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Colony Versus Population Variation in Susceptibility and Resistance to Dark Spot Syndrome in the Caribbean Coral Siderastrea Siderea

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Colony Versus Population Variation in Susceptibility and Resistance to Dark Spot Syndrome in the Caribbean Coral Siderastrea Siderea DISEASES OF AQUATIC ORGANISMS Vol. 69: 53–65, 2006 Published March 23 Dis Aquat Org Colony versus population variation in susceptibility and resistance to dark spot syndrome in the Caribbean coral Siderastrea siderea Deborah J. Gochfeld1,*, Julie B. Olson2, Marc Slattery1, 3 1National Center for Natural Products Research, PO Box 1848, University of Mississippi, University, Mississippi 38677, USA 2Department of Biological Sciences, PO Box 870344, University of Alabama, Tuscaloosa, Alabama 35487, USA 3Department of Pharmacognosy, PO Box 1848, University of Mississippi, University, Mississippi 38677, USA ABSTRACT: Scleractinian corals appear to be increasingly susceptible to pathogenic diseases, yet it is poorly understood why certain individuals, populations or species are more susceptible to diseases than others. Clearly an understanding of mechanisms of disease resistance in corals is essential to our understanding of patterns of disease incidence and virulence; this work must begin by examining the colony and population levels of organization. The Caribbean coral Siderastrea siderea exhibits vari- ability in susceptibility to dark spot syndrome (DSS), a disease of unknown origin that can result in tissue necrosis. On the reef scale, variability in DSS prevalence in S. siderea occurred through time, but was not correlated with site, seawater temperature or depth. We monitored colonies of S. siderea affected by DSS, as well as their nearest neighbor controls, for 2 years in the Bahamas and found a marked decline in extent of DSS infection in October of both years. A preliminary survey of antimi- crobial activity in S. siderea indicated selective activity against certain ecologically relevant bacteria. To assess whether changes in chemical defenses were responsible for the observed temporal vari- ability in DSS prevalence, we sampled S. siderea for qualitative and quantitative analysis of chemi- cal variability between resistant and susceptible colonies of S. siderea. These data suggest that phenotypic plasticity in antimicrobial activity may impact microbial settlement and/or survival. KEY WORDS: Coral disease · Siderastrea siderea · Caribbean · Disease prevalence · Disease resistance · Chemical defense · Antimicrobial activity · Dark spot syndrome Resale or republication not permitted without written consent of the publisher INTRODUCTION diseases have been shown to cause either tissue necro- sis (i.e. death of individual polyps) or mortality of the In the marine environment, epidemic outbreaks of entire coral colony (Rosenberg & Loya 2004). Of the previously unknown diseases have been reported with many coral diseases now recognized (actual number of alarming frequency over the past 3 decades (Harvell diseases depends on the reference cited), etiologic et al. 1999). Among scleractinian corals, recent years agents have been identified for only a few: aspergillo- have seen both an increased prevalence of diseases sis (Aspergillus sydowii; Geiser et al. 1998, reviewed and an increased number of species infected (Goreau by Smith & Weil 2004), black band disease (BBD) et al. 1998, Richardson 1998, Green & Bruckner 2000, (microbial consortium; reviewed by Richardson 2004), Porter et al. 2001, Rosenberg & Loya 2004). Depending plague type II (Aurantimonas coralicida; Richardson on the spatial scale examined, either the population- or et al. 1998, Denner et al. 2003), white pox (Serratia community-level effects of these diseases may be sig- marcescens; Patterson et al. 2002), bacterial bleaching nificant (Gladfelter 1982, Lessios 1988, Edmunds 1991, (Vibrio shiloi [= V. shilonii]; Kushmaro et al. 2001) and Porter & Meier 1992, Peters 1997). A number of these tissue lysis (V. coralliilyticus; Ben-Haim et al. 2003, *Email: [email protected] © Inter-Research 2006 · www.int-res.com 54 Dis Aquat Org 69: 53–65, 2006 Rozenblat & Rosenberg 2004). The sources of these sources of protection from disease (note their absence pathogens in the marine environment are not entirely in a review by Hayes & Goreau 1998, but inclusion in a clear, but anthropogenic influences are thought to be later review by Sutherland et al. 2004). Many gorgo- important. For example, S. marcescens, a common nians have antimicrobial activity (Jensen et al. 1996), human fecal enterobacterium (Patterson et al. 2002), and Kim et al. (2000a,b) found that crude extracts from may enter the ocean from water treatment plants several Caribbean gorgonian species inhibited spore (Sutherland & Ritchie 2004, Sutherland et al. 2004). germination of Aspergillus sydowii. However, only a The common soil fungus A. sydowii may be trans- few studies have identified pure compounds with ported during African dust storms and deposited on antimicrobial activity (Gram et al. 1996, Slattery 1999). Caribbean coral reefs, where it becomes pathogenic to Whereas antimicrobial chemical defenses are wide- sea fans (Shinn et al. 2000, Garrison et al. 2003). spread in soft-bodied marine invertebrates, including The emergence of new marine diseases and the soft corals (recently reviewed in Kelman 2004), there increased vulnerability of corals to diseases are have been very few investigations of chemical de- believed to have arisen from range shifts of known fenses in scleractinian corals. Gochfeld (1997) demon- pathogens (Harvell et al. 1999), the evolution of more strated chemical defenses against predatory fish in the virulent pathogens, and/or compromised host defenses Hawaiian coral Porites compressa and in several (Hayes & Goreau 1998, Carey 2000). Several re- Caribbean corals (D. J. Gochfeld unpubl.). In a pre- searchers have suggested that development of patho- liminary survey of Australian corals, Koh (1997) identi- genesis in coral tissues depends on lowered coral fied variable antimicrobial activity of crude extracts resistance resulting from anthropogenic or environ- against several marine microbes with no known patho- mental stress (Peters 1993, Geiser et al. 1998, Harvell genic effects on corals. Kelman (2004) found minimal et al. 1999, 2002, Carey 2000). Indeed, there is some antimicrobial activity of Red Sea corals against marine evidence that the microbial consortium responsible for bacteria. It is unclear whether antimicrobial meta- BBD is more prevalent on corals subject to anthro- bolites in corals are constitutive defenses that are pogenic stress (Taylor 1983, Antonius 1985, Kuta & always present (i.e. genetically fixed) or inducible Richardson 2002), and correlative studies suggest that defenses (i.e. ‘those defenses that are fabricated when the incidence of certain diseases is higher on reefs needed and dismantled when not needed’; Karban & exposed to anthropogenic influences (Green & Bruck- Baldwin 1997, Tollrian & Harvell 1999) produced in ner 2000, Sutherland et al. 2004). Temperature stress, direct response to pathogen assault. due to increased frequency and severity of El Niño Dark spot syndrome (DSS), also called dark spots Southern Oscillation (ENSO) events and global warm- disease, was first described in the 1990s (Garzon- ing, has clearly taken a toll on corals in terms of stress Ferreira & Gil 1998) and has since been observed and mortality due to bleaching (Harvell et al. 1999, throughout the Caribbean (Weil et al. 2000, Borger 2002, Rosenberg & Ben-Haim 2002). There is evidence 2003, Gil-Agudelo et al. 2004, Weil 2004). Because DSS that host resistance and/or pathogen virulence are also was described only recently, relatively little is known impacted either directly or indirectly by these stresses about this disease. DSS is manifested by darkened (Toren et al. 1998, Rozenblat & Rosenberg 2004, areas on otherwise seemingly healthy coral tissue. Sutherland et al. 2004). Stress has been demonstrated These purple to brown areas may gradually enlarge to reduce production (Cronin & Hay 1996, Slattery and a depression may form in the coral skeleton, with 1999) or efficacy (Alker et al. 2001) of chemical subsequent necrosis and invasion by algae. DSS may defenses (see below), which might account for this persist for long periods, or the infection may disappear increased susceptibility to infectious microorganisms without any evident damage. DSS affects several spe- that might otherwise be deterred by antimicrobial cies of scleractinian corals (Weil et al. 2000, Garzon- compounds. Although many researchers are presently Ferreira et al. 2001, Gil-Agudelo & Garzon-Ferreira monitoring coral reefs for disease incidence, there is 2001, Weil 2004) but at our study sites in the Bahamas, little known about why certain individuals, popula- it most frequently affects the massive coral Siderastrea tions or species are more susceptible to disease than siderea. In fact, S. siderea appears to be among the others. most susceptible species to several coral diseases Chemical defenses are well documented in marine (Porter et al. 2001, Borger 2003, Weil 2004). Although invertebrates (see reviews by Paul 1992, Pawlik 1993, DSS may progress slowly and cause low levels of coral McClintock & Baker 2001), and whereas several necrosis, its high incidence and prevalence on researchers have demonstrated antimicrobial activities Caribbean reefs and the fact that it affects important for these chemical defenses (e.g. Sammarco & Coll reef building species suggest that this disease may be 1992, Walls et al. 1993, Wahl et al. 1994, Slattery et al. important to overall coral reef health. DSS is known to 1997), few studies have considered them as potential vary on both temporal and spatial scales. Increasing
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