Skip to main content

Episodic heterogeneous decline and recovery of coral cover in the Indian Ocean

Coral Reefs volume 30, pages 739–752 (2011)Cite this article

Abstract

Long-term changes in coral cover for the Caribbean and the Pacific/Southeast Asia regions (PSEA) have proven extremely useful in assessing the main drivers, magnitude and timescales of change. The one major coral reef region where such assessments have not been made is the Indian Ocean (IO). Here, we compiled coral cover survey data from across the IO into a database of ~2,000 surveys from 366 coral reef sites collected between 1977 and 2005. The compilation shows that the 1998 mass coral bleaching event was the single most important and widespread factor influencing the change in coral cover across the region. The trend in coral cover followed a step-type function driven by the 1998 period, which differs from findings in the Caribbean and the PSEA regions where declines have been more continuous and mostly began in the 1980s. Significant regional variation was observed, with most heterogeneity occurring during and after 1998. There was a significant relationship between cover and longitude for all periods, but the relationship became stronger in the period immediately after 1998. Before 1998, highest coral cover was observed in the central IO region, while this changed to the eastern region after 1998. Coral cover and latitude displayed a significant U-shaped relationship immediately after 1998, due to a large decrease in cover in the northern-central regions. Post-1998 coral cover was directly correlated to the impact of the disturbance; areas with the lowest mortality having the highest cover with India–Sri Lanka being an outlier due to its exceptionally high recovery. In 1998, reefs within Marine Protected Areas (MPAs) were more heavily impacted than unmanaged reefs, losing significantly greater total cover. MPA recovery was greater such that no differences were observed by 2001–2005. This study indicates that the regional patterns in coral cover distribution in the IO are driven mainly by episodic and acute environmental stress.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Aronson RB, Precht WF (2006) Conservation, precaution, and Caribbean reefs. Coral Reefs 25:441–450

    Article  Google Scholar 

  • Ateweberhan M, McClanahan TR (2010) Relationship between historical sea-surface temperature variability and climate change-induced coral mortality in the western Indian Ocean. Mar Pollut Bull 60:964–970

    Article  CAS  PubMed  Google Scholar 

  • Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: an ecological assessment of the long-term impacts, recovery trends and future outlooks. Estuar Coast Shelf Sci 80:435–471

    Article  Google Scholar 

  • Bell JD, Galzin R (1984) Influence of live coral cover on coral-reef fish communities. Mar Ecol Prog Ser 15:265–274

    Article  Google Scholar 

  • Bellwood DR, Hughes TP, Folke C, Nystrom M (2004) Confronting the coral reef crisis. Nature 429:827–832

    Article  CAS  PubMed  Google Scholar 

  • Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS One 2:e711

    Article  PubMed  PubMed Central  Google Scholar 

  • Carleton JH, Done TJ (1995) Quantitative video sampling of coral reef benthos: large-scale application. Coral Reefs 14:35–46

    Article  Google Scholar 

  • Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortes J, Delbeek JC, DeVantier L (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Edinger EN, Jompa J, Limmon GV, Widjatmoko W, Risk MJ (1998) Reef degradation and coral biodiversity in Indonesia: effects of land-based pollution, destructive fishing practices and changes over time. Mar Pollut Bull 36:617–630

    Article  CAS  Google Scholar 

  • Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960

    Article  CAS  PubMed  Google Scholar 

  • Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2005) Hurricanes and Caribbean coral reefs: impacts, recovery patterns, and role in long-term decline. Ecology 86:174–184

    Article  Google Scholar 

  • Garpe KC, Yahya SAS, Lindahl U, Ohman MC (2006) Long-term effects of the 1998 coral bleaching event on reef fish assemblages. Mar Ecol Prog Ser 315:237–247

    Article  Google Scholar 

  • Glynn PW, Mate JL, Baker AC, Calderon MO (2001) Coral bleaching and mortality in panama and ecuador during the 19971998 El NinoSouthern Oscillation Event: spatial/temporal patterns and comparisons with the 1982–1983 event. Bull Mar Sci 69:79–109

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graham NAJ, Wilson SK, Jennings S, Polunin NVC, Robinson JAN, Bijoux JP, Daw T (2007) Lag effects in the impacts of mass coral bleaching on coral reef fish, fisheries, and ecosystems. Conserv Biol 21:1291–1300

    Article  PubMed  Google Scholar 

  • Graham NAJ, Chabanet P, Evans RD, Jennings S, Letourneur Y, MacNeil MA, McClanahan TR, Öhman MC, Polunin NVC, Wilson SK (2011) Extinction vulnerability of coral reef fishes. Ecol Lett 14:341–348

    Article  PubMed  PubMed Central  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, Alasdair JE, Sheppard CRC (2008) Climate warming, Marine Protected Areas and the ocean-scale integrity of coral reef ecosystems. PlosONE 3(8):e3039

    Article  Google Scholar 

  • Hastings A (1980) Disturbance, coexistence, history, and competition for space. Theor Popul Biol 18:363–373

    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 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  PubMed  Google Scholar 

  • Hughes TP, Ayre D, Connell JH (1992) The evolutionary ecology of corals. Trend Ecol Evol 7:292–295

    Article  CAS  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, 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 S, 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 

  • Idjadi JA, Edmunds PJ (2006) Scleractinian corals as facilitators for other invertebrates on a Caribbean reef. Mar Ecol Prog Ser 319:117–127

    Article  Google Scholar 

  • Jones GP, McCormick MI, Srinivasan M, Eagle JV (2004) Coral decline threatens fish biodiversity in marine reserves. Proc Natl Acad Sci USA 101:8251–8258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindén O, Sporrong N (1999) Coral reef degradation in the Indian Ocean: Status reports and project presentations 1999. CORDIO

  • Linden O, Souter D, Wilhelmsson D, Obura D (2002) Coral reef degradation in the Indian Ocean: status report 2002. http://cmsdata.iucn.org/downloads/cordio_status_report_2002.pdf

  • Maina J, Venus V, McClanahan TR, Ateweberhan M (2008) Modelling susceptibility of coral reefs to environmental stress using remote sensing data and GIS models. Ecol Model 212:180–199

    Article  Google Scholar 

  • Maynard JA, Anthony KRN, Marshall PA, Masiri I (2008) Major bleaching events can lead to increased thermal tolerance in corals. Mar Biol 155:173–182

    Article  Google Scholar 

  • McClanahan TR (2008) Response of the coral reef benthos and herbivory to fishery closure management and the 1998 ENSO disturbance. Oecologia 155:169–177

    Article  CAS  PubMed  Google Scholar 

  • McClanahan TR, Maina J (2003) Response of coral assemblages to the interaction between natural temperature variation and rare warm-water events. Ecosystems 6:551–563

    Article  Google Scholar 

  • McClanahan T, Muthiga N, Mangi S (2001) Coral and algal changes after the 1998 coral bleaching: interaction with reef management and herbivores on Kenyan reefs. Coral Reefs 19:380–391

    Article  Google Scholar 

  • McClanahan T, Polunin N, Done T (2002) Ecological states and the resilience of coral reefs. Conserv Ecol 6:18

    Article  Google Scholar 

  • McClanahan TR, Baird AH, Marshall PA, Toscano MA (2004) Comparing bleaching and mortality responses of hard corals between southern Kenya and the Great Barrier Reef, Australia. Mar Pollut Bull 48:327–335

    Article  CAS  PubMed  Google Scholar 

  • McClanahan TR, Maina J, Moothien Pillay R, Baker AC (2005) Effects of geography, taxa, water flow, and temperature variation on coral bleaching intensity in Mauritius. Mar Ecol Prog Ser 298:131–142

    Article  Google Scholar 

  • McClanahan TR, Ateweberhan M, Muhando C, Maina J, Mohammed SM (2007a) Effects of climate and seawater temperature variation on coral bleaching and mortality. Ecol Monogr 77:503–525

    Article  Google Scholar 

  • McClanahan TR, Ateweberhan M, Sebastian CR, Graham NAJ, Wilson SK, Bruggemann H, Guillaume M (2007b) Western Indian Ocean coral communities, bleaching responses, and susceptibility to extinction. Mar Ecol Prog Ser 337:1–13

    Article  Google Scholar 

  • McClanahan TR, Ateweberhan M, Ruiz Sebastian C, Graham NAJ, Wilson SK, Bruggemann JH, Guillaume MMM (2007c) Predictability of coral bleaching from synoptic satellite and in situ temperature observations. Coral Reefs 26:695–701

    Article  Google Scholar 

  • Mohamed SM, Muhando C, Machano H (2002) Assessment of coral reef degradation in Tanzania; Results of Coral Reef Monitoring 1999–2002. In: Linden O, Souter D, Wilhelmsson D, Obura D (eds) Coral reef degradation in the Indian Ocean, status report 2002. CORDIO, Kalmar, Sweden, pp 21–30

    Google Scholar 

  • Muhando CA, Mohammed MS (2002) Coral reef benthos and fisheries in Tanzania before and after the 1998 bleaching and mortality event. Western Indian Ocean. J Mar Sci 1:43–52

    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 

  • Norström AV, 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 

  • Nyström M, Folke C, Moberg F (2000) Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol Evol 15:413–417

    Article  PubMed  Google Scholar 

  • Obura DO (2001) Can differential bleaching and mortality among coral species offer useful indicators for assessment and management of reefs under stress? Bull Mar Sci 69:421–442

    Google Scholar 

  • Obura DO (2005) Resilience and climate change: lessons from coral reefs and bleaching in Western Indian Ocean. Estuar Coast Shelf Sci 63:353–372

    Article  Google Scholar 

  • Podesta GP, Glynn PW (2001) The 1997–98 El Nino event in Panama and Galapagos: an update of thermal stress indices relative to coral bleaching. Bull Mar Sci 69:43–59

    Google Scholar 

  • Pratchett MS, Munday PL, Wilson SK, Graham NAJ, Cinner JE, Bellwood DR, Jones GP, Polunin NVC, McClanahan TR (2008) Effects of climate-induced coral bleaching on coral-reef fishes—ecological and economic consequences. Oceanogr Mar Biol Annu Rev 46:251–296

    Article  Google Scholar 

  • Sandin SA, Smith JE, DeMartini EE, Dinsdale EA, Donner SD, Friedlander AM, Konotchick T, Malay M, Maragos JE, Obura D, Pantos O, Paulay G, Richie M, Rohwer F, Schroeder RE, Walsh S, Jackson JBC, Knowlton N, Sala E (2008) Baselines and degradation of coral reefs in the northern Line Islands. PLoS ONE 3:e1548

    Article  PubMed  PubMed Central  Google Scholar 

  • Scheer G (1974) Investigation of coral reefs at Rasdu Atoll in the Maldives with the quadrat method according to phytosociology. Proc 2nd Coral Reef Symp 2:655–670

    Google Scholar 

  • Schutte V, Selig ER, Bruno JF (2010) Regional spatio-temporal trends in Caribbean coral reef benthic communities. Mar Ecol Prog Ser 402:115–122

    Article  Google Scholar 

  • Selig ER, Bruno JF (2010) A global analysis of the effectiveness of Marine Protected Areas in preventing coral loss. PLoS One 5:e9278

    Article  PubMed  PubMed Central  Google Scholar 

  • Sheppard C, Al-Husiani M, Al-Jamali F, Al-Yamani F, Baldwin R, Bishop J, Benzoni F, Dutrieux E, Dulvy NK, Durvasula SRV, Jones DA, Loughland R, Medio D, Nithyanandan M, Pilling GM, Polikarpov I, Price ARG, Purkis S, Riegl B, Saburova M, Namin KS, Taylor O, d Simon Wilson KZ (2010) The Gulf: A young sea in decline. Mar Pollut Bull 60:13–38

    Article  CAS  PubMed  Google Scholar 

  • Sheppard CRC (1999) Changes in coral cover on reefs of Chagos over eighteen years. In: Sheppard CRC, Seaward MRD (eds) Ecology of the Chagos Archipelago. Westbury Publishing, Great Britain, pp 91–100

    Google Scholar 

  • Sheppard CRC (2003) Predicted recurrences of mass coral mortality in the Indian Ocean. Nature 425:294–297

    Article  CAS  PubMed  Google Scholar 

  • Sheppard CRC, Harris A, Sheppard ALS (2008) Archipelago-wide coral recovery patterns since 1998 in the Chagos Archipelago, central Indian Ocean. Mar Ecol Prog Ser 362:109–117

    Article  Google Scholar 

  • Souter D, Linden O (eds) (2005) Coral reef degradation in the Indian Ocean. Status report 2005. CORDIO, Univ. of Kalmar, Sweden

    Google Scholar 

  • Souter D, Obura D, Lindén O (2000) Coral reef degradation in the Indian Ocean. Status report 2000. CORDIO. SAREC Marine Science Program, Stockholm, Sweden

    Google Scholar 

  • Spencer T, Teleki KA, Bradshaw C, Spalding MD (2000) Coral bleaching in the southern Seychelles during the 1997–1998 Indian Ocean warm event. Mar Pollut Bull 40:569–586

    Article  CAS  Google Scholar 

  • Sweatman H, Delean S, Syms S (2011) Assessing loss of coral cover on Australia’s Great Barrier Reef over two decades, with implications for longer-term trends. Coral Reefs 30:521–531

    Article  Google Scholar 

  • Turner J, Klaus R (2005) Coral reefs of the Mascarenes, Western Indian Ocean. Philos Trans R Soc Lond A 363:229–250

    Article  Google Scholar 

  • Turner J, Hardman E, Klaus R, Fagoonee I, Daby D, Baghooli R, Persands S (2000) The reefs of Mauritius. In: Souter D, Obura D, Lindén O (eds) Coral reef degradation in the Indian Ocean. Status report 2000. CORDIO, SAREC Marine Science Program, Stockholm, Sweden

    Google Scholar 

  • Wilkinson C (2002) Status of coral reefs of the world: 2002. Australian Institute of Marine Science, Townsville

    Google Scholar 

  • Wilkinson C (2004) Status of coral reefs of the world: 2004. Australian Inst of Marine Science, Townsville

    Google Scholar 

  • Wilkinson CR (1999) Global and local threats to coral reef functioning and existence: review and predictions. Mar Freshw Res 50:867–878

    Article  Google Scholar 

  • Wilson SK, Graham NAJ, Polunin NVC (2007) Appraisal of visual assessments of habitat complexity and benthic composition on coral reefs. Mar Biol 151:1069–1076

    Article  Google Scholar 

Download references

Acknowledgments

The Wildlife Conservation Society supported this study through a number of sources: the World Bank Targeted Research Group on Coral Bleaching and Western Indian Ocean Science for Management Program (MASMA). The database is a product of the hard work of many scientists and volunteers who contributed data to "Reef Check" and published results in peer-reviewed and non-reviewed reports.

Author information

Authors and Affiliations

  1. School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK

    M. Ateweberhan & C. R. C. Sheppard

  2. Coral Reef Conservation Project, P.O. Box 99470, Mombasa, Kenya

    M. Ateweberhan & T. R. McClanahan

  3. Marine Program, Wildlife Conservation Society, Bronx, NY, 10430, USA

    T. R. McClanahan

  4. ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD, 4811, Australia

    N. A. J. Graham

Authors
  1. M. Ateweberhan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. R. McClanahan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. A. J. Graham
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. R. C. Sheppard
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Ateweberhan.

Additional information

Communicated by Biology Editor Dr. Hugh Sweatman

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 135 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Ateweberhan, M., McClanahan, T.R., Graham, N.A.J. et al. Episodic heterogeneous decline and recovery of coral cover in the Indian Ocean. Coral Reefs 30, 739–752 (2011). https://doi.org/10.1007/s00338-011-0775-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-011-0775-x

Keywords

  • ENSO
  • Climatic disturbance
  • Climate change impact
  • Coral bleaching
  • Coral reef management
  • Ecological vulnerability
  • Marine reserves
  • Recovery
  • Regional variation