In recent years outbreaks of a lethal white syndrome (WS) affecting many species in several Caribbean reefs have been reported. The nature, timing, and regional spread of the outbreak in the Caribbean region (AGRRA, 2019), strongly suggest a similar outbreak in the NE Mexican Caribbean (Álvarez-Filip et al., 2019) as well as that previously reported for Florida (Precht et al., 2016). In recent publications, these outbreaks have been named “stony coral tissue loss disease” (SCTLD; FKNMS (Florida Keys National Marine Sanctuary), 2018), although in our surveys signs also correspond to the white plague type II (WP-II) description (Richardson et al., 1998). The spreading spatial patterns have suggested a primary infectious causal agent and diminishing tissue loss rates in affected colonies treated with antibiotics reinforce the idea that a bacterial infection is involved in SCTDL syndrome development (Neely et al., 2020). Nevertheless, so far, although several putative bacterial agents have been proposed (Aeby et al., 2019; Meyer et al., 2019; Paul et al., 2019; Iwanowicz et al., 2020; Thomé et al., 2021) no causality has been demonstrated, only association, which is not evidenced enough (Hill, 1965; Evans, 1976). Moreover, given the above, it seems that opportunistic pathogens may play a confusing role to the extent that Aeby et al. (2019) consider that not just bacteria, but viruses or even protozoa may play a causal role in the SCTLD. In contrast, Landsberg et al. (2020), ponder the possibility that there may be no infectious agent in the primary etiology of the SCTLD.

Disease transmission of infectious diseases may occur by direct contact between diseased and susceptible organisms or by indirect transmission by vector-borne (mechanical or biological) and in the case of the marine environment by water-borne transmission (Shore and Caldwell, 2019). In one host one parasite system, the diseased triad (host, pathogen, and environment) can be equally applied to disease transmission, instead of the classic one pathogen–one host point of view (Antonovics, 2017). And a more complex panorama arises for disease transmission in highly diverse ecological systems, more so if subject to continuous environmental change (Webster et al., 2017; Brooks and Boeger, 2019). It is considered that a primary infection outbreak tends to show a spatial dependence in diseased corals (Muller and van Woesik, 2012; Thrusfield, 2016). However, Jolles et al. (2002) argue that a clustered distribution of diseased colonies follows a random one and is determined by direct colony contact, a secondary transmission process. Zvuloni et al. (2009) found a clustered distribution of Black Band disease affected colonies at very small spatial scales in dense multispecies coral assemblages. In contrast, Sharp et al. (2020) report no clustered distribution for SCTLD in multispecies assemblages at relatively small scales in Florida, whereas, Muller et al. (2020) report significant clustering at different large spatial scales for SCTLD, also along the Florida reef tract. Webster et al. (2017) point out that in complex ecosystems many simultaneous transmission modes may coexist, further confounding spatial patterns interpretation.

However, our present insight into outbreak transmission patterns in the reef environment is based on multispecies coral assemblages that may not adequately describe the single species response. To improve our understanding of the spatial spread of this WS outbreak at the species level, we studied the temporal incidence variation along with the outbreak in two populations of the highly susceptible scleractinian coral Pseudodiploria strigosa (Precht et al., 2016; Álvarez-Filip et al., 2019; Landsberg et al., 2020) in northern Mexican Caribbean reefs. To characterize the incidence patterns we analyze the WS incidence spatial distribution patterns at several intervals during the outbreak to find out to what extent colony proximity was a determining factor in the spatial distribution incidence patterns of this WS in P. strigosa. We also contrast survival probabilities and the temporal patterns of apparently healthy colonies to become diseased among the relatively nearby two study sites, to further describe the dynamics of the outbreak.

We decided to maintain the hypernym of WS for this outbreak because: (a) the uncertainty of identifying a coral disease simply by visual signs in the field (Work and Aeby, 2006; Thrusfield, 2016); (b) that many “old” Caribbean coral diseases, such as the plagues as originally described are still extant; and (c) that in our surveys we observed both SCTLD and WP-II specific disease signs (SCTLD: tissue sloughing and multifocal lesions. WP-II: basal initiation and unifocal rapid in-colony spread).

A remarkable finding of this study was the different dynamics in the WS outbreak in P. strigosa surveyed populations of the study sites, notwithstanding the two sites are relatively close to each other and in similar environmental settings. Although site surveys started within a week of each other the initially recorded WS prevalence at the Bocana site (44%) was five times greater than at Picudas sites (8.5%), even though P. strigosa colony density at Picudas was more than twice the one at Bocana. This first finding shows that the WS outbreak started at Picudas site, about the same time that our survey started, but earlier at the Bocana site and/or that P. strigosa colonies at Bocana site were more susceptible to the WS. If the outbreak should have occurred simultaneously at both sites it would have resulted in relatively similar survival probabilities, if not lower at Picudas, due to its higher colony density; unless P. strigosa colonies resistance to the WS in Picudas was higher than at Bocana.

A possible outbreak starting time for the Bocana site can be roughly estimated by finding the median time to disease onset, since our observations started, and subtracting that period from our initial survey dates. A median time of apparently healthy colonies to become diseased of 74 days was obtained (pooling data from both sites), with a bootstrapped 95% confidence interval of 60–90 days. The 2–3 months range comprised by the confidence interval roughly corresponds with the probable time frame of the outbreak in the northern Mexican Caribbean as reported by Álvarez-Filip et al. (2019). On the other hand, the median time to disease onset in Bocana colonies since observations started was of 97 days, suggesting that the outbreak developed earlier at that site.

The WS outbreak progression in terms of time to disease onset in apparently healthy colonies was not constant or progressively decreasing at neither site. Trends that may be expected by continuous successful transmission and decreasing host abundance, respectively, if nearest neighbor distances were important. Instead, a multimodal distribution of time to disease onset data was found for both sites, implying a wavy frequency in the WS sign’s appearance. Furthermore, the modal location for each site was different for Bocana (modes at 17 and 151 days from study initiation), and three for Picudas (modes at 70, 129, and 184 days). While at Bocana both modes had a similar percentage of the data (Figure 6), in Picudas the first mode at 70 days has the most of data, and the other two were quite smaller and with similar values. The wavy frequency in the time to disease onset data, suggests different events of successful transmission whereas the large amplitude of the main modes is probably related to large variability in colony resistance to the WS. In this late case, amplitudes of main modes at both sites are similarly wide and in that sense at both sites colony resistance is variable. As the outbreak in our study sites progressed, many colonies died, and live colony density was greatly reduced, thus increasing average nearest neighbor distances, and still, the WS incidence continued unabated, even in colder winter months.

Incidence spatial patterns of the WS outbreak, throughout the study, don’t reflect the surveyed population spatial patterns. Also, a transition of incidence spatial patterns was observed, indicating that the dynamics of this WS outbreak are complex even at small spatial scales. The initial Picudas incidence patterns showed clustering suggesting a nearest neighbor relation in the transmission of the disease; and if so, probably driven by the relatively high colony density at the site. Later surveys, however, showed a transition to random distribution patterns, although many apparently healthy colonies remained in the surveyed area. On the other hand, at the Bocana site the incidence distribution pattern was random in the summer period, but in the winter period transition toward an overdispersed pattern; probably an effect of a reduced population of susceptible colonies in the study area. Jolles et al. (2002) reported that Aspergillosis in the sea fan Gorgonia ventalina had different distribution patterns as the outbreak developed. At low prevalence levels the distribution pattern of diseased colonies was random, but a transition to clustered distribution at high prevalence levels; due to direct contact after the initial long-distance water-borne driven outbreak. An apparent lack of colony density dependence for the spread of coral diseases has also been documented in Florida reefs for outbreaks of WP-II (Richardson et al., 1998), of a WS (Precht et al., 2016; Rippe et al., 2019), and SCTDL (Sharp et al., 2020). In our study, lack of spatial dependence seems to extend to very small spatial scales as no simultaneous (not observed in the same survey) disease WS signs development were observed in colonies that grew in direct contact. Nevertheless, although few colony pairs were registered, the shorter period of the apparently healthy colony to become diseased in diseased-healthy pairs suggests that direct contact enhances colony susceptibility to this WS. More so, as there were no cases where a WS lesion appeared in the contact area of a colony pair.

On the other hand, given the density independence of the incidence events, multimodal distributions may be related to periodic transport events of the causal agent or necessary additional factors to trigger the WS disease (Sokolow, 2009) at the spatial scale of the study areas. It may also imply different transmission events and mechanisms for this WS outbreak (Shore and Caldwell, 2019). Precht et al. (2016) infer that the WS they observed in Florida was water-borne transmitted due to the low density of coral colonies. Muller et al. (2020) shared this point of view after assessing the rates of spread of SCTLD in the Florida reef tract. Dobbelaere et al. (2020), modeling the SCTLD in the Florida reef tract, consider that the disease is likely to be transported by currents as a neutrally buoyant material. Zvuloni et al. (2009) claimed that even at very short-inter colony distances and high colony densities waterborne transmission of a Black Band disease was the main mechanism for a clustered distribution of diseased colonies, in the absence of biological vectors. If there is a primary agent of the disease and is waterborne transported (Precht et al., 2016; Dobbelaere et al., 2020; Muller et al., 2020) given the short distance between our sites (1,200 m) and high water connectivity in the study area, probably the WS outbreak should have started more or less simultaneously at both study sites.

Clemens and Brandt (2015) reported that white plagues are transmitted effectively by Coralliophilia abbreviata, a corallivorous snail, and also through water even when filtered. Williams and Miller (2005) reported that white band disease in Acropora cervicornis was transmitted both by direct colony contact and also by C. abbreviate. In the present study, we observed the fireworm Hermodice carunculata, feeding on tissue remnants of the WS lesion of a P. strigosa colony at Picudas site in one of the surveys; but not on the adjacent, apparently healthy coral tissue (Figure 9). There were no sightings of fireworms or other coral predators such as C. abbreviata feeding on healthy P. strigosa colonies. Noonan and Childress (2020) report active biological vectoring for SCTLD by butterflyfishes in Florida, the first biological vector report to our knowledge. Passive biological vectors had also been suggested, as the macroalgae Halimeda opuntia (Nugues et al., 2004) or sediment biofilm (Richardson, 1996). These reports point out the possibility of several co-occurring transmission mechanisms (Clemens and Brandt, 2015), during the disease outbreak in our study sites. And the observed particular outcomes may have depended on minor variations in local conditions and colony stress history, as well on the epigenetics of both hosts and potential primary and secondary pathogens present through the outbreak (Webster et al., 2017; Zaneveld et al., 2017).

The importance of changing ecosystems effects in coral disease etiology has been stressed by many authors, from the ecological (i.e., Hoegh-Guldberg, 1999; Sokolow, 2009; Bruno et al., 2019) to the microbiological context (i.e., Lesser et al., 2007; Zaneveld et al., 2016; Webster et al., 2017; Brooks and Boeger, 2019; Vega-Thurber et al., 2020). Models were the role of opportunistic pathogens, and stress-driven reduced host resistance should perhaps be the norm, rather than the exception (Lesser et al., 2007). Such interactions are likely to result in greater susceptibility to disease as a result of unbalanced coral microbiomes (Zaneveld et al., 2017), leading both to host depressed immune response and reduce overall performance (Harvell et al., 2007). In addition, environmental degradation can lead to the emergence of new strains of presently purported pathogens or even new ones (Ellner et al., 2007; Vega-Thurber et al., 2009). For instance, all colonies in our study sites developed the WS but at different times and with varying survival periods, strongly suggest that individual colony condition played a role in susceptibility to the disease and its progression within a colony. But also opens the possibility that different diseases are co-occurring in the WS outbreak. If Landsberg et al. (2020) consideration that there may be no primary infectious etiology in the SCTLD holds, then multiple secondary bacterial pathogens associated with the SCTLD (Aeby et al., 2019; Meyer et al., 2019; Paul et al., 2019; Iwanowicz et al., 2020; Landsberg et al., 2020) and for a more general WS as well (Thomé et al., 2021), may play an important role in these diseases development. As it is well known that external stressors may compromise host immunity (Harvell et al., 2007; Glasl et al., 2016) and/or produce an imbalance in the structure and diversity of the coral microbiome, contributing to the proliferation of opportunistic pathogens (Lesser et al., 2007; Muller and van Woesik, 2012; Woodley et al., 2016; Sweet and Bulling, 2017; Meyer et al., 2019).

Two main drivers of coral diseases so far considered are increased seawater temperatures and poor water quality, both individually and synergistically (Wang et al., 2018). Coral diseases seem to bear a positive relationship with high seawater temperatures, but not with low seawater temperatures (Jones et al., 2004; Bruno and Selig, 2007; Zvuloni et al., 2009; Heron et al., 2010; Beeden et al., 2012; Ruiz-Moreno et al., 2012). However, at our sites, despite the decrease of apparently healthy colonies, the proportion of newly diseased colonies per interval between summer and winter surveys showed no significant difference. Thomé et al. (2021) observed that WS lesion progression was not hinder during winter at Picudas site and Álvarez-Filip et al. (2019) observed newly WS diseased colonies in relatively nearby Cozumel Island in winter. If this WS causality is water-borne, the winter strong north winds may contribute to this density-independent pattern by transporting fomites (Dobbelaere et al., 2020) resulting in waves of effective local transmissions; despite the lower seawater temperatures.

Global and regional stressful factors further confound local factors’ relevance, for instance, Precht et al. (2016), considered that a previous thermal bleaching event was of importance in triggering a WS Florida outbreak, a posteriori identify as SCTLD (Landsberg et al., 2020). At our sites, no previous strong bleaching occurred but a potential stressful factor affecting these reefs could be the Sargassum spp. brown tides (Van Tussenbroek et al., 2017). The decomposition of thousands of tons of these algae on the shore deteriorates water quality, increases nutrient input reduces transparency, pH, and oxygen levels, and increases ammonia, phosphorus, and concentration of toxic metals (Van Tussenbroek et al., 2017; Rodríguez-Martínez et al., 2020). These brown tides were associated with the mortality of seagrass beds and fauna (Van Tussenbroek et al., 2017; Rodríguez-Martínez et al., 2019). However, the potential effects of brown tides and drifting Sargasso mats, are coastal broad, and is difficult to imagine a differential effect at the small spatial scale of our study sites. The same holds regarding the relatively low coastal waters quality, pre-Sargasso events, in the Puerto Morelos coastal waters due to explosive coastal development and inadequate water treatment practices (Carruthers et al., 2005; Hernández-Terrones et al., 2011; Van Tussenbroek et al., 2017; Rodríguez-Martínez et al., 2020).

The difference in direct anthropogenic effects between both sites is on the level of recreational activities. Bocana site receives many snorkelers and scuba divers, whereas the Picudas site is rarely visited. The risks of coral reef tourism-related activities for coral biota are well known (Lamb et al., 2014; Zaneveld et al., 2016; Spalding et al., 2017) but are difficult to demonstrate. For instance, some level of stressful effects from snorkeling and scuba diving on the Bocana coral assemblages may be suspected, but directly linking it to the particular WS outbreak dynamics by association is no demonstration.

We have described in detail the dynamics of the outbreak events at our study sites and shown differences in the dynamics of this WS outbreak at the study sites including a lag in disease outbreak, discontinuous events of the time to disease onset, lack of colony density dependence for the spread of the WS, unhampered incidence in winter months and extremely high morbidity. All indications of a complex and powerful phenomenon, even at the small spatial scales of this study. However, explaining the observed patterns is pending. In this context, further investigations with not-so-aggressive diseases may provide a better natural model to understand the processes behind such complex patterns. Meanwhile, we must recognize that these recent outbreaks are but a continuation of the lethal coral epizootics that had decimated Caribbean reefs, during the last 40 years. And doing so, as has been proposed in many other works, preserving a good environmental quality at the local reef scale may effectively contribute to reducing the susceptibility of corals to WS, but also any other extant or future diseases.

The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author.

EG-U performed the samplings, analyzed the data, prepared the figures and tables, authored, reviewed the drafts of the manuscript, and approved the final draft. EJ-D conceived, designed and performed the samplings, analyzed the data, authored, or reviewed drafts of the manuscript, and approved the final draft. Both authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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