Coral Reefs

, Volume 37, Issue 4, pp 1245–1257 | Cite as

Coral reefs respond to repeated ENSO events with increasing resistance but reduced recovery capacities in the Lakshadweep archipelago

  • S. YadavEmail author
  • T. Alcoverro
  • R. Arthur


The resilience of reefs to repeated, increasingly frequent thermal disturbance is a dynamic balance between resistance and recovery pathways. The Lakshadweep archipelago in the central Indian Ocean has experienced three El Niño Southern Oscillation (ENSO) events in 1998, 2010 and 2016. Using a multi-decadal monitoring of 6 shallow reefs, we estimated reef resistance and coral recovery after each of these bleaching events. Even as the severity of each ENSO event increased over time, coral mortality decreased from 87% post-1998 to 44% after 2010 and 31% after 2016. In contrast, benthic recovery after 2010 was more protracted than after 1998, with a fourfold decrease in recovery rates between the two time periods. This has resulted in a 40% decline in absolute coral cover in the last 2 decades from 51.6% in 1998 to 11% in 2017. We examined the demographic and compositional mechanisms underlying these two recovery trajectories by monitoring coral recruitment, juvenile, and young adult compositions for 5 yr after 1998 and 2010. While coral juvenile densities were comparable after each of these disturbances, densities of fast-growing Acroporids had reduced from > 1 m−2 post-1998 to 0.09 m−2 post-2010. This was reflected in the composition of coral communities in 2003 and 2015, which differed in its dominant coral taxa, with a dramatic decline in Acropora and an increase in the cover of Porites by 2015. While the dominance of resistant taxa like Porites signals a shift to a system adapting to recurrent thermal anomalies, the reduction in fast-growing, habitat-forming corals like Acropora is driving a major decline in recovery rates with time. Given the frequency of current warming events, the increased reef resistance over the last 2 decades is likely not sufficient to also ensure gains in coral cover in Lakshadweep’s reefs.


Bleaching Scleractinian corals Life-history strategy Community composition Reef recovery Indian Ocean 



This study was supported by grants from The Rufford Foundation, the Pew Marine Fellowships (0025864) and The Spanish National Research Council (Memorandum of understanding between CEAB-IMEDEA-NCF). We thank the Department of Science and Technology and the Department of Tourism (SPORTS), Lakshadweep, for permits and logistical support and Rucha Karkarey, Mayuresh Gangal, Pooja Rathod, Vardhan Patankar, Aaron Lobo, Amod Zambre, Aditi Pophale and MK Ibrahim for their invaluable help in the field during the course of this study. We would also like to thank Abinand Reddy, Jordi Pagès and Susanna Pinedo for help and advice with analytical approaches and three anonymous reviewers for valuable comments on this manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

338_2018_1735_MOESM1_ESM.docx (5.8 mb)
Supplementary material 1 (DOCX 5966 kb)


  1. Alonso D, Pinoyl-Gallemi A, Alcoverro T, Arthur R (2015) Fish community reassembly after a coral mass mortality: higher trophic groups are subject to increased rates of extinction. Ecol Lett 18:451–461CrossRefGoogle Scholar
  2. Alvarez-Filip L, Dulvy NK, Gill JA, Côté IM, Watkinson AR (2009) Flattening of Caribbean coral reefs: region-wide declines in architectural complexity. Proc R Soc Lond B Biol Sci 276:3019–3025CrossRefGoogle Scholar
  3. Arthur R, Done TJ, Marsh H (2005) Benthic recovery four years after al El Niño-induced coral mass mortality in the Lakshadweep atolls. Curr Sci (Bangalore) 89(4):694–699Google Scholar
  4. Arthur R, Done TJ, Marsh H, Harriott V (2006) Local processes strongly influence post-bleaching benthic recovery in the Lakshadweep Atolls. Coral Reefs 25:427–440CrossRefGoogle Scholar
  5. Ateweberhan M, McClanahan TR, Graham NAJ (2011) Episodic heterogenous decline and recovery of coral cover in the Indian Ocean. Coral Reefs 30:739–752CrossRefGoogle Scholar
  6. Baird AH, Marshall PA (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar Ecol Prog Ser 237:133–141CrossRefGoogle Scholar
  7. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models using lme4. Journal of Statistical Software 67(1):1–48CrossRefGoogle Scholar
  8. Bellwood DR, Hoey AS, Ackerman JL, Depczynski M (2006) Coral bleaching, reef fish community phase shifts and the resilience of coral reefs. Glob Change Biol 12:1587–1594CrossRefGoogle Scholar
  9. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833CrossRefGoogle Scholar
  10. Berumen ML, Pratchett MS (2006) Recovery without resilience: persistent disturbance and long-term shifts in the structure of fish and coral communities at Tiahura Reef, Moorea. Coral Reefs 25:647–653CrossRefGoogle Scholar
  11. Bozec Y-M, Mumby PJ (2014) Synergistic impacts of global warming on the resilience of coral reefs. Phil Trans R Soc B 370:20130267CrossRefGoogle Scholar
  12. Cheal AJ, MacNeil MA, Emslie MJ, Sweatman H (2017) The threat to coral reefs from more intense cyclones under climate change. Global Change Biology 23:1511–1524CrossRefGoogle Scholar
  13. Cinner JE, Huchery C, MacNeil MA, Graham NAJ, McClanahan TR, Maina J, Maire E, Kittinger JN, Hicks CC, Mora C, Allison EH, D’Agata S, Hoey A, Feary DA, Crowder L, Williams ID, Kulbicki M, Vigliola L, Wantiez L, Edgar G, Stuart-Smith RD, Sandin SA, Green AL, Hardt MJ, Beger M, Friedlander A, Campbell SJ, Holmes KE, Wilson SK, Brokovich E, Brooks AJ, Cruz-Motta JJ, Booth DJ, Chabanet P, Gough C, Tupper M, Ferse SCA, Sumaila UR, Mouillot D (2016) Bright spots among the world’s coral reefs. Nature 535(7612):416–419CrossRefGoogle Scholar
  14. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18:117–143CrossRefGoogle Scholar
  15. Clarke KR, Gorley RN (2006) PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, p 192Google Scholar
  16. Coker DJ, Graham NAJ, Pratchett MS (2012) Interactive effects of live coral and structural complexity on the recruitment of reef fishes. Coral Reefs 31:919–927CrossRefGoogle Scholar
  17. Coker DJ, Wilson SK, Pratchett MS (2013) Importance of live coral habitat for reef fishes. Rev Fish Biol Fish 24:89–126CrossRefGoogle Scholar
  18. Cooper W, Lirman D, Schmale M, Lipscomb D (2007) Consumption of coral spat by histophagic ciliates. Coral Reefs 26:249–250CrossRefGoogle Scholar
  19. Darling ES, McClanahan TR, Côté IM (2013) Life histories predict coral community disassembly under multiple stressors. Glob Change Biol 19:1930–1940CrossRefGoogle Scholar
  20. Darling ES, Alvarez-Filip L, Oliver TA, McClanahan TR, Côté IM (2012) Evaluating life-history strategies of reef corals from species traits. Ecol Lett 15:1378–1386CrossRefGoogle Scholar
  21. Darling ES, Graham NAJ, Januchowski-Hartley FA, Nash KL, Pratchett MS, Wilson SK (2017) Relationships between structural complexity, coral traits, and reef fish assemblages. Coral Reefs 36(2):561–575CrossRefGoogle Scholar
  22. Diaz-Pulido G, McCook LJ, Dove S, Berkelmans R, Roff G, Kline DI, Weeks S, Evans RD, Williamson DH, Hoegh-Guldberg O (2009) Doom and Boom on a Resilient Reef: Climate Change, Algal Overgrowth and Coral Recovery. PLoS ONE 4:e5239CrossRefGoogle Scholar
  23. Diffenbaugh NS, Singh D, Mankin JS, Horton DE, Swain DL, Touma D, Charland A, Liu Y, Haugen M, Tsiang M, Rajaratnam B (2017) Quantifying the influence of global warming on unprecedented extreme climate events. PNAS 114:4881–4886CrossRefGoogle Scholar
  24. Done TJ (1999) Coral community adaptability to environmental change at the scales of regions, reefs and reef zones. American Zoologist 39:66–79CrossRefGoogle Scholar
  25. Done TJ, Dayton PK, Dayton AE, Steger R. Regional and local variability in recovery in shallow coral communities: Moorea, French Polynesia and central Great Barrier Reef (1991) Coral Reefs 9:4:183-192Google Scholar
  26. Done TJ, Lm D, Turak E, Fisk DA, Wakeford M, van Woesik R (2010) Coral growth on three reefs: development of recovery benchmarks using a space for time approach. Coral Reefs 29:815–833CrossRefGoogle Scholar
  27. Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate Extremes: Observations, Modeling, and Impacts. Science 289:2068–2074CrossRefGoogle Scholar
  28. Edmunds PJ (2017) Unusually high coral recruitment during the 2016 El Niño in Mo’orea, French Polynesia. PLoS ONE 12(10):e0185167CrossRefGoogle Scholar
  29. Golbuu Y, Victor S, Penland L, Idip D, Emaurois C, Okaji K, Yukihira H, Iwase A, Van Woesik R (2007) Palau’s coral reefs show differential habitat recovery following the 1998-bleachinge event. Coral Reefs 26:319CrossRefGoogle Scholar
  30. Graham NAJ, Chabanet P, Evans RD, Jennings S, Letourneur Y, Aaron MacNeil M, McClanahan TR, Öhman MC, Polunin NVC, Wilson SK (2011) Extinction vulnerability of coral reef fishes. Ecology Letters 14:341–348CrossRefGoogle Scholar
  31. Green DH, Edumunds PJ, Carpenter RC (2008) Increasing relative abundance of Porites asteroids on Caribbean reefs mediated by an overall decline in coral cover. Mar Ecol Prog Ser 359:1–10CrossRefGoogle Scholar
  32. Grime J, Pierce S (2012) The evolutionary strategies that shape ecosystems. Wiley-Blackwell, Oxford, UKCrossRefGoogle Scholar
  33. Guest JR, Low J, Tun K, Wilson B, Ng C, Raingeard D, Ulstrup KE, Tanzil JT, Todd PA, Toh TC, McDougald D (2016) Coral community response to bleaching on a highly disturbed reef. Sci Rep 6:20717CrossRefGoogle Scholar
  34. Halpern CB (1988) Early successional pathways and the resistance and resilience of forest communities. Ecology 69:1703–1715CrossRefGoogle Scholar
  35. Hoegh-Guldberg O (1999) Climate change, coral bleaching, and the future of the world’s coral reefs. Marine and Freshwater Research 50(8):839–866CrossRefGoogle Scholar
  36. Hughes TP (1994) Catastrophes, phase-shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551CrossRefGoogle Scholar
  37. Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263CrossRefGoogle Scholar
  38. Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365CrossRefGoogle Scholar
  39. 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, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933CrossRefGoogle Scholar
  40. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377CrossRefGoogle Scholar
  41. Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs J-PA, Hoey AS, Hoogenboom M, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83CrossRefGoogle Scholar
  42. Jaini M, Advani S, Shanker K, Oommen M, Namboothri N (2017) History, culture, infrastructure and export markets shape fisheries and reef accessibility in India’s contrasting oceanic islands. Envir Cons: 1–8Google Scholar
  43. Januchowski-Hartley FA, Graham NAJ, Wilson SK, Jennings S, Perry CT (2017) Drivers and predictions of coral reef carbonate budget trajectories. Proc R Soc B 284:20162533CrossRefGoogle Scholar
  44. Johns KA, Osborne KO, Logan M (2014) Contrasting rates of coral recovery and reassembly in coral communities on the Great Barrier Reef. Coral Reefs 33:553–6563CrossRefGoogle Scholar
  45. Jones GP, McCormick MI, Srinivasan M, Eagle JV (2004) Coral decline threatens fish biodiversity in marine reserves. Proc Natl Acad Sci USA 101:8251–8253CrossRefGoogle Scholar
  46. Karkarey R, Kelkar N, Lobo AS, Arthur R (2014) Long-lived groupers require structurally stable reefs in the face of repeated climate change disturbances. Coral Reefs 33:289–302CrossRefGoogle Scholar
  47. Karkarey R, Alcoverro T, Kumar S, Arthur T (2017) Coping with catastrophe: foraging plasticity enables a benthic predator to survive in rapidly degrading coral reefs. Animal Behaviour 131:13–22CrossRefGoogle Scholar
  48. Kerry JT, Bellwood DR (2012) The effect of coral morphology on shelter selection by coral reef fishes. Coral Reefs 31(2):415–424CrossRefGoogle Scholar
  49. Knowlton N (2001) The future of coral reefs. Proc Natl Acad Sci USA 98:5419–5425CrossRefGoogle Scholar
  50. Liu G, Strong AE, Skirving WJ and Arzayus LF (2006) Overview of NOAA Coral Reef Watch Program’s Near-Real-Time Satellite Global Coral Bleaching Monitoring Activities. Proceedings of the 10th International Coral Reef Symposium, Okinawa: 1783-1793Google Scholar
  51. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131CrossRefGoogle Scholar
  52. Madin JS, Anderson KD, Andreasen MH, Bridge TC, Cairns SD, Connolly SR, Darling ES, Diaz M, Falster DS, Franklin EC (2016) Gates RD (2016) The Coral Trait Database, a curated database of trait information for coral species from the global oceans. Sci Data 3:160017CrossRefGoogle Scholar
  53. Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163CrossRefGoogle Scholar
  54. McClanahan TR, Ateweberhan M, Graham NAJ, Wilson SK, Ruiz Sebastián C, Guillaume MMM, Bruggemann JH (2007) Western Indian Ocean coral communities: bleaching responses and susceptibility to extinction. Mar Ecol Prog Ser 337:1–13CrossRefGoogle Scholar
  55. McManus JW, Polsenberg JF (2006) Coral-algal phase shifts on coral reefs: Ecological and environmental aspects. Prog Oceanogr 60:263–279CrossRefGoogle Scholar
  56. Nakajima Y, Nishikawa A, Iguchi A, Sakai K (2010) Gene flow and genetic diversity of a broadcast-spawning coral in northern peripheral populations. PLoS ONE 5(6):e11149CrossRefGoogle Scholar
  57. O’Connor MI, Bruno JF, Gaines SD, Halpern BS, Lester SE, Kinlan BP (2007) Weiss JM (2007) Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation. PNAS 104(4):1266–1271CrossRefGoogle Scholar
  58. Palumbi SR, Barshis DJ, Traylor-Knowles N, Bay RA (2014) Mechanisms of reef coral resistance to future climate change. Science 344:859–898CrossRefGoogle Scholar
  59. Pearson RG (1981) Recovery and recolonization of coral reefs. Mar Ecol Prog Ser 1:105–122CrossRefGoogle Scholar
  60. Penin L, Adjeroud M (2013) Relative importance of recruitment and post-settlement processes in the maintenance of coral assemblages in an insular, fragmented reef system. Mar Ecol Prog Ser 473:149–162CrossRefGoogle Scholar
  61. Penin L, Michonneau F, Baird AH, Connolly SR, Pratchett MS, Kayal M, Adjeroud M (2010) Early post-settlement mortality and the structure of coral assemblages. Mar Ecol Prog Ser 408:55–64CrossRefGoogle Scholar
  62. Perry CT, Morgan KM (2017) Bleaching drives collapse in reef carbonate budgets and reef growth potential on southern Maldives reefs. Sci Rep 7:40581CrossRefGoogle Scholar
  63. Pratchett MS, Coker DJ, Jones GP, Munday PL (2012) Specialization in habitat use by coral reef damselfish and their susceptibility to habitat loss. Ecol Evol 2:2168–2180CrossRefGoogle Scholar
  64. Pratchett MS, Baird AH, Bauman AH, Burt JA (2016) Abundance and composition of juvenile corals reveals divergent trajectories for coral assemblages across the United Arab Emirates. Mar Poll Bull 114:1031–1035CrossRefGoogle Scholar
  65. Pratchett MS, Munday P, Wilson SK, Graham NA, Cinner JE, Bellwood DR, Jones GP, Polunin NV, McClanahan TR (2008) Effects of climate-induced coral bleaching on coral-reef fishes, ecological and economic consequences. Oceanogr Mar Biol Annu Rev 46:251–296Google Scholar
  66. Pratchett MS, Anderson KD, Hoogenboom MO, Widman E, Baird AH, Pandolfi JM, Edmunds PJ, Lough JM (2015) Spatial, temporal and taxonomic variation in coral growth—implications for the structure and function of coral reef ecosystems. Oceanography and Marine Biology: An Annual Review 53:215–296Google Scholar
  67. Putnam HM, Edmunds PJ (2017) Fan TY (2017) Effect of temperature on the settlement choice and photophysiology of larvae from the reef coral Stylophora pistillata. Biological Bulletin 215(2):135–142CrossRefGoogle Scholar
  68. R Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  69. Rueden CT, Schindelin J, Hiner MC, DeZonia BE, Walter AE, Arena ET, Eliceiri KW (2017) Imagej 2: ImageJ for the next generation of scientific image data. BMC Bioinf 18:529CrossRefGoogle Scholar
  70. Riegl BM, Sheppard CRC, Purkis SJ (2012) Human Impact on Atolls Leads to Coral Loss and Community Homogenisation: A Modeling Study. PLoS ONE 7(6):e36921CrossRefGoogle Scholar
  71. Ritson-Williams R, Arnold S, Fogarty N, Steneck RS, Vermeij MJA, Paul VJ (2009) New perspectives on ecological mechanisms affecting coral recruitment on reefs. Smithson Contrib Mar Sci 38:437–457CrossRefGoogle Scholar
  72. Robinson CT (2012) Long-term changes in community assembly, resistance, and resilience following experimental floods. Ecological Applications 22:1949–1961CrossRefGoogle Scholar
  73. Roff G, Mumby PJ (2012) Global disparity in the resilience of coral reefs. Trends Ecol Evol 27(7):404–413CrossRefGoogle Scholar
  74. Sousa WP (1984) The role of disturbance in natural communities. Ann Rev Ecol Syst 15:353–391CrossRefGoogle Scholar
  75. Southwood TRE (1988) Tactics, strategies and templets. OIKOS 52:3–18CrossRefGoogle Scholar
  76. Suchley A, Alvarez-Filip L (2017) Herbivory facilitates growth of a key reef-building Caribbean coral. Ecol Evol 7:11246–11256CrossRefGoogle Scholar
  77. Syms C, Jones GP (2000) Disturbance, habitat structure, and the dynamics of a coral reef fish community. Ecology 81:2714–2729CrossRefGoogle Scholar
  78. Trapon ML, Pratchett MS, Hoey AS (2013) Spatial variation in abundance, size and orientation of juvenile corals related to the biomass of parrotfishes on the Great Barrier Reef, Australia. PLoS ONE 8:e57788CrossRefGoogle Scholar
  79. Van Woesik R, Sakai K, Ganase A, Loya Y (2011) Revisiting the winners and the losers a decade after coral bleaching. Mar Ecol Prog Ser 434:67–76CrossRefGoogle Scholar
  80. Vermeij MJA (2005) Substrate composition and adult distribution determine recruitment patterns in a Caribbean brooding coral. Marine Ecology Progress Series 295:123–133CrossRefGoogle Scholar
  81. Wilkinson CR (1996) Global change and coral reefs: impacts on reefs, economies and human culture. Global Change Biology 2:547–558CrossRefGoogle Scholar
  82. Yadav S, Rathod P, Alcoverro T, Arthur R (2015) “Choice” and destiny: the substrate composition and mechanical stability of settlement structures can mediate coral recruit fate in post-bleached reefs. Coral Reefs 35:211–222CrossRefGoogle Scholar
  83. Young T, Chase J, Huddleston RT (2001) Community succession and assembly: comparing, contrasting and combining paradigms in the context of ecological restoration. Ecological Restoration 19:5–18CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Nature Conservation FoundationMysoreIndia
  2. 2.Marine Biology Graduate ProgramUniversity of Hawai‘i at MānoaHonoluluUSA
  3. 3.Centre d’Estudis Avançats de Blanes (CEAB-CSIC)BlanesSpain

Personalised recommendations