Spatial variation in the functional characteristics of herbivorous fish communities and the resilience of coral reefs

Ecological Applications

Volumn 23, Issue 1, 2013, Pages 174-188

  Cheal, Alistair J ^a   Emslie, Michael ^a   MacNeil, M Aaron ^a   Miller, Ian ^a   Sweatman, Hugh ^a  

^a AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

Author keywords

Coral reefs; Ecosystem resilience; Functional diversity; Functional group; Functional redundancy; Herbivory; Macroalgae; Management; Phase shift; Reef fishes; Resilience threshold; Turbidity

Indexed keywords

COMMUNITY STRUCTURE; CONTINENTAL SHELF; CORAL REEF; ECOSYSTEM MANAGEMENT; ECOSYSTEM RESILIENCE; ECOSYSTEM SERVICE; ENVIRONMENTAL DEGRADATION; ENVIRONMENTAL FACTOR; FUNCTIONAL GROUP; GRAZING; HERBIVORE; HERBIVORY; MACROALGA; MORTALITY; SPATIAL VARIATION; SPECIES RICHNESS; TROPICAL REGION; TURBIDITY; VULNERABILITY; WATER QUALITY;

AUSTRALIA; CORAL SEA; GREAT BARRIER REEF; PACIFIC OCEAN; QUEENSLAND;

ANTHOZOA; PISCES;

WATER;

ANIMAL; ARTICLE; CHEMISTRY; CORAL REEF; DEMOGRAPHY; FISH; HERBIVORY; PHYSIOLOGY;

ANIMALS; CORAL REEFS; DEMOGRAPHY; FISHES; HERBIVORY; WATER;

MLCS; MLOWN;

EID: 84875768251     PISSN: 10510761     EISSN: None     Source Type: Journal    
DOI: 10.1890/11-2253.1     Document Type: Article

References (81)

1. Allen, C. R., L. Gunderson, and A. R. Johnson. 2005. The use of discontinuities and functional groups to assess relative resilience in complex systems. Ecosystems 8: 958-966.
2. Anderson, M. J. 2001. A new method for non-parametric multivariate analysis of variance. Australian Journal of Ecology 26: 32-46.
3. Anderson, M. J., and C. J. F. ter Braak. 2002. Permutation tests for multi-factorial analysis of variance. Journal of Statistical Computation and Simulation 73: 85-113.
4. Bellwood, D. R., and J. H. Choat. 1990. A functional analysis of grazing in parrotfishes (family Scaridae): the ecological implications. Environmental Biology of Fishes 28: 189-214.
5. Bellwood, D. R., T. P. Hughes, C. Folke, and M. Nyström. 2004. Confronting the coral reef crisis. Nature 429: 827-833.
6. Bonaldo, R. M., and D. R. Bellwood. 2008. Size dependent variation in the functional role of the parrotfish Scarus rivulatus on the Great Barrier Reef, Australia. Marine Ecology Progress Series 360: 237-244.
7. Bruno, J. F., H. Sweatman, W. F. Precht, E. R. Selig, and V. G. W. Schutte. 2009. Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology 90: 1478-1484.
8. Burkepile, D. E., and M. E. Hay. 2008. Herbivore species richness and feeding complementarity affect community structure and function on a coral reef. Proceedings of the National Academy of Sciences USA 105: 16201-16206.
9. Burkepile, D. E., and M. E. Hay. 2010. Impact of herbivore identity on algal succession and coral growth on a Caribbean reef. PLos ONE 5(1):e8963.
10. Cheal, A. J., M. Emslie, I. Miller, and H. Sweatman. 2012. The distribution of herbivorous fishes on the Great Barrier Reef. Marine Biology 159: 1143-1154.
11. Cheal, A. J., M. A. MacNeil, E. Cripps, M. J. Emslie, M. Jonker, B. Schaffelke, and H. Sweatman. 2010. Coralmacroalgal phase shifts or reef resilience: links with diversity and functional roles of herbivorous fishes on the Great Barrier Reef. Coral Reefs 29: 1005-1015.
12. Cheal, A. J., S. K. Wilson, M. J. Emslie, A. M. Dolman, and H. Sweatman. 2008. Responses of reef fish communities to coral declines on the Great Barrier Reef. Marine Ecology Progress Series 372: 211-223.
13. Darwin, C. 1859. On the origin of species by means of natural selection or the preservation of favoured races in the struggle for life. First edition. John Murray, London, UK
14. De'ath, G., and K. Fabricius. 2010. Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef. Ecological Applications 20: 840-850.
15. Done, T. J. 1982. Patterns in the distribution of coral communities across the central Great Barrier Reef. Coral Reefs 1: 95-107.
16. Done, T. J., E. Turak, M. Wakeford, L. DeVantier, A. McDonald, and D. Fisk. 2007. Decadal changes in turbid water coral communities at Pandora Reef: loss of resilience or too soon to tell? Coral Reefs 26: 789-805.
17. Dorazio, R., J. Royle, B. Söderström, and A. Glimskär. 2006. Estimating species richness and accumulation by modeling species occurrence and detectability. Ecology 87: 842-854.
18. Emslie, M. J., A. J. Cheal, H. S. Sweatman, and S. Delean. 2008. Recovery from disturbance of coral and reef fish communities on the Great Barrier Reef, Australia. Marine Ecology Progress Series 371: 177-190.
19. Fabricius, K. E. 2005. Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Marine Pollution Bulletin 50: 125-146.
20. Fabricius, K., and G. De'ath. 2001. Environmental factors associated with the spatial distribution of crustose coralline algae on the Great Barrier Reef. Coral Reefs 19: 303-309.
21. Fabricius, K., G. De'ath, L. McCook, E. Turak, and D. McB. Williams. 2005. Changes in algal, coral and fish assemblages along water quality gradients on the inshore Great Barrier Reef. Marine Pollution Bulletin 51: 384-398.
22. Fischer, J., D. B. Lindenmayer, S. P. Blomberg, R. Montague- Drake, A. Felton, and J. A. Stein. 2007. Functional richness and relative resilience of bird communities in regions with different land use intensities. Ecosystems 10: 964-974.
23. Folke, C. 2006. Resilience: the emergence of a perspective for social-ecological systems analyses. Global Environmental Change 16: 253-267.
24. Folke, C., S. Carpenter, B. Walker, M. Scheffer, T. Elmqvist, L. Gunderson, and C. S. Holling. 2004. Regime shifts, resilience and biodiversity in ecosystem management. Annual Review of Ecology, Evolution, and Systematics 35: 557-581.
25. Fox, R. J., and D. R. Bellwood. 2007. Quantifying herbivory across a coral reef depth gradient. Marine Ecology Progress Series 339: 49-59.
26. Fox, R. J., and D. R. Bellwood. 2008. Direct versus indirect methods of quantifying herbivore grazing impact on a coral reef. Marine Biology 154: 325-334.
27. Froese, R., and D. Pauly. 2006. FishBase. http://www.fishbase.org
28. Graham, N. A. J., S. K. Wilson, S. Jennings, N. V. C. Polunin, J. Robinson, J. P. Bijoux, and T. M. Daw. 2007. Lag effects in the impacts of mass coral bleaching on coral reef fish, fisheries and ecosystems. Conservation Biology 21:1291-1300.
29. Green, A. L., and D. R. Bellwood. 2009. Monitoring functional groups of herbivorous fishes as indicators of coral reef resilience. A practical guide for coral reef managers in the Asia Pacific region. IUCN Working Group on Climate Change And Coral Reefs. IUCN, Gland, Switzerland.
30. Gust, N., J. H. Choat, and J. L. Ackerman. 2002. Demographic plasticity in tropical reef fishes. Marine Biology 140:1039-1051.
31. Gust, N., J. H. Choat, and M. I. McCormick. 2001. Spatial variability in reef fish distribution, abundance, size and biomass: a multi-scale analysis. Marine Ecology Progress Series 214: 237-251.
32. Halford, A., A. J. Cheal, D. Ryan, and D. McB. Williams. 2004. Resilience to large-scale disturbance in coral and reef assemblages on the Great Barrier Reef. Ecology 85:1892-1905.
33. Halford, A., and A. Thompson. 1996. Visual census surveys of reef fish. Australian Institute of Marine Science, Townsville, Australia.
34. Hatcher, B. G., and A. W. D. Larkum. 1983. An experimental analysis of factors controlling the standing crop of the epilithic algal community on a coral reef. Journal of Experimental Marine Biology and Ecology 69: 61-84.
35. Hoegh-Guldberg, O., et al. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318:1737-1742.
36. Holling, C. S. 1973. Resilience and stability of ecological systems. Annual Review of Ecology and Systematics 4: 1-23.
37. Hooper, D. U., et al. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75: 3-35.
38. Hughes, T. P. 1994. Catastrophes, phase shifts and large-scale degradation of a Caribbean coral reef. Science 265:1547-1551.
39. Hughes, T. P., et al. 2003. Climate change, human impacts and the resilience of coral reefs. Science 301: 929-933.
40. Hughes, T. P., N. A. J. Graham, J. B. C. Jackson, P. J. Mumby, and R. S. Steneck. 2010. Rising to the challenge of sustaining coral reef resilience. Trends in Ecology and Evolution 25: 633-642.
41. Hughes, T. P., M. J. Rodrigues, D. R. Bellwood, D. Ceccarelli, O. Hoegh-Guldberg, L. McCook, N. Moltschaniwskyj, M. S. Pratchett, R. S. Steneck, and B. Willis. 2007. Phase shifts, herbivory and the resilience of coral reefs to climate change. Current Biology 17: 360-365.
42. Hutchings, P., S. Ahyong, M. Byrne, R. Przeslawski, and G. Worheide. 2007. Vulnerability of benthic invertebrates of the Great Barrier Reef to climate change. Pages 309-356 in J. E. Johnson and P. A. Marshall, editors. Climate change on the Great Barrier Reef: a vulnerability assessment. Great Barrier Reef Marine Park Authority and Greenhouse Office, Townsville, Australia.
43. Jackson, J. B., et al. 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293: 629-637.
44. Jonker, M., K. Johns, and K. Osborne. 2008. Surveys of benthic reef communities using underwater digital photography and juvenile coral counts. Australian Institute of Marine Science, Townsville, Australia.
45. Kiessling, W. 2005. Long-term relationships between ecological stability and biodiversity in Phanerozoic reefs. Nature 433: 410-413.
46. Klumpp, D. W., and A. D. McKinnon. 1989. Temporal and spatial patterns in primary production of a coral-reef epilithic algal community. Journal of Experimental Marine Biology and Ecology 131: 1-22.
47. Larcombe, P., and K. J. Wolfe. 1999. Increased sediment supply to the Great Barrier Reef will not increase sediment accumulation at most coral reefs. Coral Reefs 18: 163-169.
48. Lawrence, D., R. Kenchington, and S. Woodley. 2002. The Great Barrier Reef: finding the right balance. Melbourne University Press, Melbourne, Australia.
49. Ledlie, M. H., N. A. J. Graham, J. C. Bythell, S. K. Wilson, S. Jennings, N. V. C. Polunin, and J. Hardcastle. 2007. Phase shifts and the role of herbivory in the resilience of coral reefs. Coral Reefs 26: 641-653.
50. Leis, J. M., and M. I. McCormick. 2002. The biology, behavior and ecology of the pelagic, larval stage of coral reef fishes. Pages 171-200 in P. F. Sale, editor. Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic Press, San Diego, California, USA
51. Lewis, S. M. 1986. The role of herbivorous fishes in the organization of a Caribbean reef community. Ecological Monographs 56: 183-200.
52. MacArthur, R. H. 1955. Fluctuations of animal populations, and a measure of community stability. Ecology 36: 533-536.
53. MacKenzie, D., J. Nichols, J. Royle, K. Pollock, J. Hines, and L. Bailey. 2006. Occupancy estimation and modeling; inferring patterns and dynamics of species occurrence. Elsevier, San Diego, California, USA
54. MacNeil, M. A., N. A. J. Graham, J. E. Cinner, N. K. Dulvy, P. A. Loring, S. Jennings, N. V. C. Polunin, A. T. Fisk, and T. R. McClanahan. 2010. Transitional states in marine fisheries: adapting to predicted global change. Philosophical Transactions of the Royal Society B 365: 3753-3763.
55. MacNeil, M. A., E. Tyler, C. Fonnesbeck, S. P. Rushton, and M. J. Conroy. 2008. Accounting for detectability in reef fish biodiversity estimates. Marine Ecology Progress Series 367: 249-260.
56. Mallela, J., C. Roberts, C. Harrod, and C. R. Goldspink. 2007. Distributional patterns and community structure of Caribbean coral reef fishes within a river impacted bay. Journal of Fish Biology 70: 523-537.
57. Mantyka, C. S., and D. R. Bellwood. 2007. Direct evaluation of macroalgal removal by herbivorous coral reef fishes. Coral Reefs 26: 435-442.
58. McArdle, B. H., and M. J. Anderson. 2001. Fitting multivariate models to community data: a comment on distance based redundancy analysis. Ecology 82: 290-297.
59. McClanahan, T. R., N. A. J. Graham, M. A. MacNeil, N. A. Muthiga, J. E. Cinner, J. H. Bruggemann, and S. K. Wilson. 2011. Critical thresholds and tangible targets for ecosystem based management of coral reef fisheries. Proceedings of the National Academy of Sciences USA 108: 17230-17233.
60. McCook, L. J., and I. R. Price. 1997. Macroalgal distributions on the Great Barrier Reef: a review of patterns and causes. Pages 37-46 in The Great Barrier Reef: science, use and management: a national conference, Proceedings. Volume 2. Great Barrier Reef Marine Park Authority, Townsville, Australia.
61. McCulloch, M., S. Fallon, T. Wyndham, E. Hendy, J. Lough, and D. Barnes. 2003. Coral record of increased sediment flux to the inner Great Barrier Reef since European settlement. Nature 421: 727-730.
62. Mumby, P. J. 2006. The impact of exploiting grazers (Scaridae) on the dynamics of Caribbean coral reefs. Ecological Applications 16: 747-769.
63. Mumby, P. J., A. Hastings, and H. J. Edwards. 2007. Thresholds and the resilience of Caribbean coral reefs. Nature 450: 98-101.
64. Nemeth, M., and R. Appeldoorn. 2009. The distribution of herbivorous coral reef fishes within fore-reef habitats: the role of depth, light and rugosity. Caribbean Journal of Science 45: 247-253.
65. Nyström, M., N. A. J. Graham, J. Lokrantz, and A. V. Norström. 2008. Capturing the cornerstones of coral resilience: linking theory to practice. Coral Reefs 27: 795-809.
66. 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(3):e17516.
67. Pandolfi, J. M., R. H. Bradbury, E. Sala, T. P. Hughes, K. A. Bjorndal, R. G. Cooke, D. McArdle, L. McClenachan, M. J. H. Newman, G. Paredes, R. R. Warner, and J. B. C. Jackson. 2003. Global trajectories of the long-term decline of coral reef ecosystems. Science 301: 955-958.
68. Peterson, G., C. R. Allen, and C. S. Holling. 1998. Ecological resilience, biodiversity, and scale. Ecosystems 1: 6-18.
69. Russ, G. 1984. Distribution and abundance of herbivorous grazing fishes in the central Great Barrier Reef I. Levels of variability across the entire continental shelf. Marine Ecology Progress Series 20: 23-24.
70. Russ, G. R. 2003. Grazer biomass correlates more strongly with production than biomass of algal turfs on coral reefs. Coral Reefs 22: 63-67.
71. Russ, G. R., and L. J. McCook. 1999. Potential effects of a cyclone on benthic algal production and yield to grazers on coral reefs across the central Great Barrier Reef. Journal of Experimental Marine Biology and Ecology 235: 237-254.
72. Sweatman, H., A. J. Cheal, G. J. Coleman, M. J. Emslie, K. Johns, M. Jonker, I. R. Miller, and K. Osborne. 2008. Long term monitoring of the Great Barrier Reef. Status Report No. 8. Australian Institute of Marine Science, Townsville, Australia.
73. Tilman, D., D. Wedin, and J. Knopps. 1996. Productivity and sustainability influenced by biodiversity in grasslands ecosystems. Nature 379: 718-720.
74. Vermeij, M. J. A., M. L. Dailer, and C. M. Smith. 2011. Crustose coralline algae can suppress growth and recruitment of macroalgae on Hawaiian coral reefs. Marine Ecology Progress Series 422: 1-7.
75. Walker, B. 1992. Biodiversity and ecological redundancy. Conservation Biology 6: 18-23.
76. Walker, B., C. S. Holling, S. R. Carpenter, and A. Kinzig. 2004. Resilience, adaptability and transformability in social-ecological systems. Ecology and Society 9(2):5. http://www.ecologyandsociety.org/vol9/iss2/art5
77. Wenger, A. S., J. L. Johansen, and G. P. Jones. 2011. Suspended sediment impairs habitat choice and chemosensory discrimination in two coral reef fishes. Coral Reefs 30: 879-887.
78. Williams, D. McB. 1982. Patterns in the distribution of fish communities across the central Great Barrier Reef. Coral Reefs 1: 35-43.
79. Williams, D. McB., 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.
80. Williams, I. D., N. V. C. Polunin, and V. J. Hendrick. 2001. Limits to grazing by herbivorous fishes and the impact of low coral cover on macroalgal abundance on a coral reef in Belize. Marine Ecology Progress Series 222: 187-196.
81. Worm, B., et al. 2006. Impacts of biodiversity loss on ocean ecosystem services. Science 314: 787-790.