Coral reefs provide numerous ecosystem services including support of robust fisheries and tourism industries. Over the last half-century, however, natural and anthropogenic stressors including pollution, overfishing, disease, and ocean warming have contributed to widespread degradation of coral reefs throughout the Tropical Western Atlantic (Eakin et al., 2010; Jackson et al., 2014; Woodley et al., 2016; Gil-Agudelo et al., 2020; Cróquer et al., 2021). Flower Garden Banks National Marine Sanctuary (FGBNMS) is a high coral cover reef ecosystem in the northwest Gulf of Mexico that has shown remarkable resilience despite declines in coral reef health elsewhere (Aronson et al., 2005; Johnston et al., 2016). East and West Flower Garden Bank (FGB) are two of the 17 banks within the sanctuary, and are located along the outer continental shelf, approximately 190 km south of the Texas-Louisiana border ( Figure 1 ). The banks range in depth from 16–150 m and support extensive coral reef communities to 46 m depths, including many Caribbean coral, sponge, and fish species. Portions of the reef have been monitored annually since 1989, with mean coral cover at East and West FGB remaining near or above 50%, dominated by reef-building species Pseudodiploria strigosa, Colpophyllia natans, and Orbicella spp. (Aronson et al., 2005; Johnston et al., 2016; Johnston et al., 2020).

It has been hypothesized that the depth and remoteness of East and West FGB have buffered them from extreme temperature, disease outbreaks, and other sources of mass mortality plaguing other shallower, coastal reef habitats throughout the region (Aronson et al., 2005; Johnston et al., 2016). There have been isolated instances of localized coral mortality events due to thermal stress-related bleaching (Johnston et al., 2019b), hurricanes and storms (Robbart et al., 2009; Wright et al., 2019; Shore et al., 2021), hypoxia (Johnston et al., 2019a; Kealoha et al., 2020; Doyle et al., 2022), and disease (Borneman and Wellington, 2005). Following these events, coral recovery has often been rapid, with few persistent changes in community composition or coral cover over time (2020; Johnston et al., 2016). During routine monitoring of both banks in late August 2022, disease lesions of unknown etiology were observed on brain and star corals, including P. strigosa, C. natans, O. faveolata, and O. franksi.

Disease outbreaks are of increasing concern, especially as the Caribbean region is a hotspot of coral diseases (Weil et al., 2006; Ruiz-Moreno et al., 2012; van Woesik and Randall, 2017), experiencing recurring disease outbreaks such as white plague from the 1970s through the mid-2000s (reviewed in Cróquer et al., 2021). White plague produces lesions at colony margins leading to rapid tissue loss and mortality (Richardson et al., 1998; Bythell et al., 2004). White plague affects nearly 40 species and is now considered endemic to much of the Tropical Western Atlantic (Cróquer et al., 2021). Despite identification of Aurantimonas coralicida in white plague (Type II)-affected corals, a universal white plague pathogen has not been confirmed, and it has been hypothesized that white plague signs may be caused by multiple etiologies. The most recent coral disease described to date, stony coral tissue loss disease (SCTLD), was first reported in September 2014 off the coast of southeast Florida (Precht et al., 2016), and has become the most lethal coral disease ever recorded due to its swift spread across colonies and reefs, extensive tissue necrosis, and high mortality rates affecting at least 22 species (NOAA, 2018; Kramer et al., 2019). SCTLD is characterized by subacute to acute tissue loss resulting in the exposure of the coral skeleton below, and often begins as focal (single) or multifocal lesions. For both white plague and SCTLD, patterns of tissue loss typically radiate outward from focal lesions, or advance in a linear or crescent band from the margin or base of the colony, and often progress across the entire colony leading to complete colony mortality within weeks to months (Precht et al., 2016; Cróquer et al., 2021; Meiling et al., 2021).

SCTLD constitutes an ongoing epizootic event in the Caribbean, and is currently in an epidemic phase at some locations and an endemic phase in others (Aeby et al., 2021; Cróquer et al., 2021). SCTLD’s etiology remains unknown, yet both direct and waterborne transmission routes are hypothesized to occur (Aeby et al., 2019; Muller et al., 2020; Studivan et al., 2022a; Studivan et al., 2022b). While corals affected by SCTLD respond to antibiotic treatments (Neely et al., 2021; Shilling et al., 2021; Walker et al., 2021), it remains uncertain whether bacteria are primary causative agents or a secondary infection. Virus-like particles and genomic sequence signatures have been observed in infected samples and associated with algal symbionts of the family Symbiodiniaceae (Miller et al., 2020; Work et al., 2021; Veglia et al., 2022). SCTLD has spread continuously since 2014, affecting the entirety of Florida’s coral reefs from Martin County to the Dry Tortugas, and several locations in the Caribbean, including Belize, the Dominican Republic, Jamaica, Puerto Rico, Saint Martin, and the U.S. Virgin Islands (Kramer et al., 2019). Many coral species that are highly susceptible to SCTLD and sentinels of disease onset in Florida, such as Meandrina meandrites and Dichocoenia stokesii, are rarely observed at FGBNMS (Clark et al., 2014; NOAA, 2018). Thus, high cover species such as P. strigosa and C. natans constitute the highly susceptible species within the sanctuary.

While it was unknown if the observed lesions at FGBNMS were SCTLD, white plague, or another disease altogether, a series of rapid response cruises were conducted in September and October 2022 according to action items in the FGB SCTLD Preparedness Plan (Johnston, 2021). Monitoring and research activities focused on 1) characterizing the signs and epidemiological aspects of the disease across FGB and within long-term monitoring sites, 2) treating affected coral colonies with Base 2B plus amoxicillin, and 3) collecting baseline images through repetitive photostations and photomosaics. In this brief research report, we describe the initial signs of this new and unusual disease event observed at East and West FGB from August through October 2022.

Coral diseases in the Tropical Western Atlantic have increased significantly during the past 40 years, dramatically impacting foundational reef-building species (Acropora spp., Orbicella spp., Pseudodiploria spp., C. natans, S. siderea, Montastraea cavernosa, etc.; Woodley et al., 2016; Cróquer et al., 2021). Despite widespread coral reef declines in recent decades throughout the Tropical Western Atlantic (Jackson et al., 2014), East and West FGB corals have changed very little since they were first assessed in the early 1970s, have recovered from coral bleaching events when they occurred, and showed minimal signs of disease (2019a; 2019b; Borneman and Wellington, 2005; Johnston et al., 2016; Gil-Agudelo et al., 2020). In 2003 and 2004, Borneman and Wellington (2005) conducted baseline surveys to document the extent of coral disease at East and West FGB, as they reported previous disease observations from FGB were unreliable due to confusion with predation, competition, and other factors including lack of sampling and histological examination. Results of this study found that few known Caribbean diseases were documented at East and West FGB, and that disease signs that were observed were often inconsistent with established coral disease pathologies. Of the 1,220 coral colonies surveyed for tissue loss diseases by Borneman and Wellington (2005), only one putative case of white plague was observed (0.08% prevalence). Since 2009, disease observations in annual benthic surveys within East and West FGB monitoring sites have ranged from 0–0.3% (Johnston et al., 2020).

During the summer of 2022, daily seawater temperature at depth (21 m and 27 m) was typical for summer months at FGBNMS (Johnston et al., 2019b). Bleaching threshold curves for East and West FGB suggest that more than 50 days above 29.5°C would initiate bleaching in these locations (Johnston et al., 2019b); however, only 27 days at East FGB (between June and September 2022) and 21 days at West FGB (June and August 2022) were above this threshold, suggesting that the observed tissue loss was not likely due to thermal stress in 2022. It is noted, however, that over the past decade, a significant seawater warming trend both at depth (~ 20 m) and in surface waters has been observed at FGB (Johnston et al., 2019b; Manzello et al., 2021). Other water quality parameters measured during the response, including pH, salinity, and DO, were within limits considered typical for coral reefs located in the Western Atlantic; however, lowered salinity following early summer peak in river discharge in combination with warm summer water temperatures may have contributed to compounded stress on the reef.

The recent disease outbreak at East and West FGB is unusual in terms of prevalence on this near-pristine reef system; however, at the time of this report, many uncertainties remain. Based on photography and diver observations alone, it is difficult to determine if the recent disease observed is SCTLD or a type of white plague, as these diseases manifest in a similar manner (Gintert et al., 2019; Cróquer et al., 2021), or whether the event described here is driven by a disease state of some other etiology. Examinations of histology, gross morphology, microbial and ‘omics signatures, quantification of lesion progression rates, as well as transmission experiments (to assess susceptibility) are among the diagnostic information urgently needed for stony coral species to facilitate comparison of the disease signs observed at FGB with the case definitions for white plague and SCTLD to help determine the nature of the ongoing event. A concerning observation was that the most SCTLD-susceptible species at FGBNMS (P. strigosa and C. natans) were the most affected; however, the overall prevalence of lesions at FGB was lower than at epidemic sites in the Caribbean region (Precht et al., 2016; NOAA, 2018). In addition, few observations of diseases and their progression on colony surfaces exist for the upper mesophotic reef habitats (~ 50 m), which are fairly extensive and well developed at FGBNMS (but see Brandt et al., 2021; Chaves-Fonnegra et al., 2021; Williams et al., 2021). Lesions could manifest differently at mesophotic depths as a function of light availability, depth-adapted algal symbionts (Correa et al., 2009) and/or lower temperatures than are typical of lesions described in case studies from shallow reefs (Miller and Richardson, 2015; Chaves-Fonnegra et al., 2021).

The factors influencing transmission of the ongoing disease at FGB require assessment. There is evidence that both SCTLD and white plague can be transmitted directly through tissue contact and the water column (Aeby et al., 2019; Muller et al., 2020; Cróquer et al., 2021). Biotic vectors may also be affecting the spread of this disease among colonies within East and West FGB. The high density of corals at FGB may itself facilitate disease transmission. Many colonies are space limited by the high cover on the banks (nearly 50%), and many colony margins are immediately adjacent to one another. In addition, divers on disease response cruises observed corallivory from parrotfish and fireworms, with the former removing relatively large areas of coral tissue and skeleton at lesion areas and colony margins. Recent reviews of predator behavior in coral disease dynamics found that corallivores may target lesion-affected coral tissue with often-unknown ecological consequences, but in several cases, predators may exacerbate disease impacts through the transportation or hosting of pathogens (Nicolet et al., 2018; Renzi et al., 2022). Parrotfish and/or butterflyfish corallivory may suppress lesion progression through the partial or complete removal of disease-associated tissue (Titus et al., 2022), or contrarily, exacerbate spread through oral or fecal deposition (but see Nicolet et al., 2018). Regardless, additional observations and more research over time are needed to discern potential mechanisms of coral disease spread in FGBNMS.

The resilience of FGBNMS coral reefs, often thought to result from their depth, remote location, and relatively stable environment from surrounding deep water, may be challenged as coral disease outbreaks and climate change effects intensify (Dee et al., 2019; Manzello et al., 2021; Lawman et al., 2022). For example, the dominant coral species at FGBNMS are considered to be highly- to moderately-susceptible to SCTLD, white plague, and other coral diseases. These species comprise 47% of the absolute benthic cover in the long-term monitoring sites (O. franksi: 30%; P. strigosa: 8%; C. natans: 2%; O. faveolata: 3%; O. annularis: 1%; and M. cavernosa: 3%; Johnston et al., 2020). While it is presently unclear which disease is affecting corals at FGB, an outbreak of a highly-virulent disease presents a substantial threat to the persistence of this system. Both SCTLD and white plague have been shown to have major impacts on coral reef ecosystems in the wider Caribbean (reviewed in Cróquer et al., 2021). Disease risk in FGBNMS is amplified by the difficulty in accessing, monitoring, and treating corals at these sites due to their remoteness, particularly during the winter months when weather conditions in the northwest Gulf of Mexico make dive operations challenging.

Regardless of the etiology of the current disease event, the response framework outlined in the FGB SCTLD Preparedness Plan completed the year prior (Johnston, 2021) allowed resource managers and research partners to mobilize quickly and respond efficiently to collect observational data and conduct sampling for disease diagnostic analyses. This included the collection of 386 discrete samples from 182 coral colonies to investigate causative agents and cellular manifestation of lesions. Tissue samples of disease-affected and visually healthy coral colonies were collected for downstream analyses with partner institutions, including transmission electron microscopy (TEM), histopathology, dsRNA-Immunofluorescence (Coy et al., 2022) and ‘omics (algal symbiont, bacteria and virus profiling, metagenomics/metatranscriptomics) from C. natans, P. strigosa, and/or O. faveolata. In addition, 50 mucus samples were collected from C. natans, P. strigosa, M. cavernosa, O. franksi, and O. faveolata species for probiotic screening to better understand how some bacterial symbionts can potentially serve as an alternative treatment option for coral hosts. As disease monitoring continues at the banks, additional samples from other species will be collected when possible if signs of disease are documented.

Disease progression will also be documented on future monitoring cruises, including additional images at repetitive monitoring stations and additional samples for microbial and ‘omics time series (Martindale et al., 2021; Shore et al., 2021). In addition to photostations surveyed during the initial disease response cruises, high-resolution photomosaics were collected using a custom rig consisting of a single SLR (EOS Rebel SL3, Canon) and two GoPro (HERO6) cameras. These photomosaics will be analyzed as part of NCRMP efforts to provide a landscape view of disease patterns and monitoring of large reef areas through time.

Whether the putative disease signs documented at East and West FGB do in fact indicate the presence of SCTLD, a type of white plague, or another disease, epidemic-level rapid coral tissue loss of any kind is likely to be detrimental to the FGB reef ecosystem. This is especially true given that intervention methods developed thus far have not shown success as a preventative treatment and are labor-intensive (Neely et al., 2021; Shilling et al., 2021; Walker et al., 2021). While antibiotic treatments may in some cases be used to promote recovery of individual lesions, the effort, time, and resources to repeatedly treat a remote, high-coral cover reef system are not presently feasible, especially since treatments do not necessarily mitigate disease spread, emergence of new lesions on treated colonies, or transport of pathogens. To what extent the arrival of this putative disease may threaten the health of the FGB reef system is unknown at this time, and the question remains whether the inherent resilience and remoteness of this reef ecosystem will buffer the impact severity and potential recovery. Through continued monitoring, research, and response, this question will be addressed, and collaborative analysis of samples collected will hopefully allow for a better understanding of the etiology of this disease outbreak at FGB.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

All authors contributed to the study conception and design. Data collection was performed by MJ, MS, IE, AC, NB, RE, KE, RH, XH, MN, KO’C, AP-C, and AS. Data analysis, tables, and graphics were prepared by MJ and MS. The manuscript was written by MJ, MS, IE, and AC. Authors contributing to sample analyses were MS, IE, AC, XH, NB, and BU. Funding was provided by GS, JV, XH, and AC. All authors provided input on previous versions of the manuscript. All authors contributed to the article and approved the submitted version.