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AMBIO

, Volume 43, Issue 3, pp 361–376 | Cite as

Evidence of Large-Scale Chronic Eutrophication in the Great Barrier Reef: Quantification of Chlorophyll a Thresholds for Sustaining Coral Reef Communities

  • Peter R. F. Bell
  • Ibrahim Elmetri
  • Brian E. Lapointe
Review

Abstract

Long-term monitoring data show that hard coral cover on the Great Barrier Reef (GBR) has reduced by >70 % over the past century. Although authorities and many marine scientists were in denial for many years, it is now widely accepted that this reduction is largely attributable to the chronic state of eutrophication that exists throughout most of the GBR. Some reefs in the far northern GBR where the annual mean chlorophyll a (Chl a) is in the lower range of the proposed Eutrophication Threshold Concentration for Chl a (~0.2–0.3 mg m−3) show little or no evidence of degradation over the past century. However, the available evidence suggests that coral diseases and the crown-of-thorns starfish will proliferate in such waters and hence the mandated eutrophication Trigger values for Chl a (~0.4–0.45 mg m−3) will need to be decreased to ~0.2 mg m−3 for sustaining coral reef communities.

Keywords

Coral reefs Eutrophication Corallivores Coral skeletal disease Coral bleaching 

Notes

Acknowledgments

Stafford Bettridge provided several underwater video clips. Paul Treloar, Anisul Islam, and Stephen Coombs prepared the SeaWiFS and CZCS images from data provided free of charge from the NASA archives. This support is gratefully acknowledged. Also, we wish to thank the reviewers of the manuscript who provided a number of constructive suggestions. This is contribution #1904 from the Harbor Branch Oceanographic Institute at Florida Atlantic University, Ft. Pierce, FL.

References

  1. Aeby, G.S., G.J. Williams, E.C. Franklin, J. Kenyon, E.F. Cox, S. Coles, and T.M. Work. 2011. Patterns of coral disease across the Hawaiian archipelago: Relating disease to environment. PLoS ONE 6: e20370.CrossRefGoogle Scholar
  2. AIMS. 2012. Australian Institute of Marine Science, Townsville. Retrieved 10 November, 2012, from http://e-atlas.org.au/geoserver/www/map.html?v=2&z=5&ll=-18,148&n=1&m0=ea-Natural_Earth_2:V,Chlorophyll-Chlorophyll-micro_grams_per_litre:V.
  3. Antonius, A., and B. Riegl. 1997. A possible link between coral diseases and a corallivorous snail (Drupella cornus) outbreak in the Red Sea. Atoll Research Bulletin 477: 1–9.CrossRefGoogle Scholar
  4. Ayukai, T., K. Okaji, and J.S. Lucas. 1997. Food limitation in the growth and development of crown-of-thorns starfish in the Great Barrier Reef. In Proceedings of the 8th International Coral Reef Symposium, vol. 1, 621–626. Panama: Smithsonian Tropical Research Institute.Google Scholar
  5. Bell, J.L. 1988. Optimal feeding by gastropod larvae: Patches and picoplankton. American Zoologist 28: 167A.Google Scholar
  6. Bell, P.R.F. 1991. Status of eutrophication in the Great Barrier Reef Lagoon. Marine Pollution Bulletin 23: 89–93.CrossRefGoogle Scholar
  7. Bell, P.R.F. 1992. Eutrophication and coral reefs—Some examples in the Great Barrier Reef Lagoon. Water Research 26: 553–568.CrossRefGoogle Scholar
  8. Bell, P.R.F., and I. Elmetri. 1995. Ecological indicators of large scale eutrophication in the Great Barrier Reef (GBR) Lagoon. AMBIO 24: 208–215.Google Scholar
  9. Bell, P.R.F., and I. Elmetri. 1998. Large-scale eutrophication in the Great Barrier Reef Lagoon—Causes of the problem and some possible solutions. In Chemeca 98, Australasian Chemical Engineering Conference. Paper No. 305, ed. R.B. Newell, and C.J. Smith, Institution of Engineers, Australia, Barton, 12 pp.Google Scholar
  10. Bell, P.R.F., and I. Elmetri. 2007. Some chemical factors regulating the growth of Lyngbya majuscula in Moreton Bay, Australia: Importance of sewage discharges. Hydrobiologia 592: 359–371.CrossRefGoogle Scholar
  11. Bell, P.R.F., and A.J. Gabric. 1990. The use of field survey and satellite remote sensing in determining the extent and causes of eutrophication in the Great Barrier Reef Lagoon, Australia. In Proceedings of the Fourth Pacific Congress on Marine Science and Technology, vol. II, 25–32. Tokyo: PACON 90.Google Scholar
  12. Bell, P.R.F., and A.J. Gabric. 1991. Must GBR pollution become chronic before management reacts? Search 22: 117–119.Google Scholar
  13. Bell, P.R.F., I. Elmetri, and P. Uwins. 1999. Nitrogen fixation of Trichodesmium spp. in the Great Barrier Reef Lagoon-importance to the overall nitrogen budget. Marine Ecology Progress Series 186: 119–126.CrossRefGoogle Scholar
  14. Bell, P.R.F., B.E. Lapointe, and I. Elmetri. 2007. Reevaluation of ENCORE: Support for the eutrophication threshold model for coral reefs. AMBIO 36: 416–424.CrossRefGoogle Scholar
  15. Bell, P.R.F., I. Elmetri, and B.E. Lapointe. 2012. Synoptic scale monitoring supports the coral reef eutrophication threshold model. Retrieved August 15, 2012, from http://www.icrs2012.com/eposters/P227.pdf.
  16. Boyett, H.V. 2006. The ecology and microbiology of black band disease and brown band syndrome on the Great Barrier Reef. MSc Thesis. Townsville, Australia: James Cook University.Google Scholar
  17. Brando, V.E., T. Schroeder, and A.G. Dekker. 2010. Reef rescue marine monitoring program: using remote sensing for GBR wide water quality. Retrieved January 5, 2013, from http://www.rrrc.org.au/publications/downloads/372b--378_CSIRO_final-report_15Apr2010.pdf.
  18. Brodie, J., and J. Waterhouse. 2012. A critical review of environmental management of the ‘not so Great’ Barrier Reef. Estuarine, Coastal and Shelf Science 104–105: 1–22.CrossRefGoogle Scholar
  19. Brodie, J., K. Fabricius, G. De’ath, and K. Okaji. 2005. Are increased nutrient inputs responsible for more outbreaks of crown-of-thorns starfish? An appraisal of the evidence. Marine Pollution Bulletin 51: 266–278.CrossRefGoogle Scholar
  20. Brodie, J., G. De’ath, M. Devlin, M. Furnas, and M. Wright. 2007. Spatial and temporal patterns of near-surface chlorophyll a in the Great Barrier Reef lagoon. Marine & Freshwater Research 58: 342–353.CrossRefGoogle Scholar
  21. Brodie, J., T. Schroeder, K. Rohde, J. Faithful, B. Masters, A. Dekker, V. Brando, and M. Maughan. 2010. Dispersal of suspended sediments and nutrients in the Great Barrier Reef lagoon during river-discharge events: Conclusions from satellite remote sensing and concurrent flood-plume sampling. Marine & Freshwater Research 61: 651–664.CrossRefGoogle Scholar
  22. Bruckner, A.W., R.J. Bruckner, and E.H. Williams Jr. 1997. Spread of a black-band disease epizootic through the coral reef system in St. Ann’s Bay, Jamaica. Bulletin of Marine Science 61: 919–928.Google Scholar
  23. Bruno, J.F., and E.R. Selig. 2007. Regional decline of coral cover in the Indo-Pacific: Timing, extent, and subregional comparisons. PLoS ONE 2: e711.CrossRefGoogle Scholar
  24. Bruno, J.F., L.E. Petes, C.D. Harvell, and A. Hettinger. 2003. Nutrient enrichment can increase the severity of coral diseases. Ecological Letters 6: 1056–1061.CrossRefGoogle Scholar
  25. Cervino, J.M., R.L. Hayes, S.W. Polson, S.C. Polson, T.G. Goreau, R.J. Martinez, and G.W. Smith. 2004. Relationship of Vibrio species infection and elevated temperatures to yellow blotch/band disease in Caribbean Corals. Applied and Environmental Microbiology 70: 6855–6864.CrossRefGoogle Scholar
  26. De’ath, G., K.E. Fabricius, H. Sweatman, and M. Puotinen. 2012. The 27-year decline of coral cover on the Great Barrier Reef and its causes, 1–5. Retrieved October 2, 2012, from www.pnas.org/cgi/doi/10.1073/pnas.1208909109.
  27. Delean, S., and G. De’ath. 2008. Spatial and temporal patterns of indicators of reef health on the Great Barrier Reef. Report to the Marine and Tropical Sciences Research Facility. Reef and Rainforest Research Centre Limited, Cairns, 116 pp.Google Scholar
  28. Elmetri, I., and P.R.F. Bell. 2004. Effects of phosphorus on the growth and nitrogen fixation rates of Lyngbya majuscula: implications for management in Moreton Bay, Queensland. Marine Ecology Progress Series 281: 27–35.Google Scholar
  29. Endean, R., and W. Stablum. 1973. The apparent extent of recovery of reefs of Australia’s Great Barrier Reef devastated by the crown-of-thorns starfish. Atoll Research Bulletin 168: 1–41.CrossRefGoogle Scholar
  30. Fabricius, K.E., K. Okaji, and G. De’ath. 2010. Three lines of evidence to link outbreaks of the crown-of-thorns seastar Acanthaster planci to the release of larval food limitation. Coral Reefs 29: 593–605.Google Scholar
  31. Falkowski, P.G., Z. Dubinsky, L. Muscatine, and L. McCloskey. 1993. Population control in symbiotic corals. BioScience 43: 606–611.CrossRefGoogle Scholar
  32. Fu, F., Y. Zhang, P.R.F. Bell, and D. Hutchins. 2005. Phosphate uptake and growth kinetics of Trichodesmium (Cyanobacteria) isolates from the North Atlantic Ocean and the Great Barrier Reef, Australia. Journal of Phycology 41: 62–73.CrossRefGoogle Scholar
  33. Gabric, A.J., P. Hoffenberg, and W. Boughton. 1990. Spatio-temporal variability in surface chlorophyll distribution in the central Great Barrier Reef as derived from CZCS imagery. Australian Journal of Marine and Freshwater Research 41: 313–324.CrossRefGoogle Scholar
  34. GBRMPA. 2010. Water Quality Guidelines for the Great Barrier Reef Marine Park Revised Edition. Great Barrier Reef Marine Park Authority. Retrieved May 1, 2012, from http://elibrary.gbrmpa.gov.au/jspui/handle/11017/432.
  35. Goreau, T.J., J. Cervino, M. Goreau, R. Hayes, M. Hayes, L. Richardson, G. Smith, K. DeMeyer, et al. 1998. Rapid spread of diseases in Caribbean coral reefs. Revista de Biología Tropical 46: 157–171.Google Scholar
  36. Greve, W., and T.R. Parsons. 1977. Photosynthesis and fish production: Hypothetical effects of climate change and pollution. Helgoländer Wissenschaftliche Meeresuntersuchungen 30: 666–671.CrossRefGoogle Scholar
  37. Haapkyla, J., R.K.F. Unsworth, M. Flavell, D.G. Bourne, B. Schaffelke, and B.L. Willis. 2011. Seasonal rainfall and runoff promote coral disease on an inshore reef. PLoS ONE 6: e16893.CrossRefGoogle Scholar
  38. Hughes, T. 1994. Catastrophes, phase-shifts and large-scale degradation of a Caribbean coral reef. Science 265: 1547–1551.Google Scholar
  39. Hughes, T.P., A.M. Szmant, R. Steneck, R. Carpenter, and S. Miller. 1999. Algal blooms on coral reefs: What are the causes? Limnology and Oceanography 44: 1583–1586.CrossRefGoogle Scholar
  40. Ikeda, T., M. Gilmartin, N. Revelante, A.W. Mitchell, J.H. Carleton, P. Dixon, S.M. Hutchinson, E. Fay Hing, et al. 1980. Biological, chemical and physical observations in inshore waters of the Great Barrier Reef, North Queensland 1975-1978. Data Report AIMS-OS-80-1, Australian Institute of Marine Science Townsville, 56 pp.Google Scholar
  41. Kerry, J. 2011. Relationship between corals and fishes on the Great Barrier Reef. Australian Institute of Marine Science (AIMS). Retrieved November 9, 2012, from http://e-atlas.org.au/content/relationship-between-corals-and-fishes-great-barrier-reef.
  42. Kinsey, D.W. 1991. Can we resolve the nutrient issue for the reef? Search 22: 119–121.Google Scholar
  43. Kline, D.I., N.M. Kuntz, M. Breitbart, N. Knowlton, and F. Rohwer. 2006. Role of elevated organic carbon levels and microbial activity in coral mortality. Marine Ecology Progress Series 314: 119–125.Google Scholar
  44. Koop, K., D. Booth, A. Broadbent, J. Brodie, D. Bucher, D. Capone, J. Coll, W. Dennison, et al. 2001. ENCORE: The effect of nutrient enrichment on coral reefs. Synthesis of results and conclusions. Marine Pollution Bulletin 42: 91–120.CrossRefGoogle Scholar
  45. Kroon, F.J., P.M. Kuhnert, B.L. Henderson, S.N. Wilkinson, A. Kinsey-Henderson, B. Abbott, J.E. Brodie, and R.D.R. Turner. 2012. River loads of suspended solids, nitrogen, phosphorus and herbicides delivered to the Great Barrier Reef lagoon. Marine Pollution Bulletin 65: 167–181.CrossRefGoogle Scholar
  46. Kuta, K.G., and L.L. Richardson. 2002. Ecological aspects of black band disease of corals: Relationships between disease incidence and environmental factors. Coral Reefs 21: 393–398.Google Scholar
  47. Lapointe, B.E. 1989. Caribbean coral reefs: Are they becoming algal reefs. Sea Frontiers, March–April, 83–84.Google Scholar
  48. Lapointe, B.E. 1997. Nutrient thresholds–Bottom-up control of macroalgal blooms on coral reefs in Jamaica and South East Florida. Limnology and Oceanography 42: 1119–1131.CrossRefGoogle Scholar
  49. Lapointe, B.E., and M.A. Mallin. 2011. Nutrient enrichment and eutrophication on fringing coral reefs of Bonaire and Curaçao, Netherlands Antilles. Report to the United Nations Environment Programme for the NACRI Coral Reef Monitoring Program, Harbor Branch Oceanographic Institute, Ft. Pierce Fl, 42 pp.Google Scholar
  50. Lapointe, B.E., P. Barile, and W.R. Matzie. 2004. Anthropogenic nutrient enrichment of seagrass and coral reef communities in the Lower Florida Keys: Discrimination of local versus regional nitrogen sources. Journal of Experimental Marine Biology and Ecology 308: 23–58.CrossRefGoogle Scholar
  51. Lapointe B., B. Bedford, and R. Baumberger. 2007. Looe Key, FL: Nutrients and climate change pose threat to coral reefs. In Effects of Nutrient enrichment in the nation’s estuaries: A decade of change, 104–105. Retrieved August 30, 2013, from http://ccma.nos.noaa.gov/publications/eutroupdate/.
  52. Larkum, A.W.D., and A.D.L. Steven. 1994. ENCORE: The effect of nutrient enrichment on coral reefs. 1. Experimental design and research programme. Marine Pollution Bulletin 29: 112–120.CrossRefGoogle Scholar
  53. Laws, E.A., and D.G. Redalje. 1979. Effect of sewage enrichment on phytoplankton population of a subtropical estuary. Pacific Science 33: 129–144.Google Scholar
  54. Littler, M.M., P.R. Taylor, and D.S. Littler. 1983. Algal resistance to herbivory on a Caribbean barrier reef. Coral Reefs 2: 111–118.CrossRefGoogle Scholar
  55. Littler, M.M., D.S. Littler, and B.L. Brooks. 2009. Herbivory, nutrients, stochastic events, and relative dominances of benthic indicator groups on coral reefs: A review and recommendations. Smithsonian Contributions to the Marine Sciences 38: 401–414. doi: 10.5479/si.01960768.38.401.CrossRefGoogle Scholar
  56. Lucas, J.S. 1982. Quantitative studies of feeding and nutrition during larval development of the coral reef asteroid Acanthaster planci (L.). Journal of Experimental Marine Biology and Ecology 65: 173–193.Google Scholar
  57. Marubini, F., and P.S. Davies. 1996. Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals. Marine Biology 127: 319–328.CrossRefGoogle Scholar
  58. McCook, L.J., I.R. Price, and D.W. Klumpp. 1997. Macroalgae on the GBR: Causes or consequences, indicators or models of reef degradation. In Proceedings of the 8th International Coral Reef Symposium, vol. 2, 1851–1856. Panama: Smithsonian Tropical Research Institute.Google Scholar
  59. Middleton, J.H., P. Coutis, D.A. Griffin, A. Macks, A. McTaggart, M.A. Merrifield, and G.J. Nippard. 1994. Circulation and water mass characteristics of the Southern Great Barrier Reef. Australian Journal of Marine and Freshwater Research 45: 1–18.CrossRefGoogle Scholar
  60. Moyer, J.T., W.K. Emerson, and M. Ross. 1982. Massive destruction of scleractinian corals by the muricid gastropod Drupella in Japan and the Philippines. Nautilis 96: 69–82.Google Scholar
  61. Nagelkerken, I. 2006. Relationship between anthropogenic impacts and bleaching-associated tissue mortality of corals in Curaçao (Netherlands Antilles). Revista de Biologia Tropical 54: 31–44.Google Scholar
  62. Nugues, M.M., and R.P.M. Bak. 2009. Brown-band syndrome on feeding scars of the crown-of-thorn starfish Acanthaster planci. Coral Reefs 28: 507–510.CrossRefGoogle Scholar
  63. Olson, R.R. 1987. In situ culturing as a test of the larval starvation hypothesis for the Crown-of-Thorns Starfish, Acanthaster planci. Limnology and Oceanography 32: 895–904.CrossRefGoogle Scholar
  64. Osborne, K., A.M. Dolman, S.C. Burgess, and K.A. Johns. 2011. Disturbance and the dynamics of coral cover on the Great Barrier Reef (1995–2009). PLoS ONE 6: e17516.CrossRefGoogle Scholar
  65. Revelante, N., and M. Gilmartin. 1982. Dynamics of phytoplankton in the Great Barrier Reef lagoon. Journal of Plankton Research 4: 47–76.CrossRefGoogle Scholar
  66. Richardson, A.J., A. Bakun, G.C. Hays, and M.J. Gibbons. 2009. The jellyfish joyride: Causes, consequences and management responses to a more gelatinous future. Trends in Ecology & Evolution 24: 312–322.CrossRefGoogle Scholar
  67. Risk, M.J. 1999. Paradise lost: How marine science failed the world’s coral reefs. Marine & Freshwater Research 50: 831–837.CrossRefGoogle Scholar
  68. Ryther, J.H., and C.B. Officer 1981. Impact of nutrient enrichment on water uses. In Estuaries and nutrients, ed. B.J. Neilson, and L.E. Cronin, 247–261 Clifton: Humana Press.Google Scholar
  69. Saville-Kent, W. 1893. The Great Barrier Reef of Australia: Its products and potentialities, 387 pp. London: W.H. Allen & Co. Ltd. (reproduced Melbourne: John Currey, O’Neil Pty Ltd., 1972).Google Scholar
  70. Smith, S.V., W.J. Kimmerer, E.A. Laws, R.E. Brock, and T.W. Walsh. 1981. Kaneohe Bay sewage diversion experiment: Perspectives on ecosystem responses to nutritional perturbation. Pacific Science 35: 279–395.Google Scholar
  71. Sweatman, H., A. Cheal, G. Coleman, M. Emslie, K. Johns, M. Jonker, I. Miller, and K. Osborne. 2008. Long term monitoring of the Great Barrier Reef, status report number 8. Australian Institute of Marine Science, Townsville, 369 pp.Google Scholar
  72. Tomascik, T., and F. Sander. 1985. Effects of eutrophication on reef building corals I. Growth rate of the reef-building coral Montastrea annularis. Marine Biology 87: 143–155.CrossRefGoogle Scholar
  73. Tomascik, T., and F. Sander. 1987. Effects of eutrophication on reef building corals II. Structure of scleractinian coral communities on fringing reefs, Barbados, West Indies. Marine Biology 94: 53–75.CrossRefGoogle Scholar
  74. Voss, J.D., and L.L. Richardson. 2006. Nutrient enrichment enhances black band disease progression in corals. Coral Reefs 25: 569–576.CrossRefGoogle Scholar
  75. Wachenfeld, D.R. 1995. Long term trends in the status of coral reef-flat benthos—The use of historical photographs, State of the Great Barrier Reef World Heritage Area Workshop. GBRMPA Workshop Series 23: 134–148.Google Scholar
  76. Walker, T.A. 1991. Is the reef really suffering from chronic pollution? Search 22: 115–117.Google Scholar
  77. Webb, K.L., W.D. DuPaul, W. Wiebe, W. Sottille, and R.E. Johannes. 1975. Enewetak (Eniwetok) Atoll: Aspects of nitrogen cycle on a coral reef. Limnology and Oceanography 20: 198–210.CrossRefGoogle Scholar
  78. Williams, D.M., and A.I. Hatcher. 1983. Structure of fish communities on outer slopes of inshore, mid-shelf and outer shelf reefs of the Great Barrier Reef. Marine Ecology Progress Series 10: 239–250.Google Scholar
  79. Willis, B.L., C.A. Page, and E.A. Dinsdale. 2004. Coral disease on the Great Barrier Reef. In Coral health and disease, ed. E. Rosenberg, and Y. Loya, 69–104. Berlin: Springer.Google Scholar
  80. Wooldridge, S.A., and T.J. Done. 2009. Improved water quality can ameliorate effects of climate change on corals. Ecological Applications 19: 1492–1499.CrossRefGoogle Scholar
  81. Wulff, F., B.D. Eyre, and R. Johnstone. 2011. Nitrogen versus phosphorus limitation in a subtropical coastal embayment (Moreton Bay; Australia): Implications for management. Ecological Modelling 222: 120–130.CrossRefGoogle Scholar

Copyright information

© Royal Swedish Academy of Sciences 2013

Authors and Affiliations

  • Peter R. F. Bell
    • 1
  • Ibrahim Elmetri
    • 2
  • Brian E. Lapointe
    • 3
  1. 1.School of Chemical/Environmental EngineeringUniversity of QueenslandSt LuciaAustralia
  2. 2.AMZA LtdWellingtonNew Zealand
  3. 3.Harbor Branch Oceanographic InstituteFlorida Atlantic UniversityFort PierceUSA

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