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Major mass mortalities of the most frequently affected marine benthic organisms are here summarized, reporting the causes, dynamics and documented effects of these phenomena.

The sessile mode of life is widespread in a variety of marine phyla. Sessile life requires a stable substratum. On the benthos, motile life stages and sessile adults compete for rigid surfaces making non-living, i.e. inanimate, hard substratum a limited resource. Epibiosis is a direct consequence of surface limitation and results in spatially close associations between two or more living organisms belonging to the same or different species. These associations can be specifically guided by host chemistry resulting in species-specific symbiotic or pathogenic assemblages. Most colonizers, however, are non-specific substratum generalists. The ecological consequences for the overgrown host (basibiont) and the colonizer (epibiont) can be positive and negative. The predominantly disadvantageous nature of epibiosis by microorganisms for the basibiont has resulted in a variety of defence mechanisms against microcolonizers, including physical and chemical modes of action. Besides antimicrobial effects of secondary metabolites emanating from the host, recent studies increasingly demonstrate that epibiotic bacteria associated with the host deter growth and attachment of co-occurring bacterial species or new epibiotic colonizers competing for the same niche.

Understanding the dynamics of resistance is particularly important for understanding the impacts of disease and predicting evolutionary outcomes for diseases. Predictive epidemiological models include not only terms for transmission of infectious microorganisms, but also terms for host resistance. In susceptible-infected-resistant (SIR) epidemiological models, timing and degree of resistance can determine the spread rate and impact of disease (Anderson and May 1979, 1991). Resistance 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, e.g., pathogenic microorganism, toxin, drug (Stedman 1995).” An organism that is immune to an infectious disease will not acquire it because it has a particular suite of complex structural and functional features. These features prevent the pathogenic microorganism from entering, surviving in, or multiplying within its body and causing disease by disrupting key cellular metabolic processes through the release of toxins or enzymes or by altering its structure (e.g., tissue damage through scarring), or causing cell death. Many factors can affect the condition of this system and the response to a pathogen that an individual host is capable of generating at a particular time. The interaction of host and pathogen, and how they are affected by changing environmental conditions, can affect the populations of both organisms (Garnett and Holmes 1996).

Part I Regional aspects of coral reef health and disease 1 The coral reefs of Eilat, Red Sea: past, present and future - three decades of coral community structure studies Yossi Loya 2 Coral Reef Diseases in the Wider Caribbean Ernesto Weil 3 Coral disease on the Great Barrier Reef Bette L. Willis, Cathie A. Page, and Elizabeth A. Dinsdale 4 Coral Diseases in Gulf of Mexico Reefs Eric Jordan-Dahlgren and Rosa E. Rodriguez-Martinez 5 Coral Bleaching: Signs of Change in Southern Japan Rob van Woesik, Akiyuki Irikawa, and Yossi Loya 6 Coral bleaching in a temperate sea: from colony physiology to population ecology Maoz Fine and Yossi Loya 7 Coral bleaching, diseases and mortality in the western Indian Ocean Tim McClanahan Part II Microbial ecology and physiology of corals 8 Symbiont diversity on coral reefs and its relationship to bleaching resistance and resilience Andrew C. Baker 9 Stress effects on metabolism and photosynthesis of hermatypic corals Noga Stambler and Zvy Dubinsky 10 What can regeneration tell us about coral disease? Esti Kramarsky-Winter 11 Bacteria as a source of coral nutrition Ariel Kushmaro and Esti Kramarsky-Winter 12 Antimicrobial activity of sponges and corals Dovi Kelman 13 Microbial communities of coral surface mucopolysaccharide layers Kim B. Ritchie and Garriet W. Smith 14 Culture-independent analyses of coral-associated microbes Forrest Rohwer and Scott Kelly Part III Coral diseases 15 Aspergillosis of Gorgonians Garriet W. Smith and Ernesto Weil 16 White pox disease of the Caribbean elkhorn coral, Acropora palmata Kathryn Patterson Sutherland and Kim B. Ritchie 17 Temperature-regulated bleaching and tissue lysis of Pocillopora damicornis by the novel pathogen Vibriocoralliilyticus Yael Ben-Haim Rozenblat and Eugene Rosenberg 18 Black Band Disease Laurie L. Richardson 19 Dark spots disease and yellow band disease, two poorly known coral diseases with high incidence in Cabibbean reefs Diego L. Gil-Agudelo, Garriet W. Smith, Jaime Garzon-Ferreira, and Ernesto Weil, Dirk Petersen 20 White plague, white band and other 'white' diseases John Bythell, Olga Pantos, and Laurie Richardson 21 Monitoring the health of coral reef ecosystems using community metabolism Jack Silverman, Boaz Lazar, and Jonathan Erez 22 Coral resistance to disease Kerri M. Mullen, Ester C. Peters, and C. Drew Harvell Part IV Coral bleaching 23 Temperature stress and coral bleaching Paul J. Jokiel 24 The adaptive hypothesis of bleaching Robert W. Buddemeier, Andrew C. Baker, Daphne C. Fautin, and J. Rebeca Jacobs 25 The bacterial disease hypothesis of coral bleaching Eugene Rosenberg 26 Coral reefs and projections of future change Ove Hoegh-Guldberg Subject Index

Populations of the most common Caribbean reef-building coral, Acropora palmata, are being decimated by white pox disease, with losses of living cover in the Florida Keys National Marine Sanctuary (FKNMS) averaging 88%. Elkhorn coral plays a significant role in the structural and functional integrity of Caribbean coral reef ecosystems. A. palmata is an important shallow water species, providing elevated rates of calcium carbonate deposition (Adey 1978) and a highly complex three-dimensional structure of the shallow water fore reef. This keystone species provides shelter and food for reef organisms and aids in the protection of coastal regions by serving as a buffer between land and sea. Severe population declines of A. palmata in the FKNMS and elsewhere in the Caribbean have led to the identification of this species as a candidate for inclusion on the Endangered Species List (Diaz-Soltero 1999).

Coral reefs are diverse and important communities in tropical and subtropical marine environments. Hermatypic corals play a key role in forming the structure of coral reefs and in providing substrata and shelter for a wide variety of organisms. The symbiotic association between corals and their photosynthetic algae (zooxanthellae) is one of the primary keys to coral success in this ecosystem (Fallowski et al. 1984; Sebens 1994). Hermatypic corals attain a large part of their nutrition from photosynthetic products of the zooxanthellae, which are located in their gastrodermal cell layer. However, corals must utilize other particulate matter to gain enough nitrogen and phosphorus to grow (Sorokin 1990; Sebens 1994; Schlichter and Brendelberger 1998; Rosenfeld et al. 1999; Anthony and Fabricius 2000).

Black band disease (BBD) was the first coral disease to be reported in the literature (Antonius 1973). It was first noted on reefs of Belize in the western Caribbean, and was described as a striking microbial assemblage that formed a band which moved across apparently healthy coral colonies, actively destroying coral tissue and leaving behind the bare coral skeleton (Fig. 18.1). The band appeared dark, which was the basis of the descriptive name. During this same decade, two additional coral diseases were reported, white plague (Dustan 1977) and white band (Gladfelter et al. 1977). BBD differed from the other two in that a very obvious microbial biomass was associated with the pathology, whereas no discernible microorganisms were observable for white plague or white band. Despite the distinct presence of a dense microbial community associated with active coral tissue lysis, identification of the BBD pathogen has proven to be challenging and is still the subject of ongoing investigation.

The influence of microbes on coral reefs has been underappreciated, even though it is widely recognized that Bacteria, Archaea, and unicellular eukaryotes are vital components of all marine ecosystems. Several studies have applied modern microbial ecology methods to investigate the microbes living with reef organisms. These new avenues of research are changing our view of how coral reefs function. This chapter is intended to make these new findings accessible to those interested in interdisciplinary studies of coral and microbial ecology. A model of how microbes are structured on healthy corals is proposed, as is the hypothesis that disrupting this structure leads to coral disease and death.

Bacteria and other microorganisms are ubiquitous in the marine environment. They are taxonomically diverse, biologically active and colonize all marine habitats, from the deep oceans to the shallowest estuaries (Austin 1988; Rheinheimer 1992), as well as coral reefs (Ducklow 1990). Living benthic marine organisms such as sponges and corals are frequently colonized by bacteria. Sponges are known to harbor a diverse range of microorganisms (Bergquist 1978; Wilkinson 1978). In some cases, up to 50% of the sponge weight was attributed to their symbiotic bacteria (Wilkinson 1978). The surface of living corals is covered by mucus (Ducklow and Mitchell 1979a). This mucus layer is colonized by bacteria, allowing the establishment of a bacterial community that can be characteristic to a particular coral species (Mitchell and Chet 1975; Ducklow and Mitchell 1979b; Rublee et al. 1980; Segal and Ducklow 1982; Ritchie et al. 1994; Rohwer et al. 2002). Some of these bacteria can be pathogenic to sponges and corals, and may initiate disease, such as tissue necrosis in sponges (Webster et al. 2002), and several diseases in corals, such as black band disease (Antonius 1985; Carlton and Richardson 1995), white plague type II (Smith et al. 1996; Richardson et al. 1998), tissue necrosis (Hodgson 1990; Ben-Haim and Rosenberg 2002), and even bleaching of the Mediterranean scleractinian coral Oculina patagonica (Kushmaro et al. 1996, 1997). On the other hand, bacteria could serve as beneficial symbionts or as benign associates. For example, Gil-Turnes et al. (1989) showed that bacteria on the surface of externally held eggs of the shrimp Palaeman macrodactylus produce a metabolite that inhibits fungal infections that are lethal to the eggs. Therefore, sponges and corals need the ability to regulate the bacteria they encounter and to resist microbial colonization and the invasion of potential pathogens in order to prevent possible detrimental effects. One method of combating microbial attack is by chemical defense.

Over the past few decades, coral reef communities around the world have been experiencing increasingly stressful conditions due to a combination of natural and detrimental anthropogenic factors. In the Caribbean, coral reefs have experienced significant losses in hard coral cover due in part to local habitat degradation, over-fishing, pollutant input, bleaching, hurricanes and more recently, diseases (Porter and Meier 1992, Ginsburg 1993; Aronson and Precht 1997; Epstein et al. 1998; Harvell et al. 1999; Wilkinson 2000; Weil 2001). These factors, acting alone or in synergy, can be highly variable on spatial and temporal scales, making it difficult to identify and characterize a single or combined cause(s) of reef deterioration. Bleaching events, for example, have increased in frequency and intensity in the last two decades and their impact has been highly variable both spatially and temporarily. In the Caribbean, bleaching has caused variable, but generally low, coral mortality, unlike the mass mortalities of the scale observed in the Indo-Pacific. In contrast, few coral diseases, with low prevalence and restricted geographic distributions, have been reported for the Indo-Pacific as compared to the Caribbean. The latter has been dubbed a “disease hot spot” because of the fast emergence, high prevalence and virulence of coral reef diseases and syndromes; their widespread geographic distribution, and the frequent epizootic events with significant coral mortalities (Epstein et al. 1998; Hayes and Goreau 1998; Green and Bruckner 2000; Weil et al. 2002). In the last few decades, for example, epizootic events have resulted in significant losses in coral cover, biodiversity and habitat (loss of spatial heterogeneity), and today, diseases have possibly become the most important factor in the deterioration dynamics of Caribbean coral reefs (Hughes 1994; Aronson and Precht 200 lb; Bruckner 2002; Weil 2002).

Although commonly reported among disease occurrences of reef corals (Weil et al. 2002), the “white” diseases are probably the most enigmatic. There are a number of these diseases, or syndromes, and confusion arises because of the very similar disease signs that are present in association with each of them. The ‘white syndromes’ include white band disease (Antonius 198 lb; Gladfelter 1982), more recently divided into two groups, white band type I and white band type II (Ritchie and Smith 1998); white plague (or simply plague; Dustan 1977), again recently divided into white plague types (WP) I, II and III (Richardson et al. 1998a, b, 2001); and ‘stress-related necrosis’, “patchy necrosis”, or ‘shut-down reaction’ (Antonius 1981a; Peters 1983, 1984). Confusion between white plague and white band disease is problematic because the visible signs of the diseases are virtually identical in that there is a sharp, distinct line between apparently healthy coral tissue and freshly exposed coral skeleton with no obvious microbial material present. At times, some types of both white band and white plague may have a zone of bleached coral tissue at the disease boundary, but in both cases this is usually transient and variable. The distinction has been based primarily on the host species affected, with Acropora species in the Caribbean commonly reported to be affected by white band disease and other scleractinian species, including massive species, affected by white plague. Early studies (e.g. Antonius 1981a, b) used the terms interchangeably and any historical analysis must therefore account for both diseases. Both Antonius (1981b) and Peters (1984) reported the presence of white band disease on a number of massive corals as well as the branching acroporids. More recently, investigators have been studying the etiology of a coral disease associated with white lesions (Bythell et al. 2002), which appears similar to WPI as well as patchy necrosis.

Coral disease is one of the most recent in a series of threats that is challenging the resilience of coral reef communities and is of particular concern because it may interact with and augment the impacts of other commonly recognised threats to coral health (e.g. bleaching, over-exploitation of fish stocks, destructive fishing practices and coastal developments). Since the first report of coral disease by Antonius in 1973, the rate of discovery of new diseases has increased dramatically with more than 29 coral diseases now described (Green and Bruckner 2000, Weil, this Vol.). Although coral disease is emerging as one of the major causes of coral reef deterioration in the Caribbean (Hayes and Goreau 1998; Harvell et al. 2002; Weil et al. 2002), at present we know very little about the ecology or pathology of coral disease on Indo-Pacific reefs. The comparatively few reports of coral disease from Indo-Pacific reefs, despite the region encompassing more than 80% of reefs worldwide (Bryant et al. 1998) is in contrast to the high proportion (>65%) of records in the Global Disease Database from the Caribbean reef region, now widely considered to be a coral disease hotspot (Green and Bruckner 2000; Weil, this Vol.). Such comparisons suggest that either disease is genuinely more prevalent in the Caribbean or lack of studies in other reef regions is underestimating its distribution and abundance. Distinguishing between these two alternatives represents an important step in advancing global epizootiological studies.

Scientists of diverse interests, and even laymen, are beginning to understand what is meant by a “microbial mat”. But this knowledge is still superficial even for the specialist, both figuratively and literally. Most of what we know of microbial mats up to this point is still relegated to the superficial upper layer or layers which are usually composed mainly of photosynthetic prokaryotes. It is these that are responsible for the accretion and for the conversion of atmospheric and aqueous CO2 into reduced energy-rich compounds on which the rest of the community is dependent. It is also these superficial layers that define most of the Precambrian remnants of microbial mats, the lithified mats or stromatolites which also contain the microfossils that are often recognizable as morphotypes of cyanobacteria. The laminae or underzones of even living mats are still “black boxes” for the most part, with little known of the actual microbial makeup, the matrix of exopolymers, and of the species interactions and metabolic activities. Although the microbial mat community may be regarded as an ecosystem characterized by primarily a molecular flow of carbon and chemical energy (since grazing invertebrates and even smaller phagotrophs are generally rare or absent), most mat communities are now known to be of considerable taxonomic and biochemical complexity, and a great diversity of communities exists.