Skip to main content

Advertisement

Log in

Macroalgal herbivory on recovering versus degrading coral reefs

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Macroalgal-feeding fishes are considered to be a key functional group on coral reefs due to their role in preventing phase shifts from coral to macroalgal dominance, and potentially reversing the shift should it occur. However, assessments of macroalgal herbivory using bioassay experiments are primarily from systems with relatively high coral cover. This raises the question of whether continued functionality can be ensured in degraded systems. It is clearly important to determine whether the species that remove macroalgae on coral-dominated reefs will still be present and performing significant algal removal on macroalgal-dominated reefs. We compared the identity and effectiveness of macroalgal-feeding fishes on reefs in two conditions post-disturbance—those regenerating with high live coral cover (20–46 %) and those degrading with high macroalgal cover (57–82 %). Using filmed Sargassum bioassays, we found significantly different Sargassum biomass loss between the two conditions; mean assay weight loss due to herbivory was 27.9 ± 4.9 % on coral-dominated reefs and 2.2 ± 1.1 % on reefs with high macroalgal cover. However, once standardised for the availability of macroalgae on the reefs, the rates of removal were similar between the two reef conditions (4.8 ± 4.1 g m−2 h−1 on coral-dominated and 5.3 ± 2.1 g m−2 h−1 on macroalgal-dominated reefs). Interestingly, the Sargassum-assay consumer assemblages differed between reef conditions; nominally grazing herbivores, Siganus puelloides and Chlorurus sordidus, and the browser, Siganus sutor, dominated feeding on high coral cover reefs, whereas browsing herbivores, Naso elegans, Naso unicornis, and Leptoscarus vaigiensis, prevailed on macroalgal-dominated reefs. It appeared that macroalgal density in the surrounding habitat had a strong influence on the species driving the process of macroalgal removal. This suggests that although the function of macroalgal removal may continue, the species responsible may change with context, differing between systems that are regenerating versus degrading.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Almeida AJ, Marques A, Saldanha L (1999) Some aspects of the biology of three fish species from the seagrass beds at Inhaca Island, Mozambique. Cybium 23:369–376

    Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth, UK

    Google Scholar 

  • Arthur R, Done TJ, Marsh H, Harriott V (2006) Local processes strongly influence post-bleaching benthic recovery in the Lakshadweep Islands. Coral Reefs 25:427–440

    Article  Google Scholar 

  • Baayen RH (2011) languageR: Data sets and functions with “Analyzing Linguistic Data: A practical introduction to statistics” http://cran.r-project.org/package=languageR

  • Bates D, Maechler M, Bolker B (2011) lme4: Linear mixed-effects models using S4 classes http://cran.r-project.org/package=lme4

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

    Article  CAS  PubMed  Google Scholar 

  • Bellwood DR, Hoey AS, Hughes TP (2012) Human activity selectively impacts the ecosystem roles of parrotfishes on coral reefs. Proc R Soc Lond B Biol Sci 279:1621–1629

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bennett S, Bellwood DR (2011) Latitudinal variation in macroalgal consumption by fishes on the Great Barrier Reef. Mar Ecol Prog Ser 426:241–252

    Article  Google Scholar 

  • Borsa P, Lemer S, Aurelle D (2007) Patterns of lineage diversification in rabbitfishes. Mol Phylogenet Evol 44:427–435

    Article  CAS  PubMed  Google Scholar 

  • Bouchon-Navaro Y, Harmelin-Vivien ML (1981) Quantitative distribution of herbivorous reef fishes in the Gulf of Aqaba (Red Sea). Mar Biol 63:79–86

    Article  Google Scholar 

  • Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128–3139

    Article  PubMed  Google Scholar 

  • Cheal AJ, Emslie M, MacNeil MA, Miller I, Sweatman H (2013) Spatial variation in the functional characteristics of herbivorous fish communities and the resilience of coral reefs. Ecol Appl 23:174–188

    Article  PubMed  Google Scholar 

  • Choat JH, Robertson DR (2002) Age-based studies on coral reef fishes. In: Sale PF (ed) Coral reef fishes. Academic Press, London, UK

    Google Scholar 

  • Choat JH, Robbins WD, Clements KD (2004) The trophic status of herbivorous fishes on coral reefs. Mar Biol 145:445–454

    Article  Google Scholar 

  • Chong-Seng KM, Mannering TD, Pratchett MS, Bellwood DR, Graham NAJ (2012) The influence of coral reef benthic condition on associated fish assemblages. PLoS ONE 7:e42167

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, UK

    Google Scholar 

  • Clarke KR, Somerfield PJ, Chapman MG (2006) On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray-Curtis coefficient for denuded assemblages. J Exp Mar Biol Ecol 330:55–80

    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 

  • Daw TM, Robinson J, Graham NAJ (2011a) Perceptions of trends in Seychelles artisanal trap fisheries: comparing catch monitoring, underwater visual census and fishers’ knowledge. Environ Conserv 38:75–88

    Article  Google Scholar 

  • Daw TM, Maina J, Cinner JE, Robinson J, Wamukota A (2011b) The spatial behaviour of artisanal fishers: Implications for fisheries management and development (Fishers in Space), Western Indian Ocean Marine Science Association, p 79

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

    Article  Google Scholar 

  • Elmqvist T, Folke C, Nyström M, Peterson G, Bengtsson J, Walker BH, Norberg J (2003) Response diversity, ecosystem change, and resilience. Front Ecol Environ 1:488–494

    Article  Google Scholar 

  • Folke C, Carpenter SR, Walker BH, Scheffer M, Elmqvist T, Gunderson L, Holling CS (2004) Regime shifts, resilience, and biodiversity in ecosystem management. Annual Review of Ecology, Evolution, and Systematics 35:557–581

    Article  Google Scholar 

  • Fox RJ, Bellwood DR (2008) Remote video bioassays reveal the potential feeding impact of the rabbitfish Siganus canaliculatus (f: Siganidae) on an inner-shelf reef of the Great Barrier Reef. Coral Reefs 27:605–615

    Article  Google Scholar 

  • Froese R, Pauly D (2012) FishBase. World Wide Web electronic publication. www.fishbase.org, version (08/2012)

  • Goatley CHR, Bellwood DR (2011) The roles of dimensionality, canopies and complexity in ecosystem monitoring. PLoS ONE 6:e27307

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Goreau TJ, McClanahan TR, Hayes R, Strong A (2000) Conservation of coral reefs after the 1998 global bleaching event. Conserv Biol 14:5–15

    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 Central  PubMed  Google Scholar 

  • Graham NAJ, Bellwood DR, Cinner JE, Hughes TP, Norström AV, Nyström M (2013) Managing resilience to reverse phase shifts in coral reefs. Front Ecol Environ 11:541–548

    Article  Google Scholar 

  • Graham NAJ, McClanahan TR, MacNeil MA, Wilson SK, Polunin NVC, Jennings S, Chabanet P, Clark S, Spalding MD, Letourneur Y, Bigot L, Galzin R, Öhman MC, Garpe KC, Edwards AJ, Sheppard CRC (2008) Climate warming, marine protected areas and the ocean scale integrity of coral reef ecosystems. PLoS ONE 3:e3039

    Article  PubMed Central  PubMed  Google Scholar 

  • Grandcourt EM (1999) The population biology of a selection of exploited reef fish from the Seychelles and Great Barrier Reef. M.Sc. thesis, James Cook University

  • Grandcourt EM, Cesar HSJ (2003) The bio-economic impact of mass coral mortality on the coastal reef fisheries of the Seychelles. Fish Res 60:539–550

    Article  Google Scholar 

  • Green AL, Bellwood DR (2009) Monitoring functional groups of herbivorous reef fishes as indicators of coral reef resilience - A practical guide for coral reef managers in the Asia Pacific region. Switzerland, IUCN working group on Climate Change and Coral Reefs, Gland, p 70

    Google Scholar 

  • Hatcher BG (1988) Coral reef primary productivity: A beggar’s banquet. Trends Ecol Evol 3:106–111

    Article  CAS  PubMed  Google Scholar 

  • Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156

    Article  Google Scholar 

  • Hicks CC, McClanahan TR (2012) Assessing gear modifications needed to optimize yields in a heavily exploited, multi-species, seagrass and coral reef fishery. PLoS ONE 7:e36022

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hoey AS, Bellwood DR (2009) Limited functional redundancy in a high diversity system: single species dominates key ecological process on coral reefs. Ecosystems 12:1316–1328

    Article  Google Scholar 

  • Hoey AS, Bellwood DR (2010) Cross-shelf variation in browsing intensity on the Great Barrier Reef. Coral Reefs 29:499–508

    Article  Google Scholar 

  • Hoey AS, Bellwood DR (2011) Suppression of herbivory by macroalgal density: a critical feedback on coral reefs? Ecol Lett 14:267–273

    Article  PubMed  Google Scholar 

  • Holmes TH, Wilson SK, Travers MJ, Langlois TJ, Evans RD, Moore GI, Douglas RA, Shedrawi G, Harvey ES, Hickey K (2013) A comparison of visual- and stereo-video based fish community assessment methods in tropical and temperate marine waters of Western Australia. Limnol Oceanogr Methods 11:337–350

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642

    Article  PubMed  Google Scholar 

  • Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis BL (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365

    Article  CAS  PubMed  Google Scholar 

  • Jennings S, Grandcourt EM, Polunin NVC (1995) The effects of fishing on the diversity, biomass and trophic structure of Seychelles’ reef fish communities. Coral Reefs 14:225–235

    Article  Google Scholar 

  • Johansson CL, van de Leemput IA, Depczynski M, Hoey AS, Bellwood DR (2013) Key herbivores reveal limited functional redundancy on inshore coral reefs. Coral Reefs 32:963–972

    Article  Google Scholar 

  • Johnson KH (2000) Trophic-dynamic considerations in relating species diversity to ecosystem resilience. Biol Rev Camb Philos Soc 75:347–376

    Article  CAS  PubMed  Google Scholar 

  • Klanten SO, van Herwerden L, Choat JH, Blair D (2004) Patterns of lineage diversification in the genus Naso (Acanthuridae). Mol Phylogenet Evol 32:221–235

    Article  CAS  PubMed  Google Scholar 

  • Klassen RHG, Nolet BA, Bankert D (2006) Movement of foraging Tundra swans explained by spatial pattern in cryptic food densities. Ecology 87:2244–2254

    Article  Google Scholar 

  • Kulbicki M, Guillemot N, Amand M (2005) A general approach to length-weight relationships for New Caledonian lagoon fishes. Cybium 29:235–252

    Google Scholar 

  • Ledlie M, Graham NAJ, Bythell J, 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 

  • Lefèvre CD, Bellwood DR (2011) Temporal variation in coral reef ecosystem processes: herbivory of macroalgae by fishes. Mar Ecol Prog Ser 422:239–251

    Article  Google Scholar 

  • Letourneur Y (1998) Length-weight relationship of some marine fish species in Reunion Island, Indian Ocean. Naga 21:37–39

    Google Scholar 

  • Li F, Yu S, Mao Y, Ye N (2010) Regeneration of germlings and seedlings development from cauline leaves of Sargassum thunbergii. Journal of Developmental Biology and Tissue Engineering 2:14–17

    CAS  Google Scholar 

  • McClanahan TR, Hicks CC (2011) Changes in life history and ecological characteristics of coral reef fish catch composition with increasing fishery management. Fish Manage Ecol 18:50–60

    Article  Google Scholar 

  • McClanahan TR, Hendrick V, Rodrigues MJ, Polunin NVC (1999) Varying responses of herbivorous and invertebrate-feeding fishes to macroalgal reduction on a coral reef. Coral Reefs 18:195–203

    Article  Google Scholar 

  • Michael PJ, Hyndes GA, Vanderklift MA, Vergés A (2013) Identity and behaviour of herbivorous fish influence large-scale spatial patterns of macroalgal herbivory in a coral reef. Mar Ecol Prog Ser 482:227–240

    Article  Google Scholar 

  • Mumby P (2009) Phase shifts and the stability of macroalgal communities on Caribbean coral reefs. Coral Reefs 28:761–773

    Article  Google Scholar 

  • Mumby PJ, Hastings A, Edwards HJ (2007) Thresholds and the resilience of Caribbean coral reefs. Nature 450:98–101

    Article  CAS  PubMed  Google Scholar 

  • Nakamura Y, Horinouchi M, Nakai T, Sano M (2003) Food habits of fishes in a seagrass bed on a fringing coral reef at Iriomote Island, southern Japan. Ichthyol Res 50:15–22

    Article  Google Scholar 

  • 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 23:1632–1644

    Article  PubMed  Google Scholar 

  • Nash KL, Graham NAJ, Januchowski-Hartley FA, Bellwood DR (2012) Influence of habitat condition and competition on foraging behaviour of parrotfishes. Mar Ecol Prog Ser 457:113–124

    Article  Google Scholar 

  • Nyström M (2006) Redundancy and response diversity of functional groups: implications for the resilience of coral reefs. Ambio 35:30–35

    PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Pratchett MS, Hoey AS, Wilson SK, Messmer V, Graham NAJ (2011) Changes in biodiversity and functioning of reef fish assemblages following coral bleaching and coral loss. Diversity 3:424–452

    Article  Google Scholar 

  • Purcell SW, Bellwood DR (1993) A functional analysis of food procurement in two surgeonfish species, Acanthurus nigrofuscus and Ctenochaetus striatus (Acanthuridae). Environ Biol Fishes 37:139–159

    Article  Google Scholar 

  • R Development Core Team (2011) R: A language and environment for statistical computing. http://www.R-project.org/

  • Rasher DB, Hoey AS, Hay ME (2013) Consumer diversity interacts with prey defences to drive ecosystem function. Ecology 94:1347–1358

    Article  PubMed  Google Scholar 

  • Robinson J, Samoilys MA, Grandcourt E, Julie D, Cedras M, Gerry C (2011) The importance of targeted spawning aggregation fishing to the management of Seychelles’ trap fishery. Fish Res 112:96–103

    Article  Google Scholar 

  • Rosenfeld JS (2002) Functional redundancy in ecology and conservation. Oikos 98:156–162

    Article  Google Scholar 

  • Scheffer M, Carpenter S, Foley JA, Folke C, Walker BH (2001) Catastrophic shifts in ecosystems. Nature 413:591–596

    Article  CAS  PubMed  Google Scholar 

  • Spalding MD, Jarvis GE (2002) The impact of the 1998 coral mortality on reef fish communities in the Seychelles. Mar Pollut Bull 44:309–321

    Article  CAS  PubMed  Google Scholar 

  • Stockwell B, Jadloc CRL, Abesamis RA, Alcala AC, Russ GR (2009) Trophic and benthic responses to no-take marine reserve protection in the Philippines. Mar Ecol Prog Ser 389:1–15

    Article  Google Scholar 

  • Unsworth RKF, Taylor JD, Powell A, Bell JJ, Smith DJ (2007) The contribution of scarid herbivory to seagrass ecosystem dynamics in the Indo-Pacific. Estuar Coast Shelf Sci 74:53–62

    Article  Google Scholar 

  • Vergés A, Bennett S, Bellwood DR (2012) Diversity among macroalgae-consuming fishes on coral reefs: a transcontinental comparison. PLoS ONE 7:e45543

    Article  PubMed Central  PubMed  Google Scholar 

  • Vergés A, Vanderklift MA, Doropoulos C, Hyndes GA (2011) Spatial patterns in herbivory on a coral reef are influenced by structural complexity but not by algal traits. PLoS ONE 6:e17115

    Article  PubMed Central  PubMed  Google Scholar 

  • Vermeij MA, Heijden R, Olthuis J, Marhaver K, Smith J, Visser P (2013) Survival and dispersal of turf algae and macroalgae consumed by herbivorous coral reef fishes. Oecologia 171:417–425

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Walker BH, Kinzig A, Langridge J (1999) Plant attribute diversity, resilience, and ecosystem function: The nature and significance of dominant and minor species. Ecosystems 2:95–113

    Article  Google Scholar 

  • Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10

    Article  PubMed  Google Scholar 

  • Williams ID, Polunin NVC, Hendrick VJ (2001) Limits to grazing by herbivorous fishes and the impact of low coral cover on macroalgal abundance on a coral reef in Belize. Mar Ecol Prog Ser 222:187–196

    Article  Google Scholar 

  • 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 41:279–309

    Google Scholar 

  • Wilson SK, Depczynski M, Fisher R, Holmes TH, O’Leary RA, Tinkler P (2010) Habitat associations of juvenile fish at Ningaloo Reef, Western Australia: the importance of coral and algae. PLoS ONE 5:e15185

    Article  PubMed Central  PubMed  Google Scholar 

  • Wilson SK, Graham NAJ, Fisher R, Robinson J, Nash KL, Chong-Seng KM, Polunin NVC, Aumeeruddy R, Quatre R (2012) Effect of macroalgal expansion and marine protected areas on coral recovery following a climatic disturbance. Conserv Biol 26:995–1004

    Article  PubMed  Google Scholar 

  • Woodland DJ, Randall JE (1979) Siganus puelloides, a new species of rabbitfish from the Indian Ocean. Copeia 1979:390–393

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Savelieve AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York, USA

    Book  Google Scholar 

Download references

Acknowledgments

This study was funded by the Australian Research Council, a Western Indian Ocean Marine Science Association Marine Research Grant, and the Seychelles Fishing Authority through the Seychelles/European Union Fisheries Partnership Agreement. We thank A. Hoey for many helpful discussions, J. Robinson, C. Gerry, C. Jean-Baptiste, G. Berke for field assistance, C. Huchery for assistance with video analysis, and four anonymous reviewers for helpful comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to K. M. Chong-Seng.

Additional information

Communicated by Biology Editor Dr. Mark Vermeij

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 763 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chong-Seng, K.M., Nash, K.L., Bellwood, D.R. et al. Macroalgal herbivory on recovering versus degrading coral reefs. Coral Reefs 33, 409–419 (2014). https://doi.org/10.1007/s00338-014-1134-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-014-1134-5

Keywords

Navigation