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Stony coral tissue loss disease decimated Caribbean coral populations and reshaped reef functionality

  • Dungan, M. L., Miller, T. E. & Thomson, D. A. Catastrophic decline of a top carnivore in the Gulf of California rocky intertidal zone. Science 216, 989–991 (1982).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Pounds, J. A. et al. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439, 161–167 (2006).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Nicholls, H. Mysterious die-off sparks race to save saiga antelope. Nature 1–2. https://doi.org/10.1038/nature.2015.17675 (2015).

  • Daszak, P., Cunningham, A. A. & Hyatt, A. D. Emerging infectious diseases of wildlife – Threats to biodiversity and human health. Science 287, 443–449 (2000).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Peters, E. C. Diseases of Coral Reef Organisms. in Coral Reefs in the Anthropocene (ed. Birkeland, C.) 147–178 (Springer Netherlands, 2015). https://doi.org/10.1007/978-94-017-7249-5_8.

  • Weil, E. Coral Reef Diseases in the Wider Caribbean. in Coral Health and Disease (eds. Rosenberg, E. & Loya, Y.) 35–68 (Springer, 2004). https://doi.org/10.1007/978-3-662-06414-6_2.

  • Harvell, C. D. et al. Coral diseases, Environmental drivers and the balance between corals and microbial associates. Oceanography 20, 172–195 (2007).

    Article 

    Google Scholar 

  • Lessios, H. A., Robertson, D. R. & Cubit, J. D. Spread of Diadema mass mortality through the Caribbean. Science 226, 335–337 (1984).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Perry, C. T. & Alvarez-Filip, L. Changing geo-ecological functions of coral reefs in the Anthropocene. Funct. Ecol. 33, 976–988 (2019).

    Google Scholar 

  • Aronson, R. B. & Precht, W. F. White-band disease and the changing face of Caribbean coral reefs. in. Hydrobiologia 460, 25–38 (2001).

    Article 

    Google Scholar 

  • Alvarez-Filip, L., Dulvy, N. K., Gill, J. a, Côté, I. M. & Watkinson, A. R. Flattening of Caribbean coral reefs: region-wide declines in architectural complexity. Proceedings. Biological sciences / The Royal Society 276, 3019–3025 https://doi.org/10.1098/rspb.2009.0339 (2009).

  • Estrada-Saldívar, N., Jordán-Dahlgren, E., Rodriguez-Martinez, R. E., Perry, C. T. & Alvarez-Filip, L. Functional consequences of the long-term decline of reef-building corals in the Caribbean: evidence of across-reef functional convergence. R. Soc. Open Sci. 6, 1–15 (2019).

    Article 

    Google Scholar 

  • Cramer, K. L. et al. Widespread loss of Caribbean acroporid corals was underway before coral bleaching and disease outbreaks. Sci. Adv. 6 https://doi.org/10.1126/sciadv.aax9395 (2020).

  • Bruno, J. F. et al. Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol. 5, 1220–1227 (2007).

    CAS 
    Article 

    Google Scholar 

  • Vega Thurber, R. et al. Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Glob. Change Biol. 20, 544–554 (2014).

    Article 

    Google Scholar 

  • Wear, S. L. & Thurber, R. V. Sewage pollution: Mitigation is key for coral reef stewardship. Ann. N. Y. Acad. Sci. 1355, 15–30 (2015).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Randall, C. J. & Van Woesik, R. Some coral diseases track climate oscillations in the Caribbean. Sci. Rep. 7, 1–8 (2017).

    CAS 
    Article 

    Google Scholar 

  • Lapointe, B. E., Brewton, R. A., Herren, L. W., Porter, J. W. & Hu, C. Nitrogen enrichment, altered stoichiometry, and coral reef decline at Looe Key, Florida Keys, USA: a 3 ‑ decade study. Marine Biology 166, (Springer Berlin Heidelberg, 2019) https://doi.org/10.1007/s00227-019-3538-9.

  • Precht, W. F., Gintert, B. E., Robbart, M. L., Fura, R. & van Woesik, R. Unprecedented disease-related coral mortality in Southeastern Florida. Sci. Rep. 6, 1–11 (2016).

    Article 
    CAS 

    Google Scholar 

  • Kramer, P. R., Roth, L. & Lang, J. Map of Coral Cover of Susceptible Coral Species to SCTLD. (2020). Available at: www.agrra.org. ArcGIS Online.

  • Aeby, G. S. et al. Pathogenesis of a tissue loss disease affecting multiple species of corals along the Florida Reef Tract. Front. Mar. Sci. 6, 1–18 (2019).

    Article 

    Google Scholar 

  • Landsberg, J. H. et al. Stony coral tissue loss disease in Florida is associated with disruption of Host–Zooxanthellae Physiology. Front. Mar. Sci. 7, 1–24 (2020).

    Article 

    Google Scholar 

  • Work, T. M. et al. Viral-like particles are associated with endosymbiont pathology in Florida Corals affected by stony coral tissue loss disease. Front. Mar. Sci. 8, 1–18 (2021).

    Article 

    Google Scholar 

  • Alvarez-Filip, L., Estrada-Saldívar, N., Pérez-Cervantes, E., Molina-Hernández, A. & González-Barrios, F. J. A rapid spread of the Stony Coral Tissue Loss Disease outbreak in the Mexican Caribbean. PeerJ https://doi.org/10.7717/peerj.8069 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gintert, B. E. et al. Regional coral disease outbreak overwhelms impacts from local dredge project. Environ. Monit. Assess. 191, 1–39 (2019).

    Article 

    Google Scholar 

  • Muller, E. M., Sartor, C., Alcaraz, N. I. & van Woesik, R. Spatial epidemiology of the stony-coral-tissue-loss disease in Florida. Front. Mar. Sci. 7, 11 (2020).

    Article 

    Google Scholar 

  • Estrada-Saldívar, N., Quiroga-García, B. A., Pérez-Cervantes, E., Rivera-Garibay, O. O. & Alvarez-Filip, L. Effects of the stony coral tissue loss disease outbreak on coral communities and the benthic composition of cozumel reefs. Front. Mar. Sci. 8, 1–13 (2021).

    Article 

    Google Scholar 

  • Neely, K. L., Lewis, C. L., Lunz, K. & Kabay, L. Rapid population decline of the Pillar coral Dendrogyra cylindrus along the Florida Reef Tract. Front. Mar. Sci. 8 https://doi.org/10.3389/fmars.2021.656515 (2021).

  • Rippe, J. P., Kriefall, N. G., Davies, S. W. & Castillo, K. D. Differential disease incidence and mortality of inner and outer reef corals of the upper Florida Keys in association with a white syndrome outbreak. Bull. Mar. Sci. 95, 305–316 (2019).

    Article 

    Google Scholar 

  • Sharp, W. C., Shea, C. P., Maxwell, K. E., Muller, E. M. & Hunt, J. H. Evaluating the small-scale epidemiology of the stony-coral -tissue-loss-disease in the middle. PLOS ONE 15, 1–25 (2020).

    Article 
    CAS 

    Google Scholar 

  • Estrada-Saldívar, N. et al. Reef-scale impacts of the stony coral tissue loss disease outbreak. Coral Reefs https://doi.org/10.1007/s00338-020-01949-z (2020).

    Article 

    Google Scholar 

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

    Article 

    Google Scholar 

  • McWilliam, M. et al. Biogeographical disparity in the functional diversity and redundancy of corals. Proc. Natl Acad. Sci. 115, 3084–3089 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Suchley, A. & Alvarez-Filip, L. Local human activities limit marine protection efficacy on Caribbean coral reefs. Conserv. Lett. 11, 1–9 (2018).

    Article 

    Google Scholar 

  • Hernández-Terrones, L. et al. Groundwater Pollution in a Karstic Region (NE Yucatan): baseline nutrient content and flux to coastal ecosystems. Water Air Soil Pollut. 218, 517–528 (2011).

    Article 
    CAS 

    Google Scholar 

  • Cejudo, E., Acosta-González, G., Ortega-Camacho, D. & Ventura-Sanchez, K. Water quality in natural protected areas in Cancun, Mexico: A historic perspective for decision makers. Reg Stud Mar Sci 48 https://doi.org/10.1016/j.rsma.2021.102035 (2021).

  • Iwanowicz, D. D. et al. Explor. Stony Coral Tissue Loss Dis. Bact. Pathobiome https://doi.org/10.1017/CBO9781107415324.004 (2020).

    Article 

    Google Scholar 

  • Studivan, M. S. et al. Reef sediments can act as a stony coral tissue loss disease vector. Front. Mar. Sci. 8, 1–15 (2022).

    Article 

    Google Scholar 

  • Bruno, J. F., Petes, L. E., Harvell, C. D. & Hettinger, A. Nutrient enrichment can increase the severity of coral diseases. Ecol. Lett. 6, 1056–1061 (2003).

    Article 

    Google Scholar 

  • Aeby, G. S. et al. Changing stony coral tissue loss disease dynamics through time in Montastraea cavernosa. Front. Mar. Sci. 8, 1–13 (2021).

    Article 

    Google Scholar 

  • Perry, C. T. et al. Regional-scale dominance of non-framework building corals on Caribbean reefs affects carbonate production and future reef growth. Glob. Change Biol. 21, 1153–1164 (2015).

    Article 

    Google Scholar 

  • Toth, L. T. et al. The unprecedented loss of Florida’s reef‐building corals and the emergence of a novel coral‐reef assemblage. Ecology e02781. https://doi.org/10.1002/ecy.2781 (2019).

  • Alves, C. et al. Twenty years of change in benthic communities across the Belizean Barrier Reef. PLoS ONE 17, 1–36 (2022).

    Google Scholar 

  • Bruno, J. F. Implications for reef restoration efforts. Science 345, 879–880 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Rodríguez-Martínez, R. E., Banaszak, A. T., McField, M. D., Beltrán-Torres, A. & Alvarez-Filip, L. Assessment of Acropora palmata in the mesoamerican reef system. PLoS ONE 9, 1–7 (2014).

    Google Scholar 

  • Mudge, L., Alves, C., Figueroa-Zavala, B. & Bruno, J. F. Assessment of Elkhorn coral populations and associated herbivores in Akumal, Mexico. Front. Mar. Sci. 6, 1–12 (2019).

    Article 

    Google Scholar 

  • Baums, I. B., Miller, M. W. & Hellberg, M. E. Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol. Ecol. 14, 1377–1390 (2005).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Perry, C. T. et al. Changing dynamics of Caribbean reef carbonate budgets: emergence of reef bioeroders as critical controls on present and future reef growth potential. Proc. R. Soc. B: Biol. Sci. 281, 20142018–20142018 (2014).

    Article 

    Google Scholar 

  • Molina-Hernández, A., González-Barrios, F. J., Perry, C. T. & Álvarez-Filip, L. Two decades of carbonate budget change on shifted coral reef assemblages: Are these reefs being locked into low net budget states?: Caribbean reefs carbonate budget trends. Proc. Royal Soc. B: Biol. Sci. 287. https://doi.org/10.1098/rspb.2020.2305rspb20202305 (2020).

  • Perry, C. T. et al. Loss of coral reef growth capacity to track future increases in sea level. Nature 558, 396–400 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Enochs, I. C. et al. Ocean acidification enhances the bioerosion of a common coral reef sponge: Implications for the persistence of the Florida Reef Tract. Bull. Mar. Sci. 91, 271–290 (2015).

    Article 

    Google Scholar 

  • Veron, J., Stafford-Smith, M., DeVantier, L. & Turak, E. Overview of distribution patterns of zooxanthellate Scleractinia. Front. Mar. Sci. 2, 1–19 (2015).

    Google Scholar 

  • Miller, M. W., Lohr, K. E., Cameron, C. M., Williams, D. E. & Peters, E. C. Disease dynamics and potential mitigation among restored and wild staghorn coral, Acropora cervicornis. PeerJ 2014, 1–30 (2014).

    Google Scholar 

  • Hughes, A. R. & Stachowicz, J. J. Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc. Natl Acad. Sci. USA 101, 8998–9002 (2004).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Sokolow, S. H. Effects of a changing climate on the dynamics of coral infectious disease: A review of the evidence. Dis. Aquat. Org. 87, 5–18 (2009).

    Article 

    Google Scholar 

  • Bellwood, D. R. et al. Coral reef conservation in the Anthropocene: Confronting spatial mismatches and prioritizing functions. Biol. Conserv. 236, 604–615 (2019).

    Article 

    Google Scholar 

  • Grosso-Becerra, M. V., Mendoza-Quiroz, S., Maldonado, E. & Banaszak, A. T. Cryopreservation of sperm from the brain coral Diploria labyrinthiformis as a strategy to face the loss of corals in the Caribbean. Coral Reefs 40, 937–950 (2021).

    Article 

    Google Scholar 

  • Edmunds, P. J. Long-term dynamics of coral reefs in St. John, US Virgin Islands. Coral Reefs 21, 357–367 (2002).

    Article 

    Google Scholar 

  • Vermeij, M. J. A. Early life-history dynamics of Caribbean coral species on artificial substratum: The importance of competition, growth and variation in life-history strategy. Coral Reefs 25, 59–71 (2006).

    Article 

    Google Scholar 

  • Webster, F. J., Babcock, R. C., Van Keulen, M. & Loneragan, N. R. Macroalgae inhibits larval settlement and increases recruit mortality at Ningaloo Reef, Western Australia. PLoS ONE 10, 1–14 (2015).

    CAS 

    Google Scholar 

  • Suchley, A., McField, M. D. & Alvarez-Filip, L. Rapidly increasing macroalgal cover not related to herbivorous fishes on Mesoamerican reefs. PeerJ 4, e2084 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Contreras-Silva, A. et al. A meta-analysis to assess long-term spatiotemporal changes of benthic coral and macroalgae cover in the Mexican caribbean. 1–12. https://doi.org/10.1038/s41598-020-65801-8 (2020).

  • Meiling, S. S., Muller, E. M., Smith, T. B. & Brandt, M. E. 3D photogrammetry reveals dynamics of stony coral tissue loss disease (SCTLD) Lesion progression across a thermal stress event. Front. Mar. Sci. 7, 1–12 (2020).

    Article 

    Google Scholar 

  • Espinosa-Andrade, N., Suchley, A., Reyes-Bonilla, H. & Alvarez-Filip, L. The no-take zone network of the Mexican Caribbean: assessing design and management for the protection of coral reef fish communities. Biodivers. Conserv. https://doi.org/10.1007/s10531-020-01966-y (2020).

  • Lang, J. C., Marks, K. W., Kramer, P. R., Kramer, P. A. & Ginsburg, R. N. AGRRA Protocols. Version 5.5. The Atlantic and Gulf Rapid Reef Assessment (AGRRA) Program. (2012).

  • Burke, L., Reytar, K., Spalding, M. & Perry, A. Reefs risk. Natl Geographic https://doi.org/10.1016/0022-0981(79)90136-9 (2011).

    Article 

    Google Scholar 

  • Chollett, I., Müller-Karger, F. E., Heron, S. F., Skirving, W. & Mumby, P. J. Seasonal and spatial heterogeneity of recent sea surface temperature trends in the Caribbean Sea and southeast Gulf of Mexico. Mar. Pollut. Bull. 64, 956–965 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Cox, C., Valdivia, A., McField, M., Castillo, K. & Bruno, J. F. Establishment of marine protected areas alone does not restore coral reef communities in Belize. Mar. Ecol. Prog. Ser. 563, 65–79 (2017).

    Article 

    Google Scholar 

  • Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Article 

    Google Scholar 

  • Core Team, R. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria: URL https://www.R-project.org/ (2020).

  • Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Riddle, D. Coral reproduction, part one: A natural coral spawning in Hawaii, The cauliflower coral (Pocillopora meandrina). Adv. Aquarist’s Online Mag. 7, 10–16 (2008).

    Google Scholar 

  • Madin, J. S. et al. The Coral Trait Database, a curated database of trait information for coral species from the global oceans. Sci. Data 3, 160017 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • McWilliam, M., Pratchett, M. S., Hoogenboom, M. O. & Hughes, T. P. Deficits in functional trait diversity following recovery on coral reefs. Proc. Royal Soc. B: Biol. Sci. 287. https://doi.org/10.1098/rspb.2019.2628 (2020).

  • Hughes, T. P. et al. Global warming transforms coral reef assemblages. Nature https://doi.org/10.1038/s41586-018-0041-2 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Oksanen, J. Vegan: community ecology package version 1.8-6. http://cran.r-project.org (2007).

  • Maechler, M. et al. Cluster: Cluster Analysis Basics and Extensions. R package version 2.1.3. https://CRAN.R-project.org/package=cluster (2022).

  • CLARKE, K. R. Non‐parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18, 117–143 (1993).

    Article 

    Google Scholar 

  • Clarke, K. R. & Warwick, R. M. Change in marine communities: an approach to statistical analysis and interpretation. 2nd edition. Primer-E, Plymouth. Plymouth, United Kingsom: PRIMER-E 172 (2001).

  • Lavorel, S. et al. Assessing functional diversity in the field – Methodology matters! Funct. Ecol. 22, 134–147 (2008).

    Google Scholar 

  • Ricotta, C. & Moretti, M. CWM and Rao’s quadratic diversity: A unified framework for functional ecology. Oecologia 167, 181–188 (2011).

    PubMed 
    Article 

    Google Scholar 

  • Villéger, S., Mason, N. W. H. & Mouillot, D. New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89, 2290–2301 (2008).

    PubMed 
    Article 

    Google Scholar 

  • Denis, V., Ribas-Deulofeu, L., Sturaro, N., Kuo, C. Y. & Chen, C. A. A functional approach to the structural complexity of coral assemblages based on colony morphological features. Sci. Rep. 7, 1–11 (2017).

    Article 

    Google Scholar 

  • Teixidó, N. et al. Functional biodiversity loss along natural CO2 gradients. Nat. Commun. 9, 1–9 (2018).

    Article 
    CAS 

    Google Scholar 

  • Laliberté, E. et al. FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0-12. (2014).

  • González-Barrios, F. J. & Alvarez-Filip, L. A framework for measuring coral species-specific contribution to reef functioning in the Caribbean. Ecol. Indic. 95, 877–886 (2018).

    Article 

    Google Scholar 

  • Patterson, K. L. et al. The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata. Proc. Natl Acad. Sci. 99, 8725–8730 (2002).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Edmunds, P. J. & Elahi, R. The demographics of a 15-year decline in covers of the Caribbean reef coral Montastraea annularis. Ecol. Monogr. 77, 3–18 (2007).

    Article 

    Google Scholar 

  • Eakin, C. M. et al. Caribbean corals in crisis: Record thermal stress, bleaching, and mortality in 2005. PLoS ONE 5. https://doi.org/10.1371/journal.pone.0013969 (2010).


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