The rising tide of ocean diseases: Unsolved problems and research priorities

New studies have detected a rising number of reports of diseases in marine organisms such as corals, molluscs, turtles, mammals, and echinoderms over the past three decades. Despite the increasing disease load, microbiological, molecular, and theoretical tools for managing disease in the world's oceans are underdeveloped. Review of the new developments in the study of these diseases identifies five major unsolved problems and priorities for future research: (1) detecting origins and reservoirs for marine diseases and tracing the flow of some new pathogens from land to sea; (2) documenting the longevity and host range of infectious stages; (3) evaluating the effect of greater taxonomic diversity of marine relative to terrestrial hosts and pathogens; (4) pinpointing the facilitating role of anthropogenic agents as incubators and conveyors of marine pathogens; (5) adapting epidemiological models to analysis of marine disease.

Coral reefs in a century of rapid environmental change

Coral reefs are the most diverse marine ecosystem and embrace possibly millions of plant, animal and protist species. Mutualistic symbioses are a fundamental feature of coral reefs that have been used to explain their structure, biodiversity and existence. Complex inter-relationships between hosts, habitats and symbionts belie closely coupled nutrient and community dynamics that create the circumstances for something from nothing (or the oasis in a nutrient desert). The flip side of these dynamics is a close dependency between species, which results in a series of non-linear relationships as conditions change. These responses are being highlighted as anthropogenic influences increase across the world's tropical and subtropical coastlines. Caribbean as well as Indo-Pacific coral populations are now in a serious decline in many parts of the world. This has resulted in a significant reorganization of how coral reef ecosystems function. Among the spectra of changes brought about by humans is rapid climate change. Mass coral bleaching - the loss of the dinoflagellate symbionts from reef-building corals - and mortality has affected the world's coral reefs with increasing frequency and intensity since the late 1970s. Mass bleaching events, which often cover thousands of square kilometres of coral reefs, are triggered by small increases (+1-3degreesC) in water temperature. These increases in sea temperature are often seen during warm phase weather conditions (e.g. ENSO) and are increasing in size and magnitude. The loss of living coral cover (e.g. 16% globally in 1998, an exceptionally warm year) is resulting in an as yet unspecified reduction in the abundance of a myriad of other species. Projections from general circulation models (GCM) used to project changes in global temperature indicate that conditions even under the mildest greenhouse gas emission scenarios may exceed the thermal tolerances of most reef-building coral communities. Research must now explore key issues such as the extent to which the thermal tolerances of corals and their symbionts are dynamic if bleaching and disease are linked; how the loss of high densities of reef-building coral will affect other dependent species; and, how the loss of coral populations will affect the millions of people globally who depend on coral reefs for their daily survival.

Pumice rafting and faunal dispersion during 2001-2002 in the Southwest Pacific: record of a dacitic submarine explosive eruption from Tonga

A new influx of sea-rafted pumice reached the eastern coast of Australia in October 2002, approximately 1 year after a felsic, shallow-marine explosive eruption at a previously unknown volcano (0403-091) along the Tofua volcanic arc (Tonga). The eruption produced floating pumice rafts that first became stranded in Fiji in November 2001, approximately I month after the eruption. Strandings of sea-rafted pumice along shorelines have been the only record of products from this submarine explosive eruption at the remote, submerged volcano. Computed drift trajectories of the sea-rafted pumice using numerical models of southwest Pacific surface wind fields and ocean currents indicate two cyclonic systems disturbed the drift of pumice to eastern Australia, as well as the importance of the combined wave and direct wind effect on pumice trajectory. Pumice became stranded along at least two-thirds (>2000 km) of the coastline of eastern Australia, being deposited on beaches during a sustained period of fresh onshore winds. Typical amounts of pumice initially stranded on beaches were 500-4000 individual clasts per in, and a minimum volume estimate of pumice that arrived to eastern Australia is 1.25 x 10(5) m(3). Pumice was beached below maximum tidal/storm surge levels and was quickly reworked back into the ocean, such that the concentration of beached pumice rapidly dissipated within weeks of the initial stranding, and little record of this stranding event now exists. Most stranded pumice clasts ranged in size from 2 to 5 cm in diameter; the largest measured clasts were 10 cm in Australia and 20 cm in Fiji. The pumice has a low phenocryst content (3500 km) and period of pumice floatation (greater than or equal to1 year), confirm the importance of sea-rafted pumice as a long-distance dispersal mechanism for marine organisms including marine pests and harmful invasive species. Billions of individual rafting pumice clasts can be generated in a single small-volume eruption, such as observed here, and the geological implications for the transport of sessile taxa over large distances are significant. An avenue for future research is to examine whether speciation events and volcanicity are linked; the periodic development of globalism for some taxa (e.g., corals, gastropods, bryozoa) may correlate in time and/or space with voluminous silicic igneous events capable of producing >10(6) km(3) of silicic pumice-rich pyroclastic material and emplaced into ocean basins. (C) 2004 Elsevier B.V. All rights reserved.

Effect of early marine diagenesis on coral reconstructions of surface-ocean 13C/12C and carbonate saturation state

Recent research suggests that future decreases in the carbonate saturation state of surface seawater associated with the projected build-up of atmospheric CO2 could cause a global decline in coral reef-building capacity. Whether significant reductions in coral calcification are underway is a matter of considerable debate. Multicentury records of skeletal calcification extracted from massive corals have the potential to reconstruct the progressive effect of anthropogenic changes in carbonate saturation on coral reefs. However, early marine aragonite cements are commonly precipitated from pore waters in the basal portions of massive coral skeletons and, if undetected, could result in apparent nonlinear reductions in coral calcification toward the present. To address this issue, we present records of coral skeletal density, extension rate, calcification rate, δ13C, and δ18O for well preserved and diagenetically altered coral cores spanning ∼1830-1994 A.D. at Ningaloo Reef Marine Park, Western Australia. The record for the pristine coral shows no significant decrease in skeletal density or δ13C indicative of anthropogenic changes in carbonate saturation state or δ13C of surface seawater (oceanic Suess effect). In contrast, progressive addition of early marine inorganic aragonite toward the base of the altered coral produces an apparent ∼25% decrease in skeletal density toward the present, which misleadingly matches the nonlinear twentieth century decrease in coral calcification predicted by recent modeling and experimental studies. In addition, the diagenetic aragonite is enriched in 13C, relative to coral aragonite, resulting in a nonlinear decrease in δ13C toward the present that mimics the decrease in δ13C expected from the oceanic Suess effect. Taken together, these diagenetic changes in skeletal density and δ13C could be misinterpreted to reflect changes in surface-ocean carbonate saturation state driven by the twentieth century build-up of atmospheric CO2. Copyright 2004 by the American Geophysical Union.

Testing the 'photoinhibition' model of coral bleaching using chemical inhibitors

Explants of the hard coral Seriatopora hystrix were exposed to sublethal concentrations of the herbicide diuron DCMU (N'-(3,4-dichlorophenyl,-N,N-dimethylurea)) and the heavy metal copper. Pulse amplitude modulated (PAM) chlorophyll fluorescence techniques were used to assess the effects on the photosynthetic efficiency of the algal symbionts in the tissue (in Symbio), and chlorophyll fluorescence and counts of symbiotic algae (normalised to surface area) were used to assess the extent of coral bleaching. At 30 mug DCMU l(-1), there was a reduction in both the maximum effective quantum yield (DeltaF/F-m') and maximum potential quantum yield (F-v/F-m) of the algal symbionts in symbio. Corals subsequently lost their algal symbionts and discoloured (bleached), especially on their upper sunlight-exposed surfaces. At the same DCMU concentration but under low light (5% of growth irradiance), there was a marked reduction in DeltaF/F-m' but only a slight reduction in F-v/F-m and slight loss of algae. Loss of algal symbionts was also noted after a 7 d exposure to concentrations as low as 10 mug DCMU l(-1) under normal growth irradiance, and after 14 d exposure to 10 mug DCMU l(-1) under reduced irradiance. Collectively the results indicate that DCMU-induced bleaching is caused by a light-dependent photoinactivation of algal symbionts, and that bleaching occurs when F-v/F-n, (measured 2 h after sunset) is reduced to a value of less than or equal to 0.6. Elevated copper concentrations (60 mug Cu l(-1) for 10 h) also induced a rapid bleaching in S. hystrix but without affecting the quantum yield of the algae in symbio. Tests with isolated algae indicated that substantially higher concentrations (300 mug Cu l(-1) for 8 h) were needed to significantly reduce the quantum yield. Thus, copper-induced bleaching occurs without affecting the algal photosynthesis and may be related to effects on the host (animal). It is argued that warm-water bleaching of corals resembles both types of chemically induced bleaching, suggesting the need for an integrated model of coral bleaching involving the effect of temperature on both host (coral) and algal symbionts.

High-frequency winter cooling and reef coral mortality during the Holocene climatic optimum

A detailed ecological, micro-structural and skeletal Sr/Ca study of a 3.42 m thick Goniopora reef profile from an emerged Holocene reef terrace at the northern South China Sea reveals at least nine abrupt massive Goniopora stress and mortality events occurred in winter during the 7.0-7.5 thousand calendar years before present (cal. ka BP) (within the Holocene climatic optimum). Whilst calculated Sr/Ca-SST (sea surface temperature) maxima during this period are comparable to those in the 1990s, Sr/Ca-SST minima are significantly lower, probably due to stronger winter monsoons. Such generally cooler winters, superimposed by further exceptional winter cooling on inter-annual to decadal scales, may have caused stress and mortality of the corals about every 50 years. Sea level rose by similar to 3.42 m during this period, with present sea-level reached at similar to 7.3 ka BP and a sea-level highstand of at least similar to 1.8 m occurred at similar to 7.0 ka. The results show that it took about 20-25 years for a killed Goniopora coral reef to recover. (C) 2004 Elsevier B.V. All rights reserved.

Storm cycles in the last millennium recorded in Yongshu Reef, southern South China Sea

Large storm-relocated Porites coral blocks are widespread on the reef flats of Nansha area, southern South China Sea. Detailed investigations of coral reef ecology, geomorphology and sedimentation on Yongshu Reef indicate that such storm-relocated blocks originated from large Porites lutea corals growing on the spurs within the reef-front living coral zone. Because the coral reef has experienced sustained subsidence and reef development during the Holocene, dead corals were continuously covered by newly growing coral colonies. For this reason, the coral blocks must have been relocated by storms from the living sites and therefore the ages of these storm-relocated corals should approximate the times when the storms occurred. Rapid emplacement of these blocks is also evidenced by the lack of coral overgrowth, encrustation or subtidal alteration. U-series dating of the storm-relocated blocks as well as of in situ reef flat corals suggests that, during the last 1000 years, at least six strong storms occurred in 1064 +/- 30, 1210 +/- 5-1201 +/- 4, 1336 +/- 9, 1443 +/- 9, 1685 +/- 8-1680 +/- 6, 1872 +/- 15 AD, respectively, with an average 160-year cycle (110-240 years). The last storm, which occurred in 1872 15 AD, also led to mortality of the reef flat corals dated at similar to 130 years ago. Thus, the storm had significant impacts on coral reef ecology and morphology. (C) 2004 Elsevier B.V. All rights reserved.

Sea surface temperature variations recorded on coralline Sr/Ca ratios during Mid-Late Holocene in Leizhou Peninsula

High-resolution Sr/Ca ratios of two Porites corals from Leizhou Peninsula were measured using inductively coupled plasma atomic spectrometry (ICP-AES). TIMS U-Th dating reveals that the life-spans of the two corals are 489500 AD and 539-530 BC, respectively. Monthly sea surface temperatures (SSTs) during these two periods can be reconstructed from their skeletal Sr/Ca ratios. The results reveal that SSTs during 539-530 BC were roughly the same as those during 1990-2000 AD in this area, indicating a relative warm climate period. However, the period of 489-500 AD was significantly cooler, with annual mean SST, the 10-a average of minimum monthly winter SSTs and the 10-a average of maximum monthly summer SSTs being about 2, 2.9 and 1degreesC lower than that in the 1990s, respectively. Such climate patterns agree well with the phenological results recorded in the historic documents in other areas of China.

Rare earth element geochemistry of Late Devonian reefal carbonates, canning basin, Western Australia: Confirmation of a seawater REE proxy in ancient limestones

Rare earth element and yttrium (REE+Y) concentrations were determined in 49 Late Devonian reefal carbonates from the Lennard Shelf, Canning Basin, Western Australia. Shale-normalized (SN) REE+Y patterns of the Late Devonian samples display features consistent with the geochemistry of well-oxygenated, shallow seawater. A variety of different ancient limestone components, including microbialites, some skeletal carbonates (stromatoporoids), and cements, record seawater-like REE+Y signatures. Contamination associated with phosphate, Fe-oxides and shale was tested quantitatively, and can be discounted as the source of the REE+Y patterns. Co-occurring carbonate components that presumably precipitated from the same seawater have different relative REE concentrations, but consistent REE+Y patterns. Clean Devonian early marine cements (n = 3) display REE+Y signatures most like that of modern open ocean seawater and the highest Y/Ho ratios (e.g., 59) and greatest light REE (LREE) depletion (average Nd-SN/Yb-SN = 0.413, SD = 0.076). However, synsedimentary cements have the lowest REE concentrations (e.g., 405 ppb). Non-contaminated Devonian microbialite samples containing a mixture of the calcimicrobe Renalcis and micritic thrombolite aggregates in early marine cement (n = 11) have the highest relative REE concentrations of tested carbonates (average total REE = 11.3 ppm). Stromatoporoid skeletons, unlike modern corals, algae and molluscs, also contain well-developed, seawater-like REE patterns. Samples from an estuarine fringing reef have very different REE+Y patterns with LREE enrichment (Nd-SN/Yb-SN > 1), possibly reflecting inclusion of estuarine colloidal material that contained preferentially scavenged LREE from a nearby riverine input source. Hence, Devonian limestones provide a proxy for marine REE geochemistry and allow the differentiation of co-occurring water masses on the ancient Lennard Shelf. Although appropriate partition coefficients for quantification of Devonian seawater REE concentrations from out data are unknown, hypothetical Devonian Canning Basin seawater REE patterns were obtained with coefficients derived from modern natural proxies and experimental values. Resulting Devonian seawater patterns are slightly enriched in LREE compared to most modem seawaters and suggest higher overall REE concentrations, but are very similar to seawaters from regions with high terrigenous inputs. Our results suggest that most limestones should record important aspects of the REE geochemistry of the waters in which they precipitated, provided they are relatively free of terrigenous contamination and major diagenetic alteration from fluids with high, non-seawater-like REE contents. Hence, we expect that many other ancient limestones will serve as seawater REE proxies, and thereby provide information on paleoceanography, paleogeography and geochemical evolution of the oceans. Copyright (C) 2004 Elsevier Ltd.

Endolithic algae photoacclimate to increased irradiance during coral bleaching

The photoacclimation of endolithic algae ( of the genus Ostreobium) inhabiting the skeleton of the Mediterranean coral Oculina patagonica during a bleaching event was examined. Pulse amplitude modulated (PAM) chlorophyll fluorescence techniques in situ were used to assess the photosynthetic efficiency of endolithic algae in the coral skeleton and the symbiotic dinoflagellates (zooxanthellae) in the coral tissue. Relative photosynthetic electron transport rates (ETRs) of the endolithic algae under bleached areas of the colony were significantly higher than those of endolithic algae from a healthy section of the colony and those of zooxanthellae isolated from the same section. Endolithic algae under healthy parts of the colony demonstrated an ETRmax of 16.5% that of zooxanthellae from tissue in the same section whereas endolithic algae under bleached sections showed ETRmax values that were 39% of those found for healthy zooxanthellae. The study demonstrates that endolithic algae undergo photoacclimation with increased irradiance reaching the skeleton. As PAM fluorometry has become a major tool for assessing levels of stress and bleaching in corals, the importance of considering the contribution of the endolithic algae to the overall chlorophyll fluorescence measured is highlighted.

Dynamics of a temperature-related coral disease outbreak

During the austral summer of 2001/2002, a coral epizootic occurred almost simultaneously with a bleaching event on the fringing reefs of Magnetic Island (Great Barrier Reef region), Australia. This resulted in a 3- to 4-fold increase in the mean percentage of partial mortality rate in a population of the hard coral Montipora aequituberculata. The putative disease state, ‘atramentous necrosis’, was observed on both bleached and normally-pigmented M. aequituberculata, and presented blackened lesions that spread within days across the colony surface and throughout the population. Diseased portions of the corals were only visible for 3 to 4 wk, with diseased tissues becoming covered in sediment and algae, which rapidly obscured evidence of the outbreak. Diseased colonies were again observed in the summer of 2002/2003 after being absent over the 2002 winter. Analysis of when diseased and bleached corals were first observed, and when and where the mortality occurred on individual colonies, indicated virtually all the mortality over the summer could be attributed to the disease and not to the bleaching. Fluorescence in situ hybridisation (FISH) techniques and cloning, and analysis of the 16S rRNA genes from diseased coral tissue, identified a mixed microbial assemblage in the diseased tissues particularly within the Alphaproteobacteria, Firmicutes and Bacteroidetes. While it is not possible in this study to distinguish between a disease-causing microbial community versus secondary invaders, the bacterial 16S rDNA sequences identified within the blackened lesions demonstrated high similarity to sequences from black band disease and white plague infected corals, suggesting either common aetiological agents or development of a bacterial community that is specific to degrading coral tissues. Temperature-induced coral disease outbreaks, with the potential for elevated levels of mortality, may represent an added problem for corals during the warmer summer months and an added dimension to predicted increases in water temperature from climate change.

Use of X-radiographs to distinguish members of the Montastraea annularis reef-coral species complex

Recent work suggests the Montastraea annularis species complex consists of at least three species, which can be distinguished qualitatively in the field using features related to colony growth (e.g. overall growth form. bumpiness, growth along the colony edge). However, when whole colonies are not available and surfaces are eroded, identification becomes problematic when relying on such characteristics. Characters based on internal skeletal structures are less prone to loss due to taphonomic processes. Previous work has shown that internal corallite architectural features measured in transverse thin sections can be used to distinguish species. To determine whether internal colony-level features measured on X-radiographs can be used. eight characters related to corallite budding and accretionary growth were measured on specimens representing three modern members of the M. annularis species complex (M. annularis, M. flaveolata and M. franksi), as well as two fossil forms (columnar and organ-pipe). All eight characters showed significant differences among species. Discriminant function analysis using seven of these characters resulted in distinct species groupings In canonical scores plots and a 100% classification success for specimens from Panama. These results suggest that measurements made on X-radiographs provide a useful tool for quantitatively distinguishing members of the M. annularis complex as well as between other massive reef corals.

Overlapping species boundaries and hybridization within the Monastraea "annularis" reef coral complex in the Pleistocene of the Bahama Islands

Recent molecular analyses indicate that many reef coral species belong to hybridizing species complexes or "syngameons." Such complexes consist of numerous genetically distinct-species or lineages, which periodically split and/or fuse as they extend through time. During splitting and fusion, morphologic intermediates form and species overlap. Here we focus on processes associated with lineage fusion, specifically introgressive hybridization, and the recognition of such hybridization in the fossil record. Our approach involves comparing patterns of ecologic and morphologic overlap in genetically characterized modern species with fossil representatives of the same or closely related species. We similarly consider the long-term consequences of past hybridization on the structure of modern-day species boundaries. Our study involves the species complex Montastraea annularis s.l. and is based in the Bahamas, where, unlike other Caribbean locations, two of the three members of the complex today are not genetically distinct. We measured and collected colonies along linear transects across Pleistocene reef terraces of last interglacial age (approximately 125 Ka) on the islands of San Salvador, Andros, and Great Inagua. We performed quantitative ecologic and morphologic analyses of the fossil data, and compared patterns of overlap among species with data from modern localities where species are and are not genetically distinct. Ecologic and morphologic analyses reveal "moderate" overlap (>10%, but statistically significant differences) and sometimes "high" overlap (no statistically significant differences) among Pleistocene growth forms (= "species"). Ecologic analyses show that three species (massive, column, organ-pipe) co-occurred. Although organ-pipes had higher abundances in patch reef environments, columnar and massive species exhibited broad, completely overlapping distributions and had abundances that were not related to reef environment. For morphometric analyses, we used multivariate discriminant analysis on landmark data and linear measurements. The results show that columnar species overlap "moderately" with organ-pipe and massive species. Comparisons with genetically characterized colonies from Panama show that the Pleistocene Bahamas species have intermediate morphologies, and that the observed "moderate" overlap differs from the morphologic separation among the three modern species. In contrast, massive and columnar species from the Pleistocene of the Dominican Republic comprise distinct morphologic clusters, similar to the modern species; organ-pipe species exhibit "low" overlap (

Coral mortality increases wave energy reaching shores protected by reef flats: Examples from the Seychelles

In the granitic Seychelles, many shores and beaches are fringed by coral reef flats which provide protection to shores from erosion by waves. The surfaces of these reef flats support a complex ecology. About 10 years ago their seaward zones were extensively covered by a rich coral growth, which reached approximately to mean low water level, but in 1998 this was largely killed by seawater warming. The resulting large expanses of dead coral skeletons in these locations are now disintegrating, and much of the subsequent modest recovery by new coral recruitment was set back by further mortalities. A mathematical model of wave energy reaching shorelines protected by coral reef flats has been applied to 14 Seychelles reefs. It is derived from equations which predict: (1) the raised water level, or wave set-up, on reef flats resulting from wave breaking, which depends upon offshore wave height and period, depth of still water over the reef flat and the reef crest profile, and (2) the decay of energy from reef edge to shoreline that is affected by width of reef flat, surface roughness, sea level rise and 'pseudo-sea level rise' created by increased depth resulting from disintegration of coral colonies. The model treats each reef as one entity, but because biota and zonation on reef flats are not homogenous, all reefs are divided into four zones. In each, cover by both living and dead biota was estimated for calculation of parameters, and then averaged to obtain input data for the model. All possible biological factors were taken into account, such as the ability of seagrass beds to grow upwards to match expected sea level rise, reduction in height of the reef flat in relation to sea level as zones of dead corals decay, and the observed 'rounding' of reef crests as erosion removes corals from those areas. Estimates were also made of all these factors for a time approximately a decade ago, representing a time before the mass coral mortality, and for approximately a decade in the future when the observed rapid state of dead coral colony disintegration is assumed to have reached an end point. Results of increased energy over the past decade explain observations of erosion in some sites in the Seychelles. Most importantly, it is estimated that the rise in energy reaching shores protected by fringing reefs will now accelerate more rapidly, such that the increase expected over the next decade will be approximately double than that seen over the past decade. (c) 2005 Elsevier Ltd. All rights reserved.

Effects of the herbicide diuron on the early life history stages of coral

The effects of the herbicide diuron on the early life history stages of broadcast spawning and brooding corals were examined in laboratory experiments. Fertilisation of Acropora millepora and Montipora aequituberculata oocytes were not inhibited at diuron concentrations of up to 1000 mu gl(-1). Metamorphosis of symbiont-free A. millepora larvae was only significantly inhibited at 300 mu gl(-1) diuron. Pocillopora damicornis larvae, which contain symbiotic dinoflagellates, were able to undergo metamorphosis after 24h exposure to diuron at 1000 mu gl(-1). Two-week old P. damicornis recruits on the other hand were as susceptible to diuron as adult colonies, with expulsion of symbiotic dinoflagellates (bleaching) evident at 10 mu gl(-1) diuron after 96 h exposure. Reversible metamorphosis was observed at high diuron concentrations, with fully bleached polyps escaping from their skeletons. Pulse amplitude modulation (PAM) chlorophyll fluorescence techniques demonstrated a reduction in photosynthetic efficiency (Delta F/F'(m)) in illuminated P. dami- cornis recruits after a 2h exposure to 1 mu gl(-1) diuron. The dark-adapted quantum yields (F-v/F-m also declined, indicating chronic photoinhibition and damage to photosystem H. Crown Copyright (c) 2004 Published by Elsevier Ltd. All rights reserved.