Abstract
Repeated bouts of coral bleaching threaten the long-term persistence of coral reefs and associated communities. Here, we document the short- and long-term impacts of heatwave events on coral and fish assemblages, based on regular surveys of 18 reefs of the granitic islands of Seychelles over 23 yr. Extreme heat events in 1998 and 2016 led to bleaching-associated declines in coral cover, whilst between these years there was an interim period of coral recovery on some reefs. Coral decline and recovery were primarily due to changes in the cover of branching coral, particularly those from the families Acroporidae and Pocilloporidae. Surveys during the 2016 bleaching found that 95% of the 468 Acropora and Pocillopora colonies observed were either bleached or recently dead. The extent of bleaching and subsequent mortality were best explained by a priori assessments of community susceptibility to heat stress. One year later (2017), coral cover had fallen by 70% and average coverage across the 18 reefs was at 6%, similar to levels recorded in 2005, 7 yr after the 1998 bleaching. Decline in coral following the 2016 bleaching coincided with reduced abundance of fish < 11 cm TL, particularly corallivores, invertivores and mixed diet feeders. These changes are likely to foreshadow more widespread loss once the habitat structure erodes. Accordingly, 7 yr after the 1998 bleaching, when coral skeletons and reef structure had collapsed on some reefs, abundance of both large- and small-bodied fish had declined. We show that fluctuation in the cover of branching coral is positively associated with changes in the abundance of small-bodied fish which contribute to ecological processes and high diversity, suggesting branching corals are a keystone structure. Increased frequency of bleaching threatens the capacity of branching corals to fully recover after disturbances, reducing the amplitude of boom bust cycles of these corals and the keystone habitat structure they provide reef fish.
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References
Barlow J, França F, Gardner TA, Hicks CC, Lennox GD, Berenguer E, Castello L, Economo EP, Ferreira J, Guenard B (2018) The future of hyperdiverse tropical ecosystems. Nature 559:517–526
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 12:1587–1594
Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833
Birkeland C (2004) Ratcheting down the coral reefs. BioScience 54:1021–1027
Burnham KP, Anderson DR (2003) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer Verlag, New York
Coker DJ, Wilson SK, Pratchett MS (2014) Importance of live coral habitat for reef fishes. Rev Fish Biol Fish 24:89–126
Cole AJ, Pratchett MS, Jones GP (2008) Diversity and functional importance of coral-feeding fishes on tropical coral reefs. Fish Fish 9:286–307
Cramer KL, Jackson JBC, Angioletti CV, Leonard-Pingel J, Guilderson TP (2012) Anthropogenic mortality on coral reefs in Caribbean Panama predates coral disease and bleaching. Ecol Lett 15:561–567
Darling ES, Alvarez-Filip L, Oliver TA, McClanahan TR, Côté IM (2012) Evaluating life-history strategies of reef corals from species traits. Ecol Lett 15:1378–1386
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 36:561–575
Fisher R, Wilson SK, Sin TM, Lee AC, Langlois TJ (2018) A simple function for full-subsets multiple regression in ecology with R. Ecol Evol 8:6104–6113
Froese R, Pauly D (2012) FishBase. http://www.fishbase.org
Goreau T, McClanahan T, Hayes R, Strong A (2000) Conservation of coral reefs after the 1998 global bleaching event. Conserv Biol 14:5–15
Graham NA, Wilson SK, Jennings S, Polunin NV, Bijoux JP, Robinson J (2006) Dynamic fragility of oceanic coral reef ecosystems. Proc Natl Acad Sci 103:8425–8429
Graham NAJ, Jennings S, MacNeil MA, Mouillot D, Wilson SK (2015) Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518:94–97
Graham NAJ, Nash KL (2013) The importance of structural complexity in coral reef ecosystems. Coral Reefs 32:315–326
Graham NAJ, Wilson SK, Jennings S, Polunin NVC, Robinson J, Bijoux JP, Daw TM (2007) Lag effects in the impacts of mass coral bleaching on coral reef fish, fisheries, and ecosystems. Conserv Biol 21:1291–1300
Greenstein BJ, Curran HA, Pandolfi JM (1998) Shifting ecological baselines and the demise of Acropora cervicornis in the western North Atlantic and Caribbean Province: a Pleistocene perspective. Coral Reefs 17:249–261
Hempson TN, Graham NAJ, MacNeil MA, Hoey AS, Wilson SK (2018) Ecosystem regime shifts disrupt trophic structure. Ecol Appl 28:191–200
Hoey A, Howells E, Johansen J, Hobbs J-P, Messmer V, McCowan D, Wilson S, Pratchett M (2016) Recent advances in understanding the effects of climate change on coral reefs. Diversity 8:12
Holbrook SJ, Brooks AJ, Schmitt RJ (2002a) Variation in structural attributes of patch-forming corals and in patterns of abundance of associated fishes. Mar Freshw Res 53:1045–1053
Holbrook SJ, Brooks AJ, Schmitt RJ (2002b) Predictability of fish assemblages on coral patch reefs. Mar Freshw Res 53:181–188
Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83
Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377
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 Biol Sci 284:20162533
Jennings S, Marshall SS, Polunin NVC (1996) Seychelles’ marine protected areas: comparative structure and status of reef fish communities. Biol Conserv 75:201–209
Kerry JT, Bellwood DR (2015) Do tabular corals constitute keystone structures for fishes on coral reefs? Coral Reefs 34:41–50
Komyakova V, Jones GP, Munday PL (2018) Strong effects of coral species on the diversity and structure of reef fish communities: A multi-scale analysis. PLoS ONE 13:e0202206
Manning AD, Fischer J, Lindenmayer DB (2006) Scattered trees are keystone structures–implications for conservation. Biol Conserv 132:311–321
McClanahan TR, Ateweberhan M, Graham NAJ, Wilson SK, Sebastian CR, Guillaume MM, Bruggemann JH (2007) Western Indian Ocean coral communities: bleaching responses and susceptibility to extinction. Mar Ecol Prog Ser 337:1–13
Mellin C, MacNeil MA, Cheal AJ, Emslie MJ, Julian Caley M (2016) Marine protected areas increase resilience among coral reef communities. Ecol Lett 19:629–637
Menge BA, Berlow EL, Blanchette CA, Navarrete SA, Yamada SB (1994) The keystone species concept: variation in interaction strength in a rocky intertidal habitat. Ecol Monogr 64:249–286
Moberg F, Folke C (1999) Ecological goods and services of coral reef ecosystems. Ecol Econ 29:215–233
Moore JAY, Bellchambers LM, Depczynski MR, Evans RD, Evans SN, Field SN, Friedman KJ, Gilmour JP, Holmes TH, Middlebrook R, Radford BT, Ridgway T, Shedrawi G, Taylor H, Thomson DP, Wilson SK (2012) Unprecedented mass bleaching and loss of coral across 12° of latitude in Western Australia in 2010–11. PLoS ONE 7:e51807
Perry CT, Alvarez-Filip L, Graham NA, Mumby PJ, Wilson SK, Kench PS, Manzello DP, Morgan KM, Slangen AB, Thomson DP (2018) Loss of coral reef growth capacity to track future increases in sea level. Nature 558:396–400
Perry CT, Murphy GN, Graham NAJ, Wilson SK, Januchowski-Hartley FA, East HK (2015) Remote coral reefs can sustain high growth potential and may match future sea-level trends. Sci Rep 5:18289
Polunin NVC, Roberts CM (1993) Greater biomass and value of target coral-reef fishes in two small Caribbean marine reserves. Mar Ecol-Prog Ser 100:167–167
Pratchett M, Anderson K, Hoogenboom M, Widman E, Baird A, Pandolfi J, Edmunds P, Lough J (2015) Spatial, temporal and taxonomic variation in coral growth- implications for the structure and function of coral reef ecosystems. Oceanogr Mar Biol Annu Rev 53:215–296
Pratchett MS, Hoey AS, Wilson SK (2014) Reef degradation and the loss of critical ecosystem goods and services provided by coral reef fishes. Curr Opin Environ Sustain 7:37–43
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 46:251–296
Renema W, Pandolfi JM, Kiessling W, Bosellini FR, Klaus JS, Korpanty C, Rosen BR, Santodomingo N, Wallace CC, Webster JM (2016) Are coral reefs victims of their own past success? Sci Adv 2:e1500850
Robinson JPW, Wilson SK, Robinson J, Gerry C, Lucas J, Assan C, Govinden R, Jennings S, Graham NAJ (2019) Productive instability of coral reef fisheries after climate-driven regime shifts. Nat Ecol Evol 3:13–190
Robinson JPW, Wilson SK, Graham NAJ (In review) Abiotic and biotic controls on coral recovery 16 years after mass bleaching. Coral Reefs CORE-D-18-00197R1
Roff G, Clark TR, Reymond CE, Zhao J, Feng Y, McCook LJ, Done TJ, Pandolfi JM (2013) Palaeoecological evidence of a historical collapse of corals at Pelorus Island, inshore Great Barrier Reef, following European settlement. Proc R Soc B 280:20122100
Shedrawi G, Falter JL, Friedman KJ, Lowe RJ, Pratchett MS, Simpson CJ, Speed CW, Wilson SK, Zhang Z (2017) Localised hydrodynamics influence vulnerability of coral communities to environmental disturbances. Coral Reefs 36:861–872
Stella JS, Pratchett MS, Hutchings PA, Jones GP (2011) Coral associated invertebrates: Diversity, ecological importance and vulnerability to disturbance. Oceanogr Mar Biol Annu Rev 49:43–82
Tews J, Brose U, Grimm V, Tielbörger K, Wichmann MC, Schwager M, Jeltsch F (2004) Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J Biogeogr 31:79–92
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 434:67–76
Veron JEN (1986) Corals of Australia and the Indo-pacific. Angus & Robertson, Sydney
Wen CKC, Pratchett MS, Almany GR, Jones GP (2013) Patterns of recruitment and microhabitat associations for three predatory coral reef fishes on the southern Great Barrier Reef, Australia. Coral Reefs 32:389–398
Wilson SK, Fisher R, Pratchett MS, Graham NAJ, Dulvy NK, Turner RA, Cakacaka A, Polunin NVC, Rushton SP (2008) Exploitation and habitat degradation as agents of change within coral reef fish communities. Glob Change Biol 14:2796–2809
Wilson SK, Graham NAJ, Fisher R, Robinson J, Nash K, Chong-Seng K, 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
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
Wilson SK, Graham NAJ, Pratchett MS, Jones GP, Polunin NVC (2006) Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient? Glob Change Biol 12:2220–2234
Wood SN (2017) Generalized additive models: an introduction with R. Chapman and Hall/CRC, London
Wooldridge SA (2016) Excess seawater nutrients, enlarged algal symbiont densities and bleaching sensitive reef locations: 1. Identifying thresholds of concern for the Great Barrier Reef, Australia. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2016.04.054
Acknowledgements
We thank Seychelles Fishing Authority, Seychelles Marine Parks Authority, Nature Seychelles and Global Vision International for field assistance. The project was funded via grants from the Leverhulme Trust, Australian Research Council and the Royal Society. Data on coral and fish assemblages in 1994 were collected and kindly provided by Simon Jennings. Rebecca Fisher provided statistical advice.
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Wilson, S.K., Robinson, J.P.W., Chong-Seng, K. et al. Boom and bust of keystone structure on coral reefs. Coral Reefs 38, 625–635 (2019). https://doi.org/10.1007/s00338-019-01818-4
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DOI: https://doi.org/10.1007/s00338-019-01818-4