Coral Reefs

, Volume 37, Issue 3, pp 929–937 | Cite as

Sediment addition drives declines in algal turf yield to herbivorous coral reef fishes: implications for reefs and reef fisheries

  • Sterling B. Tebbett
  • David R. BellwoodEmail author
  • Steven W. Purcell


Coral reefs around the world are changing rapidly, with overfishing of herbivorous fishes and increased sediment inputs being two of the major local-scale stressors. We therefore assessed the effects of sediment loads and overfishing on the nutritional quality and yield to grazing fishes of algal turfs, within the epilithic algal matrix, on a coral reef at Lizard Island, Australia. Low, ambient and high sediment loads were maintained on turf-covered coral tiles, with and without grazer exclusion cages, for 1 month. Subsequently, algal turfs were removed and analysed for organic carbon and nitrogen content. Under grazer exclusion, sediment additions decreased algal turf biomass by approximately 63%, while algal turf biomass was the highest on tiles with sediments removed. In the presence of grazing fishes, algal turfs in all treatments were cropped by grazers to similar low biomass levels. Nitrogen content of algal turfs followed a similar trend. Effectively, added sediments decreased the potential yield of algal turf biomass and nitrogen to grazing fishes by an average of 2000 and 3300%, respectively. Sediments profoundly affect algal turf yield to grazing herbivorous fishes and, therefore, the productivity of algal turf-based food chains, potentially diminishing reef-based fisheries.


Epilithic algal matrix Fish Great Barrier Reef Productivity Sediments Trophodynamics 



We thank M. Emslie, J. Colquhoun, D. Hocking, Z. Rosser, K. Bonair, D. Zeller, A. Miles, J. Semmens, M. Fogg, K. Buckley, G. Smith and Lizard Island Research Station staff for field and laboratory support; three anonymous reviewers for helpful comments. Financial support was provided by a James Cook University Merit Research Grant (SWP), an Australian Museum Postgraduate Grant (SWP) and the Australian Research Council (DRB, Grant Number: CE140100020).

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Supplementary material

338_2018_1718_MOESM1_ESM.doc (602 kb)
Supplementary material 1 (DOC 602 kb)


  1. Adam TC, Duran A, Fuchs CE, Roycroft MV, Rojas MC, Ruttenberg BI, Burkepile DE (2018) Comparative analysis of foraging behavior and bite mechanics reveals complex functional diversity among Caribbean parrotfishes. Mar Ecol Prog Ser 597:207–220CrossRefGoogle Scholar
  2. Anderson JM, Ingram JS (1989) Tropical soil biology and fertility: a handbook of methods. CAB International, AberystwythGoogle Scholar
  3. Baethgen WE, Alley MM (1989) A manual colorimetric procedure for measuring ammonium nitrogen in soil and plant Kjedahl digests. Commun Soil Sci Plant Anal 20:961–969CrossRefGoogle Scholar
  4. Ban SS, Graham NAJ, Connolly SR (2014) Evidence for multiple stressor interactions and effects on coral reefs. Glob Chang Biol 20:681–697CrossRefPubMedGoogle Scholar
  5. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7Google Scholar
  6. Bellwood DR, Fulton CJ (2008) Sediment-mediated suppression of herbivory on coral reefs: decreasing resilience to rising sea levels and climate change? Limnol Oceanogr 53:2695–2701CrossRefGoogle Scholar
  7. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833CrossRefPubMedGoogle Scholar
  8. Bellwood DR, Tebbett SB, Bellwood O, Mihalitsis M, Morais RA, Streit RP, Fulton CJ (2018) The role of the reef flat in coral reef trophodynamics: past, present, and future. Ecol Evol 8:4108–4119CrossRefPubMedPubMedCentralGoogle Scholar
  9. Birrell CL, McCook LJ, Willis BL (2005) Effects of algal turfs and sediment on coral settlement. Mar Pollut Bull 51:408–414CrossRefPubMedGoogle Scholar
  10. Bonaldo RM, Bellwood DR (2011) Spatial variation in the effects of grazing on epilithic algal turfs on the Great Barrier Reef, Australia. Coral Reefs 30:381–390CrossRefGoogle Scholar
  11. Brodie JE, Pearson RG (2016) Ecosystem health of the Great Barrier Reef: time for effective management action based on evidence. Estuar Coast Shelf Sci 183:438–451CrossRefGoogle Scholar
  12. Brown KT, Bender-Champ D, Bryant DEP, Dove S, Hoegh-Guldberg O (2017) Human activities influence benthic community structure and the composition of the coral-algal interactions in the central Maldives. J Exp Mar Bio Ecol 497:33–40CrossRefGoogle Scholar
  13. Bruno JF, Sweatman H, Precht WF, Selig ER, Schutte VGW (2009) Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology 90:1478–1484CrossRefPubMedGoogle Scholar
  14. Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128–3139CrossRefPubMedGoogle Scholar
  15. Burkepile DE, Hay ME (2009) Nutrient versus herbivore control of macroalgal community development and coral growth on a Caribbean reef. Mar Ecol Prog Ser 389:71–84CrossRefGoogle Scholar
  16. Carpenter RC (1985) Relationships between primary production and irradiance in coral reef algal communities. Limnol Oceanogr 30:784–793CrossRefGoogle Scholar
  17. Cheal AJ, MacNeil MA, Cripps E, Emslie MJ, Jonker M, Schaffelke B, Sweatman H (2010) Coral-macroalgal phase shifts or reef resilience: links with diversity and functional roles of herbivorous fishes on the Great Barrier Reef. Coral Reefs 29:1005–1015CrossRefGoogle Scholar
  18. Clausing RJ, Annunziata C, Baker G, Lee C, Bittick SJ, Fong P (2014) Effects of sediment depth on algal turf height are mediated by interactions with fish herbivory on a fringing reef. Mar Ecol Prog Ser 517:121–129CrossRefGoogle Scholar
  19. Clements KD, German DP, Piché J, Tribollet AD, Choat JH (2017) Integrating ecological roles and trophic resources on coral reefs: multiple lines of evidence identify parrotfishes as microphages. Biol J Linn Soc 120:729–751Google Scholar
  20. Comeros-Raynal MT, Choat JH, Polidoro BA, Clements KD, Abesamis R, Craig MT, Lazuardi ME, McIlwain J, Muljadi A, Myers RF, Nañola CL Jr, Pardede S, Rocha LA, Russell B, Sanciangco JC, Stockwell B, Harwell H, Carpenter KE (2012) The likelihood of extinction of iconic and dominant herbivores and detritivores of coral reefs: the parrotfishes and surgeonfishes. PLoS One 7:e39825CrossRefPubMedPubMedCentralGoogle Scholar
  21. Condy M, Cinner JE, McClanahan TR, Bellwood DR (2015) Projections of the impacts of gear-modification on the recovery of fish catches and ecosystem function in an impoverished fishery. Aquat Conserv Mar Freshw Ecosyst 410:396–410CrossRefGoogle Scholar
  22. Craig PC, Choat JH, Axe LM, Saucerman S (1997) Population biology and harvest of a coral reef surgeonfish (Acanthurus lineatus) in American Samoa. Fish Bull 95:680–693Google Scholar
  23. Crossman DJ, Choat JH, Clements KD, Hardy T, McConochie J (2001) Detritus as food for grazing fishes on coral reefs. Limnol Oceanogr 46:1596–1605CrossRefGoogle Scholar
  24. Flores F, Hoogenboom MO, Smith LD, Cooper TF, Abrego D, Negri AP (2012) Chronic exposure of corals to fine sediments: lethal and sub-lethal impacts. PLoS One 7:e37795CrossRefPubMedPubMedCentralGoogle Scholar
  25. Fong CR, Bittick SJ, Fong P (2018) Simultaneous synergist, antagonist and additive interactions between multiple local stressors all degrade algal turf communities on coral reefs. J Ecol 106:1390–1400CrossRefGoogle Scholar
  26. Fong P, Paul VJ (2011) Coral reef algae. In: Dubinsky Z, Stambler N (eds) Coral Reefs: an ecosystem in transition. Springer, Dordrecht, pp 241–272CrossRefGoogle Scholar
  27. Goatley CHR, Bellwood DR (2011) The roles of dimensionality, canopies and complexity in ecosystem monitoring. PLoS One 6:e27307CrossRefPubMedPubMedCentralGoogle Scholar
  28. Goatley CHR, Bellwood DR (2013) Ecological consequences of sediment on high-energy coral reefs. PLoS One 8:e77737CrossRefPubMedPubMedCentralGoogle Scholar
  29. Goatley CHR, Bonaldo RM, Fox RJ, Bellwood DR (2016) Sediments and herbivory as sensitive indicators of coral reef degradation. Ecol Soc 21:29CrossRefGoogle Scholar
  30. Gordon SE, Goatley CHR, Bellwood DR (2016) Composition and temporal stability of benthic sediments on inner-shelf coral reefs. Mar Pollut Bull 111:178–183CrossRefPubMedGoogle Scholar
  31. Gowan JC, Tootell JS, Carpenter RC (2014) The effects of water flow and sedimentation on interactions between massive Porites and algal turf. Coral Reefs 33:651–663CrossRefGoogle Scholar
  32. Graham NAJ, Bellwood DR, Cinner JE, Hughes TP, Norstrom AV, Nyström M (2013) Managing resilience to reverse phase shifts in coral reefs. Front Ecol Environ 11:541–548CrossRefGoogle Scholar
  33. Hamilton RJ, Almany GR, Brown C, Pita J, Peterson NA, Choat JH (2017) Logging degrades nursery habitat for an iconic coral reef fish. Biol Conserv 210:273–280CrossRefGoogle Scholar
  34. Harris JL, Lewis LS, Smith JE (2015) Quantifying scales of spatial variability in algal turf assemblages on coral reefs. Mar Ecol Prog Ser 532:41–57CrossRefGoogle Scholar
  35. Hatcher BG (1988) Coral reef primary productivity: a beggar’s banquet. Trends Ecol Evol 3:106–111CrossRefPubMedGoogle Scholar
  36. Hughes TP (1994) Catastrophes, phase shifts and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551CrossRefPubMedGoogle Scholar
  37. Hughes TP, Barnes ML, Bellwood DR, Cinner JE, Cumming GS, Jackson JBC, Kleypas J, van de Leemput IA, Lough JM, Morrison TH, Palumbi SR, Van Nes EH, Scheffer M (2017a) Coral reefs in the Anthropocene. Nature 546:82–90CrossRefPubMedGoogle Scholar
  38. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TCL, Butler I, Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Eakin M, Figueira W, Gilmour J, Harrison HB, Heron SF, Hoey AS, Hobbs J-PA, Hoogenboom MO, Kennedy EV, Kuo C-Y, Lough JM, Lowe RJ, Liu G, McCulloch MT, Malcolm H, McWilliam M, Pandolfi JM, Pears R, Pratchett MS, Schoepf V, Simpson T, Skirving W, Sommer B, Torda G, Wachenfeld D, Willis BL, Wilson SK (2017b) Global warming and recurrent mass bleaching of corals. Nature 543:373–377CrossRefPubMedPubMedCentralGoogle Scholar
  39. Jackson JBC, Donovan MK, Cramer KL, Lam V (2014) Status and trends of Caribbean coral reefs: 1970–2012. Global Coral Reef Monitoring Network, WashingtonGoogle Scholar
  40. Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638CrossRefPubMedGoogle Scholar
  41. Jouffray J-B, Nyström M, Norstrom AV, Williams ID, Wedding LM, Kittinger JN, Williams GJ (2014) Identifying multiple coral reef regimes and their drivers across the Hawaiian archipelago. Philos Trans R Soc B 370:20130268CrossRefGoogle Scholar
  42. Kelly ELA, Eynaud Y, Williams ID, Sparks RT, Dailer ML, Sandin SA, Smith JE (2017) A budget of algal production and consumption by herbivorous fish in an herbivore fisheries management area, Maui. Hawaii. Ecosphere 8:e01899CrossRefGoogle Scholar
  43. Khan JA, Goatley CHR, Brandl SJ, Tebbett SB, Bellwood DR (2017) Shelter use by large reef fishes: long-term occupancy and the impacts of disturbance. Coral Reefs 36:1123–1132CrossRefGoogle Scholar
  44. Klumpp DW, McKinnon AD (1992) Community structure, biomass and productivity of epilithic algal communities on the Great Barrier Reef: dynamics at different spatial scales. Mar Ecol Prog Ser 86:77–89CrossRefGoogle Scholar
  45. Kramer MJ, Bellwood O, Bellwood DR (2013) The trophic importance of algal turfs for coral reef fishes: the crustacean link. Coral Reefs 32:575–583CrossRefGoogle Scholar
  46. Maina J, de Moel H, Zinke J, Madin J, McClanahan T, Vermaat JE (2013) Human deforestation outweighs future climate change impacts of sedimentation on coral reefs. Nat Commun 4:1986CrossRefPubMedPubMedCentralGoogle Scholar
  47. Mazerolle MJ (2015) AICcmodavg: Model selection and multimodel inference based on (Q)AIC(c). R package version 2.0-3Google Scholar
  48. McCook LJ, Ayling T, Cappo M, Choat JH, Evans RD, De Freitas DM, Heupel M, Hughes TP, Jones GP, Mapstone B, Marsh H, Mills M, Molloy FJ, Pitcher CR, Pressey RL, Russ GR, Sutton S, Sweatman H, Tobin R, Wachenfeld DR, Williamson DH (2010) Adaptive management of the Great Barrier Reef: a globally significant demonstration of the benefits of networks of marine reserves. Proc Natl Acad Sci 107:18278–18285CrossRefPubMedGoogle Scholar
  49. McCulloch M, Fallon S, Wyndham T, Hendy E, Lough J, Barnes D (2003) Coral record of increased sediment flux to the inner Great Barrier Reef since European settlement. Nature 421:727–730CrossRefPubMedGoogle Scholar
  50. Muthukrishnan R, Fong P (2014) Multiple anthropogenic stressors exert complex, interactive effects on a coral reef community. Coral Reefs 33:911–921CrossRefGoogle Scholar
  51. Nash KL, Graham NAJ, Bellwood DR (2013) Fish foraging patterns, vulnerability to fishing, and implications for the management of ecosystem function across scales. Ecol Appl 23:1632–1644CrossRefPubMedGoogle Scholar
  52. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2014) nlme:linear and nonlinear mixed effects models. R package version 3.1-118Google Scholar
  53. Pollock FJ, Lamb JB, Field SN, Heron SF, Schaffelke B, Shedrawi G, Bourne DG, Willis BL (2014) Sediment and turbidity associated with offshore dredging increase coral disease pevalence on nearby reefs. PLoS One 9:e102498CrossRefPubMedPubMedCentralGoogle Scholar
  54. Purcell SW (1996) A direct method for assessing sediment load in epilithic algal communities. Coral Reefs 15:211–213CrossRefGoogle Scholar
  55. Purcell SW (1997) The role of sediments in epilithic algal communities on coral reefs. Ph.D. thesis. James Cook University, TownsvilleGoogle Scholar
  56. Purcell SW (2000) Association of epilithic algae with sediment distribution on a windward reef in the northern Great Barrier Reef, Australia. Bull Mar Sci 66:199–214Google Scholar
  57. Purcell SW, Bellwood DR (2001) Spatial patterns of epilithic algal and detrital resources on a windward coral reef. Coral Reefs 20:117–125CrossRefGoogle Scholar
  58. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  59. Rasher DB, Engel S, Bonito V, Fraser GJ, Montoya JP, Hay ME (2012) Effects of herbivory, nutrients, and reef protection on algal proliferation and coral growth on a tropical reef. Oecologia 169:187–198CrossRefPubMedGoogle Scholar
  60. Ricardo GF, Jones RJ, Nordborg M, Negri AP (2017) Settlement patterns of the coral Acropora millepora on sediment-laden surfaces. Sci Total Environ 609:277–288CrossRefPubMedGoogle Scholar
  61. Russ GR (1987) Is rate of removal of algae by grazers reduced inside territories of tropical damselfishes? J Exp Mar Bio Ecol 110:1–17CrossRefGoogle Scholar
  62. Russ GR (2003) Grazer biomass correlates more strongly with production than with biomass of algal turfs on a coral reef. Coral Reefs 22:63–67Google Scholar
  63. Russ GR, McCook LJ (1999) Potential effects of a cyclone on benthic algal production and yield to grazers on coral reefs across the central Great Barrier Reef. J Exp Mar Bio Ecol 235:237–254CrossRefGoogle Scholar
  64. Scott FJ, Russ GR (1987) Effects of grazing on species composition of the epilithic algal community on coral reefs of the central Great Barrier Reef. Mar Ecol Prog Ser 39:293–304CrossRefGoogle Scholar
  65. Seemann J, González CT, Carballo-Bolaños R, Berry K, Heiss GA, Struck U, Leinfelder RR (2014) Assessing the ecological effects of human impacts on coral reefs in Bocas del Toro, Panama. Environ Monit Assess 186:1747–1763CrossRefPubMedGoogle Scholar
  66. Smith JE, Brainard R, Carter A, Grillo S, Edwards C, Harris J, Lewis L, Obura D, Rohwer F, Sala E, Vroom PS, Sandin S (2016) Re-evaluating the health of coral reef communities: baselines and evidence for human impacts across the central Pacific. Proc R Soc B 283:20151985CrossRefPubMedGoogle Scholar
  67. Smith JE, Hunter CL, Smith CM (2010) The effects of top-down versus bottom-up control on benthic coral reef community structure. Oecologia 163:497–507CrossRefPubMedGoogle Scholar
  68. Steneck RS (1997) Crustose corallines, other algal functional groups, herbivores and sediments: complex interactions along reef productivity gradients. In: Proceedings of the 8th international coral reef symposium 1:695–700Google Scholar
  69. Storlazzi CD, Norris BK, Rosenberger KJ (2015) The influence of grain size, grain color, and suspended-sediment concentration on light attenuation: why fine-grained terrestrial sediment is bad for coral reef ecosystems. Coral Reefs 34:967–975CrossRefGoogle Scholar
  70. Tebbett SB, Goatley CHR, Bellwood DR (2017a) Clarifying functional roles: algal removal by the surgeonfishes Ctenochaetus striatus and Acanthurus nigrofuscus on coral reefs. Coral Reefs 36:803–813CrossRefGoogle Scholar
  71. Tebbett SB, Goatley CHR, Bellwood DR (2017b) The effects of algal turf sediments and organic loads on feeding by coral reef surgeonfishes. PLoS One 12:e0169479CrossRefPubMedPubMedCentralGoogle Scholar
  72. Tebbett SB, Goatley CHR, Bellwood DR (2017c) Fine sediments suppress detritivory on coral reefs. Mar Pollut Bull 114:934–940CrossRefPubMedGoogle Scholar
  73. Tebbett SB, Goatley CHR, Bellwood DR (2017d) Algal turf sediments and sediment production by parrotfishes across the continental shelf of the northern Great Barrier Reef. PLoS One 12:e0170854CrossRefPubMedPubMedCentralGoogle Scholar
  74. Wilkinson C (2008) Status of coral reefs of the World: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, TownsvilleGoogle Scholar
  75. Williams S, Carpenter R (1990) Photosynthesis/photon flux density relationships among components of coral reef algal turfs. J Phycol 26:36–40CrossRefGoogle Scholar
  76. Wilson SK, Bellwood DR, Choat JH, Furnas MJ (2003) Detritus in the epilithic algal matrix and its use by coral reef fishes. Oceanogr Mar Biol Annu Rev 41:279–309Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.College of Science and Engineering and ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  2. 2.National Marine Science CentreSouthern Cross UniversityCoffs HarbourAustralia

Personalised recommendations