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Branching coral as a macroalgal refuge in a marginal coral reef system

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Abstract

Marginal coral reef systems may provide valuable insights into the nature of ecosystem processes in systems on the trajectory towards a phase shift to an alternate ecosystem state. This study investigates the process of herbivory in a marginal coral reef system in the Keppel Islands at the southern end of the Great Barrier Reef. Branching Acropora coral and the brown macroalga Lobophora variegata occupied up to 95% of the reef crest substratum at the three surveyed reefs. Feeding rates of herbivorous fishes and removal rates of Lobophora were directly quantified within areas of branching Acropora and on planar surfaces. Feeding rates by herbivorous fishes were habitat dependent with the highest bite rates being found in planar habitats for both Lobophora and the epilithic algal matrix (EAM) by 1–2 orders of magnitude, respectively. Feeding rates on Lobophora were, however, much lower than rates on the EAM. The low rates of Lobophora removal and significantly lower rates of herbivory in branching habitats were consistent with the high biomass of this brown alga throughout the Keppel Islands and with its distribution on reef crests, where Lobophora biomass was 20 times greater in branching than in planar habitats. This lack of feeding by herbivorous fishes within branching coral habitats in the Keppel Islands contrasts with the typical role of coral and topographic complexity on herbivores on coral reefs and highlights the potential for complex interactions between algae, corals and fishes on coral reefs. On marginal systems, herbivory may modify algal distributions but may be unable to contain the proliferation of algae such as Lobophora.

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References

  • Bellwood DR, Choat JH (1990) A functional analysis of grazing in parrotfishes (family Scaridae)—the ecological implications. Environ Biol Fish 28:189–214

    Article  Google Scholar 

  • Bellwood D, Wainwright P (2001) Locomotion in labrid fishes: implications for habitat use and cross-shelf biogeography on the Great Barrier Reef. Coral Reefs 20:139–150

    Article  Google Scholar 

  • Bellwood DR, Hughes TP, Folke C, Nystrom M (2004) Confronting the coral reef crisis. Nature 429:827–833

    Article  CAS  PubMed  Google Scholar 

  • Bellwood DR, Hughes TP, Hoey AS (2006) Sleeping functional group drives coral-reef recovery. Curr Biol 16:2434–2439

    Article  CAS  PubMed  Google Scholar 

  • Choat JH (1991) The biology of herbivorous fishes on coral reefs. In: Sale PF (ed) The ecology of fishes on coral reefs. Academic Press, San Diego, pp 120–155

    Google Scholar 

  • Choat JH, Clements KD, Robbins WD (2002) The trophic status of herbivorous fishes on coral reefs 1: dietary analyses. Mar Biol 140:613–623

    Article  CAS  Google Scholar 

  • Coen L, Tanner C (1989) Morphological variation and differential susceptibility to herbivory in the tropical brown alga Lobophora variegata. Mar Ecol Prog Ser 54:287–298

    Article  Google Scholar 

  • Cvitanovic C, Bellwood D (2009) Local variation in herbivore feeding activity on an inshore reef of the Great Barrier Reef. Coral Reefs 28:127–133

    Article  Google Scholar 

  • DeVantier LM, De’ath G, Turak E, Done TJ, Fabricius KE (2006) Species richness and community structure of reef-building corals on the nearshore Great Barrier Reef. Coral Reefs 25:329–340

    Article  Google Scholar 

  • Devlin MJ, Brodie J (2005) Terrestrial discharge into the Great Barrier Reef Lagoon: nutrient behavior in coastal waters. Mar Pollut Bull 51:9–22

    Article  CAS  PubMed  Google Scholar 

  • Diaz-Pulido G, McCook L, Dove S, Berkelmans R, Roff G, Kline D, Weeks S, Evans R, Williamson D, Hoegh-Guldberg O (2009) Doom and boom on a resilient reef: climate change, algal overgrowth and coral recovery. PLoS One 4:e5239

    Article  PubMed  Google Scholar 

  • Done TJ (1992) Phase shifts in coral reef communities and their ecological significance. Hydrobiologia 247:121–132

    Article  Google Scholar 

  • Elvidge C, Dietz J, Berkelmans R, Andréfouët S, Skirving W, Strong A, Tuttle B (2004) Satellite observation of Keppel Islands (Great Barrier Reef) 2002 coral bleaching using IKONOS data. Coral Reefs 23:123–132

    Google Scholar 

  • Floeter SR, Behrens MD, Ferreira CEL, Paddack MJ, Horn MH (2005) Geographical gradients of marine herbivorous fishes: patterns and processes. Mar Biol 147:1435–1447

    Article  Google Scholar 

  • Fox RJ, Bellwood DR (2007) Quantifying herbivory across a coral reef depth gradient. Mar Ecol Prog Ser 339:49–59

    Article  Google Scholar 

  • Graham NAJ, Wilson SK, Jennings S, Polunin NVC, Bijoux JP, Robinson J (2006) Dynamic fragility of oceanic coral reef ecosystems. Proc Natl Acad Sci USA 103:8425–8429

    Article  CAS  PubMed  Google Scholar 

  • Harmelin-Vivien M (2002) Energetics and fish diversity on coral reefs. In: Sale PF (ed) Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic Press, New York, pp 265–274

    Google Scholar 

  • Hay ME (1981a) Herbivory algal distribution and the maintenance of between habitat diversity on a tropical fringing reef. Am Nat 118:520–540

    Article  Google Scholar 

  • Hay ME (1981b) Spatial patterns of grazing intensity on a Caribbean barrier reef herbivory and algal distribution. Aquat Bot 11:97–110

    Article  Google Scholar 

  • Hay M (1984) Predictable spatial escapes from herbivory: how do these affect the evolution of herbivore resistance in tropical marine communities? Oecologia 64:396–407

    Article  Google Scholar 

  • Hay ME, Fenical W (1988) Marine plant-herbivore interactions: the ecology of chemical defense. Annu Rev Ecol Syst 19:111–145

    Article  Google Scholar 

  • Hay M, Colburn T, Downing D (1983) Spatial and temporal patterns in herbivory on a Caribbean fringing reef: the effects on plant distribution. Oecologia 58:299–308

    Article  Google Scholar 

  • Helmuth BST, Sebens KP, Daniel TL (1997) Morphological variation in coral aggregations: branch spacing and mass flux to coral tissues. J Exp Mar Biol Ecol 209:233–259

    Article  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants—to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866

    Article  Google Scholar 

  • Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551

    Article  PubMed  Google Scholar 

  • Hughes T, Baird A, Dinsdale E, Moltschaniwskyj N, Pratchett M, Tanner J, Willis B (1999) Patterns of recruitment and abundance of corals along the Great Barrier Reef. Nature 397:59–63

    Article  CAS  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  CAS  PubMed  Google Scholar 

  • Janzen DH (1974) Tropical blackwater rivers, animals, and mast fruiting by the Dipterocarpaceae. Biotropica 6:69–103

    Article  Google Scholar 

  • Janzen DH (1976) Why bamboos wait so long to flower. Annu Rev Ecol Syst 7:347–391

    Article  Google Scholar 

  • Jompa J, McCook LJ (2002) Effects of competition and herbivory on interactions between a hard coral and a brown alga. J Exp Mar Biol Ecol 271:25–39

    Article  Google Scholar 

  • Jones A, Berkelmans R, Van Oppen M, Mieog J, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc R Soc B Biol Sci 275:1359–1365

    Article  CAS  Google Scholar 

  • Ledlie MH, Graham NAJ, Bythell JC, Wilson SK, Jennings S, Polunin NVC, Hardcastle J (2007) Phase shifts and the role of herbivory in the resilience of coral reefs. Coral Reefs 26:641–653

    Article  Google Scholar 

  • Lewis SM, Wainwright PC (1985) Herbivore abundance and grazing intensity on a Caribbean coral reef. J Exp Mar Biol Ecol 87:215–228

    Article  Google Scholar 

  • Lubchenco J, Gaines SD (1981) A unified approach to marine plant-herbivore interactions. I. Populations and communities. Annu Rev Ecol Syst 12:405–437

    Article  Google Scholar 

  • McClanahan TR, Aronson RB, Precht WF, Muthiga NA (1999) Fleshy algae dominate remote coral reefs of Belize. Coral Reefs 18:61–62

    Article  Google Scholar 

  • McCook LJ (1997) Effects of herbivory on zonation of Sargassum spp. within fringing reefs of the central Great Barrier Reef. Mar Biol 129:713–722

    Article  Google Scholar 

  • 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 421:727–730

    Article  CAS  PubMed  Google Scholar 

  • Mumby PJ (2006) The impact of exploiting grazers (Scaridae) on the dynamics of Caribbean coral reefs. Ecol Appl 16:747–769

    Article  PubMed  Google Scholar 

  • Mumby PJ, Hedley JD, Zychaluk K, Harbourne AR, Blackwell PG (2006) Revisiting the catastrophic die-off of the urchin Diadema antillarum on Caribbean coral reefs: fresh insights on resilience from a simulation model. Ecol Model 196:131–148

    Article  Google Scholar 

  • Norström A, Nyström M, Lokrantz J, Folke C (2008) Alternative states on coral reefs: beyond coral-macroalgal phase shifts. Mar Ecol Prog Ser 376:295–306

    Article  Google Scholar 

  • Nystrom M, Graham NAJ, Lokrantz J, Norstrom AV (2008) Capturing the cornerstones of coral reef resilience: linking theory to practice. Coral Reefs 27:795–809

    Article  Google Scholar 

  • Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJH, Paredes G, Warner RR, Jackson JBC (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–958

    Article  CAS  PubMed  Google Scholar 

  • Paul V, Hay M (1986) Seaweed susceptibility to herbivory: chemical and morphological correlates. Mar Ecol Prog Ser 33:255–264

    Article  CAS  Google Scholar 

  • Pillans RD, Franklin CE, Tibbetts IR (2004) Food choice in Siganus fuscescens: influence of macrophyte nutrient content and availability. J Fish Biol 64:297–309

    Article  Google Scholar 

  • Randall JE (1961) Overgrazing of algae by herbivorous marine fishes. Ecology 42:812

    Article  Google Scholar 

  • Steinberg P, Paul V (1990) Fish feeding and chemical defenses of tropical brown algae in Western Australia. Mar Ecol Prog Ser 58:253–259

    Article  Google Scholar 

  • Van Woesik R, DeVantier LM, Glazebrook JS (1995) Effects of cyclone ‘Joy’ on nearshore coral communities of the Great Barrier Reef. Mar Ecol Prog Ser 128:261–270

    Article  Google Scholar 

  • Vansteveninck EDD, Breeman AM (1987a) Deep water vegetations of Lobophora variegata (Phaeophyceae) in the coral reef of Curacao—population dynamics in relation to mass mortality of the sea urchin Diadema antillarum. Mar Ecol Prog Ser 36:81–90

    Article  Google Scholar 

  • Vansteveninck EDD, Breeman AM (1987b) Deep-water populations of Lobophora variegata (Phaeophycae) on the coral-reef of Curacao—influence of grazing and dispersal on distribution patterns. Mar Ecol Prog Ser 38:241–250

    Article  Google Scholar 

  • Walker B (1992) Biodiversity and ecological redundancy. Conserv Biol 6:18–23

    Article  Google Scholar 

  • Weidner K, Lages B, da Gama B, Molis M, Wahl M, Pereira R (2004) Effect of mesograzers and nutrient levels on induction of defenses in several Brazilian macroalgae. Mar Ecol Prog Ser 283:113–125

    Article  Google Scholar 

  • Wilson S, Bellwood DR (1997) Cryptic dietary components of territorial damselfishes (Pomacentridae, Labroidei). Mar Ecol Prog Ser 153:299–310

    Article  CAS  Google Scholar 

  • Wismer S, Hoey A, Bellwood D (2009) Cross-shelf benthic community structure on the Great Barrier Reef: relationships between macroalgal cover and herbivore biomass. Mar Ecol Prog Ser 376:45–54

    Article  Google Scholar 

  • Wooldridge S, Brodie J, Furnas M (2006) Exposure of inner-shelf reefs to nutrient enriched runoff entering the Great Barrier Reef Lagoon: post-European changes and the design of water quality targets. Mar Pollut Bull 52:1467–1479

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank R. Fox, A. Hoey, C. Lefévre, V. Moccellin, J. Tanner, P. Williams and S. Wismer for invaluable field assistance and/or helpful advice. The constructive comments of L. McCook and G. Diaz-Pulido are gratefully appreciated. This study was funded by the Australian Government’s Marine and Tropical Sciences Research Facility and the Australian Research Council.

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Correspondence to D. R. Bellwood.

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Communicated by Environment Editor Prof. Rob van Woesik

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Bennett, S., Vergés, A. & Bellwood, D.R. Branching coral as a macroalgal refuge in a marginal coral reef system. Coral Reefs 29, 471–480 (2010). https://doi.org/10.1007/s00338-010-0594-5

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