Skip to main content
SpringerLink
Log in

No coral recovery three years after a major bleaching event in reefs in the Southwestern Atlantic refugium

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Mass bleaching events are growing in duration and intensity. Besides causing extensive mortality, the progressively shorter time between events disrupts the ability of reefs to recover. The unique reefs of the Southwestern Atlantic are often considered climate refugia as they have suffered less bleaching-related mortality when compared to Indo–Pacific and Caribbean reefs. However, their recovery capacity still requires investigation. In 2019, an unprecedented heatwave triggered the most severe bleaching episode recorded for Southwestern Atlantic reefs. Therefore, this study aimed to (i) document the bleaching incidence and mortality during the heatwave, and (ii) assess coral recovery over 3 years. We measured bleaching incidence and monitored coral cover through surveys in three Southern Bahia (central Brazilian coast) reefs before, during and after thermal stress. Our findings show that coral assemblages were exposed to a 5-month-long thermal anomaly, experiencing thermal stress peaking at 14.1 ºC-weeks. Roughly 70% of the coral cover was bleached, resulting in a decline of ~ 40%. Millepora alcicornis, Mussismilia braziliensis, and Mussismilia harttii were among species that mortality exceeded 50%. After 3 years, corals showed no increase in cover neither at assemblage nor species levels. This constrained recovery capacity may indicate the breakdown of the refugium, and also trade-off for resistance. Typical features of the region, such as high turbidity and the dominance of massive corals, provide these reefs with bleaching resistance, but likely also limit their recovery. With the anticipated effects of the 2023–24 El Niño–Southern Oscillation in the southern hemisphere, still unrecovered Southwestern Atlantic reefs face a substantial challenge.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The data generated and analyzed during this study are available at the Supplementary Material. Raw data may be supplied by the corresponding author upon request.

References

  • Abesamis MR, Ang JL, Robles RC, Licuanan WY (2023) Recovery of coral cover on inshore fringing reefs following mass coral bleaching in the Philippines. Coral Reefs 42:99–104

    Article  Google Scholar 

  • Adjeroud M, Michonneau F, Edmunds PJ, Chancerelle Y, De Loma TL, Penin L, Thibaut L, Vidal-Dupiol J, Salvat B, Galzin R (2009) Recurrent disturbances, recovery trajectories, and resilience of coral assemblages on a South Central Pacific reef. Coral Reefs 28:775–780

    Article  Google Scholar 

  • Angonese MS, Faria SC, Bianchini A (2022) Is citrate synthase an energy biomarker in Southwestern Atlantic corals? a comparative, biochemical approach under a simulated scenario of climate change. Coral Reefs 41:213–222

    Article  Google Scholar 

  • Anthony KR, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Biol Ecol 252:221–253

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Banha TNS, Capel KCC, Kitahara MV, Francini-Filho RB, Francini CLB, Sumida PYG, Mies M (2020) Low coral mortality during the most intense bleaching event ever recorded in subtropical Southwestern Atlantic reefs. Coral Reefs 39:515–521

    Article  Google Scholar 

  • Barley JM, Cheng BS, Sasaki M, Gignoux-Wolfsohn S, Hays CG, Putnam AB, Sheth S, Villeneuve AR, Kelly M (2021) Limited plasticity in thermally tolerant ectotherm populations: evidence for a trade-off. Proceedings of the Royal Society B: Biological Sciences 288:20210765

    Article  PubMed Central  Google Scholar 

  • Bessell-Browne P, Negri AP, Fisher R, Clode PL, Duckworth A, Jones R (2017) Impacts of turbidity on corals: the relative importance of light limitation and suspended sediments. Mar Pollut Bull 117:161–170

    Article  CAS  PubMed  Google Scholar 

  • Bleuel J, Pennino MG, Longo GO (2021) Coral distribution and bleaching vulnerability areas in Southwestern Atlantic under ocean warming. Sci Rep 11:12833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Braz GB, Lacerda CHF, Evangelista H, Güth AZ, Rumbelsperger AMB, Capel KCC, Dall’Occo PL, Mies M (2022) Unprecedented erosion of Mussismilia harttii, a major reef-building species in the Southwestern Atlantic, after the 2019 bleaching event. Coral Reefs 41:1537–1548

    Article  Google Scholar 

  • Brown KT, Barott KL (2022) The costs and benefits of environmental memory for reef-building corals coping with recurring marine heatwaves. Integr Comp Biol 62:1748–1755

    Article  PubMed  Google Scholar 

  • Cacciapaglia C, van Woesik R (2016) Climate-change refugia: shading reef corals by turbidity. Glob Change Biol 22:1145–1154

    Article  Google Scholar 

  • Castro CB, Pires DO (1999) A bleaching event on a Brazilian coral reef. Rev Bras Oceanogr 47:87–90

    Article  Google Scholar 

  • Castro CB, Pires DO (2001) Brazilian coral reefs: what we already know and what is still missing. Bull Mar Sci 69:357–371

    Google Scholar 

  • Cheng L, Abraham J, Zhu J, Trenberth KE, Fasullo J, Boyer T, Locarnini R, Zhang B, Yu F, Wan L, Chen X (2020) Record-setting ocean warmth continued in 2019. Adv Atmos Sci 37:137–142

    Article  Google Scholar 

  • Coni EO, Ferreira CM, Moura RL, Meirelles PM, Kaufman L, Francini-Filho RB (2013) An evaluation of the use of branching fire-corals (Millepora spp.) as refuge by reef fish in the abrolhos bank, eastern Brazil. Environ Biol Fishes 96:45–55

    Article  Google Scholar 

  • Connell JH (1997) Disturbance and recovery of coral assemblages. Coral Reefs 16:S101–S113

    Article  Google Scholar 

  • Connell JH, Hughes TP, Wallace CC (1997) A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecol Monogr 67:461–488

    Article  Google Scholar 

  • Costa OS Jr, Nimmo M, Attrill MJ (2008) Coastal nutrification in Brazil: a review of the role of nutrient excess on coral reef demise. J S Am Earth Sci 25:257–270

    Article  Google Scholar 

  • Darling ES, Graham NA, 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

    Article  Google Scholar 

  • De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27-year decline of coral cover on the great barrier reef and its causes. Proceedings of the National Academy of Sciences USA 109:17995–17999

    Article  Google Scholar 

  • DeCarlo TM (2020) Treating coral bleaching as weather: a framework to validate and optimize prediction skill. PeerJ 8:e9449

    Article  PubMed  PubMed Central  Google Scholar 

  • DeCarlo TM, Harrison HB, Gajdzik L, Alaguarda D, Rodolfo-Metalpa R, D’Olivo J, Liu G, Patalwala D, McCulloch MT (2019) Acclimatization of massive reef-building corals to consecutive heatwaves. Proceedings of the Royal Society B: Biological Sciences 286:20190235

    Article  PubMed Central  Google Scholar 

  • DeYoung B, Barange M, Beaugrand G, Harris R, Perry RI, Scheffer M, Werner F (2008) Regime shifts in marine ecosystems: detection, prediction and management. Trends Ecol Evol 23:402–409

    Article  PubMed  Google Scholar 

  • Dietzel A, Bode M, Connolly SR, Hughes TP (2020) Long-term shifts in the colony size structure of coral populations along the great barrier reef. Proceedings of the Royal Society B: Biological Sciences 287:20201432

    Article  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Douglas AE (2003) Coral bleaching––how and why? Mar Pollut Bull 46:385–392

    Article  CAS  PubMed  Google Scholar 

  • Duarte GAS, Villela HDM, Deocleciano M, Silva D, Barno A, Cardoso PM, Vilela CLS, Rosado P, Messias CSMA, Chacon MA, Santoro EP, Olmedo DB, Szpilman M, Rocha LA, Sweet M, Peixoto RS (2020) Heat waves are a major threat to turbid coral reefs in Brazil. Front Mar Sci 7:179

    Article  Google Scholar 

  • Eakin CM, Morgan JA, Heron SF, Smith TB, Liu G, Alvarez-Filip L, Baca B, Bartels E, Bastidas C, Bouchon C, Brandt M et al (2010) Caribbean corals in crisis: record thermal stress, bleaching, and mortality in 2005. PLoS ONE 5:e13969

    Article  PubMed  PubMed Central  Google Scholar 

  • Eakin CM, Liu G, Gomez AM, De La Cour JL, Heron SF, Skirving WJ, Geiger EF, Tirak KV, Strong AE (2016) Global coral bleaching 2014–2017: status and an appeal for observations. Reef Encounter 31:20–26

    Google Scholar 

  • Edmunds PJ, Elahi R (2007) The demographics of a 15-year decline in cover of the caribbean reef coral montastraea annularis. Ecol Monogr 77:3–18

    Article  Google Scholar 

  • Elliff CI, Kikuchi RK (2017) Ecosystem services provided by coral reefs in a southwestern atlantic archipelago. Ocean Coast Manag 136:49–55

    Article  Google Scholar 

  • Ferreira BP, Costa MB, Coxey MS, Gaspar AL, Veleda D, Araújo M (2013) The effects of sea surface temperature anomalies on oceanic coral reef systems in the southwestern tropical Atlantic. Coral Reefs 32:441–454

    Article  Google Scholar 

  • Ferreira LC, Grillo AC, Repinaldo Filho FP, Souza FN, Longo GO (2021) Different responses of massive and branching corals to a major heatwave at the largest and richest reef complex in South Atlantic. Mar Biol 168:54

    Article  CAS  Google Scholar 

  • Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65

    Article  Google Scholar 

  • Floeter SR, Rocha LA, Robertson DR, Joyeux JC, Smith-Vaniz WF, Wirtz P, Edwards AJ, Barreiros JP, Ferreira CEL, Gasparini JL, Brito A, Falcón JM, Bowen BW, Bernardi G (2008) Atlantic reef fish biogeography and evolution. J Biogeogr 35:22–47

    Article  Google Scholar 

  • Fonseca JS, Mies M, Paranhos A, Taniguchi S, Güth AZ, Bícego MC, Marques JA, Marangoni LFB, Bianchini A (2021) Isolated and combined effects of thermal stress and copper exposure on the trophic behavior and oxidative status of the reef-building coral Mussismilia harttii. Environ Pollut 268:115892

    Article  Google Scholar 

  • Francini Filho RB, Moura RL (2008) Dynamics of fish assemblages on coral reefs subjected to different management regimes in the abrolhos bank, eastern Brazil. Aquat Conserv Mar Freshwat Ecosyst 18:1166–1179

    Article  Google Scholar 

  • Francini-Filho RB, Coni EO, Meirelles PM, Amado-Filho GM, Thompson FL, Pereira-Filho GH, Bastos AC, Abrantes DP, Ferreira CM, Gibran FZ, Güth AZ et al (2013) Dynamics of coral reef benthic assemblages of the abrolhos bank, eastern Brazil: inferences on natural and anthropogenic drivers. PLoS ONE 8:e54260

    Article  CAS  PubMed  PubMed Central  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 

  • Garrido AG, Machado LF, Pereira CM, Abrantes DP, Calderon EN, Zilberberg C (2023) Marine heatwave caused differentiated dysbiosis in photosymbiont assemblages of corals and hydrocorals during el niño 2015/2016. Microb Ecol 86:2959–2969

    Article  PubMed  Google Scholar 

  • Gaspar TL, Quimbayo JP, Ozekoski R, Nunes LT, Aued AW, Mendes TC, Garrido AG, Segal B (2021) Severe coral bleaching of Siderastrea stellata at the only atoll in the South Atlantic driven by sequential marine heatwaves. Biota Neotrop 21:e20201131

    Article  Google Scholar 

  • Gates RD, Edmunds PJ (1999) The physiological mechanisms of acclimatization in tropical reef corals. Am Zool 39:30–43

    Article  Google Scholar 

  • Gilmour JP, Smith LD, Heyward AJ, Baird AH, Pratchett MS (2013) Recovery of an isolated coral reef system following severe disturbance. Science 340:69–71

    Article  PubMed  Google Scholar 

  • Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1–17

    Article  Google Scholar 

  • Godoy L, Mies M, Zilberberg C, Pastrana Y, Amaral A, Cruz N, Pereira CM, Garrido AG, Paris A, Santos LF, Pires DO (2021) Southwestern atlantic reef-building corals mussismilia spp. are able to spawn while fully bleached. Mar Biol 168:15

    Article  CAS  Google Scholar 

  • González-Barrios FJ, Cabral-Tena RA, Alvarez-Filip L (2021) Recovery disparity between coral cover and the physical functionality of reefs with impaired coral assemblages. Glob Change Biol 27:640–651

    Article  Google Scholar 

  • Gouezo M, Golbuu Y, Fabricius K, Olsudong D, Mereb G, Nestor V, Wolanski E, Harrison P, Doropoulos C (2019) Drivers of recovery and reassembly of coral reef communities. Proceedings of the Royal Society B: Biological Sciences 286:20182908

    Article  PubMed Central  Google Scholar 

  • Gove JM, Williams GJ, Lecky J, Brown E, Conklin E, Counsell C, Davis G, Donovan MK, Falinski K, Kramer L, Kozar K et al (2023) Coral reefs benefit from reduced land–sea impacts under ocean warming. Nature 621:536–542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graham NA, Nash KL (2013) The importance of structural complexity in coral reef ecosystems. Coral Reefs 32:315–326

    Article  Google Scholar 

  • Graham NA, Nash KL, Kool JT (2011) Coral reef recovery dynamics in a changing world. Coral Reefs 30:283–294

    Article  Google Scholar 

  • Graham NA, Jennings S, MacNeil MA, Mouillot D, Wilson SK (2015) Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518:94–97

    Article  CAS  PubMed  Google Scholar 

  • Hennige SJ, Smith DJ, Perkins R, Consalvey M, Paterson DM, Suggett DJ (2008) Photoacclimation, growth and distribution of massive coral species in clear and turbid waters. Mar Ecol Prog Ser 369:77–88

    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

    Google Scholar 

  • 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 17:360–365

    Article  CAS  PubMed  Google Scholar 

  • 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 359:80–83

    Article  CAS  PubMed  Google Scholar 

  • IPCC (2021) Climate Change 2021 The Physical Science Basis. In: Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Péan C, Berger S, Caud N, Chen Y, Goldfarb L, Gomis MI, Huang M, Leitzell K, Lonnoy E, Matthews JBR, Maycock TK, Waterfield T, Yelekçi O, Yu R, Zhou B (eds) Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK and New York, NY, USA, p 2391

    Google Scholar 

  • Jackson JB, Donovan MK, Cramer KL, Lam VV (2014) Status and trends of Caribbean coral reefs. Gland, Switzerland, Global Coral Reef Monitoring Network, IUCN

    Google Scholar 

  • Johns KA, Osborne KO, Logan M (2014) Contrasting rates of coral recovery and reassembly in coral communities on the great barrier reef. Coral Reefs 33:553–563

    Article  Google Scholar 

  • Jones RJ (2008) Coral bleaching, bleaching-induced mortality, and the adaptive significance of the bleaching response. Mar Biol 154:65–80

    Article  Google Scholar 

  • Kayanne H (2017) Validation of degree heating weeks as a coral bleaching index in the northwestern pacific. Coral Reefs 36:63–70

    Article  Google Scholar 

  • Kelmo F, Attrill MJ (2013) Severe impact and subsequent recovery of a coral assemblage following the 1997–8 el niño event: a 17-year study from bahia. Brazil Plos ONE 8:e65073

    Article  CAS  PubMed  Google Scholar 

  • Keppel G, Van Niel KP, Wardell-Johnson GW, Yates CJ, Byrne M, Mucina L, Schut AG, Hopper SD, Franklin SE (2012) Refugia: identifying and understanding safe havens for biodiversity under climate change. Glob Ecol Biogeogr 21:393–404

    Article  Google Scholar 

  • Knowlton N, Jackson JB (2008) Shifting baselines, local impacts, and global change on coral reefs. PLoS Biol 6:e54

    Article  PubMed  PubMed Central  Google Scholar 

  • Krueger T, Hawkins TD, Becker S, Pontasch S, Dove S, Hoegh-Guldberg O, Leggat W, Fisher PL, Davy SK (2015) Differential coral bleaching—contrasting the activity and response of enzymatic antioxidants in symbiotic partners under thermal stress. Comp Biochem Physiol a: Mol Integr Physiol 190:15–25

    Article  CAS  PubMed  Google Scholar 

  • Leão ZMAN, Kikuchi RKP, Testa V (2003) Corals and coral reefs of Brazil. In: Cortés J (ed) Latin American Coral Reefs. Elsevier, Amsterdam, Netherlands, pp 9–52

    Chapter  Google Scholar 

  • Leão ZM, Kikuchi RKP, Oliveira MDM, Vasconcellos V (2010) Status of Eastern Brazilian coral reefs in time of climate changes. Pan-American Journal of Aquatic Sciences 5:224–235

    Google Scholar 

  • Leão ZMAN, Kikuchi RKP, Ferreira BP, Neves EG, Sovierzoski HH, Oliveira MD, Maida M, Correia MD, Johnsson R (2016) Brazilian coral reefs in a period of global change: a synthesis. Braz J Oceanogr 64:97–116

    Article  Google Scholar 

  • Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278

    Article  CAS  PubMed  Google Scholar 

  • Lian T, Wang J, Chen D, Liu T, Wang D (2023) A strong 2023/24 el niño is staged by tropical pacific ocean heat content buildup. Ocean-Land-Atmosphere Research 2:0011

    Article  Google Scholar 

  • Liu G, Heron SF, Eakin CM, Muller-Karger FE, Vega-Rodriguez M, Guild LS, De La Cour JL, Geiger EF, Skirving WJ, Burgess TF, Strong AE, Harris A, Maturi E, Ignatov 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

    Article  Google Scholar 

  • Lonzetti BC, Vieira EA, Longo GO (2022) Ocean warming can help zoanthids outcompete branching hydrocorals. Coral Reefs 41:175–189

    Article  Google Scholar 

  • Lough JM, Barnes DJ (2000) Environmental controls on growth of the massive coral Porites. J Exp Mar Biol Ecol 245:225–243

    Article  CAS  PubMed  Google Scholar 

  • Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131

    Article  Google Scholar 

  • Lucas CC, Lima IC, Garcia TM, Tavares TC, Carneiro PB, Teixeira CE, Bejarano S, Rossi S, Soares MO (2023) Turbidity buffers coral bleaching under extreme wind and rainfall conditions. Mar Environ Res 192:106215

    Article  CAS  PubMed  Google Scholar 

  • Ludescher J, Meng J, Fan J, Bunde A, Schellnhuber HJ (2023) Very early warning of a moderate-to-strong El Niño in 2023. arXiv preprint: 2301.10763.

  • Luza AL, Quimbayo JP, Ferreira CE, Floeter SR, Francini-Filho RB, Bender MG, Longo GO (2022) Low functional vulnerability of fish assemblages to coral loss in Southwestern Atlantic marginal reefs. Sci Rep 12:17164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacNeil MA, Mellin C, Matthews S, Wolff NH, McClanahan TR, Devlin M, Drovandi C, Mengersen K, Graham NA (2019) Water quality mediates resilience on the great barrier reef. Nature Ecology & Evolution 3:620–627

    Article  Google Scholar 

  • Mantiuk R, Mantiuk R, Tomaszewska A, Heidrich W (2009) Color correction for tone mapping. Computer Graphics Forum 28:193–202

    Article  Google Scholar 

  • Marangoni LFB, Mies M, Güth AZ, Banha TNS, Inague A, Fonseca JS, Dalmolin C, Faria SC, Ferrier-Pagès C, Bianchini A (2019) Peroxynitrite generation and increased heterotrophic capacity are linked to the disruption of the coral–dinoflagellate symbiosis in a scleractinian and hydrocoral species. Microorganisms 7:426

    Article  PubMed  PubMed Central  Google Scholar 

  • Marshall PA, Baird AH (2000) Bleaching of corals on the great barrier reef: differential susceptibilities among taxa. Coral Reefs 19:155–163

    Article  Google Scholar 

  • McClanahan TR (2000) Bleaching damage and recovery potential of maldivian coral reefs. Mar Pollut Bull 40:587–597

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Mcleod E, Anthony KR, Mumby PJ, Maynard J, Beeden R, Graham NA, Heron SF, Hoegh-Guldberg O, Jupiter S, MacGowan P, Mangubhai S et al (2019) The future of resilience-based management in coral reef ecosystems. J Environ Manage 233:291–301

    Article  PubMed  Google Scholar 

  • McManus LC, Forrest DL, Tekwa EW, Schindler DE, Colton MA, Webster MM, Essington TE, Palumbi SR, Mumby PJ, Pinsky ML (2021) Evolution and connectivity influence the persistence and recovery of coral reefs under climate change in the Caribbean, southwest pacific, and coral triangle. Glob Change Biol 27:4307–4321

    Article  CAS  Google Scholar 

  • Mies M, Güth AZ, Tenório AA, Banha TNS, Waters LG, Polito PS, Taniguchi S, Bícego MC, Sumida PYG (2018) In situ shifts of predominance between autotrophic and heterotrophic feeding in the reef-building coral Mussismilia hispida: an approach using fatty acid trophic markers. Coral Reefs 37:677–689

    Article  Google Scholar 

  • Mies M, Francini-Filho RB, Zilberberg C, Garrido AG, Longo GO, Laurentino E, Güth AZ, Sumida PYG, Banha TNS (2020) South Atlantic coral reefs are major global warming refugia and less susceptible to bleaching. Front Mar Sci 7:514

    Article  Google Scholar 

  • Miranda RJ, Cruz ICS, Leão ZMAN (2013) Coral bleaching in the caramuanas reef (todos os santos bay, Brazil) during the 2010 el niño event. Lat Am J Aquat Res 41:351–360

    Article  Google Scholar 

  • Morelli TL, Barrows CW, Ramirez AR, Cartwright JM, Ackerly DD, Eaves TD, Ebersole JL, Krawchuk MA, Letcher BH, Mahalovich MF, Meigs GW et al (2020) Climate-change refugia: biodiversity in the slow lane. Front Ecol Environ 2:228–234

    Article  Google Scholar 

  • Moura RL, Amado-Filho GM, Moraes FC, Brasileiro PS, Salomon PS, Mahiques MM, Bastos AC, Almeida MG, Silva JM Jr, Araujo BF, Brito FP, Rangel TP et al (2016) An extensive reef system at the amazon river mouth. Sci Adv 2:e1501252

    Article  PubMed  PubMed Central  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 

  • Mumby PJ, Mason RA, Hock K (2021) Reconnecting reef recovery in a world of coral bleaching. Limnol Oceanogr Methods 19:702–713

    Article  Google Scholar 

  • NOAA Coral Reef Watch (2018) NOAA Coral Reef Watch Version 3.1 Daily Global 5km Satellite Coral Bleaching Degree Heating Week Product. College Park, Maryland, ftp://ftp.star.nesdis.noaa.gov/pub/sod/mecb/crw/data/5km/v3.1/nc/v1.0/daily/dhw/.

  • Nogueira MM, Neves E, Johnsson R (2015) Effects of habitat structure on the epifaunal community in Mussismilia corals: does coral morphology influence the richness and abundance of associated crustacean fauna? Helgol Mar Res 69:221–229

    Article  Google Scholar 

  • Nogueira MM, Neves E, Johnsson R (2021) Effects of habitat structure on the mollusc assemblage in Mussismilia corals: evaluation of the influence of different coral growth morphology. J Mar Biol Assoc UK 101:61–69

    Article  CAS  Google Scholar 

  • Nunes BZ, Soares MD, Zanardi-Lamardo E, Castro ÍB (2023) Marine protected areas affected by the most extensive oil spill on the Southwestern Atlantic coast. Ocean and Coastal Research 71:e23028

    Article  Google Scholar 

  • Oliveira UD, Gomes PB, Cordeiro RTS, Lima GV, Pérez CD (2019) Modeling impacts of climate change on the potential habitat of an endangered Brazilian endemic coral: discussion about deep sea refugia. PLoS ONE 14:e0211171

    Article  PubMed  PubMed Central  Google Scholar 

  • Oliver JK, Berkelmans R, Eakin CM (2018) Coral bleaching in space and time. In: van Oppen MJH, Lough JM (eds) Coral bleaching: patterns, processes, causes and consequences. Springer, Berlin, pp 27–49

    Chapter  Google Scholar 

  • Ortiz JC, Wolff NH, Anthony KR, Devlin M, Lewis S, Mumby PJ (2018) Impaired recovery of the great barrier reef under cumulative stress. Sci Adv 4(7):eaar6127

    Article  PubMed  PubMed Central  Google Scholar 

  • Pereira PHC, Lima GV, Pontes AVF, Côrtes LGF, Gomes E, Sampaio CLS, Pinto TK, Miranda RJ, Cardoso ATC, Araújo JC, Seoane JCS (2022) Unprecedented coral mortality on Southwestern Atlantic (SWA) coral reefs following major thermal stress. Front Mar Sci 9:338

    Article  Google Scholar 

  • Pinheiro HT, Rocha LA, Macieira RM, Carvalho-Filho A, Anderson AB, Bender MG, Di Dario F, Ferreira CEL, Figueiredo-Filho J, Francini-Filho RB et al (2018) South-western atlantic reef fishes: zoogeographical patterns and ecological drivers reveal a secondary biodiversity centre in the atlantic ocean. Divers Distrib 24:951–965

    Article  Google Scholar 

  • Príncipe SC, Acosta AL, Andrade JE, Lotufo TMC (2021) Predicted shifts in the distributions of atlantic reef-building corals in the face of climate change. Front Mar Sci 8:673086

    Article  Google Scholar 

  • Roff G, Mumby PJ (2012) Global disparity in the resilience of coral reefs. Trends Ecol Evol 27:404–413

    Article  PubMed  Google Scholar 

  • Roth F, Saalmann F, Thomson T, Coker DJ, Villalobos R, Jones BH, Wild C, Carvalho S (2018) Coral reef degradation affects the potential for reef recovery after disturbance. Mar Environ Res 142:48–58

    Article  CAS  PubMed  Google Scholar 

  • Santana EF, Mies M, Longo GO, Menezes R, Aued AW, Luza AL, Bender MG, Segal B, Floeter SR, Francini-Filho RB (2023) Turbidity shapes shallow southwestern atlantic benthic reef communities. Mar Environ Res 183:105807

    Article  CAS  PubMed  Google Scholar 

  • Schlotheuber M, Voolstra CR, de Beer D, Camp EF, Klatt JM, Ghilardi M, Neumüller K, Ousley S, Bejarano S (2024) High temporal resolution of hydrogen peroxide (H2O2) dynamics during heat stress does not support a causative role in coral bleaching. Coral Reefs 43(13):1–15

    Google Scholar 

  • Schoepf V, Grottoli AG, Levas SJ, Aschaffenburg MD, Baumann JH, Matsui Y, Warner ME (2015) Annual coral bleaching and the long-term recovery capacity of coral. Proceedings of the Royal Society B: Biological Sciences 282:20151887

    Article  PubMed Central  Google Scholar 

  • Skirving W, Enríquez S, Hedley JD, Dove S, Eakin CM, Mason RA, De La Cour JL, Liu G, Hoegh-Guldberg O, Strong AE, Mumby PJ et al (2017) Remote sensing of coral bleaching using temperature and light: progress towards an operational algorithm. Remote Sensing 10:18

    Article  Google Scholar 

  • Skirving WJ, Heron SF, Marsh BL, Liu G, De La Cour JL, Geiger EF, Eakin CM (2019) The relentless march of mass coral bleaching: a global perspective of changing heat stress. Coral Reefs 38:547–557

    Article  Google Scholar 

  • Speelman PE, Parger M, Schoepf V (2023) Divergent recovery trajectories of intertidal and subtidal coral communities highlight habitat–specific recovery dynamics following bleaching in an extreme macrotidal reef environment. PeerJ 11:e15987

    Article  PubMed  PubMed Central  Google Scholar 

  • Steneck RS, Arnold SN, Boenish R, De León R, Mumby PJ, Rasher DB, Wilson MW (2019) Managing recovery resilience in coral reefs against climate-induced bleaching and hurricanes: a 15 year case study from Bonaire. Dutch Caribbean Frontiers in Marine Science 6:265

    Article  Google Scholar 

  • Suggett DJ, Kikuchi RK, Oliveira MD, Spanó S, Carvalho R, Smith DJ (2012) Photobiology of corals from Brazil’s near-shore marginal reefs of abrolhos. Mar Biol 159:1461–1473

    Article  Google Scholar 

  • Tebbett SB, Connolly SR, Bellwood DR (2023) Benthic composition changes on coral reefs at global scales. Nature Ecology & Evolution 7:71–81

    Article  Google Scholar 

  • Teixeira CD, Leitão RL, Ribeiro FV, Moraes FC, Neves LM, Bastos AC, Pereira-Filho GH, Kampel M, Salomon PS, Sá JA, Falsarella LN, Amario M, Abieri ML, Pereira RC, Amado-Filho GM, Moura RL (2019) Sustained mass coral bleaching (2016–2017) in Brazilian turbid-zone reefs: taxonomic, cross-shelf and habitat-related trends. Coral Reefs 38:801–813

    Article  Google Scholar 

  • Trygonis V, Sini M (2012) PhotoQuad: a dedicated seabed image processing software, and a comparative error analysis of four photoquadrat methods. J Exp Mar Biol Ecol 424:99–108

    Article  Google Scholar 

  • Vieira CA, Cupolilo F (2021) Estudo da atuação do anticiclone subtropical do Atlântico Sul (ASAS) no Parque Estadual do Rio Doce (PERD) e seu entorno na estação chuvosa. Revista Brasileira De Climatologia 28:830–857

    Article  Google Scholar 

  • Waechter LS, Luza AL, Eggertsen L, Quimbayo JP, Hanazaki N, Pinheiro HT, Giglio VJ, Cordeiro CA, Mendes TC, Luiz OJ, Dambros C, Longo GO, Almeida-Neto M, Bender MG (2023) The aesthetic value of Brazilian reefs: from species to seascape. Ocean Coast Manag 7:106882

    Google Scholar 

  • Weis VM (2008) Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066

    Article  CAS  PubMed  Google Scholar 

  • West JM, Salm RV (2003) Resistance and resilience to coral bleaching: implications for coral reef conservation and management. Conserv Biol 17:956–967

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Coral Vivo Project and its sponsors Petrobras (Programa Petrobras Socioambiental) and Arraial d’Ajuda Eco Parque. We are also grateful to Thomás Banha for providing assistance with the data, Ralf Cordeiro for comments on the manuscript, the Coral Vivo research station team for their assistance in the field, and the reviewers for their time dedicated to reviewing the manuscript. BMC acknowledges a scholarship by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). RBFF, MVK, GOL and TMCL are grateful to research productivity scholarships provided by CNPq (#309651/2021-2, #305274/2021-0, #308072/2022-7 and #312038/2020-8, respectively). SCF and MVK also thank the support from the São Paulo Research Foundation (FAPESP #2022/03105-7 and #2021/06866-6, respectively).

Funding

The authors have not disclosed any funding.

Author information

Author notes

  1. Beatriz M. Corazza and Carlos H. F. Lacerda have contributed equally to this work.

Authors and Affiliations

  1. Instituto Oceanográfico, Universidade de São Paulo. Praça Do Oceanográfico, São Paulo, SP, 191-05508-120, Brazil

    Beatriz M. Corazza, Arthur Z. Güth, Tito M. C. Lotufo, Paulo Y. G. Sumida & Miguel Mies

  2. Instituto Coral Vivo, Rua Dos Coqueiros, Santa Cruz Cabrália, São Paulo, BA, 87-45807-000, Brazil

    Carlos H. F. Lacerda, Arthur Z. Güth, Adalto Bianchini, Emiliano N. Calderon, Kátia C. C. Capel, Edmilson Conceição, Samuel C. Faria, Amana G. Garrido, Flávia M. Guebert, Marcelo V. Kitahara, Tito M. C. Lotufo, Kely P. Salvi, Carla Zilberberg & Miguel Mies

  3. Ambipar Response Fauna E Flora, Rua Manoel Feu Subtil, Vitória, ES, 60-29050-400, Brazil

    Renata K. M. Marcançoli

  4. Instituto de Ciências Biológicas, Universidade Federal Do Rio Grande, Avenida Itália, Km 8, Rio Grande, RS, 96203-900, Brazil

    Adalto Bianchini

  5. Instituto de Biodiversidade E Sustentabilidade, Universidade Federal Do Rio de Janeiro, Avenida São José Do Barreto, Macaé, RJ, 764-27965-045, Brazil

    Emiliano N. Calderon & Carla Zilberberg

  6. Centro de Biologia Marinha, Universidade de São Paulo, Rodovia Manuel Hypólito Do Rego, Km 131, São Sebastião, SP, 5-11612-109, Brazil

    Kátia C. C. Capel, Samuel C. Faria, Ronaldo B. Francini-Filho, Amana G. Garrido & Marcelo V. Kitahara

  7. Departamento de InvertebradosMuseu Nacional, Universidade Federal Do Rio de Janeiro, Quinta da Boa Vista, Rio de Janeiro, RJ, 20940-040, Brazil

    Kátia C. C. Capel

  8. Laboratório de Ecologia Marinha, Departamento de Oceanografia E Limnologia, Universidade Federal Do Rio Grande Do Norte. , Avenida Via Costeira/Senador Dinarte Mariz, Natal, RN, S/N-59014-002, Brazil

    Guilherme O. Longo

  9. Departamento de Ecologia E Zoologia, Universidade Federal de Santa Catarina. Campus Universitário, Florianópolis, SC, S/N-88040-970, Brazil

    Bárbara Segal

Authors
  1. Beatriz M. Corazza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carlos H. F. Lacerda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arthur Z. Güth
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Renata K. M. Marcançoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Adalto Bianchini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Emiliano N. Calderon
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kátia C. C. Capel
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Edmilson Conceição
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Samuel C. Faria
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ronaldo B. Francini-Filho
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Amana G. Garrido
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Flávia M. Guebert
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Marcelo V. Kitahara
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Guilherme O. Longo
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Tito M. C. Lotufo
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Kely P. Salvi
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Bárbara Segal
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Paulo Y. G. Sumida
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Carla Zilberberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Miguel Mies
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

CHF, AB, ENC, FMG, TMC, MM designed the research; CHF, EC, KPS performed fieldwork; BMC, AZG, RKMM, SCF, RBFF, TMC analyzed the data; KCCC, RBFF, AGG, MVK, GOL, TMC, BS, PYGS, CZ contributed with infrastructure/material/technical support; and all authors contributed to the manuscript.

Corresponding author

Correspondence to Miguel Mies.

Ethics declarations

Conflict of interest

On behalf of the authors, the corresponding author states that there is no conflict of interest.

Ethical approval

This is an observational study. The Chico Mendes Institute for Biodiversity Conservation (ICMBio) has confirmed that no ethical approval is required.

Additional information

Responsible Editor: C. Wild.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 161 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Corazza, B.M., Lacerda, C.H.F., Güth, A.Z. et al. No coral recovery three years after a major bleaching event in reefs in the Southwestern Atlantic refugium. Mar Biol 171, 114 (2024). https://doi.org/10.1007/s00227-024-04432-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-024-04432-3

Keywords

Search

Navigation