The evolutionary history of Symbiodinium and scleractinian hosts - Symbiosis, diversity, and the effect of climate change

Marine invertebrates representing at least five phyla are symbiotic with dinoflagellates from the genus Symbiodinium. This group of single-celled protists was once considered to be a single pandemic species, Symbiodinium microadriaticum. Molecular investigations over the past 25 years have revealed, however, that Symbiodinium is a diverse group of organisms with at least eight (A-H) divergent clades that in turn contain multiple molecular subclade types. The diversity within this genus may subsequently determine the response of corals to normal and stressful conditions, leading to the proposal that the symbiosis may impart unusually rapid adaptation to environmental change by the metazoan host. These questions have added importance due to the critical challenges that corals and the reefs they build face as a consequence of current rapid climate change. This review outlines our current understanding of the diverse genus Symbiodinium and explores the ability of this genus and its symbioses to adapt to rapid environmental change. (c) 2006 Rubel Foundation, ETH Zurich. Published by Elsevier GmbH. All rights reserved.

The impact of spectral composition and light periodicity on the activity of two antioxidant enzymes (SOD and CAT) in the coral Favia favus

In oligotrophic waters the light spectrum is mostly blue, and therefore the physiological and biochemical responses to blue light occurring in the coral tissue and in the symbiotic algae are important. Examination of the wavelength dependence of two free radical scavenger enzyme activity revealed an increase in activity in the blue light range (440-480 nm) compared to the red (640680 nm) in the full visible light (400-700 nm) range. These data show for the first time the relationship between the action spectra of photosynthesis and the activity of two main antioxidant enzymes in the symbiotic coral Favia favus. It was found that in the animal (host) the enzyme response to the spectral distribution of light was higher than that of the zooxanthellae, probably due to accumulation of free radicals within the host tissue. Furthermore, we found that the activity of these enzymes is affected in nature by the length of the day and night, and in the laboratory, by the duration of the illumination. Changes in the pigment concentrations were also observed in response to growth under the blue region and the whole PAR spectrum, while fluorescence measurements with the fast repetition rate fluorometer (FRRF) showed a decrease in the sigma cross section and a decrease in the quantum yield also in the blue part of the spectrum. These changes of scavenger enzymes activity, pigment concentration and fluorescence yield at different light spectra are vital in acclimatization and survival of corals in shallow water environments with high light radiation. (c) 2005 Elsevier B.V. All rights reserved.

Phototrophic microendoliths bloom during coral "white syndrome"

Following rapid lesion progression of white syndrome in tabular Acropora spp., the white bare skeleton gradually changes to green, a result of endolithic algae blooms (primarily Ostreobium spp.). Endolithic algal biomass and chlorophyll concentration were found to be an order of magnitude higher in the green zone compared with healthy appearing parts of each colony. Chl b to Chl a ratio increased from 1:1.6 in the healthy area to 1:2 and 1:3.5 in the white exposed skeleton and green zones, respectively. These observations together with pulse amplitude modulated (PAM) fluorometry suggest photoacclimation of the endoliths in the green zone. Histopathological microscopy revealed that the endolithic algal filaments penetrate the coral tissue. This study highlights the interaction of endolithic algae with both the skeleton and host tissue. This may have a critical role in the processes that accompany the post-disease state in reef-building corals.

Sand and nest temperatures and an estimate of hatchling sex ratio from the Heron Island green turtle (Chelonia mydas) rookery, Southern Great Barrier Reef

Sand and nest temperatures were monitored during the 2002-2003 nesting season of the green turtle, Chelonia mydas, at Heron Island, Great Barrier Reef, Australia. Sand temperatures increased from similar to 24 degrees C early in the season to 27-29 degrees C in the middle, before decreasing again. Beach orientation affected sand temperature at nest depth throughout the season; the north facing beach remained 0.7 degrees C warmer than the east, which was 0.9 degrees C warmer than the south, but monitored nest temperatures were similar across all beaches. Sand temperature at 100 cm depth was cooler than at 40 cm early in the season, but this reversed at the end. Nest temperatures increased 2-4 degrees C above sand temperatures during the later half of incubation due to metabolic heating. Hatchling sex ratio inferred from nest temperature profiles indicated a strong female bias.

A high-precision record of mid-late Holocene sea-level events from emergent coral pavements in the Houtman Abrolhos Islands, southwest Australia

Early work on sea-levels in southwest Australia claimed to recognise a Holocene sea-level highstand which was not seen in better known sea-level records elsewhere at the time. More recent work has confirmed that a mid-Holocene highstand Occurred about 6 kyr ago. As new data on oscillating sea-levels from the region have recently been published, a high continuity, precisely dated and accurately surveyed record was obtained from emergent coral pavements in the leeward Houtman Abrolhos Islands (Serventy Island), a tectonically stable region from where good-quality Holocene sea-level data have been previously obtained from corals. From the mid-Holocene highstand ca. 7 U/Th kyr ago, sea-level declined linearly during the remainder of the Holocene as the carbonate platform prograded leewards. Hydro-isostatic controls are probably significant in the record. (c) 2005 Elsevier Ltd and INQUA. All rights reserved.

Viruses: agents of coral disease?

The potential role of viruses in coral disease has only recently begun to receive attention. Here we describe our attempts to determine whether viruses are present in thermally stressed corals Pavona danai, Acropora formosa and Stylophora pistillata and zoanthids Zoanthus sp., and their zooxanthellae. Heat-shocked P. danai, A. formosa and Zoanthus sp. all produced numerous virus-like particles (VLPs) that were evident in the animal tissue, zooxanthellae and the surrounding seawater; VLPs were also seen around heat-shocked freshly isolated zooxanthellae (FIZ) from P. danai and S. pistillata. The most commonly seen VLPs were tail-less, hexagonal and about 40 to 50 nm in diameter, though a diverse range of other VLP morphotypes (e.g. rounded, rod-shaped, droplet-shaped, filamentous) were also present around corals. When VLPs around heat-shocked FIZ from S. pistillata were added to non-stressed FIZ from this coral, they resulted in cell lysis, suggesting that an infectious agent was present; however, analysis with transmission electron microscopy provided no clear evidence of viral infection. The release of diverse VLPs was again apparent when flow cytometry was used to enumerate release by heat-stressed A. formosa nubbins. Our data support the infection of reef corals by viruses, though we cannot yet determine the precise origin (i.e. coral, zooxanthellae and/or surface microbes) of the VLPs seen. Furthermore, genome sequence data are required to establish the presence of viruses unequivocally.

Pesticide and herbicide residues in sediments and seagrasses from the Great Barrier Reef world heritage area and Queensland coast

Pesticides and herbicides including organochlorine compounds have had extensive current and past application by Queensland's intensive coastal agriculture industry as web as for a wide range of domestic, public health and agricultural purposes in urban areas, The persistent nature of these types of compounds together with possible continued illegal use of banned organochlorine compounds raises the potential for continued long-term chronic exposure to plants and animals of the Great Barrier Reef. Sediment and seagrass samples were collected from 16 intertidal and 25 subtidal sampling sites between Torres Strait and Townsville, near Mackay and Gladstone, and in Hervey and Moreton Bays in 1997 and 1998 and analysed for pesticide and herbicide residues. Low levels of atrazine (0.1-0.3 mug kg(-1)), diuron (0.2-10.1 mug kg(-1)), lindane (0.08-0.19 mug kg(-1)), dieldrin (0.05-0.37 mug kg(-1)), DDT (0.05-0.26 mug kg(-1)), and DDE (0.05-0.26 mug kg(-1)) were detected in sediments and/or seagrasses. Contaminants were mainly detected in samples collected along the high rainfall, tropical coast between Townsville and Port Douglas and in Moreton Bay. Of the contaminants detected, the herbicide diuron is of most concern as the concentrations detected have some potential to impact local seagrass communities, (C) 2000 Elsevier Science Ltd. All rights reserved.

Black band disease of corals: Ecology and physiology of Phormidium corallyticum

Black band disease of corals consists of a microbial community dominated by the cyanobacteriurn Phormidium corallyticum. The disease primarily affects reef-framework coral species, Active black band disease continually opens up new substrate in reef environments by destroying coral tissue as the disease line advances across the surface of infected colonies. A field study was carried out to determine the abundance and distribution of black band disease on the reef building corals in the Florida Keys. During July of 1992 and 1993, up to 0.72% of coral colonies were infected with black band disease. Analysis of the distribution showed that the disease was clumped. Seasonal patters varied, with some coral colonies infected year round, others exhibiting reinfection from summer 1992 to summer 1993, and some colonies infected for one year only. Statistical analysis of black band disease incidence in relation to various environmental parameters revealed that black band disease was associated with relatively shallow water depths, higher temperatures, elevated nitrite levels, and decreased ortho-phosphate levels. Additional field studies determined recovery of scleractinian coral colonies damaged or killed through the activities of black band disease over a five-year period. These studies determined if the newly exposed substrate was recolonized through scleractinian recruitment, if there was overgrowth of the damaged areas by the formerly diseased colony, or if coral tissue destruction continued after the cessation of black band disease activity. Tissue loss continued on all coral colonies with only one colony exhibiting new tissue growth. The majority of recolonization was by non-reef-framework corals and octocorallians, limited recruitment by framework species was observed. Physiological studies of P. corallyticum were carried out to investigate the photosynthetic capacity of this cyanobacterium, and to determine if this species has the ability to fix dinitrogen. The results of this research demonstrated that P. corallyticum reaches maximum photosynthetic rates at very low light intensities (27.9 μE/m/sec), and that P. corallyticum is able to carry out oxygenic photosynthesis in the presence of sulfide, an ability that is uncommon in prokaryotic organisms. ^

Immunophylogenetic aspects of a gorgonian coral

One goal of comparative immunology is to derive inferences about evolutionary pathways in the development of immune-defense systems. Almost 700 million years ago, a major divergence occurred in the phylogeny of animals, spitting all descendants into either the protostome or deuterostome (includes vertebrates) lineages. Genes have evolved independently along these lineages for that amount of time. Cnidarians originated before that divergence event, and can hold clues as to which immune response genes are homologous to both lineages. This work uses the gorgonian coral, Swiftia exserta, for two major reasons: (1) because of their phylogenetic position, corals are an important animal model in studies concerning the phylogeny of immune-response genes, and (2) nothing is known about the genes controlling immunocompetence in corals. The work described here has important implications in both innate and adaptive immunity. ^ The vertebrate complement system is a major component of innate immunity. C3 is a critical component of the three pathways of complement. Because of its opsonic properties, a C3-like protein is expected to have evolved early. However, currently available data suggests that complement-like components are unique to the deuterostome lineage. This work describes the cloning and characterization of a C3-like gene from S. exserta. The deduced polypeptide sequence reveals conservation of multiple, functionally critical, sites while sharing physiochemical and structural properties with the complement components C3/C4/C5. ^ Antigen processing, via intracellular enzymatic proteasomes, is a major requirement of vertebrate adaptive immunity. These organelles have a catalytic core, through which pass intracellular proteins for degradation into peptides presentable to the immune system. LMP 7 is one component of the paralogous “immuno-proteasome”. LMP 7 is a paralog of the ubiquitous LMP X, but is restricted to vertebrates. While LMP 7 is absent in the coral, this work describes a coral LMP X gene. Phylogenetic analyses, along with hydropathy profiling of a critical portion of the invertebrate and vertebrate paralogous genes, suggests that some invertebrates have two diverging LMP X genes. In some cases, one LMP X protein shares characteristics with vertebrate LMP 7. This work presents new evidence for how the LMP X and 7 genes evolved. ^

Characterizations of the major coral diseases of the Philippines: Ulcerative white spot disease and novel growth anomalies of Porites

Coral reefs are in decline worldwide and coral disease is a significant contributing factor. However, etiologies of coral diseases are still not well understood. In contrast with the Caribbean, extremely little is known about coral diseases in the Philippines. In 2005, off Southeast Negros Island, Philippines, I investigated relationships between environmental parameters and prevalence of the two most common coral diseases, ulcerative white spot (UWS) and massive Porites growth anomalies (MPGAs). Samples were collected along a disease prevalence gradient 40.5 km long. Principal component analyses showed prevalence of MPGAs was positively correlated with water column nitrogen, organic carbon of surface sediments, and colony density. UWS was positively correlated with water column phosphorus. This is the first quantitative evidence linking anthropogenically-impacted water and sediment to a higher prevalence of these diseases. Histological and cytological alterations were investigated by comparing tissues from two distinct types of MPGA lesions (types 1 and 2) and healthy coral using light and electron microscopy. Skeletal abnormalities and sloughing, swelling, thinning, and loss of tissues in MPGAs resembled tissues exposed to bacterial or fungal toxins. Both lesion types had decreases in symbiotic zooxanthellae, which supply nutrients to corals. Notable alterations included migrations of chromophore cells (amoebocytes) (1) nocturnally to outer epithelia to perform wound-healing, including plugging gaps and secreting melanin in degraded tissues, and (2) diurnally to the interior of the tissue possibly to prevent shading zooxanthellae in order to maximize photosynthate production. Depletion of melanin (active in wound healing) in type 2 lesions suggested type 2 tissues were overtaxed and less stable. MPGAs contained an abundance of endolithic fungi and virus-like particles, which may result from higher nutrient levels and play roles in disease development. Swollen cells and mucus frequently blocked gastrovascular canals (GVCs) in MPGAs. Type 1 lesions appeared to compensate for impeded flow of wastes and nutrients through these canals with proliferation of new GVCs, which were responsible for the observed thickened tissues. In contrast, type 2 tissues were thin and more degraded. Dysplasia and putative neoplasia were also observed in MPGAs which may result from the tissue regeneration capacity being overwhelmed.

Diel Patterns of Patch Reef Community Dynamics in a Caribbean Back-Reef System

Back-reef seascapes represent critical habitat for juvenile and adult fishes. Patch reef, seagrass, and mangrove habitats form a heterogeneous mosaic, often linked by species that use reefs as structure during the day and make foraging migrations into soft-bottom habitat at night. Artificial reefs are used to model natural patch reefs, however may not function equivalently as fish habitat. To study the relative value of natural and artificial patch reefs as fish habitat, these communities in the Sea of Abaco, Bahamas were compared using roving diver surveys and time-lapse photography. Diel turnover in fish abundance, recorded with time-lapse photography and illuminated by infrared light, was quantified across midday, dusk, and night periods to explore possible effects of reef type (artificial vs. natural) on these patterns. Diurnal communities on natural reefs exhibited greater fish abundance, species richness, and functional diversity compared to artificial reefs. Furthermore, both types of reef communities exhibited a significant shift across the diel period, characterized by a decline in total fish density at night, especially for grunts (Haemulidae). Cross-habitat foraging migrations by diurnal or nocturnal species, such as haemulids, are likely central drivers of this twilight turnover and can represent important energy and nutrient subsidies. Time-lapse surveys provided more consistent measures of reef fish assemblages for the smaller artificial reef habitats, yet underestimated abundance of certain taxa and species richness on larger patch habitats when compared to the roving diver surveys. Time-lapse photography complemented with infrared light represent a valuable non-invasive approach to studying behavior of focal species and their fine-scale temporal dynamics in shallow-reef communities.

Does landscape context affect habitat value? The importance of seascape ecology in back-reef systems

Seascape ecology provides a useful framework from which to understand the processes governing spatial variability in ecological patterns. Seascape context, or the composition and pattern of habitat surrounding a focal patch, has the potential to impact resource availability, predator-prey interactions, and connectivity with other habitats. For my dissertation research, I combined a variety of approaches to examine how habitat quality for fishes is influenced by a diverse range of seascape factors in sub-tropical, back-reef ecosystems. In the first part of my dissertation, I examined how seascape context can affect reef fish communities on an experimental array of artificial reefs created in various seascape contexts in Abaco, Bahamas. I found that the amount of seagrass at large spatial scales was an important predictor of community assembly on these reefs. Additionally, seascape context had differing effects on various aspects of habitat quality for the most common reef species, White grunt Haemulon plumierii. The amount of seagrass at large spatial scales had positive effects on fish abundance and secondary production, but not on metrics of condition and growth. The second part of my dissertation focused on how foraging conditions for fish varied across a linear seascape gradient in the Loxahatchee River estuary in Florida, USA. Gray snapper, Lutjanus griseus, traded food quality for quantity along this estuarine gradient, maintaining similar growth rates and condition among sites. Additional work focused on identifying major energy flow pathways to two consumers in oyster-reef food webs in the Loxahatchee. Algal and microphytobenthos resource pools supported most of the production to these consumers, and body size for one of the consumers mediated food web linkages with surrounding mangrove habitats. All of these studies examined a different facet of the importance of seascape context in governing ecological processes occurring in focal habitats and underscore the role of connectivity among habitats in back-reef systems. The results suggest that management approaches consider the surrounding seascape when prioritizing areas for conservation or attempting to understand the impacts of seascape change on focal habitat patches. For this reason, spatially-based management approaches are recommended to most effectively manage back-reef systems.

Aspects Allogenic Memory in the Gorgonian Coral Swiftia Exserta

Accelerated graft rejection can be used to determine immune memory in the gorgonian coral swiftia exserta. The extent ofthe persistence of immune memory will be determined in this experiment using replicate sets that are time elapsed from 1, 3, and 6 month. Although corals lack circulatory systems which can be a component of adaptive systemic immunity, this study will attempt to determine whether this gorgonian coral is capable of transmitting immune information throughout its colonial body. Results showed that at each of the time points; one, three, and six months the secondary response group and the primary response group were significantly different (at p=0.001) therefore, demonstrating long term immune memory. While the primary response group and the 3rd party specificity response group were similar, both were significantly different (at p=O. 001) from the secondary response group which shows the response to be specific, with memory applicable to the original antigen. Systemic immunity was not determined to be present for 15 em and one week after initial sensitization.