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

  • ️Sat Jan 01 2022

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

Lorenzo Alvarez-Filip et al. Commun Biol. 2022.

Abstract

Diseases are major drivers of the deterioration of coral reefs and are linked to major declines in coral abundance, reef functionality, and reef-related ecosystems services. An outbreak of a new disease is currently rampaging through the populations of the remaining reef-building corals across the Caribbean region. The outbreak was first reported in Florida in 2014 and reached the northern Mesoamerican Reef by summer 2018, where it spread across the ~450-km reef system in only a few months. Rapid spread was generalized across all sites and mortality rates ranged from 94% to <10% among the 21 afflicted coral species. Most species of the family Meandrinadae (maze corals) and subfamily Faviinae (brain corals) sustained losses >50%. This single event further modified the coral communities across the region by increasing the relative dominance of weedy corals and reducing reef functionality, both in terms of functional diversity and calcium carbonate production. This emergent disease is likely to become the most lethal disturbance ever recorded in the Caribbean, and it will likely result in the onset of a new functional regime where key reef-building and complex branching acroporids, an apparently unaffected genus that underwent severe population declines decades ago and retained low population levels, will once again become conspicuous structural features in reef systems with yet even lower levels of physical functionality.

© 2022. The Author(s).

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Morpho-functional groups of Caribbean corals and their susceptibility to stony coral tissue loss disease (SCTLD).

a Hierarchical clustering dendrogram based on a Gower dissimilarity analysis and heat map representation of functional traits. Numerical values from 1 to 5 correspond to the categories listed in Table S6. The variation in color intensity within each group (light to deep) corresponds to the trait numerical value (given inside each square). b Prevalence of SCTLD for coral species across 101 reef sites in the Mexican Caribbean (n = number of colonies). We included coral colonies with total mortality whose deaths could be attributable to SCTLD. The shaded area corresponds to the prevalence of SCTLD for each morpho-functional group in (a). The asterisk (*) indicates species with >10% disease prevalence (these were considered highly susceptible species, see Methods for more details). c Pseudodiploria strigosa colony with the characteristic lesions produced by SCTLD in Puerto Morelos (July 2018). d Dendrogyra cylindrus colony afflicted with SCTLD showing extensive recent mortality in Sian Ka’an (September 2018). e A recently deceased colony of Meandrina sp. (covered by a homogenous, thin layer of filamentous algae) in Akumal (September 2018). Photo credits: Lorenzo Alvarez-Filip.

Fig. 2
Fig. 2. Prevalence of stony coral tissue loss disease (SCTLD) in highly susceptible species in the Mexican Caribbean.

a White plague-type disease prevalence in species highly susceptible to SCTLD in 35 sites surveyed before the outbreak of the disease (2016 and 2017). b SCTLD prevalence (i.e., diseased and recently deceased colonies) in highly susceptible species during or after the SCTLD outbreak (2018 and 2020). In (a) and (b), the circles represent the locations of the reefs that were sampled before and after the outbreak. The triangles represent the sites that were only surveyed during or after the outbreak. The size of the figure indicates the percentage of healthy colonies of highly susceptible species based on the total number of surveyed colonies at each site and time period (including all coral species). The insets in (a) and (b) represent the distributions of the densities of live coral colonies of highly susceptible species across all surveyed sites for each period. The data points represent each surveyed site, and the box plots depict the median (horizontal line), the first and third quartiles (box height), and 95th percentiles (whiskers). The shaded area (violin plot) depicts the kernel density showing the probability of the data at different values. Highly susceptible species are those with more than 10% disease prevalence (see Methods and Fig. 1).

Fig. 3
Fig. 3. Disease prevalence predictors in coral reefs in the Mexican Caribbean.

a Disease prevalence predictors for 101 reef sites in the Mexican Caribbean and (b) without the Banco Chinchorro reefs (86 sites). Effect sizes are the logistic mixed models with the dots and lines representing the means and 95% confidence intervals, respectively. All continuous predictive variables were scaled to z-scores with the scale function in R. In the model, categorical variables, such as coastal development (low), leeward reefs, and back-reefs, were used as arbitrary references. Asterisks denote statistical differences (*p < 0.05, **p < 0.01, ***p < 0.001).

Fig. 4
Fig. 4. Shifts in coral community composition and functioning following the stony coral tissue loss disease (SCTLD) outbreak.

a–c Principal component biplots of the shifts in the coral assemblages in 35 reef sites along the Mexican Caribbean between the pre- (blue) and post-outbreak (red) periods in (a) coral assemblages, (b) family assemblages, and (c) functional traits based on community weighted means (CWM). The points in (a–c) represent the reef sites for each period. Vectors represent the absolute contributions of families, species, and traits. The colored ellipses represent the 95% confidence intervals around the weighted average of the site scores for each period. d–f Box plots of the functional shifts between the pre- (blue) and post-outbreak (red) periods in the same reef sites with regard to (d) functional richness, (e) functional evenness, and (f) coral community calcification (Kg CaCO3 m2 yr−1). The points in (d–f) represent each surveyed reef site and box plots show the median (horizontal line), first and third quartiles (box height), and the minimum and maximum values (whiskers; excluding outliers). Species key in (b): Acer: Acropora cervicornis; AGAR_enc: Agaricia encrusting Apal: Acropora palmata; Aten: Agaricia tenuifolia; Cnat: Colpophyllia natans; Dcyl: Dendrogyra cylindrus; Dlab: Diploria labyrinthiformis; Dsto: Dichocoenia stokesii; Efas: Eusmilia fastigiata; Ffra: Favia fragum; Hcuc: Helioseris cucullata; ISOP: Isophyllia spp; MADR: Madracis spp; Mang: Mussa angulosa; Mcav: Montastraea cavernosa; MEAN: Meandrina spp; MYCE: Mycetophyllia spp; Oann: Orbicella annularis; Ofav: Orbicella faveolata; Ofra: Orbicella franksi; P_dig: Branching Porites; Past: Porites astreoides; Pcli: Pseudodiploria clivosa: Pstr: Pseudodiploria strigosa: SCOL: Scolymia spp; Sint: Stephanocoenia intersepta; Srad: Siderastrea radians; Ssid: Siderastrea siderea.

Fig. 5
Fig. 5. Conceptual diagram of the long-term trajectory of the physical functionality of Caribbean reefs based on published temporal trends (Table S4) and the recent impacts of stony coral tissue loss disease (SCTLD).

The physical functionality of reefs depends on the abundance (or cover), capacity to accumulate CaCO3, and structural complexity of each species present in the system. The stacked plot represents the functional contributions of four coral groups over time. The pie charts illustrate the proportional contributions of each coral group during three different periods. Acropora spp. and Orbicella spp. contain all the species for each of these genera and are illustrated as a single group, as they are the main reef-building corals in the Caribbean and have dominated shallow-water coral-reef habitats throughout the region in geological times. The group of massive corals includes important reef framework builders from the Diploria, Pseudodiploria, Colpophyllia, Montastraea, and Dendrogyra genera (many of which were severely affected by SCTLD and were included in the second morpho-functional group from the top in Fig. 1a). The other group includes all other coral species, which are largely classified as weedy, submassive, or foliose-digitate corals (included in the third and fourth morpho-functional groups from the top in Fig. 1a) for which little evidence of declines exists. The black arrows indicate major sources of coral decline widely recognized in the literature. White-band disease resulted in severe population declines of acroporids. The white-pox epidemic has infected many of the remaining colonies of this genus since the 1990s. Other coral-disease syndromes (e.g., white plague and Caribbean yellow band) that mainly affect Orbicella and other massive species have increased in frequency and virulence over the last three decades (e.g.,,). Coral mortality has also continued to increase in the Caribbean and is associated with warm-water bleaching events and other local-scale anthropogenic impacts,,. The grey-dashed arrows indicate that the source of stress remains, although the effects on widespread coral mortality are unclear.

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