Coral Disease at the Flower Gardens and Stetson Bank: A Report by Eric Borneman

Coral reef decline is a global phenomenon whose causes are being studied world wide. Especially in the Caribbean and tropical western Atlantic, this decline is being greatly structured by increasing frequencies and distribution of coral diseases (Richardson 1998). Disease impacts not only the coral species affected, but also the associated reef community. Human induced stressors, synergistic with disease-causing organisms, are thought to be the direct or indirect cause of much coral disease (Bruckner 2002). Environmental stresses, anthropogenic stresses, microbial pathogens, and other organisms have all been cited as contributing to or causing coral disease and mortality (Brown and Howard 1985), yet the etiology of most coral diseases remains elusive (Richardson 1998). Caribbean coral reefs have shown a continuing trend towards a phase shift from coral-dominated to algal-dominated ecosystems with diseases as one of the primary causes (Lessios et al. 1984, Aronson and Precht 2001), and such shifts have become a region-wide concern (Done 1992, Hughes 1994).

The Texas Flower Garden Banks have been part of a nationally protected marine sanctuary since 1992 and encompass the most northerly and isolated coral reefs on the North American continental shelf. They are located approximately 110 nautical miles southeast of Galveston, Texas in the northwestern Gulf of Mexico. The Flower Garden Banks have been the subject of research investigations since the early 1970's and are currently part of extensive monitoring and management activities. Long-term monitoring has been occurring since 1972, primarily to assess potential impacts of extensive oil and gas exploration and industry in the area (Schmahl and Hickerson 2000). These reefs have been recognized as among the least disturbed and most pristine coral reef communities in the Caribbean and Western Atlantic region and possess very high (44%-55%) coral coverage (Lang 1999, Causey et al. 2000). Largely unaffected by bleaching events and anthropogenic influences due to their depth, oceanic inputs, limited recreational users and isolated location, coral coverage at the Flower Garden Banks has not significantly declined since monitoring began in the early 1970's (Lang 1999, Pattengill-Semmens et al. 2000). Coral mortality is primarily due to transient increases in algal abundance, parrotfish predation, damselfish "lawns," and the corallivorous snail Coralliophila abbreviata (Gittings et al. 1993).

The second most important Caribbean hermatypic taxon, the Montastraea annularis complex, is currently, and primarily, threatened by three diseases: black band disease, yellow blotch disease, and white plague. At the Flower Garden Banks Montastraea annularis is the dominant species (29%), followed by Diploria strigosa (9%), Porites astreoides (5%), and M. cavernosa (4%) (Pattengill-Semmens et al. 2000). The latter three species are also being impacted heavily by both black band disease and white plague throughout the Caribbean and Western Atlantic, and many of the other 20+ hermatypic (reef-building) species present at the Flower Garden Banks are also susceptible to these pathologies.

The Flower Garden Banks have historically had a low incidence of coral disease. White mat disease, also referred to as ridge disease, was first reported there during monitoring activities from 1988-1991 (Deslarzes 1992). Coral disease was also monitored as a part of multiple observations on coral status and health by the Minerals Management Service (MMS) from 1992-2000 (MMS Publications 96-0046, 99-0005, and 2001-101) across 40 permanent 8m² quadrats and found to be present at very low levels. "Low" incidences of disease were reported in 25 coral transects, with 295 colonies examined during a joint AGRRA/REEF (Reef Environmental Education Foundation) survey from August 15-20 1999 (Pattengill-Semmens et al. 2000). Other studies put the incidence of coral disease at less than 2% (Gittings 1995). In addition to these monitoring projects, there is currently at least one other researcher doing preliminary investigations of coral disease at the Flower Gardens Banks (Oberding et al. 2002).

Unfortunately, many of the reports for the Flower Garden National Marine Sanctuary (FGNMS) have incorrectly identified and reported disease levels and conditions. White mat is not a recognized disease, ridge disease (also called ridge mortality disease) is probably not a disease but related to damselfish predation along the ridges of Diploria spp., and many researchers have erroneously attributed fish biting, snail predation, and bleaching events to coral disease (Bruckner 2002). There is also some question that the techniques or level of expertise developed in previous surveys may not be sufficient to correctly identify coral disease. In the majority of cases, gross examination of a specimen at one time point is inadequate to determine if, or what, disease is present, and surveys to date have relied on such observations. Samples for histological examination and determining rates of progression over time are both important in determining if, and what, disease(s) might be present. Such sampling has been inadequate or lacking in previous studies.

During several trips to these sites, I have documented true coral disease on numerous colonies and species, and at levels that appear to be higher than in previous surveys. I have observed unusually high levels numbers of corals showing signs of hyperplasms erroneously reported as neoplasms (Oberding et al. 2002)], yellow-blotch disease, black-band disease, and white plague type II. Furthermore, several pathologic conditions have been noted that do not fit the description or known etiology of any currently described coral disease (Borneman pers. obs.).

Because of the isolation of the Flower Gardens Banks from land-based influences, gyre currents that nearly prevent genetic flow from any other reefal areas, low impact from other stresses, and a healthy baseline condition of the reefs, incidences of true coral disease at these sites can provide extremely valuable models of study and are vital to the preservation of these coral reefs. The large size of colonies, high coral coverage, and low diversity of hermatypic species, most of which are known to be susceptible to disease, make this community especially vulnerable in the event of a disease epizootic.

The following is the summary and preliminary report of research conducted on coral disease at the FGNMS during the spring research cruise from May 26 - May 30, 2003. I will be doing sufficient research to produce two more preliminary reports. Subsequent to those, I will write a final summary report of my findings from this study.

May 27, 2003
Dive 1, Buoy Two, West Bank:
Dive partners: Emma Hickerson, Jenefer Savage

This dive was an overview of the site in preparation for transects and surveys of coral disease on the Flower Garden Banks. Locating the Acropora palmata first observed and photographed in February, 2003, by James Wiseman and Sarah Bernhardt, was a focus of this dive. It was found and roughly sited for more careful mapping on a subsequent dive (Figure 1). No officially named disease was noticed.

A single colony of Montastraea cavernosa was noted with an opaque white outer "coating" and somewhat abnormally withdrawn polyps. The appearance was consistent with other colonies of Faviidae I have seen occasionally in various places throughout the Caribbean. I have also seen similar abnormal morphologies in zoanthids. I think there is a possibility based, in part, on photographs from prior disease studies, preliminary work on a zoanthid disease by other workers, and my personal observations as well as analysis of corals with similar signs, that this may be an external colonization of the coral surface by the sulfur-oxidizing bacterial species, Beggiatoa sp. It is my experience that Beggiatoa colonization can result in polyps becoming "mushy" and eventually dying in patchy areas across the corallum. I recommend colonies showing such signs at the Flower Gardens be monitored to ascertain the pattern of the condition over space and time, and that samples should be taken and studied to determine the etiology of this condition. It is my impression that this pathology does not cause significant mortality in Scleractinia, nor is it particularly contagious to adjacent colonies. This may not be true for zoanthids. Beggiatoa mats are apparently common in deep areas at the FGNMS. They are nearly ubiquitous in marine environments and have been identified as single agents or components of coral diseases; for example, as a consortium member of black band disease lines and mats. The appearance of colonies affected by Beggiatoa, given the available reservoirs at the FGNMS, would not be surprising.

Figure 2. An unidentified white "film" on Montastraea cavernosa. Compare this
to the normal color pattern shown below.

Impressions: A single 30m transect was run outward from the U-bolt at mooring 2 towards the identified colony of Acropora palmata. The colony was located 27m from the U-bolt, in 71 feet of water under an outcropping topped with a Xestospongia species at a heading of 329º (NNW). A photo transect approximately 2m wide was made of the line for later analysis, and specific transect observations noted.

During random swimming of the area surrounding Mooring 2, we observed an area of Porites astreoides approximately of 20m² between 70-80 feet in depth. Most of the colonies in this area displayed signs of bleaching. This bleaching was expressed as a paling of tissues. The tissues were not totally transparent and there was no tissue loss on the colony (Figures 3,4). A quick count was made of the area and 38 affected colonies were seen. The bleaching pattern on most colonies appeared to be random, but most also showed patches or rings of visibly pale tissue that were more localized towards the colony margins. Generally affected colonies were over 30% bleached. A sample of a small, completely affected, colony was photographed and then collected. The colony was placed in a closed seawater aquarium onboard the M/V Fling. Porites astreoides located away from this patch were normally colored, as were other species within the patch. Bleaching at this depth, temperature and season is almost certainly not related to thermal stress or irradiance factors. Current models of bacterial bleaching involving Vibrio shiloi and V. corallyticus, are positively correlated with high temperatures. Conditions here would not favor the likelihood of a similar bleaching pathogen, although the patchy location, species specificity, and spreading nature of the condition would tend to indicate that investigation of a possible pathogen should be considered as an avenue for further study.

Numerous observations of "areas of abnormal accelerated growth," formerly termed hyperplasm (sensu Peters), were seen. These areas occurred most commonly on Diploria strigosa and occasionally on Montastraea faveolata and M. cavernosa (Figures 5-7). These "tumors" are common on the Flower Garden Banks and should be studied further. Their occurrence appears to be much higher on these reefs than elsewhere in the Caribbean and Indo-Pacific, and Hickerson's mention of higher than normal levels of radioactive isotopes occurring at sites in the FGNMS should be investigated for a possible role in the formation of these abnormal growth nodules.

Figures 5-7. Areas of abnormal accelerated growth, (also referred to as hyperplasia)
on Diploria strigosa, Copophyllia natans, and Montastraea cavernosa.

Analysis of the photo transect confirmed the presence of two small "areas of abnormal accelerated growth;" one on M. cavernosa and another on D. strigosa. Also notable on these transects is the apparently very high rate of fish biting leaving scars. These resulted in areas of tissue loss ranging from small, local areas to large widespread areas, and resulting in significant partial mortality to most species of coral. Also notable is the frequent and extensive number of colonies that appear to be regrowth of colonies that had experienced extensive partial, to near total, old mortality to unknown causes in the past. This transect contained numerous small colonies indicating relatively high rates of recruitment. The alga, Lobophora sp., is a significant contributor to benthic cover where substrate exists that is not colonized by scleractinians. Frequent "bare zones" of competition exist between adjacent colonies and are particularly wide between Diploria and Montastraea species.

Included on this transect (and throughout all sites visited on the Flower Garden Banks), were areas of repeated focus biting by scarids (Figure 8) and areas of damselfish algal lawn cultivation (Figure 9). The characteristic appearance of the lesions resulting from specific cases of fish biting behavior is often distinct, and has falsely led to the assumption that such lesions were either diseases (at the Flower Gardens and throughout the Caribbean) or bleaching. Scarid spot or focused biting was erroneously reported as Rapid Wasting Syndrome, and damselfish nipping on meandroid species, such as those in the genus Diploria, have been called "ridge mortality disease." It is my impression from prolonged and careful observations here, and elsewhere, that no primary disease exists that cause these signs, and that all cases result from current or past action by the behavioral biting patterns of these reef fish. The reported higher incidence of the damselfish pattern on Diploria strigosa at the Flower Gardens deserves further study, especially insofar as it relates to damsel abundance, predation, and coral preference; however, the reduced diversity of species and perhaps their "suitability" to resident damselfish for algal cultivation may be a factor at these sites. I feel it is important to note that previous and often flawed surveys of disease incidence at the FGNMS have included these conditions in estimating disease prevalence, and managers should be aware that under current understanding, these lesions should not be considered as coral diseases.

Figure 8. This parrotfish was observed making the lesion on the Diploria strigosa
below it, and this has been mistakenly classified as a disease in some past reports of
disease at the Flower Gardens.

A single colony of P. astreoides exhibiting signs of the "pale condition" described above appeared on this transect. All other colonies appear normally pigmented. The corals seen on this transect consisted of eight species: Mycetophyllia sp., M. faveolata, M. cavernosa, Madracis mirabilis, M. decactis, Diploria strigosa, P. astreoides, and Colpophyllia natans.

A 30 m transect was run approximately due north from the U-bolt. The results of this transect are listed below. A small sample of normally pigmented P. astreoides was sampled as a comparison to the "paled" colony sampled during Dive #2. Numerous other "paled" P. astreoides were observed 2-3m from the transect line, though none occurred within the 2m belt analyzed. Subsequent to running the transect, a long swim along the "sand flats" was made, and two colonies of M. cavernosa and a single colony of M. faveolata were photographed, all showing signs of the "opaque white film" described in M. cavernosa mentioned during Dive #1 (Figure 10). A morph of M. cavernosa displaying a common mottled white pattern (that is highly fluorescent under actinic or "black" light) across the colony was also photographed to compare this "normal" variation with the different "opaque white" condition (Figure 11). Additionally, one of the affected colonies also had numerous polyps within and immediately adjacent to the opaque areas that were visibly bleached with a yellowish abnormal appearance (Figure 12-13). This is consistent with similarly affected Montastraea spp. I have observed at other locations in the Caribbean (Figure 14). During this dive we also observed the common fish biting patterns and "areas of abnormal accelerated growth" as described above.

Figure 11. Montastraea spp., such as the one shown here (close-up of same colony shown on right),
and other faviids often have a highly fluorescent white pattern that is a normal tissue pattern. The normal
and abnormal patterns appear very similar at a distance.

Figures 12, 13. The white film seen in Figure 10 seemed to be related to the corallite paling/yellowing
seen here on the same and nearby colonies. This condition somewhat resembles yellow blotch disease,
but it is not the same condition.

Figure 14. A colony of Montastraea at La Parguera, Puerto Rico, showing similar signs to the
conditions shown in Figures 12, 13.

The corals seen on this transect consisted of 53 colonies of seven species in seven separate genera: M. faveolata, D. strigosa, P. astreoides, Siderastrea siderea, Colpophyllia natans, Millepora sp., and Stephanocoenia michelini. Two colonies of D. strigosa showed "areas of abnormal accelerated growth;" one colony with three nodules ranging from 5cm to 12 cm in size, the other with a single nodule approximately 4 cm in size.

Disease incidence appears to be very low with the exception of the unidentified "paling" condition of P. astreoides and the well-established incidence of tumor-like areas of abnormal accelerated growth. Overall, I had an almost intangible feeling that the corals, in general, on this bank are somehow stressed. Tissue margins of regrowth following partial mortality were not robust and the amount of partial mortality resulting from fish biting, competition, bioerosion and other factors seemed to be increasing faster than recovery. Coral coverage seemed perceptibly lower as a result than on previous visits to this bank.

May 28, 2003
Dive 4, Buoy Two, East Bank:
Dive partners: Emma Hickerson, Jenefer Savage

This dive was intended for observation of large colonies of Stephanocoenia and Madracis along the deep slope of the East Bank below 120 feet. Colonies at these deep sites seemed exceptionally healthy and robust. Shallower areas extending outward from the mooring U-bolt displayed high coral coverage and with cursory examination the colonies appeared robust and healthy. Careful observation, however, revealed a number of conditions that were more varied than those affecting the West Bank. In particular, several colonies were observed that appeared to have had black band disease (M. cavernosa) and white plague (Diploria strigosa) at some point in the recent past, but were currently not in a state of active disease progression (Figure 15). Colonies such as these should be revisited later in the year as water temperatures increase to see if active disease bands are formed.

Figure 15. The sharp line of healthy tissue and relatively recently denuded skeleton on this
Diploria strigosa is indicative of a disease line. However, some amount of algal overgrowth
had occurred, indicating active tissue loss was not currently occurring. The large white patchy
area on the front center of the colony had some corallite erosion, indicative of fish grazing at
this particular spot. This was the only area of the skeleton to show septal breakage.

Additionally, an unidentified "pale ring" condition was observed in both Diploria strigosa and Colpophyllia natans (Figure 16). This same condition was observed by Borneman and Bruckner in Puerto Rico in 2001 (Figure 17). The tissue forming a wide ring is visibly paler than surrounding tissue, although it does not appear to be severely bleached and no tissue mortality is present. Bruckner noted that the condition disappeared from Puerto Rico colonies later that year. This condition does not appear to be a threat to colony integrity; however, its appearance is abnormal or unusual and colonies should be observed for increased incidence or changes in the pathology of affected colonies.

Figure 16. The large, wide pale ring on this Diploria strigosa was seen on several
colonies, as well as on a single colony of C. natans. This is an unidentified condition.

As seen at the West Bank, areas of abnormal accelerated growth were common on both dives on this bank. Only a few colonies of P. astreoides were noticed with any "paling" condition, and their appearance was questionable enough to suggest that these colonies may not be affected by the same condition as was seen on the East Bank; rather, other stressors, shading, fish biting or competition could all have resulted in the paling. The pale colonies on this bank were not clustered, either, and the isolation further suggests that other factors are involved.

This dive was made primarily to collect samples to establish coral clonal lines, to collect corals for Dr. Cheryl Woodley's stress marker research, and to collect an area of abnormal accelerated growth. During the collections, several additional conditions on the reef were noted. A filamentous, tuft-like cyanobacteria was present growing on exposed margins of corals and on reef substrate in an abundance that was considerably higher than at other sites, and higher than had been previously observed at the FGNMS. This species occurs commonly in reefs that are undergoing significant degradation, such as in the Florida Keys. A gelatinous stranded growth that may be composed of ciliates (Borneman and Peters) was observed on several coral colonies (Figure 18). This material is, to my knowledge, uncharacterized and the role it plays in coral pathology is unknown. However, its presence, as with the tuft-like cyanobacteria seems to be correlated with degraded reefs throughout the Caribbean; its presence at the FGNMS has not been noticed during my past dives, and its occurrence causes me some degree of concern and should be investigated further.

During the sampling of a nodule on a colony of D. strigosa, a large Xestospongia had bleached and fallen apart nearby (Figure 19). This condition is a sponge necrotic disease that is currently affecting sponges throughout the Caribbean and is a source of significant mortality in susceptible sponge species, including extremely old and large sponges. A large colony of D. strigosa was also observed with a large area of white exposed skeleton with reasonably defined margins (Figure 20). A cursory glance would indicate this was an unusually large area of parrotfish focus biting, but a careful examination showed minimal damage to corallite septa; this is not usually found after repeated grazing by scarids. However, the colony lesion was not indicative of any known disease, either. The fact that this large area of skeleton was recently denuded of tissue with no algal overgrowth gave me some degree of consternation. No other corals with similar lesions were seen, and I was left with a somewhat questionable impression that it was indeed a result of parrotfish grazing. Finally, as with other sites, there was a high incidence of lesions associated with focused biting on various species. The ridge nipping of meandroid species by damselfish was equally, if not more, common than at the West Bank.

Figure 19. Xestospongia sp. that had succumbed to a sponge disease known to
affect similar species throughout the Caribbean.

Figure 20. A suspect area of exposed skeleton on a large Diploria strigosa colony.
This is probably related to parrotfish biting, although characteristic grazing scars on
the corallum were not evident.

Corals collected during this dive included: two small colonies of healthy P. astreoides, two small colony fragments of M. faveolata, and a nodule of abnormal accelerated growth from a colony of D. strigosa (Figure 21-25). These colonies were placed into a closed system aquarium onboard the M/V Fling.

This area presents somewhat of a paradox as coral coverage seems higher and coral growth appears to be more robust than the West Bank. At the same time, there were isolated incidences of various biotics and diseases that are correlated with reefs that are under stress and/or are being degraded in other areas of the greater Caribbean basin. Because of weather conditions and time constraints, only two dives were possible here. These dives were also consumed by project needs that did not allow for transects to be run during either dive. Future trips to the Flower Garden East bank will include numerous transects as this bank which needs further evaluation of disease prevalence. I suspect that disease incidence will be higher at this site later in the summer as temperatures continue to increase.

Coral coverage and diversity, with the exception of Millepora sp. and Madracis spp., are greatly reduced at Stetson Bank. No disease was found during any dive, and I have not noted any disease or unusual undescribed conditions at Stetson Bank in the past.

The Flower Gardens have historically had a very low incidence of coral disease, and past reports, surveys, and analyses may have even overestimated true disease levels. While historical "baseline" levels of disease in any ecosystem are expected, these levels are currently unknown for the most part on coral reefs. The incidence of disease at the FGNMS is well within what would be expected for species in other ecosystems, although any level of disease of benthic long-lived species such as corals might be exceptional. Disease levels noted in this preliminary report are still considered "very low," especially in comparison to other areas of the tropical western Atlantic.

Future trips will incorporate heavier use of transect data to more accurately quantify levels of disease present. Nonetheless, coral and sponge disease is present at the Flower Gardens, and includes: 1)diseases known from other locations in the Caribbean, 2) abnormal conditions observed but uncharacterized at other sites in the Caribbean, and 3) several novel pathologies reported herein. During my last trip to the FGNMS, I saw several other novel pathologies that were not seen during this trip. Overall, these reefs appear to be very healthy, but should be monitored carefully for any outbreaks or increased reports of anomalous conditions affecting the benthic species. The nature of this reserve, both in habitat, location, environmental parameters, and isolation would suggest that any epizootic disease outbreak could have implications that would negatively impact reef diversity and structure perhaps to an even greater extent than most other more common and typical reef systems in the region. In particular, the novel characteristics of the reef system at the FGNMS provide an important opportunity to study and understand the numerous pathologies affecting these reefs and others throughout the Caribbean.

I feel it is also important to ensure that anyone involved in assessing coral disease at the FGNMS in the future be familiar with this reef system and with coral pathologies to avoid confounding reports that misidentify conditions and lesions, or misrepresent what is and is not "normal." Clearly, FGNMS managers must play an integral role because of the remoteness of this area and the limited familiarity that most persons have with the sanctuary. Managers may be among the only people familiar enough with the FGNMS to be able to accurately assess changes occurring over the short term. I think that our future trips associated with the work described in this current report will prove enlightening and will provide a much more complete picture of coral disease at the FGNMS, especially if, and when, they are coupled with more complete analysis of collected samples. Once an accurate assessment of disease conditions and incidence is available, managers should be in a much better position to monitor and report changes to what is, unfortunately, a still very incomplete picture of coral disease at the Flower Gardens.

Siderastrea sp.
-Both S. radians and S. siderea exist at Stetson and I saw numerous colonies of both.

Stephanocoenia intersepta
-I'm not sure this is valid. They are all synonymized as S. michelini by both Veron and Humann.

Agaricia fragilis?
-I will get species designations for all the agariciids on the next trip here and at the Flower Gardens

The following photos were taken during the current research cruise to the Flower Gardens and may represent anomalous conditions. The signs seen in the photos are unstudied and uncharacterized, to my knowledge.

An unusual color pattern in M. cavernosa. Although I have seen colonies with similar patterns
throughout the Caribbean, and no colony mortality has been noted. I am unsure if this is a normal
or pathological condition or appearance for corals showing such patterns or signs.

An anomalous color pattern with slight paling in a deepwater Sidearastrea siderea. The patterns
here may be indicative of fish biting. However, odd color patterns like this are seen in numerous
genera and are seemingly more common at the Flower Gardens than other locations in the tropical
western Atlantic. For example, see photos below.

Left: parrotfish focused biting, erroneously called rapid wasting disease on M. faveolata.
Right: damselfish lawns, erroneously called ridge mortality disease on D. strigosa.

Left: possible white plague Type II on on D. strigosa.
Center: Colpophyllia natans with white plague, not at the Flower Gardens, for comparison.
Right: An area of abnomal accelerated growth on M. cavernosa.

Left: unknown pathology affecting C. natans.
Right: unknown pathology affecting M. faveolata.