Chapter – IV: (implemented May 2005, in colaboration with Dr.Arnfried Antonius)^4.00 - Main Page

The primal agents for a large number of syndromes and diseases are only partially known, and in some, the chain of causal events still remains obscure. However, evidence so far collected point to a combination of abiotic (physical and chemical) and biotic (microbial, etiological, epizootiological) agents.^4.6a While specific coral pathogens are known in only but a few cases, the diversity of host pathologies indicates that a range of microorganisms are involved. These organisms in turn are thought to be opportunistic species that have (1) capitalized on the reduced health of corals, (2) find it easier to recruit under the modified environmental conditions, and (3) due to forceful introduction by man have crossed from the terrestrial into the aquatic domain.

Yet, microorganisms are essential as they induce settlement and metamorphosis in a wide range of marine invertebrate species. While the primary cue reported for metamorphosis of coral larvae is calcareous coralline algae (CCA), a specific community structure of microbial biofilms triggers larval metamorphosis of scleractinia even in the absence of CCA.^4.6b Coral reef biofilms are comprised of complex bacterial and microalgal communities which are distinct at each depth and time (see fig. 4.2). That biofilm on the surface of CCA modify the surface chemistry and thereby produce morphogenic substances has been demonstrated in other investigations as well.
Biofilms affect recruitment of larval invertebrates, while removal of that film (using antibiotic treatments) resulted in a reduction of metamorphosis of for example crown-of-thorns starfish larvae (Acanthaster planci).^4.6c Thus any alteration in the natural composition of that biofilm represents a huge danger for any successful recruitment attempt of planula larvae. Already a slight shift of a beneficial microbial community could have a drastic effect on the future of an already stressed reef-ecosystem.
The decrease in stress-resistance of corals enables otherwise “harmless” viral, bacterial, fungal, protozoic, metazoic and macroparasites (incl. Arthropoda) to take advantage of the weakened host organism. This in turn further aggravates the stress-burden on the animal and often culminates in total collapse of the colony once endolithic bioeroders (etching sponges) and epilithic settlement (filamentous algae) recruit on the denuded skeleton.^4.8 As frequently observed in the recent past of human kind, such stress-related response mechanisms can be witnessed anywhere in nature and has been tragically confirmed with the disastrous accident that occurred at the Chernobyl nuclear power plant on 26^th April 1986. There, only one major abiotic stress factor has interfered with the biota surrounding the plant – radiation. As anticipated by the Connel’s intermediate disturbance hypothesis (fig.3.14 – Chapter-III) it is not the huge burst of radiation emitted at the site, but rather the chronic and long-term exposure of biota to low-dose radiation that proved to be most damaging to host organisms; i.e. the children of the Ukraine. Overall, the chronic exposure to just one abiotic stressor (here radiation) resulted in higher total morbidity, higher metabolic abnormalities and a dramatic decrease in anti-tumor protection mechanisms. The health of these kids deteriorates exorbitantly when combined with other stressors of different origin (see fig.4.2a).
This live, man-made experiment keeps doing its damaging work to the chronically exposed children of the Ukraine and thereby gruesomely reveals the parallels with the chronic stress-burden inflicted to coral reefs (as well as other aquatic and terrestrial ecosystems - compare fig.4.2b and fig.4.2c). The trouble though, is the multiplicity of distress factors introduced by humanity. Fig. 4.2d, displays yet another example of an altered bacterial biocoenosis. Healthy Caribbean colonies of Montastrea annularis reveal a different microbial compositions than the apparently healthy tissues of affected corals. Again, the observed change in bacterial community structure are most likely related to:^4.9c

• an untypical bacterial community (as a result of systemic large-scale environmental change);
• the physiological response to environmental changes is reflected in an altered mucus production by the coral, thereby altering the conditions for coral-associated bacteria;
• the antimicrobial properties of the coral colony is altered when experiencing stress, allowing the colonization of a different community of bacteria;
• environmental stress compromises the exo-symbiotic relationships with specific microbial symbionts, which in turn result in the coral being unable to support its otherwise appropriate bacterial defences;
• when tissue damage to the coral occurs, resources from the whole colony are redirected towards the area of damage. Reallocation to the affected areas alters the overall physiology and is reflected in lower mucus production, which in turn is associated with an altered microbial exo-community.

As outlined in Chapter-III, the disturbance of the oligotrophic character of tropical marine environments, the introduction of allochthonous micro-organisms via ballast water, the changes induced due to pollution by chemicals, destructive use of reefs by humans etc. usually are not seen immediately, but over time and due to the buffing capacity of the ecosystem via a gradual decline of the overall health and vitality of the reef. Whatever the manner, these agents may feed back onto the stressed ecosystem, the dramatic changes induced in this dynamic interplay of parameters and variables negatively affect coral communities and ultimately will favor those opportunists that are best adapted to the new environmental conditions.
 
Coral Diseases - A bioerosive response to averse environmental conditions:
Regardless of the pelagic, benthic or littoral domain, diseases affect almost any marine organism (with small organisms more likely to be affected by disease and less likely to recover than larger ones). Diseases affect life span, life cycle, abundance, distribution, metabolic performance, nutritional requirements, growth, reproduction, competition, as well as organismic tolerances to natural and manmade environmental stress. Even when the disease process is arrested, or results only in minimal tissue damage, depletion of cellular and energy resources may be such as to cause irreversible harm. Eventually, the affected animals are no longer able to withstand repeated bouts of disease and attain the status of a terminally ill organism. It should be mentioned though that there is a distinction in the overall effects of disease on different organisms. Whereas disease impacts the whole animal in unitary organisms, modular organisms may suffer partial mortality, which comprises colony fecundity, but does not reduce population size. And still, diseases are a major denominator of population dynamics.^4.10 Disease is defined as “any impairment (interruption, cessation, proliferation, or other disorder) of vital body functions, symptoms, or organs”. Disease are usually characterized (1) as an identifiable group of signs (observed anomalies indicative of disease), and / or (2) a recognized etiologic or causal agent, and / or (3) consistent structural alterations (e.g. developmental disorders, changes in cellular composition or morphology, and tumors).^4.11 This definition includes both infectious diseases produced by biological agents and non-infectious diseases induced by genetic mutations, malnutrition and / or environmental factors (therefore, abiotic tissue bleaching is considered a disease).^4.12 The resistance to disease on the other hand is defined as “the natural or acquired ability” of an organism to maintain its immunity to or to resist the effects of an antagonistic agent of abiotic (e.g. elevated temperature, salinity, etc.) or biotic (e.g. pathogenic micro-organism, toxin, drug, etc.).^4.13

There is general agreement in distinguishing between a stress and an infectious agent (one would never ask what is the reservoir or mode of transmission of a stress).^4.14 However, stress and disease are inter-connected by the continuum between the healthy and the sick extremes of the spectrum. For a healthy ecosystem "pathogens" regularly "tickle" the system and thereby trigger an eu-stress response (hardening), which ultimately is expressed by a new systemic balance, visible as a lush and complex ecosystem (fig.4.3). A healthy ecosystem does not imply the absence of disease – rather it is omnipresent; the difference here is that “pathogens” occupy reservoirs, and thereby are kept at bay.

As anticipated in Chapter-II (microbial intelligence and quorum sensing) bacterial associations utilize sophisticated communicative skills to establish social lives for the benefit of the group. Doing so implies a collective memory that uses and generates common knowledge, which in turn is used to develop a group identity and to recognize the presence as well as the identity of other colonies. Such learning from experience coupled with the engagement in cooperative decision-making assigns bacterial aggregations a kind of social intelligence.^4.16a As with multi-colonial communities (i.e. the bacterial biofilm found on coral mucus) "microbial" intelligence is usually used to perform specific tasks and to coordinate the work for the benefit of the entire community.^4.16b This kind of job partitioning becomes evident when considering that some bacteria keep valuable information that is costly to maintain and can be hazardous for other bacteria to store. Evidence that there is such a decision-generated response comes from the fact that the percentage of these competent cells is strictly controlled. Such information is directly transferred by conjugation to potential partners; e.g. antibiotic resistant bacteria use cross-talk to emit chemical signals thereby announcing this fact, while those in need of that information, emit pheromone-like peptides to declare their willingness to accept such information.^4.16c These kinds of biochemical messages are not only used in intra-bacterial cell–cell talk but also across colonies of different species to exchange meaningful information as well as with other organisms such as the coral host.^4.16d This enables bacterial colonies to attain the sort of behaviour so far observed only in multicellular organisms. Thereby the bacterial association achieves not only an elevated degree of complexity, but their plasticity enables them to better adapt to whatever growth conditions might be encountered.^4.16j Going a step further, this implies that bacterial genome cybernetics must possess the ability to perform information processing and to the genome accordingly;^4.16e i.e. transposable elements of non-coding parts of the DNA may be used to reconstruct new coding sequences. Rather than waiting for mutations to occur randomly, cells may keep some genetic variation on hand and move them to become phenotypically expressed if they turn out to be beneficial for their life cycles.^4.16f This response pattern is especially evident among many Gram^NEG bacterial species and becomes active once species density exceeds a threshold.^4.16g Here in particular such bacteria make use of quorum-sensing molecules, which trigger / turn-on the expression of a variety of genetic suites; e.g. virulence genes, multiple exoenzymes, antibiotic production, conjugation etc.^4.16h Thus, unfavorable environmental conditions not just stress the coral host, but also favor microbial responses that pave the way for pathogenic proliferation. Together, environmental stress and bacterial quorum sensing trigger either opportunistic infections or a breakdown in the symbiotic milieu of surface bacteria and viruses.^4.16i Studies on reservoirs and modes of transmission of infectious diseases have led to some of the most useful discoveries for combating disease of plants, and animals (incl. humans). These “localized” remedies though, should be viewed as a tool to temporarily shift the balance and to gain a temporal advantage. In the long term and from a holistic perspective, any delay in the eradication of the sources of disturbance facilitates the outbreak of similar / different and even more aggressive disease on a broader more systemic level with far more devastating consequences (e.g. so far the use of modern pharmaceuticals such as antiviral and antimicrobial medications are useful for emergency treatment, but at the same time long-term use enables these pathogens to evolve to multiple drug-resistant strains). We should keep in mind that both agonist and antagonist are parts of the same system; the elimination of one automatically disturbs the existence of the other.

Abiotically induced diseases regard those structural and functional body impairments that result only from exposure to abiotic environmental stresses such as changes in physical conditions optimal for growth (salinity, temperature, light intensity or wavelength, sedimentation, oxygen concentrations, currents) or exposures to toxic chemicals (such as heavy metals and organics like crude oil, its derivaties and even pesticides). Biotically induced diseases are those in which the etiolic agent is a living organism such as opportunistic pathogens or parasites that take advantage of a weakened host organism. Infectious agents, those that are spread from host to host, include viruses, bacteria, fungi, and protozoans (also known as microparasites), and metazoans such as helminths and arthropods (macroparasites).^4.17 Often a pathogen or true parasite does not seriously harm the coral host unless it is experiencing stress from other biotic or abiotic sources. Thus, identifying a causal agent of a particular coral diseases and assigning it either biotic or abiotic features is rather reductionistic as both types are often closely interrelated. Usually, an abiotic disease can become complicated by secondary infections from otherwise harmless micro-organisms. In general, the adaptive relationships between micro-organisms and their hosts are effective only for precise circumstances under which this adaptation evolved. Any departure from this normal state is liable to upset the equilibrium and to bring about a state of disease.^4.18 Hence, the outbreak of coral diseases has to be considered as the result of adverse environmental changes - changes that are attributable to human activities.

Environmental changes do affect the physiological equilibrium between bacteria already present in the “healthy” microbial associations of reef organisms (i.e. in MPSL) and host tissues. However, rather than stimulating bacteria living in reef sediments into becoming more virulent, these bacteria seem to have an easier task in affecting the already stressed coral population. As will be outlined further below, the role of microbes as the final agents and and the response of the coral population to disease provide some clues to the phenomenological link in the combined area of coral health, environmental stress, and disease.^4.19 Yet, still very little is known about the composition and dynamics of the natural microbial communities living in association with most reef organisms.^4.20 Thus, it is not surprising that our knowledge of microbial pathology (isolation and identification of a pathogen), etiology (macroscopic signs of relationships between the host and the pathogen), and epizootiology (local and geographic distributions, environmental correlates, host ranges, prevalence, impact, vectors, and natural reservoirs, and spatial and temporal variability, etc.) of most coral reef disease is very limited.^4.20

Although some coral species survive severe disease events (e.g. abiotically induced tissue bleaching) in the period immediately following thereafter, it still leads to major structural shifts in coral communities.^4.21 Indeed the ecological importance of diseases is not exclusively dependent on their capability to wipe out entire populations, but to some extent by the intensity the community and population dynamics of their hosts are affected – including those of related species.^4.22 The immediate change of species dynamics in species succession can be observed on recently denuded coral substratum; it immediately leads to colonization of filamentous algae (fig.4.4). If the climax community is disturbed then late-successional changes result in a bifurcation by favoring the establishment of frondose algae rather than resettlement of stony corals (compare with fig.4.3).^4.23 The loss of coral due to disease leads to long-term changes not only in the form of a loss in reef complexity, but also in the reduction in refuge for fishes and a consequently a decline in fish stocks.

As mentioned in Chapter-I (fig.1.2a) the entire reef-biomass from the virus to the whale shark roughly corresponds to those of autotrophic organisms. In fact, the large photosynthetically active area of reef surfaces, the great abundance of photosynthetic active radiation (PhAR) and inorganic carbon (CO₂), and their small size coupled with high specific productivities makes it so worrisome when key populations such as corals vanish on a vast scale.^4.25 It has been amply shown that large-scale outbreak of diseases significantly alters the structure and function of a reef-ecosystem. The increasing number of such diseases directly affects the presence of marine plants (algae and seagrass), species diversity of invertebrates (soft corals, crustaceans, echinoderms, etc.) and shows adverse effects on the macrofauna (turtles, herbivorous and carnivorous fish, etc.), thereby changing the entire structure and species composition at all trophic levels.^4.26

Today, diseases have possibly become the most important factor in the deteriorating dynamics of coral reefs – particularly those of the Caribbean. Because of the rapid emergence, high prevalence and virulence of coral diseases and syndromes, the Caribbean has been dubbed the "disease hot spot".^4.27 A similar trend, though less aggressive but still of great concern are the 22- to 150-fold increase in the abundance of white syndromes on outer-shelf reefs in the northern and southern sectors of the GBR.^4.28
Although increased awareness and regular monitoring may explain some of this increase (fig.4.5), many diseases, such as white plague, are so common and so distinctive that their first description may reasonably be assumed to be a milestone in the phenomenon influencing the population dynamics of corals.
Fig.4.2.e reveals the occurrences of coral diseases compiled from observations of variety sources, mainly from UNEP-WCMC Global Coral Disease database.^4.29b

Selected Coral Diseases: The following section gives a brief overview of diseases (both of abiotic as well as biotic character) affecting hexa-, octocorallia and coralline algae. The response of an affected organism and the so-called associated “pathogens” (at least where these are known) that most likely are involved in the triggering process and thereby evoking the characteristic physical manifestations are presented herein. Generally, the term disease should be used for any affliction for which an underlying agent has been identified, and syndrome for those afflictions for which none of this kind was found so far.^4.30
While this chapter focuses primarily on the bioerosive properties of microbial relationships, Chapter-V highlights the effects of bioerosive capabilities of higher taxa.

Black Band Disease (BBD): It affects corals worldwide and is characterized by a dark pigmented microbial mat. This mat is usually about 1 to 30mm wide and ca. 1mm thick and separates living tissue from the recently denuded skeleton. The microbial consortium that composes the band is dominated by a filamentous cyanobacterium - the identity of which has long been believed to be Phormidium corallyticum (fig.4.6).^4.31 However, recent studies utilizing molecular techniques to characterize the BBD consortium revealed that the prokaryotic members of the mat are not associated with the genus Phormidium.^4.32a 16S rRNA gene sequencing identified at least 3 different taxa of cyanobacteria associated with BBD and determined that these taxa vary between the Caribbean and Indo-Pacific. In the Caribbean, the BBD mat is dominated by an unidentified cyanobacterium most closely related to the genus Oscillatoria.

On the other hand, any Indo-Pacific-associated BBD-cyanobacterium is most closely related to the genus Trichodesmium. However, this genus (specifically T.tenue) has also been isolated from BBD mats in the Caribbean. Other microbes identified in the BBD consortium include sulfate-reducing bacteria Desulfovibrio spp., sulfide oxidizing bacteria Beggiatoa spp., a multitude of heterotrophic bacteria, and a marine fungus. So far 19 (of 66) Caribbean shallow-water scleractinian species and 45 (of approximately 400) Indo-Pacific scleractinian species are susceptible to BBD.^4.33 The microbial consortium is not homogenously distributed but rather seems to be clustered in three main strata. The uppermost stratum is occupied by cyanobacteria that undergo oxygenic photosynthesis during the day, producing an oxygen supersaturated oxic zone in the band. Furthermore, cyanobacteria adapt to the high sulfide environment of the disease band by performing oxygenic photosynthesis in the presence of sulfide. The anoxic lower stratum of the band is dominated by sulfate-reducing bacteria Desulfovibrio spp. The oxic/anoxic interface in-between contains sulfide-oxidizing bacteria Beggiatoa spp. This centermost zone migrates vertically on a daily basis in response to changes in light intensity and photosynthetic activity occurring within the band. At night and in absence of oxygen production, Desulfovibrio spp. undergo sulfate reduction, thereby increasing sulfide concentrations within the band. As a result, sulfide is present throughout the band at night and the oxic/anoxic interface migrates to the surface of the band. Presence of sulfide and anoxia at the lower stratum of the band (adjacent to coral tissue) is thought to be the cause of tissue lysis and death. Because the band directly overlies coral tissue that is being degraded, nutrients supplied by tissue mortality diffuse directly into the band, thereby providing concentrated nutritional supply to the microbial consortium, and further fueling their growth and reproduction.
BBD typically starts at the base of the coral where protective mucal secretory glands are absent and progresses at an average rate of 3mm·d^–1 across the colony (sometimes it advances even up to 10mm·d^–1).^4.34 This rapid rate of tissue loss, coupled with the slow growth rate of scleractinian corals, quickly denudes the skeleton from living coral tissue and induces colony death. However and quite frequently, BBD disappears before causing complete colony mortality. This cessation of BBD most often occurs with the onset of lower seawater temperatures. Seasonality of BBD is related to summer seawater temperatures in excess of 25°C. It is important to note that BBD has been reported year-round, even at seawater temperatures as low as 20°C, and that the cyanobacteria associated with BBD are capable of photosynthesis at temperatures as low as 18 and 20°C.^4.36 It was further noted that coral colonies killed by BBD did not show any scleractinian recruits even after 2 years of observation.^4.37 It has been proposed that BBD is correlated with other environmental and physiological stressors, including terrestrial runoff, coral overgrowth by algae, eutrophication, and pollution, including human fecal contamination. So far even the mechanism of BBD transmission remains unknown.

Coralline Algal Diseases: Although not directly associated to reef-building corals, it is noteworthy to mention diseases that affect another framework-builder, those affecting coralline algal. Like those observed in corals, such diseases, likewise have huge adverse effects on the structure and function of many reefs. Since dead corallinacea / scleractinian, no longer contribute to the productivity and carbonate accretion processes, filamentous and fleshy algae overgrow the bare skeletons. In turn, this dense secondary overgrowth inhibits settlement of coral recruits (i.e. larvae) and the potential recovery of the reef.

Coralline Lethal Disease / Syndrome (CLD/S): A few years ago it was noted that on some Caribbean reefs, and more recently in the Indian Ocean and off the Philippines the pink algal tissue of encrusting coralline algae has largely disappeared.^4.38 CLD/S reveals itself as a 1-2mm wide whitish margin. The denuded coralline thallus turns green as overgrowing filamentous algae take over (see fig 4.7). So far the causes remain unknown.^4.39 On Cades reef, in the Caribbean, up to 60% of the encrusting algae have been killed by the end of 1996.^4.40a A similar problem, although not on such a vast scale was observed during a 1998 survey while monitoring the recovery of heavily bleached reefs at the Seychelles (during the 1997/98 ENSO event). However, as a follow-up survey showed, that the recovery of corals, coincided with a lowered prevalence of CLD/S and CLOD (see below) than during the bleaching event, but both syndromes were still actively affecting coralline algae.
Thus, a 1997 reef survey in the Philippines revealed little coral mortality. The few skeletal areas available were covered with the encrusting calcareous red algae Porolithon, which was somewhat affected by CLD/S.^4.41

Coralline Lethal Orange Disease (CLOD): Already in 1994, Littler & Littler reported the appearance of a bacterial pathogen of encrusting coralline algae on reefs of a large part of the south-eastern Pacific (Cook Islands, Fiji, Solomon Islands, and PNG).^4.42 Microscopic examination highlighted motile gliding rods of a yet unidentified colonial bacterium in a mucilaginous matrix.

This pathogen reveals itself as a bright orange coloration and rapidly spreads across the algal surface, leaving behind the bleached skeletal carbonate remains of the coralline algae. When the pathogen reached the margin of the algal thallus, it formed upright filaments and globules, similar to those formed by terrestrial slime molds (fig.4.8). Experimental studies confirmed that the pathogenic globules were highly infectious to a variety of coralline algal species.^4.43a As with the above, the recent appearance of this disease likewise affects the framework structure and function of many reef sites. Because dead corallines no longer contribute to productivity and carbonate accretion processes, and fleshy algae overgrow the dead coralline algae and inhibit the settlement and growth of reef-building corals, bioeroders easily take advantage of this substratum and degrade it at an accelerated pace.

Dark Spot Disease / Syndrome (DSD/S): This syndrome is widespread throughout the Caribbean and affects 11 scleractinian species.^4.44 First it was thought that this disease impacts only the columnar morphs of the Montastraea annularis complex (M.faveolata and M.franksi), until it was recognized that similar signs were observed on Siderastrea siderea, Colpophyllia natans, M.cavernosa, and Diploria strigosa.^4.45 DSD is characterized by irregularly shaped dark spots of purple, maroon, or brown coloration on normal tissue. It can easily be associated with tissue necrosis in which, a spot expands into a characteristic dark ring separating dead skeleton from living tissue. Over long periods of time, DSD/S causes also the creation of distinct and typical depressions on the coral surface(fig.4.9). In DSD/S-affected Stephanocoenia michelinii the dark pigmented areas extends into, and stain the skeleton. In DSD-affected Siderastrea siderea the skeletal staining is not evident, but endosymbionts do appear swollen and necrotic. These observations suggest that similar signs observed on S.michelinii and S.siderea may in fact represent two different diseases. In the Caribbean, DSD/S correlates with depth (more prevalent at depths <10m) and elevated temperatures (>28ºC).

This depth-related distribution may be related to the higher prevalence (94%) of two coral species that occupy shallow depths, i.e. Siderastrea siderea and Montastraea annularis. The average loss of tissue due to the action of DSD/S was 0.51cm²/month for S.sidera and 1.33cm²/month for M.annularis, while other species show higher rates of progression. The distribution of DSD/S on Colombian reefs is clumped, indicating that the disease may be contagious and therefore of biotic origin. So far, the causal agent of DSD/S is unknown, but microbiological studies of the MPS-layers of affected colonies showed small changes in the composition of the microbial communities living in association with healthy and diseased corals. A bacterial strain metabolically related to Vibrio carchariae (compare also biotically induced TBL) was found in samples of disease corals from both species.^4.47

Pink Line Disease / Syndrome (PLD/S): This anomaly was first reported in 2001 affecting the scleractinian corals Porites compressa and P.lutea across the Indian Ocean. On Kavaratti reef (Lakshadweep island group) about 10% of P.lutea colonies were found to be affected by this syndrome leading to partial mortality of of affected colonies. PLD/S is characterized by a band of pink-pigmented tissue separating dead skeleton from apparently healthy tissue (fig.4.10). The pink-colored polyps constituting the band can vary from few millimeters to a centimeter in width.^4.50 This band may begin as a small ring and progresses outward horizontally across the coral colony.

As with other coral diseases, the zone of dead skeleton is bright white in appearance, indicating a relatively rapid rate of progression. The dead patches are subsequently colonized by the cyanobacterium Phormidium valderianum. In addition, the fungi Curvularia lunata and a hyaline non-sporulating form are found to be frequently associated with PLD/S (see also Chapter-V – Bioerosion by fungi). In addition, endosymbiotic densities in affected areas are reduced and are large-sized with much shorter doubling time when compared to the healthy tissue. Ultimately, as the diseases progresses, the symbionts are expelled indicating that physiological disruptions within the coral's soft tissue are the driving factors behind tissue necrosis. Indeed, histological analysis revealed that the cyanobacterium does not penetrate the tissue at any contact point - the only filaments found were those in the debris of destroyed tissue. As a result, it is assumed that elevated levels of pCO₂ (due to the metabolic activity of the cyanobacterium) may induce the pink coloration in the affected tissues.^4.49 Nonetheless, by applying Koch’s postulate it was possible to associate the cyanobacterium along with the fungi as the triggering organism that induces the pink coloration and coral tissue degeneration.

Red Band Syndrome (RBS): About at the same time when BBD was first documented, a similar band disease (although different in color) was detected to affect the Caribbean soft corals Gorgonia ventalina and the hard corals Montastraea annularis, M.faveolata as well as species of the genus Siderastrea.^4.51 More recently this syndrome has also been observed in the Indo-Pacific region (Fig.4.11). RBS is characterized by a red-brown to brown-black microbial mat that forms a migrating band separating recently denuded skeleton from living tissue.^4.52a

The condition was considered not to be BBD because Phormidium corallyticum, accepted at the time to be the dominant component of the BBD consortium, was not present within the red band. Instead, it was populated by other cyanobacterial species, identified as Schizothrix calcicola, S.mexicana and Oscillatoria spp. Yet, the RBS microbial consortium may include even other cyanobacteria, heterotrophic bacteria, the sulfur-oxidizing bacterium Beggiatoa sp., and the nematode Araeolaimus sp. The recent discovery that BBD is associated with at least 3 different taxa of cyanobacteria and the lack of new reports of RBS since the early 1990s, suggest that RBS may not at all be a distinct disease, but rather BBD.^4.53 While RBS is only infrequently encountered in the Caribbean, it seems that its Indo-Pacific counterpart is particularly common at the GBR (in south-east Asia and Oceania this variant is known as brown band syndrome). Affected Indo-Pacific species display a white zone between the healthy tissue and the band, which may be composed of bleached tissue and / or denuded skeleton. Recent work point at the ciliate Helicostoma nonatum as a possible pathogen. In aquaria, the brown-jelly-like condition on corals is thought to be associated with it. In aquaria, the brown-jelly-like condition on corals is thought to be associated with it. However, this ciliate infestation has not yet been reported from in-situ corals so far.^4.54

Shut Down Reaction (SDR) or Rapid Tissue Necrosis (RTN) most often affects corals contained in aquaria and occurs in two primary pathways: apoptosis and necrosis. Apoptosis can be triggered by bacteria, stress, chemicals, hypoxia, trauma, high intracellular calcium levels, and various other agents that trigger an intracellular or extracellular initiation of the apoptotic cascade. Since apoptosis is a highly conserved, noninflammatory, sequentially ordered cell death program, apoptotic cells are characterized by shrinkage, condensation and margination of nuclear chromatin followed by DNA fragmentation (laddering), membrane blebbing and other distinct cellular changes. So far, the occurrence and mechanisms by which apoptosis occurs in corals has not been well investigated. In contrast, necrosis is characterized by cellular swelling, diffuse degradation of cell contents, and is not sequentially ordered. Necrosis frequently occurs as a result of trauma and disease processes.^4.55a To date it has only rarely been observed in in-situ corals. Since SDR is comparable to a shock-related response, it usually occurs on wounded corals (e.g. tissue lesions due to physical damage inflicted by predation, diver contact, or other mechanical agents) and is always associated with synergistic abiotic environmental stressors (e.g. temperature extremes, sedimentation, etc.).^4.55b

SDR begins locally and radiates outward from the “wounded” area into obviously healthy tissue. Tissue is sloughed off at an extremely rapid rate of 10cm·h^–1. Hence, once SDR is triggered, complete colony mortality is inevitable. SDR is contagious, indicating the presence of a pathogen, which seems to be transmitted both directly and indirectly from an infected colony to a stressed, but apparently healthy colony. To trigger SDR, it is sufficient to bring neighboring colonies in physical contact with each other. As with white-band disease (especially WBD-I, see below), SDR appears to lack any consistent causal pathogen. Yet still, SDR is a highly contagious pathology. ^4.55c However, it cannot be transmitted to unstressed colonies. SDR has been experimentally induced in aquaria among six Caribbean scleractinian species.^4.56 In the Caribbean, SDR has been reported to affect only 3 individual coral colonies in the field (the species involved were Montastraea annularis and Acropora cervicornis). Prior to the reports of SDR in the Red Sea in 1997/98, new cases of the syndrome have not been documented since the first report in the late 1970s.^4.57a

Abiotically induced Tissue Bleaching (TBL): The worrying fact here is that mass coral bleaching events involve entire reefs. Indeed, 1000s of km² may be affected in any single event, which may stretch across several tropical oceans at once. Although TBL is a global phenomenon, it was unknown to the scientific literature prior to the mid 1970s.^4.58a Since tissue bleaching is associated with warming of surface waters by ~2ºC for a period exceeding a few weeks, any direct involvement of a pathogen can be excluded (although stressed colonies with an altered microbial association on the MPS-layer with a suppressed tolerance windows are the first to respond to such abiotic changes).

High irradiance of Photosynthetically Active Radiation (PhAR) and Ultra-Violet (UV), as well as other stressors (such as pollution and osmotic shock) are known to precipitate bleaching, either alone or synergistically. Mass TBL has been the most conspicuous coral disease to strike coral reefs over the past 20 years. Notably, there have been six major periods of mass bleaching (1979-80, 1982-83, 1987, 1991, 1994, 1998), all of them associated with the so-called ENSO phenomenon (El Niño - Southern Oscillation, typified by clear skies and no wind leading to increased levels of both PhAR and UV radiation (fig.4.13).

During each event and over a period of several weeks, corals loose their characteristic brown coloration and take on a brilliant white (bleached) appearance (see fig.4.14 and cover image in Chapter-I). Since the loss in pigmentation is due to the reduction in the number of endosymbionts, it is not surprising that it involves many different species of corals, thereby affecting entire reef systems, with a world-wide geographical distribution. It is generally accepted that TBL of this kind is the result of photoinhibition (a model proposed in Chapter-II). This model states that high solar irradiance, results in an excess production of oxygen free radicals and other toxic products within the chloroplast of the endosymbionts, triggering expulsion of the endosymbionts.^4.59 With bleaching extending over weeks, it removes the principle dietary powerhouse, leads to atrophy and eventually to tissue necrosis. Along with the loss of nutrients, mucus secretion, and ciliary beating, amoebocyte densities within the coral are reduced, leaving polyps more susceptible to penetration by opportunistic secondary infections of microbial origin.^4.60

Abiotically induced TBL is associated with calm and warm conditions occurring within the inter-tropical convergence zone (ITCZ). Under such conditions TBL usually starts in the southern Indian Ocean, follows the warm low-pressure monsoon moving north until it becomes evident in the northern Indian Ocean.
Species most susceptible to TBL include species with branching morphologies. Within a month of peak temperatures, these are the first ones to die.^4.61 In many cases, mortality rates may rise to as much as 80-100% within the affected area. It should be mentioned though that abiotically induced TBL can also be triggered with temperature lows falling below the bottom end of the thermal tolerance window (fig.4.14).
It is interesting to note however, that colonies of Pocillopora in the Panamanian Pacific that contained members of Symbiodinium clade C were susceptible to bleaching, while conspecific colonies containing Symbiodinium in clade D were unusually resistant to bleaching.^4.62a

If adverse abiotic conditions are limited in duration, individual corals experiencing TBL may recover and regain their endosymbionts from the surrounding water column (compare ABH, chapter-II). Often these coral colonies are more likely to re-acquire symbionts that are more resistant to bleaching.^4.63 Although such species do reflect higher resilience to additional abiotic anomalies the swap in endosymbiont clade is often associated with reduced growth rates (poor calcification rates) and somewhat lowered reproductive capacities that may last for years.^4.64 Eventually and without additional disturbances, recovery at the “reef level” occurs through asexual propagation and growth of surviving colonies and / or by recruitment and growth of sexually produced larvae (“ecological resilience”).

Biotically Induced Tissue Bleaching (TBL): Until recently, it was believed that TBL is an exclusively abiotically triggered disease. However, biotically induced TBL is triggered by bacterial strains with Gram^NEG properties. These strains are found within the genus Vibrio, which have extensive representation in marine ecosystems as both benign and symbiotic forms (e.g. luminescent forms are symbiotic with a range of fish and squids).^4.65 Vibrio species are typically aerobic, rod-shaped and include the causal agent responsible for Cholera in humans (Vibrio cholerae).^4.66 Yet, related microbiological species of this genus cause a significant reduction in the overall endosymbiotic algal populations of affected coral species. Furthermore, the percentage of Vibrio metabolic groups reveal that bacterial populations tend to increase during bleaching, but return to previous levels during recovery (see fig.4.2b). It is very likely that qualitative (and often quantitative) changes in coral MPSL during bleaching events favor patoghenic micro-organisms due to the increase in available carbon sources (i.e. decaying tissue).^4.67 In the Mediterranean Sea, bleaching of the allochthonous coral Oculina patagonica can be induced by an infection with the bacterium V.shiloi (fig.4.15) whereas bleaching and tissue lysis in Pocillopora damicornis (Indian Ocean and Red Sea) is induced by V.coralliilyticus (fig.4.16). Vibrio-induced bleaching and lysis are always associated with elevated seawater temperatures exceeding 24.5°C, and therefore are examples of secondary responses due to environmental stresses. Thus, diseases with etiologies associated with both abiotic and biotic factors result in immuno-compromised hosts.^4.68 Since Koch’s postulates were fulfilled and bleaching was induced upon infection in apparently healthy corals, these two Vibrio-strains are considered "real pathogens".^4.69

Vibrio shiloi-induced bleaching (VSB) of Oculina patagonica is arguably one of the thoroughly studied coral diseases in terms of etiology and mechanism of pathogenesis. And still, it should be noted that O.patagonica is not an autochthonous species of the Mediterranean, but a recent immigrant from the Atlantic Oceanan.^4.70 Thus, the equilibrium between the coral and local marine organisms may not have been understood properly.^4.71 However, the infection begins as V.shiloi is chemotactically attracted to the ß-galactoside-containing receptor on the MPSL of O.patagonica. Once the contact is established the bacteria penetrates the epidermis of the host coral, where it starts to transform into a viable (but non-culturable state), to multiply and to produce both heat-stable and heat-sensitive toxins that target symbiotic algae, termed "toxin P". These proline-rich dodecapeptides bind to the endosymbionts and inhibit photosynthesis. In the presence of ammonia or NH₄Cl the bacteria ultimately contributes to coral bleaching, indicating that eutrophication does influence the severity of the symptoms.^4.72a

Usually, the high concentration of oxygen and resulting oxygen radicals produced by the endosymbionts during photosynthesis is highly toxic to bacteria and is one of the mechanisms by which corals usually resist infection (see Chapter-II). In order to survive inside the host coral, V.shiloi produces anti-oxidant enzymes such as superoxide dismutase (SOD). However, sufficient levels of both "toxin P" and SOD can only be produced under conditions of elevated seawater temperature (e.g. 30°C). Thus, during winter, when water temperatures drop to 16°C, intracellular V.shiloi lyse and die. Only then can corals affected by VSB recover. Since it seems that V.shiloi can survive the temperature shift inside the coral host, the coral itself may play a role in seasonal demise of the pathogen by reinfecting itself the following summer. During winter and at least in part, the marine fireworm Hermodice carunculata serves as a reservoir and a vector of V.shiloi (0.6-2.9·E⁸ V.shiloi cells per worm were found). Whereas in summer, when the worm feeds on O.patagonica, the VSB pathogen is transmitted to just a few coral colonies, indirectly restarting the infection process and facilitating the spread from colony to colony.^4.73

Vibrio coralliilyticus induced bleaching (VCB) is host-specific as it affects only the scleractinian coral Pocillopora damicornis and possibly closely related species such as Stylophora pistillata.^4.74a After adhesion to the MPSL is complete (approx. after 12h) this Gram^NEG bacteria begins to penetrate into the coral, (from 24-72h), the intracellular bacteria multiply to reach densities of up to 1·E⁹ bacteria per coral fragment. VCB produces a potent extracellular protease which causes bleaching and lysis of coral tissue (bleached corals develop a high degree of necroses). It triggers bleaching at 24.5 to 25.0°C seawater, and tissue lysis and colony death at 27 to 29°C. Bleaching does not precede lysis at temperatures greater than 27°C. VCB is infectious and can be transmitted through direct contact between an infected coral colony and an un-infected neighbor. V.coralliilyticus produces an extracellular protease that may play a role in pathogenesis, and production of this enzyme increases with temperatures greater than 24°C.

Elevated seawater temperature and solar irradiation, including UV, increases either pathogen virulence or host susceptibility, or both. Since V.coralliilyticus is widespread (was isolated in the Indian Ocean, Red Sea, and in the Atlantic Ocean), it is assumed that this VCB is of frequent and circum-tropical occurrence.^4.75

Tumors (TUM): A tumor is an abnormal tissue proliferation and, in corals, is often associated with abnormal skeletal growth. Tumors result from neoplasia, hyperplasia, or hypertrophy. Such coral anomalies are characterized by: (1) thinning of coral tissue covering anomalies, (2) increased porosity of coral skeleton, (3) loss of mucous secretory cells and nematocysts, (4) loss of endosymbionts, (5) loss, reduction, or degeneration of normal polyp structures, and (6) reduced fecundity.^4.76 These anomalies pose a serious threat to affected corals. Compromised primary defense mechanism due to TUM and impaired mucus secretion inhibits removal of foreign material from the coral surface, contributes to cell death and increases the coral’s susceptibility to invasion by filamentous algae. In addition, porous skeletons are more susceptible to storm-related damage.

Neoplasia (neoplasm, or calcioblastic epithelioma) characterizes an uncontrolled cell proliferation. The coenosteal skeleton of the affected area is more porous and connects the polyps by tiny canals – this alone facilitates the exchange of nutrients throughout the colony and in particular of the diseased region. The polyps disappear from the margin of the tumor toward its center, and there is an increase in coenosteal skeleton, so that the center of the tumor attains a smooth appearance (fig.4.17). In addition, the unusually porous and globular mass of the skeleton is raised above the surface of the colony and has only few discernible polyp structures. The cells found in the tumor are "bubbled" in appearance and resemble the more metabolically active and rapidly dividing cells of growing branch tips. Like them, the diseased regions lack symbiotic algae as well as secretory mucus cells. This facilitates sediment accumulation and thereby easily damages the underlying tissue. Furthermore, calicoblastic epitheliomas damage portions of coral branches, leaving them more susceptible to invasion by boring organisms which themselves lead to increased breakage and fragmentation rates. With no polyps present in the affected area the coral produces reduced numbers of eggs and sperm.^4.77a

Histopathological analysis confirmed that tumorous tissues are undifferentiated and differ to those of healthy areas. These calcified protuberant masses on branching corals loose their normal structure and consist of undifferentiated calicoblastic epithelial cells. These calicoblastic epitheliomas result from proliferation of calicoblasts and associated tissues and are characterized by raised (up to 1cm high), irregularly shaped, smooth, white lumps that develop on all parts of the coral colony. Due to the rapid metabolic rate of the tumor, the rate of skeleton deposition is much quicker than normal, unaffected tissue.^4.78 Mean growth rate of tumors are around 0.12mm·d^–1 or 25 to 44mm· yr^–1. ^4.79 The cause(s) of neoplasms in hard corals are still unknown. Both genetic (mutations of the genome and/or programmatic changes in gene expression of the coral cells) and environmental factors (such as ultraviolet radiation, etc.) appear to affect the distribution of tumor-bearing colonies. So far a direct relationship has not been identified.^4.80 Acroporids appear to be the most susceptible to neoplasia, and this may be due to the rapid growth rates implied in this genus (a healthy Acropora palmata colony is capable of linear extension rates of 47 to 99mm·yr^–1). In the Caribbean, calicoblastic epitheliomas affect mainly Acroporidae, whereas throughout the Indo-Pacific it has been reported on A.valenciennesi and A.valida.^4.81 With the exception of microorganism-induced nodule or gall formation (e.g. fig.5.26, Chapter V), the etiology of coral skeletal anomalies is unknown. Solar UV radiation has been hypothesized as a possible initiator of neoplasia formation.

Hyperplasia (hypertrophy, gigantism, corallite distortion) is characterized by accelerated growth through a rapid increase in the number of cells (non-neoplastic proliferation), but otherwise retain their typical "normal" cellular structures (fig.4.18). Patterns of ridges and valleys (in brain corals) or circular polyps (star corals) in affected regions are pronounced (largely increased cell sizes), and protrude above the colony surface. Depending on the species, the raised spherical masses can project up to 4.5cm above the surface of the colony. Observations on Magnetic Island (GBR) found that 18-24% of populations of Platygyra pini and P.sinensis are affected.^4.82a

In some cases it was found that polyp hypertrophy characterized by gall formation is the result of a parasite-induced proliferation within the tissues. These lesions for example on Madrepora spp. develop when the crustacean Petrarca madreporae, an obligate endoparasite of corals, invades a normal coral polyp as a larva and matures within the polyp. It results in the formation of an enlarged (hypertrophied) corallite with abnormal septae (see Chapter V). The scleractinian corals P.lobata, P.lutea, Manicina areolata, and Montastraea cavernosa can detect invasion by endolithic fungi and respond by surrounding the site of fungal penetration within a layer of thickened calcium carbonate produced by hypertrophied calicoblasts. Skeletal anomalies caused by tumors affect 16 Caribbean and 24 Indo-Pacific Scleractinian species, 1 Caribbean hydrozoan, and at least 5 species of Caribbean gorgonians.^4.82b

White Band Disease (WBD): As with most other diseases, WBD ravages almost since three decades throughout the Caribbean and has decimated large coral populations on a regional level.^4.83a The loss of tissue results in a distinct band or line of bare white skeleton so characteristic for WBD. Recently, the disease has been re-grouped according to their varying expressions observed in nature. The rapidly progressing form has been renamed WBD-I; it affects both branching Acropora palmata and A.cervicornis and distinguishes itself from the more slowly progressing WBD II, which affects exclusively A.cervicornis. WBD-I causes extensive mortality as it progresses with up to 2cm·d^–1 and usually develops at the base or branch of a coral colony and progresses upward toward branch tips in a concentric ring (fig.4.19).

In WBD-I, the white band of recently denuded skeleton is adjacent to a necrotic front of normally pigmented living tissue. On the other hand, WBD-II is distinguished from former by a 2-20cm wide band of “living but bleached” tissue that separates the normally pigmented tissue from the denuded skeleton. Since bleaching of the tissue in WBD-II occurs in rapid but interrupted waves, the gradually moving necrotic margin is eventually capable to catch up. Although WBD-II progresses a lot slower than type I, the difference between them fades once the necrotic margin has merged with the bleached front. As with the other, WBD II can develop at the base of a coral colony and progress upward. However, it is also capable of developing at tips of branches to progress downward.^4.84 Histopathological examination of WBD I-diseased tissue of apparently healthy Acropora palmata and A.cervicornis revealed the presence of Gram^NEG rod-shaped bacterial aggregates in the calcioblastic (skeleton-producing) epidermis that lined the gastrovascular canals of the porous skeleton, and are more abundant in diseased corals than in apparently healthy corals. However, other apparently healthy and diseased acroporids do not contain aggregates. Since no consistent assemblage of microorganisms could be found at the junction separating the sloughed off tissue from the bare coral skeleton, the role of bacterial mediators in WBD-I remains uncertain. This is different in the case of WBD-II. Here it was possible to document a shift in the composition microbiological populations present on and within the surface MPS-layer; in particular a shift from pseudomonads to one dominated by Vibrio carchariae (compare TBL).^4.85 Due to the difficulty in maintaining healthy corals of Caribbean acroporids in laboratory aquaria, attempts to fulfill Koch’s postulates with V.charcharia were unsuccessful, thus leaving the significance of the bacterium in the dark.

White Plague Disease (WPL): White plague has affected the Caribbean and since the 1970s but was likewise observed on Indo-Pacific corals a decade later. Previously grouped under WBD, it became soon obvious that there are major differences, and more recently experts tend to differentiate it further into three sub-categories.
WPL-I, the Caribbean variation, is characterized by a sharp boundary layer that separates normal from necrotic tissue. Yet unknown coccoid bacteria occupy this interface. Histopathology of WPL-I affected tissues show necrotic lesions at their boundaries accompanied by dense clusters of coccoid bacteria. The necrotic band migrates with a rate of 3mm/day. Currently some 13 Caribbean scleractinian (including the very rare Dendrogyra cylindrus) are affected by WBD-I (fig.4.20).
WPL-II is not much different, only the fact that a recently discovered new bacterial genus with the representing species Aurantimonas coralicida makes it different.^4.86a So far pathogenesis and transmission of WPL-II are not understood.^4.86b In addition, 16S rDNA sequencing indicates that A.coralicida is not the only microorganism associated with a WPL-II affecting Caribbean corals. At this stage, the highest disease prevalence of WPL-II has been recorded for Dichocoenia stokesi (fig.4.21).
Because it affects small coral colonies (normally 10cm in diameter), tissue loss occurs at rates of up to 2cm/day, thereby routinely killing entire colonies in two to three days (with mortality rates as high as 38%). ^4.86e

Another aspect of WPL-II that differentiates it from type-I is its rapid rate of progression (around 2cm·d^–1), and the irregularly shaped front "eating" its way into the normal tissue. At times, a narrow band of bleached tissue (2 to 3 mm wide) separates the normally pigmented part from the bare skeleton. However, it is more common to find a disease line resembling that of WPL-I, i.e. healthy tissue is immediately adjacent to recently denuded tissue – in this case differentiation is almost impossible. Another distinguishing characteristic of WPL-II is that infection most often begins at the base of the coral colony where protective mucal-secretory glands are absent and progresses upward in a concentric ring around the entire colony.^4.86 The number of species affected by WPL-II is increasing and currently includes 32 species of scleractinian corals affected on Caribbean reefs - the reservoir is still not known.^4.87
WPL type III, first seen on Florida reefs in 1999, spreads even more rapidly than the other two, to reach extremely high rates in the order of dm/day. It starts on the sides or top of colonies and greatly exceeds loss rates attributed to WPL-I and II. It exclusively affects large colonies (3 to 4m in diameter) such as the massive Montastraea annularis and Colpophyllia natans.^4.88 Like with WPL-I, the reservoir and the causal agent(s) of WPL-III are likewise unknown.

White Pox Disease (WPX): White pox disease, also termed acroporid serratiosis or patchy necrosis, was first documented in 1996 on reefs off Key West, Florida and is now observed throughout the Caribbean. The disease exclusively affects Acropora palmata, and is caused by the common fecal enterobacterium Serratia marcescens, a Gram^NEG bacterium of the Enterobacteriaceae family (fig.4.22). It is found in feces of humans and other animals, in water and soil and has been found in the marine environment of sewage-polluted estuaries.^4.89a Coral colonies affected by WPX are characterized by irregularly shaped distinct white patches of recently exposed skeleton, surrounded by a necrotic front of normally pigmented living tissue. Lesions range in area from a few square centimeters to >80cm² and develop simultaneously at various locations of the colony surface. These heterogeneously distributed white patches and the potential tissue loss across the coral colony distinguishes WPX from WBD (since both affect A.palmata, the latter develops at the base of a coral or branch and progresses upward toward the branch tip in a concentric ring, whereas the former is randomly distributed).

With these characteristics, sings of WPX are easily differentiated from those of coral bleaching (TBL) and predation scars produced by the corallivorous snail Coralliophila abbreviata (see Chapter-V). The loss of coral tissue occurs radially along the perimeter of the lesion at an average rate of 2.5cm²·d^-1, and is greatest during periods of seasonally elevated temperature and rainfall. WPX is highly contagious, with nearby neighbors most susceptible to infection. Between 1996 and 2002, the average loss of A.palmata due to WPX in Florida alone was 85%.^4.90 Such severe population declines of a community’s most important primary producer and shallow water framework builder has led to the identification of A.palmata as a candidate for inclusion on the Endangered Species List.^4.91

Yellow Blotch Disease (YBL): This disease has been reported throughout the Caribbean since 1994. YBL affects 9 scleractinian coral species, but most often affects the upper surfaces of Montastraea annularis, M.faveolata, and occasionally Agaricia agaricites, Diplora labyrinthiformis, D.strigosa, Favia fragum, Porites asteroids, and Colpophyllia natans.^4.92a Massive, 200- to 300-year-old colonies of M.faveolata have been found to be severely affected by it. YBL is characterized by circular to irregularly shaped patches or bands of discolored coral tissue. At the beginning, no “band” of clean, denuded skeleton is usually present. However, as the disease progresses, the tissue in the center of the patch dies and the area fills with sediment and filamentous algae, resulting in a band of yellow tissue around the enlarging sediment patch (it was previously termed yellow-band disease, fig.4.23).

Rings or bands of yellow translucent tissue, which may in turn be surrounded by rings or bands of pale brown to bright-white (bleached) tissue, surround the dead zone. Apparently healthy tissue engulfs the outer regions of YBL lesions. Bacterial communities living on healthy M.annularis are markedly different to those ones with signs of YBL and seem to be similar to that seen in other diseases, in that several bacterial strains metabolically related to the genus Vibrio (compare TBL) were found in the mucus of diseased corals.^4.93 The rate of tissue loss associated with YBL is very slow at approximately 0.6cm per month. YBL-affected coral tissue has approximately 41-97% fewer algal symbionts than apparently healthy tissue does. In addition, these endosymbionts appear vacuolated and lack organelles. The algal symbionts within yellow and normal tissues from YBL-affected M.annularis, M.faveolata, and M.franksi were found to be of clade A, the source of the characteristic yellow color of YBL lesions. Unaffected tissues instead, were dominated by Symbiodinium sp., clade C, the taxon most common in healthy corals in depths of 1 to 10m. Furthermore, YBL associated endosymbionts have lower mitotic indices (number of dividing cells dropped from 2.5% to nearly 0%). As a result it has been suggested that YBD could actually be assigned an endosymbiotic rather than a coral disease; i.e. it kills the coral host by in-situ damage originating from the endosymbionts.^4.94 The causal agent of YBL is still unknown, a consortium of four different Vibrio-species, sea-water temperature rise (temperatures in-between 26-30ºC) and nutrient enrichment seem to increase the severity of this disease.^4.95
Yellow Band Disease (YBD) or Ring Bleaching: Although it is not yet certain that the reported sightings in the Red Sea of similarly diseased corals are identical to those observed in the Caribbean, it seems likely that they are related to each other.^4.96 First observed in the Gulf of Oman, Arabian Sea in the late 1990s, YBD manifests itself as a broad yellow-pigmented band (tissue and microbial mat) that migrates across healthy coral tissue. The similarities to BBD are striking insofar, as where the yellow band moves over healthy tissue, a band of decaying and sloughed-off tissue is observed. However, the entire area denuded by the infection often retains the characteristic yellow color. The presence of a microbial mat suggests that the Indo-Pacific form of YBD may be a variant of BBD. In addition, the rate of tissue loss is correlated with seasonally elevated temperature and peaks with about 20mm/week in summer, compared to half the rate in winter. YBD is easily transmissible from infected colonies to healthy colonies.^4.97 So far, 12 species are known to be affected by YBD include Acropora clathrata, A.pharaonis, A.tenuis, A.florida, Porites lutea, P.lichen, P.nodifera, Turbidina reniformis, and Cyphastrea microphthalma.^4.98 In any case, serious loss of coral tissue due to these diseases is occurring throughout the Caribbean and in the Arabian Gulf.^4.99