fisheries stock assessment methods (R package version 0.8.24)Google Scholar
  149. Parsons TR, Maika Y, Lalli CM (1984) Determination of chlorophylls and total carotenoids: spectrophotometric method. In: Parsons TR, Maika Y, Lalli CM (eds) A Manual of chemical and biological methods for seawater analysis. Pergamon Press, New York, pp 101–106.  https://doi.org/10.1016/b978-0-08-030287-4.50032-3 CrossRefGoogle Scholar
  150. Patterson KL, Porter JW, Ritchie KB, Polson SW, Mueller E, Peters EC, Santavy DL, Smith GW (2002) The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata. Proc Natl Acad Sci USA 99(13):8725–8730.  https://doi.org/10.1073/pnas.092260099 CrossRefPubMedGoogle Scholar
  151. Pew Oceans Commission (2003) America’s living oceans: charting a course for sea change. Pew Oceans Commission, Arlington, pp 1–166Google Scholar
  152. Pilson ME, Betzer SB (1973) Phosphorus flux across a coral reef. Ecology 54(3):581–588.  https://doi.org/10.2307/1935343 CrossRefGoogle Scholar
  153. Porter JW (2002) Introduction: the Everglades, Florida Bay, and Coral Reefs of the Florida Keys. In: Porter JW, Porter KG (eds) The Everglades, Florida Bay, and Coral Reefs of the Florida Keys. CRC Press, Boca Raton, pp 1–16Google Scholar
  154. Porter JW, Meier OW (1992) Quantification of loss and change in Floridian reef coral populations. Am Zool 32(6):625–640.  https://doi.org/10.1093/icb/32.6.625 CrossRefGoogle Scholar
  155. Porter JW, Dustan P, Jaap WC, Patterson KL, Kosmynin V, Wheaton JL, Meier O, Patterson ME, Parsons ME (2001) Patterns of spread of coral disease in the Florida Keys. 2000. Hydrobiologia 460(1):1–24.  https://doi.org/10.1023/A:101317761 CrossRefGoogle Scholar
  156. Porter JW, Kosmynin V, Patterson KL, Porter KG, Jaap WC, Wheaton JL, Hackett K, Lybolt M, Tsokos CP, Yanev G, Marcinek DM (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. CRC Press, Boca Raton, pp 749–769.  https://doi.org/10.1201/9781420039412-32 CrossRefGoogle Scholar
  157. Pratte ZA, Longo GO, Burns AS, Hay ME, Stewart FJ (2018) Contact with turf algae alters the coral microbiome: contact versus systemic impacts. Coral Reefs 37(1):1–13.  https://doi.org/10.1007/s00338-017-1615-4 CrossRefGoogle Scholar
  158. Rabalais NN, Turner RE, Diaz RJ, Justić D (2009) Global change and eutrophication of coastal waters. ICES J Mar Sci 66(7):1528–1537.  https://doi.org/10.1093/icesjms/fsp047 CrossRefGoogle Scholar
  159. Rädecker N, Pogoreutz C, Voolstra CR, Wiedenmann J, Wild C (2015) Nitrogen cycling in corals: the key to understanding holobiont functioning? Trends Microbiol 23(8):490–497.  https://doi.org/10.1016/j.tim.2015.03.008 CrossRefPubMedGoogle Scholar
  160. Redfield AC (1958) The biological control of chemical factors in the environment. Am Sci 46(3):230A–221. http://www.jstor.org/stable/27827150
  161. Richardson LL, Goldberg WM, Carlton RG, Halas JC (1998) Coral disease outbreak in the Florida Keys: plague type II. Rev Biol Trop 46(Suppl 5):187–198Google Scholar
  162. Risk MJ (1999) Paradise lost: how marine science failed the world’s coral reefs. Mar Freshw Res 50(8):831–837.  https://doi.org/10.1071/mf99067 CrossRefGoogle Scholar
  163. River GF, Edmunds PJ (2001) Mechanisms of interaction between macroalgae and scleractinians on a coral reef in Jamaica. J Exp Mar Biol Ecol 261(2):159–172.  https://doi.org/10.1016/s0022-0981(01)00266-0 CrossRefPubMedGoogle Scholar
  164. Rivera-Monroy VH, Twilley RR (1996) The relative role of denitrification and immobilization in the fate of inorganic nitrogen in mangrove sediments (Terminos Lagoon, Mexico). Limnol Oceanogr 41(2):284–296.  https://doi.org/10.4319/lo.1996.41.2.0284 CrossRefGoogle Scholar
  165. Robblee MB, Barber TR, Carlson PR Jr, Durako MJ, Fourqurean JW, Muehlstein LK, Porter D, Yarbro LA, Zieman RT, Zieman JC (1991) Mass mortality of the tropical seagrass Thalassia testudinum in Florida Bay (USA). Mar Ecol Prog Ser 71(3):297–299CrossRefGoogle Scholar
  166. Rockström J, Steffen W, Noone K, Persson Å, Chapin FS III, Lambin EF, Lenton TM, Scheffer M, Folke C, Schellnhuber HJ, Nykvist B (2009) A safe operating space for humanity. Nature 461(7263):472.  https://doi.org/10.1038/461472a CrossRefPubMedPubMedCentralGoogle Scholar
  167. Rogers CS (1990) Responses of coral reefs and reef organisms to sedimentation. Mar Ecol Prog Ser 62:185–202.  https://doi.org/10.3354/meps062185 CrossRefGoogle Scholar
  168. Rose CD, Sharp WC, Kenworthy WJ, Hunt JH, Lyons WG, Prager EJ, Valentine JF, Hall MO, Whitfield PE, Fourqurean JW (1999) Overgrazing of a large seagrass bed by the sea urchin Lytechinus variegatus in Outer Florida Bay. Mar Ecol Prog Ser 190:211–222CrossRefGoogle Scholar
  169. Rosset S, Wiedenmann J, Reed AJ, D’Angelo C (2017) Phosphate deficiency promotes coral bleaching and is reflected by the ultrastructure of symbiotic dinoflagellates. Mar Pollut Bull 118(1–2):180–187.  https://doi.org/10.1016/j.marpolbul.2017.02.044 CrossRefPubMedPubMedCentralGoogle Scholar
  170. Rudnick DT, Chen Z, Childers DL, Fontaine TD (1999) Phosphorus and nitrogen inputs to Florida Bay: the importance of the Everglades watershed. Estuaries 22(2):398–416.  https://doi.org/10.2307/1353207 CrossRefGoogle Scholar
  171. Ruzicka RR, Colella MA, Porter JW, Morrison JM, Kidney JA, Brinkhuis V, Lunz KS, Macaulay KA, Bartlett LA, Meyers MK, Colee J (2013) Temporal changes in benthic assemblages on Florida Keys reefs 11 years after the 1997/1998 El Niño. Mar Ecol Prog Ser 28(489):125–141CrossRefGoogle Scholar
  172. Ruzicka RR, Colella M, Brinkhuis V, Huebner L, Cummings K, Boisvert T, Halperin A, Ellis A (2017) Unpublished data. Coral Reef Evaluation and Monitoring Project. Fish and Wildlife Research Institute/Florida Fish and Wildlife Conservation Commission, Saint PetersburgGoogle Scholar
  173. Ryther JH, Dunstan WM (1971) Nitrogen, phosphorus, and eutrophication in the coastal marine environment. Science 171(3975):1008–1013.  https://doi.org/10.1126/science.171.3975.1008 CrossRefPubMedGoogle Scholar
  174. Santavy DL, Campbell J, Quarles RL, Patrick JM, Harwell LM, Parsons M, MacLaughlin L, Halas J, Mueller E, Peters EC, Hawkridge J (2006) The epizootiology of coral diseases in South Florida. EPA/600/R-05/146. U.S. Environmental Protection Agency, Gulf Ecology Division, Gulf BreezeGoogle Scholar
  175. Savoye N, Aminot A, Treguer P, Fontugne M, Naulet N, Kérouel R (2003) Dynamics of particulate organic matter δ15N and δ13C during spring phytoplankton blooms in a macrotidal ecosystem (Bay of Seine, France). Mar Ecol Prog Ser 255:27–41.  https://doi.org/10.3354/meps255027 CrossRefGoogle Scholar
  176. Selig ER, Casey KS, Bruno JF (2012) Temperature-driven coral decline: the role of marine protected areas. Glob Change Biol 18(5):1561–1570.  https://doi.org/10.1111/j.1365-2486.2012.02658.x CrossRefGoogle Scholar
  177. Shangguan Y, Glibert PM, Alexander JA, Madden CJ, Murasko S (2017) Nutrients and phytoplankton in semienclosed lagoon systems in Florida Bay and their responses to changes in flow from Everglades restoration. Limnol Oceanogr 62(S1):S327–S347.  https://doi.org/10.1002/lno.10599 CrossRefGoogle Scholar
  178. Sharp WC (2000) Destructive urchin grazing in a seagrass bed in Western Florida: when should resources managers intervene? Florida Bay Watch, Tavernier. http://nsgl.gso.uri.edu/flsgp/flsgpg00009.pdf
  179. Shinn EA, Hudson JH, Robbin DM, Lidz BH (1982) Spurs and grooves revisited: construction versus erosion, Looe Key Reef, Florida. In: Proceedings of the fourth international coral reef congress, pp 475–483Google Scholar
  180. Sinha E, Michalak AM, Balaji V (2017) Eutrophication will increase during the 21st century as a result of precipitation changes. Science 357(6349):405–408.  https://doi.org/10.1126/science.aan2409 CrossRefPubMedGoogle Scholar
  181. Smith NP (1994) Long-term Gulf-to-Atlantic transport through tidal channels in the Florida Keys. Bull Mar Sci 54:602–609Google Scholar
  182. Smith NP, Pitts PA (2002) Regional-scale and long-term transport patterns in the Florida Keys. In: Porter JW, Porter KG (eds) The Everglades, Florida Bay, and Coral Reefs of the Florida Keys. CRC Press, Boca Raton, pp 343–360Google Scholar
  183. Smith SV, Kimmerer WJ, Laws EA, Brock RE, Walsh TW (1981) Kaneohe Bay sewage diversion experiment: perspectives on ecosystem responses to nutritional perturbation. Pac Sci 35(4):279–395Google Scholar
  184. Smith TB, Purcell J, Barito JF (2007) The rocky intertidal biota of the Florida Keys: fifty-two years of change after Stephenson and Stephenson (1950). Bull Mar Sci 80(1):1–19Google Scholar
  185. Somerfield PJ, Jaap WC, Clarke KR, Callahan M, Hackett K, Porter J, Lybolt M, Tsokos C, Yanev G (2008) Changes in coral reef communities among the Florida Keys, 1996–2003. Coral Reefs 27(4):951–965.  https://doi.org/10.1007/s00338-008-0390-7 CrossRefGoogle Scholar
  186. State of Florida (1974) Final Report and Recommendations for the Proposed Florida Keys Area of Critical State Concern. Department of Administration, Department of State Planning, Bureau of Land and Water Management, TallahasseeGoogle Scholar
  187. Steinman J (1995) Red tide killing Keys fish. Key West Citizen, Key WestGoogle Scholar
  188. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton.  https://doi.org/10.1515/9781400885695
  189. Stevens WK (1997) A bay is sick. Will the cure make it worse? The New York Times. http://www.nytimes.com/1997/04/15/science/a-bay-is-sick-will-the-cure-make-it-worse.html. Accessed 01 March 2018
  190. Stumpf RP, Culver ME, Tester PA, Tomlinson M, Kirkpatrick GJ, Pederson BA, Truby E, Ransibrahmanakul V, Soracco M (2003) Monitoring Karenia brevis blooms in the Gulf of Mexico using satellite ocean color imagery and other data. Harmful Algae 2:147–160.  https://doi.org/10.1016/S1568-9883(02)00083-5 CrossRefGoogle Scholar
  191. Sutherland KP, Shaban S, Joyner JL, Porter JW, Lipp EK (2011) Human pathogen shown to cause disease in the threatened eklhorn coral Acropora palmata. PLoS One 6(1–7):E23468.  https://doi.org/10.1371/journal.pone.0023468 CrossRefPubMedPubMedCentralGoogle Scholar
  192. Szmant AM, Forrester A (1996) Water column and sediment nitrogen and phosphorus distribution patterns in the Florida Keys, USA. Coral Reefs 15(1):21–41.  https://doi.org/10.1007/BF01626075 CrossRefGoogle Scholar
  193. Taylor WR (1960) Marine algae of the eastern tropical and subtropical coasts of the Americas. University of Michigan Press, Ann Arbor, p 870Google Scholar
  194. Technicon (1973) Nitrate and nitrite in water and wastewater. Industrial method number 100-70W. In: Conflo IV Operating Manual. Revision A-122 4730. Thermo Scientific Technicon Industrial Systems, TarrytownGoogle Scholar
  195. Thermo Scientific (2007) Conflo IV Operating Manual. Revision A-122 4730Google Scholar
  196. Tomascik T, Sander F (1985) Effects of eutrophication on reef-building corals. Mar Biol 87(2):143–155.  https://doi.org/10.1007/bf00392901 CrossRefGoogle Scholar
  197. Tomascik T, Sander F (1987) Effects of eutrophication on reef-building corals. Mar Biol 94(1):53–75.  https://doi.org/10.1007/bf00392900 CrossRefGoogle Scholar
  198. Toth LT, Kuffner IB, Stathakopoulos Shinn EA (2018) A 3,000-year lag between the geological and ecological shutdown of Florida’s coral reefs. Glob Chang Biol 24(11):5471–5483.  https://doi.org/10.1111/gcb.14389 CrossRefPubMedGoogle Scholar
  199. Trenberth KE, Hoar TJ (1996) The 1990–1995 El Niño-Southern Oscillation event: longest on record. Geophys Res Lett 23(1):57–60CrossRefGoogle Scholar
  200. Trimble PJ, Marban JA, Molina M, Sculley SP (1990) Special Report: Analysis of the 1989–1990 drought. Water Resources Division, Department of Research and Evaluation, South Florida Water Management District, West Palm BeachGoogle Scholar
  201. Urban NH, Davis SM, Aumen NG (1993) Fluctuations in sawgrass and cattail densities in Everglades Water Conservation Area 2A under varying nutrient, hydrologic and fire regimes. Aquat Bot 46(3–4):203–223.  https://doi.org/10.1016/0304-3770(93)90002-e CrossRefGoogle Scholar
  202. USACE, South Florida Water Management District (SFWMD) (1999) Central and Southern Florida Project Comprehensive Review Study: Final Integrated Feasibility Report and Programmatic Environmental Impact Statement. United States Army Corps of Engineers, JacksonvilleGoogle Scholar
  203. Van Woesik R, Tomascik T, Blake S (1999) Coral assemblages and physico-chemical characteristics of the Whitsunday Islands: evidence of recent community changes. Mar Freshw Res 50(5):427–440.  https://doi.org/10.1071/mf97046 CrossRefGoogle Scholar
  204. Vega-Thurber RL, Burkepile DE, Correa AM, Thurber AR, Shantz AA, Welsh R, Pritchard C, Rosales S (2012) Macroalgae decrease growth and alter microbial community structure of the reef-building coral, Porites astreoides. PLoS One 7(9):e44246.  https://doi.org/10.1371/journal.pone.0044246 CrossRefPubMedPubMedCentralGoogle Scholar
  205. Vega-Thurber RL, Burkepile DE, Fuchs C, Shantz AA, McMinds R, Zaneveld JR (2014) Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Glob Chang Biol 20(2):544–554.  https://doi.org/10.1111/gcb.12450 CrossRefPubMedGoogle Scholar
  206. Vermeij MJ, Van Moorselaar I, Engelhard S, Hörnlein C, Vonk SM, Visser PM (2010) The effects of nutrient enrichment and herbivore abundance on the ability of turf algae to overgrow coral in the Caribbean. PLoS One 5(12):e14312.  https://doi.org/10.1371/journal.pone.0014312 CrossRefPubMedPubMedCentralGoogle Scholar
  207. Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7(3):737–750.  https://doi.org/10.1890/1051-0761(1997)007%5b0737:haotgn%5d2.0.co;2 CrossRefGoogle Scholar
  208. Voss JD, Richardson LL (2006) Nutrient enrichment enhances black band disease progression in corals. Coral Reefs 25(4):569–576.  https://doi.org/10.1007/s00338-006-0131-8 CrossRefGoogle Scholar
  209. Wagner DE, Kramer P, Van Woesik R (2010) Species composition, habitat, and water quality influence coral bleaching in southern Florida. Mar Ecol Prog Ser 408:65–78.  https://doi.org/10.3354/meps08584 CrossRefGoogle Scholar
  210. Wang L, Shantz AA, Payet JP, Sharpton TJ, Foster A, Burkepile DE, Vega Thurber R (2018) Corals and their microbiomes are differentially affected by exposure to elevated nutrients and a natural thermal anomaly. Front Mar Sci 5:101.  https://doi.org/10.3389/fmars.2018.00101 CrossRefGoogle Scholar
  211. Ward-Paige CA, Risk MJ, Sherwood OA, Jaap WC (2005) Clionid sponge surveys on the Florida Reef Tract suggest land-based nutrient inputs. Mar Pollut Bull 51(5):570–579.  https://doi.org/10.1016/j.marpolbul.2005.04.006 CrossRefPubMedGoogle Scholar
  212. Wheaton JL, Japp WC (1988) Corals and other prominent benthic Cnidaria of Looe Key National Marine Sanctuary. Florida Marine Research Publications, Florida, p 43Google Scholar
  213. White MW, Porter JW (1985) The establishment and monitoring of two permanent photograph transects in Looe Key and Key Largo National Marine Sanctuaries (Florida Keys). In: Proceedings of the fifth international coral reef congress, pp 531–537Google Scholar
  214. Wickham H (2009) ggplot2: Elegant Graphics for Data Analysis (Use R). Springer, New YorkGoogle Scholar
  215. Wiebe WJ, Johannes RE, Webb KL (1975) Nitrogen fixation in a coral reef community. Science 188(4185):257–259.  https://doi.org/10.1126/science.188.4185.257 CrossRefPubMedGoogle Scholar
  216. Wiedenmann J, D’Angelo C, Smith EG, Hunt AN, Legiret FE, Postle AD, Achterberg EP (2013) Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat Clim Change 3(2):160–164.  https://doi.org/10.1038/nclimate1661 CrossRefGoogle Scholar
  217. Wilkinson CR (1996) Global change and coral reefs: impacts on reefs, economies and human cultures. Glob Change Biol 2(6):547–558.  https://doi.org/10.1111/j.1365-2486.1996.tb00066.x CrossRefGoogle Scholar
  218. Wilkinson CC (2004) Status of coral reefs of the world: 2004. Australian Institute of Marine Science, Cape FergusonGoogle Scholar
  219. Williams SL, Carpenter RC (1988) Nitrogen-limited primary productivity of coral reef algal turfs: potential contribution of ammonium excreted by Diadema antillarum. Mar Ecol Prog Ser 47:145–152.  https://doi.org/10.3354/meps047145 CrossRefGoogle Scholar
  220. Wolff NH, Mumby PJ, Devlin M, Anthony K (2018) Vulnerability of the Great Barrier Reef to climate change and local pressures. Glob Change Biol 24(5):1978–1991.  https://doi.org/10.1111/gcb.14043 CrossRefGoogle Scholar
  221. Woods J (2010) Surface water discharge and salinity monitoring of coastal estuaries in Everglades National Park, USA, in support of the Comprehensive Everglades Restoration Plan. In: Proceedings of the third international perspective on current and future state of water resources and the environment, ChennaiGoogle Scholar
  222. Wooldridge SA (2009) Water quality and coral bleaching thresholds: formalising the linkage for the inshore reefs of the Great Barrier Reef, Australia. Mar Pollut Bull 58(5):745–751.  https://doi.org/10.1016/j.marpolbul.2008.12.013 CrossRefPubMedGoogle Scholar
  223. Wooldridge SA (2014) Assessing coral health and resilience in a warming ocean: why looks can be deceptive. BioEssays 36(11):1041–1049.  https://doi.org/10.1002/bies.201400074 CrossRefPubMedGoogle Scholar
  224. Wooldridge SA, Done TJ (2009) Improved water quality can ameliorate effects of climate change on corals. Ecol Appl 19(6):1492–1499.  https://doi.org/10.1890/08-0963.1 CrossRefPubMedGoogle Scholar
  225. Yentsch CS, Yentsch CM, Cullen JJ, Lapointe B, Phinney DA, Yentsch SW (2002) Sunlight and water transparency: cornerstones in coral research. J Exp Mar Biol Ecol 268(2):171–183.  https://doi.org/10.1016/s0022-0981(01)00379-3 CrossRefGoogle Scholar
  226. Zaneveld JR, Burkepile DE, Shantz AA, Pritchard CE, McMinds R, Payet JP, Welsh R, Correa AM, Lemoine NP, Rosales S, Fuchs C (2016) Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat Commun 7:11833.  https://doi.org/10.1038/ncomms11833 CrossRefPubMedPubMedCentralGoogle Scholar
  227. Zhao J, Hu C, Lapointe B, Melo N, Johns EM, Smith RH (2013) Satellite-observed black water events off Southwest Florida: implications for coral reef health in the Florida Keys National Marine Sanctuary. Remote Sens 5(1):415–431.  https://doi.org/10.3390/rs5010415 CrossRefGoogle Scholar
  228. Zieman JC (1987) A review of certain aspects of the life, death, and distribution of the seagrasses of the southeastern United States 1960–1985. Fla Mar Res Publ 42:53–76Google Scholar
  229. Zimmerman CF, Price MT, Montgomery JP (1977) Operations methods and quality control of Technicon AutoAnalyzer® systems for nutrient determinations in seawater. Technical Report No. 11. Harbor Branch Foundation, Fort PieceGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Harbor Branch Oceanographic InstituteFlorida Atlantic UniversityFort PierceUSA
  2. 2.Odum School of EcologyUniversity of GeorgiaAthensUSA
  3. 3.College of Marine ScienceUniversity of South FloridaSt. PetersburgUSA

Personalised recommendations