Esther C. Peters

The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata

Populations of the shallow-water Caribbean elkhorn coral, Acropora palmata, are being decimated by white pox disease, with losses of living cover in the Florida Keys typically in excess of 70%. The rate of tissue loss is rapid, averaging 2.5 cm2⋅day−1, and is greatest during periods of seasonally elevated temperature. In Florida, the spread of white pox fits the contagion model, with nearest neighbors most susceptible to infection. In this report, we identify a common fecal enterobacterium, Serratia marcescens, as the causal agent of white pox. This is the first time, to our knowledge, that a bacterial species associated with the human gut has been shown to be a marine invertebrate pathogen.

Cellular Responses in Sea Fan Corals: Granular Amoebocytes React to Pathogen and Climate Stressors

Background Climate warming is causing environmental change making both marine and terrestrial organisms, and even humans, more susceptible to emerging diseases. Coral reefs are among the most impacted ecosystems by climate stress, and immunity of corals, the most ancient of metazoans, is poorly known. Although coral mortality due to infectious diseases and temperature-related stress is on the rise, the immune effector mechanisms that contribute to the resistance of corals to such events remain elusive. In the Caribbean sea fan corals (Anthozoa, Alcyonacea: Gorgoniidae), the cell-based immune defenses are granular acidophilic amoebocytes, which are known to be involved in wound repair and histocompatibility. Methodology/Principal Findings We demonstrate for the first time in corals that these cells are involved in the organismal response to pathogenic and temperature stress. In sea fans with both naturally occurring infections and experimental inoculations with the fungal pathogen Aspergillus sydowii, an inflammatory response, characterized by a massive increase of amoebocytes, was evident near infections. Melanosomes were detected in amoebocytes adjacent to protective melanin bands in infected sea fans; neither was present in uninfected fans. In naturally infected sea fans a concurrent increase in prophenoloxidase activity was detected in infected tissues with dense amoebocytes. Sea fans sampled in the field during the 2005 Caribbean Bleaching Event (a once-in-hundred-year climate event) responded to heat stress with a systemic increase in amoebocytes and amoebocyte densities were also increased by elevated temperature stress in lab experiments. Conclusions/Significance The observed amoebocyte responses indicate that sea fan corals use cellular defenses to combat fungal infection and temperature stress. The ability to mount an inflammatory response may be a contributing factor that allowed the survival of even infected sea fan corals during a stressful climate event.

Diseases of Coral Reef Organisms

All coral reef organisms are susceptible to diseases, as are terrestrial organisms, but studying these diseases can be more difficult and much remains to be learned. Although health impairments of corals were first recognized only in the early 1970s, increasing numbers of infectious and non-infectious diseases, causing morbidity and mortality in numerous species of tropical marine organisms, have now been identified in diverse species of algae, plants, invertebrates, and vertebrates. Causes of diseases include biotic, as well as abiotic, factors, but identifying a primary pathogen has been reported in only a few cases, and some of those results have been questioned as additional diagnostic tools have been applied. The multitude of stressors affecting reef organisms, particularly along heavily urbanized coastlines, as well as introductions of species to distant reefs by global transport, are contributing to concerns about extinction risks and loss of biodiversity. This chapter presents an overview of diseases of reef organisms, how diseases have adversely affected coral reefs, and new developments in disease diagnoses. The application of concepts from the field of conservation medicine are aiding our understanding of diseases and their impacts on organisms of these shallow to mesophotic ecosystems.

Coral Resistance to Disease

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).

Comprehensive characterization of skeletal tissue growth anomalies of the finger coral Porites compressa

The scleractinian finger coral Porites compressa has been documented to develop raised growth anomalies of unknown origin, commonly referred to as “tumors”. These skeletal tissue anomalies (STAs) are circumscribed nodule-like areas of enlarged skeleton and tissue with fewer polyps and zooxanthellae than adjacent tissue. A field survey of the STA prevalence in Oahu, Kaneohe Bay, Hawaii, was complemented by laboratory analysis to reveal biochemical, histological and skeletal differences between anomalous and reference tissue. MutY, Hsp90a1, GRP75 and metallothionein, proteins known to be up-regulated in hyperplastic tissues, were over expressed in the STAs compared to adjacent normal-appearing and reference tissues. Histological analysis was further accompanied by elemental and micro-structural analyses of skeleton. Anomalous skeleton was of similar aragonite composition to adjacent skeleton but more porous as evidenced by an increased rate of vertical extension without thickening. Polyp structure was retained throughout the lesion, but abnormal polyps were hypertrophied, with increased mass of aboral tissue lining the skeleton, and thickened areas of skeletogenic calicoblastic epithelium along the basal floor. The latter were highly metabolically active and infiltrated with chromophore cells. These observations qualify the STAs as hyperplasia and are the first report in poritid corals of chromophore infiltration processes in active calicoblastic epithelium areas.

Quantitative assessment of coral diseases in the Florida Keys: strategy and methodology

Natural incidences of disease among scleractinian corals are unknown, since most studies have been initiated in response to specific disease outbreaks. Our ability to distinguish elevated disease incidences influenced by anthropogenic and climatic factors is limited since current estimates are probably inflated for extrapolation to larger areas. In our study, we used quantitative assessment methods to characterize the distribution and frequency of scleractinian and gorgonian coral diseases in the south Florida region. This paper is the first in a series that will detail different aspects of our studies. In this paper, we examined the strategy and methodology developed over 2 years to optimize the experimental design of our study. Pilot surveys were conducted in 1997 to develop and test methods, select and determine suitability of sites, and obtain preliminary data to assess the variance and efficiency of the sampling design. Survey periods targeted late spring, the time when coral diseases are believed to emerge, and late summer, the time when coral diseases are believed to be most prevalent. Two strata were chosen to evaluate patterns of coral disease: the first, geographic area, consisted of reefs in the vicinity of Key West, New Grounds and the Dry Tortugas; and the second, reef type, consisted of back, fore and transitional reefs. Random radial arc transects (10 m diameter) were used to quantify 10 diseases affecting 18 species of stony corals and gorgonian sea fans over a large geographical region. During the pilot survey, we demonstrated that the outer 8–10 m segment (113 m2) was an adequate sampling area. The survey implemented important quality assurance measures for data quality control. Power analysis determined that future studies should adopt α=0.10, β=0.0383, and 1-β=0.9617 in our experimental design. The highest prevalence of disease in our study was during the 1997 summer survey, with a mean percent coral disease (MPCD) of 28% occurring at Key West area reefs, or 55% of all back reef stations. Our results do not show a clear pattern of seasonality in coral diseases within either stratum, although differences in disease distribution between reef types and geographic areas were apparent in some of the spring and summer surveys.

Immunolocalization of skeletal matrix proteins in tissue and mineral of the coral Stylophora pistillata

Significance Although various aspects of biomineralization in corals have been studied for decades, the basic mechanism responsible for the precipitation of the aragonite skeleton remains enigmatic. To address this issue, we used antibodies against key biomineralization proteins derived from the common zooxanthellate coral Stylophora pistillata to elucidate the spatial arrangement of specific skeletal matrix proteins in the skeleton and in the animal tissue. To our knowledge, our results reveal for the first time that the biomineral is produced in discrete nanoscale packages in which the secreted organic matrices remain entrapped within the crystalline units whose growth they control, leading to the formation of highly ordered, microscopic, heterologous structures, which are aggregated to form a macroscopic skeleton. The precipitation and assembly of calcium carbonate skeletons by stony corals is a precisely controlled process regulated by the secretion of an ECM. Recently, it has been reported that the proteome of the skeletal organic matrix (SOM) contains a group of coral acid-rich proteins as well as an assemblage of adhesion and structural proteins, which together, create a framework for the precipitation of aragonite. To date, we are aware of no report that has investigated the localization of individual SOM proteins in the skeleton. In particular, no data are available on the ultrastructural mapping of these proteins in the calcification site or the skeleton. This information is crucial to assessing the role of these proteins in biomineralization. Immunological techniques represent a valuable approach to localize a single component within a calcified skeleton. By using immunogold labeling and immunohistochemical assays, here we show the spatial arrangement of key matrix proteins in tissue and skeleton of the common zooxanthellate coral, Stylophora pistillata. To our knowledge, our results reveal for the first time that, at the nanoscale, skeletal proteins are embedded within the aragonite crystals in a highly ordered arrangement consistent with a diel calcification pattern. In the tissue, these proteins are not restricted to the calcifying epithelium, suggesting that they also play other roles in the coral’s metabolic pathways.

Bivalve Biomarker Workshop: overview and discussion group summaries

(1999). Bivalve Biomarker Workshop: overview and discussion group summaries. Biomarkers: Vol. 4, No. 6, pp. 391-399.

Observations of a new source of coral mortality along the Kenyan coast

In early 2002 coral mortality occurred along 600 km of coastline from Tanzania to Kenya. Astreopora, Echinopora , and Montipora species were severely affected, with Montipora being nearly eliminated from Kenyan reefs. Acropora , Platygyra , Goniopora , and massive Porites were also affected; however, Porites and Goniopora rarely died and often recovered, whereas death for most other species occurred within 2 weeks. In Echinopora and Montipora , a dull ashy tissue color and brittle skeletons characterized the early stages of this event with a mucus layer on the tissue surface in intermediate stages. Mucus and embedded debris then disappeared and surfaces were left covered in a white calcareous dust that sometimes capped a black layer. Astreopora tissues became dull and pale, and seldom produced mucus; eventually the skeleton became bare and white. Either a colorless translucent or brownish thin margin of tissue was visible between living tissue and bare skeleton, depending on species. Scanning electron micrographs of affected corals revealed the presence of fungi. Histology and staining showed that the fungi were mostly in the three genera that died from the syndrome and it may be that fungi invaded and killed corals weakened by another unidentified pathogen.

Disease dynamics and potential mitigation among restored and wild staghorn coral, Acropora cervicornis

The threatened status (both ecologically and legally) of Caribbean staghorn coral, Acropora cervicornis, has prompted rapidly expanding efforts in culture and restocking, although tissue loss diseases continue to affect populations. In this study, disease surveillance and histopathological characterization were used to compare disease dynamics and conditions in both restored and extant wild populations. Disease had devastating effects on both wild and restored populations, but dynamics were highly variable and appeared to be site-specific with no significant differences in disease prevalence between wild versus restored sites. A subset of 20 haphazardly selected colonies at each site observed over a four-month period revealed widely varying disease incidence, although not between restored and wild sites, and a case fatality rate of 8%. A tropical storm was the only discernable environmental trigger associated with a consistent spike in incidence across all sites. Lastly, two field mitigation techniques, (1) excision of apparently healthy branch tips from a diseased colony, and (2) placement of a band of epoxy fully enclosing the diseased margin, gave equivocal results with no significant benefit detected for either treatment compared to controls. Tissue condition of associated samples was fair to very poor; unsuccessful mitigation treatment samples had severe degeneration of mesenterial filament cnidoglandular bands. Polyp mucocytes in all samples were infected with suspect rickettsia-like organisms; however, no bacterial aggregates were found. No histological differences were found between disease lesions with gross signs fitting literature descriptions of white-band disease (WBD) and rapid tissue loss (RTL). Overall, our results do not support differing disease quality, quantity, dynamics, nor health management strategies between restored and wild colonies of A. cervicornis in the Florida Keys.