Abstract
Knowing the responses of high-latitude corals to thermal impacts will be critical to predicting the possibility for range expansion of reefs provoked by climate change. We, therefore, tested how oceanographic and island geography variation and subsequent interactions between chronic and acute environmental stresses would influence the temperate corals of Mauritius (~ 20°S). Specifically, we predicted higher impacts of thermal stress due to rare events on ocean-impacted windward than leeward reefs. To test this prediction, surveys of benthic cover and corals in the shallow lagoon’s perimeter reefs were repeated between 2004 and 2019—an interval with frequent warm thermal anomalies. Hard and soft coral cover declined 40% and 83%, respectively, and erect algae increased 78% over the 15-yr interval. Coral taxa were distributed along a Montipora-community axis dominant on the island’s leeward reefs and an Acropora-axis dominant on the windward reefs. Nine of the 30 originally encountered sub-genera were not observed in the second sampling, of which most losses were on the windward reefs and among taxa that were initially uncommon during the initial 2004 sampling. The largest declines occurred in the southeast where rare acute stress was higher and open-ocean conditions interacted strongly with the island. The north and western corals experienced less acute stress and greater persistence of taxa. Searching an additional 15 sites in 2019 found six of the missing coral taxa, often in deeper reef edges. Screening of potential environmental variables indicated that that skewness of the degree heating weeks and thermal stress anomalies were the strongest predictor of the changes. A chronic stress metric was more difficult to identify but water flow variability and chlorophyll-a concentrations were part of the oceanographic conditions associated with attenuated responses to acute stress. Frequent acute stress was associated with lower thermal acclimation rates over the 15-yr interval and more evident for the dominant than subdominant taxa. The extra-equatorial location of Mauritius will not ensure latitudinal sanctuary, apart from the leeward reefs.
Similar content being viewed by others
References
Abram NJ, Wright NM, Ellis B, Dixon BC, Wurtzel JB, England MH, Ummenhofer CC, Philibosian B, Cahyarini SY, Yu T-L, Shen C-C, Cheng H, Edwards L, Heslop D (2020) Coupling of Indo-Pacific climate variability over the last millennium. Nature 579:385
Anthony KRN, Hoogenboom MO, Maynard JA, Grottoli AG, Middlebrook R (2009) Energetics approach to predicting mortality risk from environmental stress: A case study of coral bleaching. Funct Ecol 23:539–550
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
Ateweberhan M, McClanahan TR, Graham NAJ, Sheppard CRC (2011) Episodic heterogeneous decline and recovery of coral cover in the Indian Ocean. Coral Reefs 30:739–752
Baker DM, Andras JP, Jordán-Garza AG, Fogel ML (2013) Nitrate competition in a coral symbiosis varies with temperature among Symbiodinium clades. The ISME Journal 7:1248–1251
Benkwitt CE, Wilson SK, Graham NAJ (2020) Biodiversity increases ecosystem functions despite multiple stressors on coral reefs. Nature Ecology & Evolution:1–8
Beyer HL, Kennedy EV, Beger M, Chen CA, Cinner JE, Darling ES, Eakin CM, Gates RD, Heron SF, Knowlton N, Obura DO (2018) Risk-sensitive planning for conserving coral reefs under rapid climate change. Conservation Letters 11:e12587
Bhagooli R, Ramah S, Kaullysing D, Mattan-Moorgawa S, Taleb-Hossenkhan N, Gopeechund A, Soondur M, Flot J-F (2017) Field observation of five Stylophora pistillata-like morphotypes near Mauritius Island. Western Indian Ocean Journal of Marine Science:67–69
Bonjean F, Lagerloef GS (2002) Diagnostic model and analysis of the surface currents in the tropical Pacific Ocean. J Phys Oceanogr 32:2938–2954
Bruno JF, Valdivia A (2016) Coral reef degradation is not correlated with local human population density. Scientific Reports 6:29778
Buddemeier RW, Baker AC, Fautin DG, Jacobs JR (2004) The adaptive hypothesis of bleaching. In: Rosenberg E, Loya Y (eds) Coral Health and Disease. Springer, Berlin Heidelberg, pp 427–444
Burnham KP, Anderson DR (1998) Model Selection and Multimodel Inference: A Practical Information-theoretic Approach. Springer, New York
Cacciapaglia C, van Woesik R (2018) Marine species distribution modelling and the effects of genetic isolation under climate change. J Biogeogr 45:154–163
Côté IM, Darling ES (2010) Rethinking ecosystem resilience in the face of climate change. PLoS Biol 8:e1000438
Couce E, Ridgwell A, Hendy EJ (2013) Future habitat suitability for coral reef ecosystems under global warming and ocean acidification. Glob Change Biol 19:3592–3606
Couch CS, Burns JH, Liu G, Steward K, Gutlay TN, Kenyon J, Eakin CM, Kosaki RK (2017) Mass coral bleaching due to unprecedented marine heatwave in Papahānaumokuākea Marine National Monument (Northwestern Hawaiian Islands). PLoS ONE 12:e0185121
Crawley MJ (2012) The R book. John Wiley & Sons, New York
Cunning R, Gillette P, Capo T, Galvez K, Baker AC (2015) Growth tradeoffs associated with thermotolerant symbionts in the coral Pocillopora damicornis are lost in warmer oceans. Coral Reefs 34:155–160
D’Angelo C, Wiedenmann J (2014) Impacts of nutrient enrichment on coral reefs: new perspectives and implications for coastal management and reef survival. Current Opinion in Environmental Sustainability 7:82–93
Darling ES, McClanahan TR, Maina J, Gurney GG, Graham NA, Januchowski-Hartley F, Cinner JE, Mora C, Hicks CC, Maire E, Puotinen M (2019) Social–environmental drivers inform strategic management of coral reefs in the Anthropocene. Nature Ecology & Evolution 3:1341–1350
Donner SD, Rickbeil GJ, Heron SF (2017) A new, high-resolution global mass coral bleaching database. PLoS ONE 12:e0175490
Eakin CM, Morgan JA, Heron SF, Smith TB, Liu G, Alvarez-Filip L, Baca B, Bartels E, Bastidas C, Bouchon C (2010) Caribbean corals in crisis: Record thermal stress, bleaching, and mortality in 2005. PLoS ONE 5:e13969
Elliott JA, Patterson MR, Staub CG, Koonjul M, Elliott SM (2018) Decline in coral cover and flattening of the reefs around Mauritius (1998–2010). PeerJ 6:e6014
Freeman LA, Kleypas JA, Miller AJ (2013) Coral reef habitat response to climate change scenarios. PLoS ONE 8:e82404
Glynn P, D’croz L (1990) Experimental evidence for high temperature stress as the cause of El Niño-coincident coral mortality. Coral Reefs 8:181–191
Golbuu Y, Victor S, Penland L, Idip D Jr, Emaurois C, Okaji K, Yukihira H, Iwase A, Van Woesik R (2007) Palau’s coral reefs show differential habitat recovery following the 1998-bleaching event. Coral Reefs 26:319–332
Gove JM, McManus MA, Neuheimer AB, Polovina JJ, Drazen JC, Smith CR, Merrifield MA, Friedlander AM, Ehses JS, Young CW, Dillon AK (2016) Near-island biological hotspots in barren ocean basins. Nature Communications 7:10581
Greenstein BJ, Pandolfi JM (2008) Escaping the heat: Range shifts of reef coral taxa in coastal Western Australia. Glob Change Biol 14:513–528
Guest JR, Low J, Tun K, Wilson B, Ng C, Raingeard D, Ulstrup KE, Tanzil JTI, Todd PA, Toh TC, McDougald D, Chou LM, Steinberg PD (2016) Coral community response to bleaching on a highly disturbed reef. Scientific Reports 6:20717
Heron SF, Maynard JA, Van Hooidonk R, Eakin CM (2016) Warming trends and bleaching stress of the world’s coral reefs 1985–2012. Scientific Reports 6:38402
Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B (2005) Effects of biodiversity on ecosystem functioning: A consensus of current knowledge. Ecol Monogr 75:3–35
Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83
Hughes TP, Kerry JT, Connolly SR, Baird AH, Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Jacobson M, Liu G, Pratchett MS, Skirving W, Torda G (2019) Ecological memory modifies the cumulative impact of recurrent climate extremes. Nature Climate Change 9:40–43
Lee ST, Keshavmurthy S, Fontana S, Takuma M, Chou WH, Chen CA (2018) Transcriptomic response in Acropora muricata under acute temperature stress follows preconditioned seasonal temperature fluctuations. BMC Research Notes 11:119–117
Liu G, Heron SF, Eakin CM, Muller-Karger FE, Vega-Rodriguez M, Guild LS, De La Cour JL, Geiger EF, Skirving WJ, Burgess TFR, Strong AE, Harris A, Maturi E, Ignatove A, Sapper J, Li J, Lynds S (2014) Reef-scale thermal stress monitoring of coral ecosystems: New 5-km global products from NOAA coral reef watch. Remote Sensing 6:11579–11606
Louis YD, Kaullysing D, Gopeechund A, Mattan-Moorgawa S, Bahorun T, Dyall SD, Bhagooli R (2016) In hospite Symbiodinium photophysiology and antioxidant responses in Acropora muricata on a coast-reef scale: implications for variable bleaching patterns. Symbiosis 68:61–72
Madin JS, Allen AP, Baird AH, Pandolfi JM, Sommer B (2016) Scope for latitudinal extension of reef corals is species specific. Frontiers of Biogeography 8:1–4
Maina J, Venus V, McClanahan TR, Ateweberhan M (2008) Modelling susceptibility of coral reefs to environmental stress using remote sensing data and GIS models in the western Indian Ocean. Ecol Model 212:180–199
Makino A, Yamano H, Beger M, Klein CJ, Yara Y, Possingham HP (2014) Spatio-temporal marine conservation planning to support high-latitude coral range expansion under climate change. Divers Distrib 20:859–871
McClanahan TR (2004) The relationship between bleaching and mortality of common corals. Mar Biol 144:1239–1245
McClanahan TR (2014) Decadal coral community reassembly on an African fringing reef. Coral Reefs 33:939–950
McClanahan TR (2017) Changes in coral sensitivity to thermal anomalies. Mar Ecol Prog Ser 570:71–85
McClanahan TR (2020a) Coral community life histories and population dynamics driven by seascape bathymetry and temperature variability. In: Reigl B (ed) Population Dynamics Of The Reef Crisis. Elsevier Science and Technology, in press.
McClanahan TR (2020b) Decadal turnover of thermally stressed coral taxa support a risk-spreading approach to marine reserve design. Coral Reefs. https://doi.org/10.1007/s00338-020-01984-w
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
McClanahan TR, Muthiga NA (2014) Community change and evidence for variable warm-water temperature adaptation of corals in Northern Male Atoll, Maldives. Mar Pollut Bull 80:107–113
McClanahan TR, Muthiga NA (2016) Similar impacts of fishing and environmental stress on calcifying organisms in Indian Ocean coral reefs. Mar Ecol Prog Ser 560:87–103
McClanahan TR, Obura D (1997) Sedimentation effects on shallow coral communities in Kenya. Journal of Experimetal Marine Biology and Ecology 209:103–122
McClanahan TR, Muthiga NA, 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
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
McClanahan TR, Ateweberhan M, Muhando CA, Maina J, Mohammed SM (2007) Effects of climate and seawater temperature variation on coral bleaching and mortality. Ecol Monogr 77:503–525
McClanahan TR, Maina JM, Muthiga NA (2011) Associations between climate stress and coral reef diversity in the Western Indian Ocean. Glob Change Biol 17:2023–2032
McClanahan TR, Donner SD, Maynard JA, MacNeil MA, Graham NA, Maina J, Baker AC, Beger M, Campbell SJ, Darling ES, Eakin CM (2012) Prioritizing key resilience indicators to support coral reef management in a changing climate. PLoS ONE 7:e42884
McClanahan TR, Ateweberhan M, Darling ES, Graham NAJ, Muthiga NA (2014) Biogeography and change among regional coral communities across the Western Indian Ocean. PLoS ONE 9:e93385
McClanahan TR, Maina J, Ateweberhan M (2015) Regional coral responses to climate disturbances and warming is predicted by multivariate stress model and not temperature threshold metrics. Climatic Change 131:607–620
McClanahan TR, Darling ES, Maina JM, Muthiga NA, D’agata S, Arthur R, Jupiter S, Wilson SK, Mangubhai S, Leblonde J, Muttaqin E, Pardede S, Nand Y, Ussi AM, Humphries AT, Patankar VJ, Guillaume MMM, Keith SA, Shedrawi G, Pagu J, Grimsditch G (2019) Temperature patterns and mechanisms influencing coral bleaching during the 2016 El Niño. Nature Climate Change. https://doi.org/10.1038/s41558-019-0576-8
McClanahan TR, Schroeder RE, Friedlander AM, Vigliola L, Wantiez L, Caselle JE, Graham NAJ, Wilson S, Edgar GJ, Stuart-Smith RD, Oddenyo RM, Cinner JC (2019) Global baselines and benchmarks for fish biomass: Comparing remote and fisheries closures. Mar Ecol Prog Ser 612:167–192
McLean M, Cuetos-Bueno J, Nedlic O, Luckymiss M, Houk P (2017) Local stressors, resilience, and shifting baselines on coral reefs. PLoS ONE 11:e0166319
Mollica NR, Cohen AL, Alpert AE, Barkley HC, Brainard RE, Carilli JE, DeCarlo TM, Drenkard EJ, Lohmann P, Mangubhai S, Pietro KR (2019) Skeletal records of bleaching reveal different thermal thresholds of Pacific coral reef assemblages. Coral Reefs
Nakamura T, Van Woesik R (2001) Water-flow rates and passive diffusion partially explain differential survival of corals during the 1998 bleaching event. Mar Ecol Prog Ser 212:301–304
Nakamura N, Kayanne H, Iijima H, McClanahan TR, Behera SK, Yamagata T (2011) Footprints of IOD and ENSO in the Kenyan coral record. Geophys Res Lett 38:L24708
Obura D, Gudka M, Abdou Rabi F, Bacha Gian S, Bijoux J, Freed S, Maharavo J, Mwaura J, Porter S, Sola E, Wickel J (2017) Coral reef status report for the western Indian Ocean. Global coral reef monitoring network (GCRMN)/international coral reef initiative (ICRI). In: Obura D, Gudka M, Rabi FB, Gian SB, Bijoux J, Sarah Freed, Maharavo J, Mwaura J, Porter S, Sola E, Wickel J, Yahya S, Ahamada S (eds). CORDIO East Africa
Palumbi SR, Barshis DJ, Traylor-Knowles N, Bay RA (2014) Mechanisms of reef coral resistance to future climate change. Science 344:895–898
Pillay RM, Terashima H, Kawasaki H (2002) The extent and intensity of the 1998 mass bleaching event on the reefs of Mauritius, Indian Ocean. Galaxea 4:43–52
Pillay RM, Terashima H, Venkatasami AA, Uchida H (2002) Field Guide to Corals of Mauritius. Albion Fisheries Research Centre, Albion, Petite Riviere, Mauritius
Pous S, Lazure P, André G, Dumas F, Halo I, Penven P (2014) Circulation around La Réunion and Mauritius islands in the south-western Indian Ocean: A modeling perspective. Journal of Geophysical Research: Oceans 119:1957–1976
Precht WF, Aronson RB (2004) Climate flickers and range shifts of reef corals. Frontiers in Ecology and Environment 2:307–314
Randall CJ, Toth LT, Leichter JJ, Maté JL, Aronson RB (2019) Upwelling buffers climate change impacts on coral reefs of the eastern tropical Pacific. Ecology. https://doi.org/10.1002/ecy.2918
Riegl BM, Sheppard CRC, Purkis SJ (2012) Human impact on atolls leads to coral loss and community homogenization: A modeling study. PLoS ONE 7:e36921
Roberts CM, McClean CJ, Veron JEN, Hawkins JP, Allen GR, McAllister DE, Mittermeier CG, Schueler FW, Spalding M, Wells F, Vynne C, Werner TB (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295:1280–1284
Safaie A, Silbiger NJ, McClanahan TR, Pawlak G, Barshis DJ, Hench JL, Rogers JS, Williams GJ, Davis KA (2018) High frequency temperature variability reduces the risk of coral bleaching. Nature Communications 9:2244
Sully S, Burkepile DE, Donovan MK, Hodgson G, van Woesik R (2019) A global analysis of coral bleaching over the past two decades. Nature Communications 10:1–5
Tanner JE (1995) Competition between scleractinian corals and macroalgae: An experimental investigation of coral growth, survival and reproduction. J Exp Mar Biol Ecol 190:151–168
Tkachenko KS, Soong K (2017) Dongsha Atoll: A potential thermal refuge for reef-building corals in the South China Sea. Marine Environmental Research 127:112–125
Van Hooidonk R, Maynard J, Tamelander J, Gove J, Ahmadia G, Raymundo L, Williams G, Heron SF, Planes S (2016) Local-scale projections of coral reef futures and implications of the Paris Agreement. Scientific Reports 6:39666
Venegas RM, Oliver T, Liu G, Heron SF, Clark SJ, Pomeroy N, Young C, Eakin CM, Brainard RE (2019) The Rarity of Depth Refugia from Coral Bleaching Heat Stress in the Western and Central Pacific Islands. Scientific Reports 9:1–12
Walker ND (1989) Sea surface temperature-rainfall relationships and associated ocean-atmosphere coupling mechanisms in the southern African region. University of Cape Town,
Wang B, Luo X, Yang YM, Sun W, Cane MA, Cai W, Yeh SW, Liu J (2019) Historical change of El Niño properties sheds light on future changes of extreme El Niño. Proc Natl Acad Sci 116:22512–22517
Zinke J, Gilmour JP, Fisher R, Puotinen M, Maina J, Darling E, Stat M, Richards ZT, McClanahan TR, Beger M, Moore C (2018) Gradients of disturbance and environmental conditions shape coral community structure for south-eastern Indian Ocean reefs. Divers Distrib 24:605–620
Acknowledgements
This work was a joint program between the Wildlife Conservation Society, the Ministry of Ocean Economy, Marine Resources, Fisheries and Shipping, Albion Fisheries Research Centre, and Mauritius Oceanography Institute. We are grateful for logistical and field assistance provided by E. Darling, Y. Heermann, J. Maina, V. Munbodhe, R. Moothien-Pillay, C. Samyan. J. Kosgei for producing the figures and tables. The work received financial support from the Tiffany & Co. and the John D. and Catherine T. MacArthur Foundations.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Topic Editor Mark Vermeij
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
McClanahan, T.R., Muthiga, N.A. Oceanic patterns of thermal stress and coral community degradation on the island of Mauritius. Coral Reefs 40, 53–74 (2021). https://doi.org/10.1007/s00338-020-02015-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-020-02015-4